# **Recent Advances in Psychopathology in Neurodevelopmental Disorders**

**From Bench to Bedside** 

Edited by Shoumitro Deb

Printed Edition of the Special Issue Published in *International Journal of Environmental Research and Public Health* 

www.mdpi.com/journal/ijerph

## **Recent Advances in Psychopathology in Neurodevelopmental Disorders: From Bench to Bedside**

## **Recent Advances in Psychopathology in Neurodevelopmental Disorders: From Bench to Bedside**

Editor

**Shoumitro Deb**

MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade • Manchester • Tokyo • Cluj • Tianjin

*Editor* Shoumitro Deb Imperial College London UK

*Editorial Office* MDPI St. Alban-Anlage 66 4052 Basel, Switzerland

This is a reprint of articles from the Special Issue published online in the open access journal *International Journal of Environmental Research and Public Health* (ISSN 1660-4601) (available at: https: //www.mdpi.com/journal/ijerph/special issues/RAiPiNDFBtB).

For citation purposes, cite each article independently as indicated on the article page online and as indicated below:

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© 2023 by the authors. Articles in this book are Open Access and distributed under the Creative Commons Attribution (CC BY) license, which allows users to download, copy and build upon published articles, as long as the author and publisher are properly credited, which ensures maximum dissemination and a wider impact of our publications.

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## **Contents**

### **About the Editor** .............................................. **vii**

#### **Freya Tyrer, Richard Morriss, Reza Kiani, Satheesh K. Gangadharan, Harish Kundaje and Mark J. Rutherford**

Health Needs and Their Relationship with Life Expectancy in People with and without Intellectual Disabilities in England

Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 6602, doi:10.3390/ijerph19116602 . . . **1**

#### **Alister Baird, Bridget Candy, Eirini Flouri, Nick Tyler and Angela Hassiotis**

The Association between Physical Environment and Externalising Problems in Typically Developing and Neurodiverse Children and Young People: A Narrative Review Reprinted from: *Int. J. Environ. Res. Public Health* **2023**, *20*, 2549, doi:10.3390/ijerph20032549 . . . **13**

#### **Tanja Sappok, Angela Hassiotis, Marco Bertelli, Isabel Dziobek and Paula Sterkenburg**

Developmental Delays in Socio-Emotional Brain Functions in Persons with an Intellectual Disability: Impact on Treatment and Support

Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 13109, doi:10.3390/ijerph192013109 . **49**

#### **Paula S. Sterkenburg, Marie Ilic, Miriam Flachsmeyer and Tanja Sappok**

More than a Physical Problem: The Effects of Physical and Sensory Impairments on the Emotional Development of Adults with Intellectual Disabilities Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 17080, doi:10.3390/ijerph192417080 . **63**

#### **Johanna Eisinger, Magdalena Dall, Jason Fogler, Daniel Holzinger and Johannes Fellinger**

Intellectual Disability Profiles, Quality of Life and Maladaptive Behavior in Deaf Adults: An Exploratory Study

Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 9919, doi:10.3390/ijerph19169919 . . . **73**

#### **Gerda de Kuijper, Joke de Haan, Shoumitro Deb and Rohit Shankar**

Withdrawing Antipsychotics for Challenging Behaviours in Adults with Intellectual Disabilities: Experiences and Views of Prescribers Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 17095, doi:10.3390/ijerph192417095 . **85**

#### **Gerda de Kuijper, Joke de Haan, Shoumitro Deb and Rohit Shankar**

Withdrawing Antipsychotics for Challenging Behaviours in Adults with Intellectual Disabilities: Experiences and Views of Experts by Experience Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 15637, doi:10.3390/ijerph192315637 . **97**

#### **Shoumitro (Shoumi) Deb, Bharati Limbu, Gemma L. Unwin and Tim Weaver**

Causes of and Alternatives to Medication for Behaviours That Challenge in People with Intellectual Disabilities: Direct Care Providers' Perspectives Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 9988, doi:10.3390/ijerph19169988 . . . **107**

#### **Matthew Sanders, Nam-Phuong T. Hoang, Julie Hodges, Kate Sofronoff, Stewart Einfeld, Bruce Tonge, Kylie Gray, et al.**

Predictors of Change in Stepping Stones Triple Interventions: The Relationship between Parental Adjustment, Parenting Behaviors and Child Outcomes Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 13200, doi:10.3390/ijerph192013200 . **121**

### **Emili Rodr´ıguez-Hidalgo, Javier Garc´ıa-Alba, Ramon Novell and Susanna Esteba-Castillo**

The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer's Disease

Reprinted from: *Int. J. Environ. Res. Public Health* **2023**, *20*, 5096, doi:10.3390/ijerph20065096 . . . **133**

**Emili Rodr´ıguez-Hidalgo, Javier Garc´ıa-Alba, Maria Bux ´o, Ramon Novell and Susana Esteba-Castillo**

The Pictorial Screening Memory Test (P-MIS) for Adults with Moderate Intellectual Disability and Alzheimer's Disease

Reprinted from: *Int. J. Environ. Res. Public Health* **2022**, *19*, 10780, doi:10.3390/ijerph191710780 . **153**

## **About the Editor**

#### **Shoumitro Deb**

Professor Shoumitro (Shoumi) Deb, MBBS, FRCPsych, MD, is a Visiting Professor of Neuropsychiatry at the Imperial College London, UK. Previously he was a full-time substantive Clinical Professor at the University of Birmingham and a Senior Lecturer in Psychiatry at Cardiff University. His seminal works include (a) being a member of the group that developed the first-ever evidence-based practice guidelines for intellectual disabilities (ID) in the UK NHS; (b) the first-ever comprehensive assessment of psychopathology in adults with ID and epilepsy; (c) a dementia screening questionnaire for adults with ID (DSQIID), which has been translated into more than 24 languages and validated; (d) the first-ever freely available online-accessible (easy-read) psychotropic medication information leaflets (http://www.ld-medication.bham.ac.uk); (e) the first-ever European Guideline (and recently updated in the *European Journal of Psychiatry*, 2022, 36, 11–25) on the assessment and diagnosis of psychiatric disorders in adults with ID; (f) national and international guidelines on the use of psychotropic medication in adults with ID (*World Psychiatry*, 2009, 8(3), 181–186); (g) the first-ever online training SPECTROM for caregivers to help reduce the overmedication of people with ID (https://spectrom.wixsite.com/project); (h) the first-ever comprehensive neuropsychiatric outcome study in adults with traumatic brain injury (TBI); (i) patient- and carer-determined outcome measures for patients with TBI; and (j) the only published RCT (feasibility) on risperidone versus placebo to treat aggression in adults with TBI. He has over 330 publications and has made over 250 presentations at national and international conferences (including many keynote speeches). He has also ran several MSc programmes in three UK Universities. Additionally, he was (a) a member of the first UK NICE GDG on epilepsy and other NICE guidelines, (b) a Fellow of the UK NIHR, (c) vice-chair of the World Psychiatric Association SPID, and (d) a member of the WHO Working Group on ICD-11.

## *Article* **Health Needs and Their Relationship with Life Expectancy in People with and without Intellectual Disabilities in England**

**Freya Tyrer 1,\*, Richard Morriss 2, Reza Kiani 3,4, Satheesh K. Gangadharan 3,4, Harish Kundaje <sup>5</sup> and Mark J. Rutherford <sup>1</sup>**


**Abstract:** Health needs are common in people living with intellectual disabilities, but we do not know how they contribute to life expectancy. We used the Clinical Practice Research Datalink (CPRD) linked with hospital/mortality data in England (2017–2019) to explore life expectancy among people with or without intellectual disabilities, indicated by the presence or absence, respectively, of: epilepsy; incontinence; severe visual loss; severe visual impairment; severe mobility difficulties; cerebral palsy and PEG feeding. Life expectancy and 95% confidence intervals were compared using flexible parametric methods. At baseline, 46.4% (total *n* = 7794) of individuals with intellectual disabilities compared with 9.7% (total *n* = 176,807) in the comparison group had ≥1 health need. Epilepsy was the most common health need (18.7% vs. 1.1%). All health needs except hearing impairment were associated with shorter life expectancy: PEG feeding and mobility difficulties were associated with the greatest loss in life years (65–68% and 41–44%, respectively). Differential life expectancy attenuated but remained (≈12% life years lost) even after restricting the population to those without health needs (additional years expected to live at 10 years: 65.5 [60.3, 71.1] vs. 74.3 [73.8, 74.7]). We conclude that health needs play a significant role but do not explain all of the differential life expectancy experienced by people with intellectual disabilities.

**Keywords:** intellectual disability; life expectancy; health needs; epilepsy; incontinence; visual; hearing; mobility; cerebral palsy; PEG feeding

#### **1. Introduction**

Addressing the burden of health inequalities is now a global priority [1–3]. Strategies to reduce these inequalities tend to focus on the most vulnerable, such as people living with disabilities or in areas of social deprivation [4–8]. Particularly at risk are those with intellectual disabilities (also known as learning disabilities in the UK) owing to a combination of genetic, social and behavioural factors [9,10]. Whilst there are measures in place to reduce health inequalities in this population, such as annual health checks [11], mortality data suggest that the situation has not improved, despite some deaths being potentially avoidable [12–14].

One of the challenges to reducing inequalities among people living with intellectual disabilities is that they are more likely than the general population to have severe health needs, including epilepsy, cerebral palsy and eating/feeding difficulties, which are known

**Citation:** Tyrer, F.; Morriss, R.; Kiani, R.; Gangadharan, S.K.; Kundaje, H.; Rutherford, M.J. Health Needs and Their Relationship with Life Expectancy in People with and without Intellectual Disabilities in England. *Int. J. Environ. Res. Public Health* **2022**, *19*, 6602. https:// doi.org/10.3390/ijerph19116602

Academic Editor: Shoumitro Deb

Received: 13 April 2022 Accepted: 25 May 2022 Published: 28 May 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

to shorten life expectancy [15]. Although not always life-limiting if managed well, they are relatively rare in the general population and so tend not to feature in population-level policy initiatives. Thus far, their individual contribution to life expectancy has not been formally investigated, but it is important to do so because this contribution may be over-inflated or seen as an inevitable consequence of having intellectual disabilities without seeking to improve health outcomes and/or quality of life for the individuals affected.

The aim of the current study was to investigate specific health needs and quantify their contribution to life expectancy in people with intellectual disabilities and to compare these findings with a cohort of individuals without intellectual disabilities. A further aim was to investigate people without any of the specified health needs to determine if loss in life years for people with intellectual disabilities remained.

#### **2. Materials and Methods**

#### *2.1. Data Sources*

This study followed the Reporting of studies Conducted using Observational Routinelycollected health Data (RECORD) checklist [16] (see Supplementary Table S1). We used the Clinical Practice Research Datalink (CPRD GOLD), linked (person-level) with hospital episode statistics (HES) and death registrations from the Office for National Statistics (approved study protocol number 19\_267). Details of the study population have been described in a previous work [12], with the exception of 23 additional individuals identified, after an amendment to the original protocol, with Cockayne and Angelman syndrome; details of these 23 individuals were received in August 2021 (due to COVID-19 delays; please see the data flow diagram in Supplementary Figure S1 for the initial extract and the study population used for the current study). Briefly, the CPRD is an electronic health record primary care research database which is broadly representative of the national population in terms of age, gender and ethnicity [17]. Only GP surgeries in England that consented to their data being linked with hospital episode statistics (HES) and death data (approximately 75% of CPRD surgeries in England) were included in this study.

#### *2.2. Sample Population*

Initial inclusion criteria for the broader programme of work on which this study was based were: registered at the GP surgery at any point between 1 January 2000 and 29 September 2019 and 10 years old or older to account for delays in reporting of diagnoses of intellectual disability in children [18]. A random sample of 980,586 people without intellectual disabilities (initially 1 million prior to exclusions; see Supplementary Figure S1) was used for the comparison group with the same eligibility criteria (but without a diagnosis of intellectual disability). For this study, data were further restricted to the 2017–2019 observation period such that people entered the study on 1 January 2017 if this was after the original date of cohort entry or were excluded if they were last seen or died before this date. The final population comprised 7794 individuals with intellectual disabilities and 176,807 individuals without intellectual disabilities (*n* = 440 of whom changed status within the observation window at their first intellectual disability diagnosis).

#### *2.3. Definition of Intellectual Disabilities and Health Needs*

Diagnostic codes (Read codes and International Classification of Diseases (ICD)-10 codes) for intellectual disabilities and health needs are reported in the Supplementary Material (Table S2). These were based on a combination of previous literature [12], free text searching of diagnostic code descriptions and clinical opinion (RK, SKG, RM). The initial choice of health needs was based on the literature in this area [19] and discussions with carers and people living with intellectual disabilities as being sufficiently severe to affect life expectancy. These were: epilepsy; incontinence (urinary or faecal); severe visual loss; severe hearing impairment; severe mobility difficulties; cerebral palsy and feeding via a percutaneous endoscopic gastrostomy (PEG) tube (i.e., as a measure of severe eating/feeding difficulties). To avoid inclusion of shorter-term health needs that had resolved over time and/or been misdiagnosed in childhood, such as epilepsy [20,21], health needs were defined as being present only if their most recent diagnosis was within 10 years of cohort entry. The exception to this was cerebral palsy, which was defined by a diagnosis ever being present given that it is a life-long condition from birth/early infancy [22].

#### *2.4. Statistical Methods*

The date of entry into the cohort was defined as the latest date according to the person and practice's characteristics: the beginning (i.e., 1 January 2017) of the observation window; the date of registration with the GP practice; the date the practice was defined as being up to standard (using the CPRD's own quality indicators); or the date the individual turned 10 years old (to align with the eligibility criteria). Because there are known delays in reporting intellectual disability diagnoses [23] and to avoid conditioning on the future, an intellectual disability status was treated as an age-dependent covariate such that people with intellectual disabilities contributed to the comparison cohort prior to their first diagnosis. Health needs were also treated as age dependent, and individuals contributed to both the presence and absence of health need at different ages if they were diagnosed with a new health need during the observation period. The date of exit was defined as: the date of the last CPRD update (29 September 2019); the date of death; the date of the end of the calendar period; the date of the last practice update or the date of transfer out of practice, whichever was first. The cohort was also sub-divided into individuals without any health needs at baseline or follow-up to assess whether life expectancy was similar between people with and without intellectual disabilities (i.e., excess mortality could be explained by the health needs).

The methodology for the life expectancy work used in this study has been described in detail elsewhere [24]. Life expectancy and 95% confidence intervals (CIs) were compared for people with and without intellectual disabilities and by the presence/absence of each health need using flexible parametric models with intellectual disability and health need status treated as age-varying covariates (and an interaction term fitted). Knots were placed according to the event distribution in the intellectual disability group for greater statistical precision. All models used 5 knots (including the boundary knots; 4 degrees of freedom (df); 3df for age-varying effects) with the exception of PEG feeding, which used 4 knots (3df; 2df for age-varying effects) owing to the small sample size.

#### **3. Results**

#### *3.1. Baseline Characteristics*

Table 1 shows the characteristics of the study population over the observation period. The characteristics of the population with each individual health need are shown in Supplementary Table S3. In comparison to the rest of the population, people with intellectual disabilities were generally younger (median age 33 vs. 43 years) and more were male (57.1% vs. 49.0%). There were also more white individuals (77.0% vs. 67.5%), although this partly reflects more complete recording of ethnicity in hospital settings (only 14.0% vs. 19.6% had missing data because more people with LD were hospitalised and had their ethnicity recorded). Most individuals (73.4%) with intellectual disabilities had no cause identified: the most common genetic/chromosomal condition reported was Down syndrome (10.9% of the individuals). People with intellectual disabilities had a substantially higher proportion of all of the health needs under investigation compared to those without intellectual disabilities, as is reflected in the greater proportion without any health needs at baseline and follow-up (53.6% vs. 90.3%; intellectual disability vs. no intellectual disability).

The largest differences between people with and without intellectual disabilities were observed for cerebral palsy, which was ≈58 times more prevalent during the 2.7-year observation window (i.e., at baseline or follow-up). Epilepsy, severe visual loss, severe mobility difficulties and PEG feeding were ≈12–22 times more prevalent; and incontinence and severe health impairment were ≈2–4 times more prevalent. The most common severe health need in people with intellectual disabilities was epilepsy, which was present in 18.7% of the individuals at baseline. For people without intellectual disabilities, incontinence was the most common health need, present in 3.8% of the individuals at baseline.

**Table 1.** Baseline and follow-up characteristics of the study population by intellectual disability and health need status.


<sup>1</sup> *n* = 440 individuals moved from no intellectual disability to intellectual disability sample at first diagnosis during observation window. <sup>2</sup> *n* = 831 (10.7%) with phenylketonuria (not defined as a specific syndrome for this study). <sup>3</sup> PEG: percutaneous endoscopic gastrostomy.

#### *3.2. Life Expectancy*

Figure 1a–g shows the life expectancy estimates and percentage of life years lost (compared with the general population without health needs), for the severe health needs under investigation, by presence/absence of the health need and intellectual disability status. The final figure (Figure 1h) shows the life expectancy estimates for people without

any of the health needs under investigation. Table 2 also presents the exact life expectancy estimates (with 95% CI) at 10, 20 and 40 years old.

**Figure 1.** (**a**–**h**) Life expectancy from 10 years of age by presence/absence of intellectual disability and health needs.

Perhaps the most striking finding from the figures is that life expectancy was substantially higher across the board in people with neither intellectual disabilities nor specified health need. At 10 years of age, these individuals could expect to live between 72.2 (absence

of severe health impairment) and 74.3 additional years (all of the health needs absent). At the same age, children with intellectual disabilities but without each specified health need lost ≈15–22% of life years compared to this first group, living, on average, an additional 57–62 years. Those with intellectual disabilities but without any of the health needs under investigation needs lost ≈12% of life years, living on average 8.9 years shorter than those with neither intellectual disabilities nor health needs.

We can see that the most severe of the health needs, regardless of intellectual disability status, were PEG feeding and severe mobility difficulties. Ten-year-old children with a PEG feeding tube could expect to live only an additional 23.0 years (95% CI 17.1–31.0) if they had intellectual disabilities and 25.7 years (95% CI 18.3–36.0) if they did not have intellectual disabilities, representing a loss in life years of ≈65–68% compared to those with neither condition. Similarly, children with severe mobility difficulties lost ≈41–44% of life years, living an additional 41–43 years only compared to the almost 73 years in those with neither condition. The disadvantages for individuals with PEG feeding tubes and severe mobility difficulties continued to be observed in adulthood (Table 2).

Of the remaining health needs, people with epilepsy had shorter life expectancy overall. Confidence overlapped at 10 years but, subsequently, having intellectual disability in addition to epilepsy incurred additional life expectancy disadvantages (see Table 2), with a loss in life years of ≈38%. Severe visual loss or incontinence was about equivalent to having intellectual disabilities without the health need in terms of life expectancy, but people with both intellectual disabilities and incontinence were again further disadvantaged, with a loss in life years of ≈34%. Conversely, we did not find an effect of severe hearing impairment on life expectancy. The effect of cerebral palsy on life expectancy was harder to determine, owing to small numbers, but those with cerebral palsy and intellectual disabilities had the shortest life expectancy compared with the those without cerebral palsy or with cerebral palsy but without intellectual disabilities, with a loss in life years of ≈43%. All of these findings were relatively consistent across the age range (Table 2).


**Table 2.** Additional years expected to live at age 10, 20 and 40 years by individual health need status and absence of health needs.


**Table 2.** *Cont*.

<sup>1</sup> Percentage of life years lost compared with people with neither intellectual disability nor the specified health need. <sup>2</sup> PEG: Percutaneous endoscopic gastrostomy.

#### **4. Discussion**

This work deepens our understanding of health inequalities in people with intellectual disabilities. By reaffirming that severe health needs make a significant contribution to the mortality disparities that people with intellectual disabilities are known to experience, our findings also reveal that they only partially explain these. After restricting the study population to those without health needs, life expectancy remained shorter for those with intellectual disabilities, with a loss in life years of 12%. Of those with the specified health needs, life expectancy was generally further shortened if intellectual disability was also present, suggesting combined disadvantages.

#### *4.1. Strengths and Limitations*

To the best of our knowledge, this is the first time that life expectancy has been explored by health needs in people with and without intellectual disabilities. The utilisation of flexible parametric methods to estimate life expectancy is also a novel component and supports previous methodological findings that borrowing strength from larger covariate samples can be an effective way of increasing statistical precision for small samples [24]. However, we recognise that life expectancy is only a crude measure of health inequalities that does not encapsulate other social determinants of health, such as deprivation, or factors that may contribute towards inequalities, such as access to and quality of healthcare provision. We are also unable to comment on other equally important health indicators, including quality of life and well-being.

As with all electronic health record data of this nature which rely on Read code and ICD diagnoses, we are unable to capture variability in the severity of health needs between people with intellectual disabilities and the general population. A particular concern is incontinence, which is likely to be less severe in the general population if it occurred and was resolved during certain life events, such as post-pregnancy [25]; it is noteworthy that almost three-quarters (73.3%) of the people in the general population with incontinence were female, compared with only half (53.2%) in the intellectual disability population (Supplementary Table S3). Moreover, both incontinence and PEG feeding may be indicative of additional comorbidities (e.g., frailty or dysphagia) rather than directly causing mortality [26,27]. Our findings nonetheless support their relationship (even if indirect) with life expectancy. Another limitation of GP health record data is that they do not provide complete information on the severity of intellectual disabilities; we are also likely to have missed people with mild intellectual disabilities who do not have significant support needs and may also be more vulnerable to abuse, discrimination and high-risk behaviours. We also recognise that many of these health needs co-occur and that they are more likely to do so if the individual also has intellectual disabilities, as is reflected in the larger proportion of individuals with at least one health need (46% vs. 10%) and high prevalence of co-occurring health needs, particularly for individuals with cerebral palsy (53% of individuals with intellectual disabilities also had epilepsy; 56% had severe mobility difficulties) and PEG feeding tubes (55% had cerebral palsy; 65% epilepsy and 70% severe mobility difficulties) (Table S3). This descriptive study does not look in more depth at the co-occurring health needs, nor does it adjust for additional clinically relevant comorbidities, such as dementia, or other social determinants of health which all contribute to the mortality disadvantages that people with intellectual disabilities experience [28]. Such issues could be explored further using propensity score methodologies or multiple logistic regression/time-to-event analyses, which are recommended to further develop the work described here.

This study took place before the COVID-19 pandemic, during which people with intellectual disabilities have been adversely affected owing to increased risk of transmission (e.g., through residential homes and community-based support) and increased risk of respiratory deaths [29–31]. People with severe health needs have also been disproportionately affected by COVID-19 [32]. In the current climate, the recommendations made here are, therefore, likely to be more relevant.

#### *4.2. Comparison with Existing Literature*

The prevalence of severe health needs found at baseline in this study is largely similar to that found in previous research carried out in the UK and internationally. The prevalence of epilepsy was 18.7% (vs. 1.1% in the general population), which corresponds with previous population-based studies from England (18.5% vs. 0.7% (matched age/gender/practice population sample) [19]) and Scotland (18.8% vs. 0.8% [10]). The prevalence of incontinence in the intellectual disability population (13.3%) was lower than previous UK estimates using the CPRD (20.5% [19]), which we attribute to the exclusion of 'H/O incontinence' and incontinence diagnoses within 10 years of cohort entry for the current study. The baseline prevalence of 3.8% found in the general population is at the lower end of the estimates of international figures of 3–18% for severe incontinence (urinary only) in adult women (about half of this for men) [33], given that many do not seek support from a healthcare provider [34]. The prevalence of PEG feeding (1.9% vs. 0.1%) also falls within the 5-year incidence rate (1.3%) of PEG procedures in England based on 17,000 per year [35].

In our study, prevalence of severe visual impairment among people with intellectual disabilities (13.0%) was lower than previous estimates in the Netherlands for visual impairment and blindness (13.8% and 5.0%, respectively) but, of the latter population, 40.6% were undiagnosed prior to study commencement [36]. We did not find a relationship between severe hearing impairment and life expectancy, which differs from previous (albeit not statistically significant) work in the general population [37].

The prevalence of cerebral palsy we reported here (8.4% vs. 0.1%) can be interpreted using information from the random general population sample. Given that this sample was drawn from 6.2 million individuals (Supplementary Figure S1) and that 0.5% of the general population sample had intellectual disabilities, and assuming a representative random sample draw, the prevalence of cerebral palsy in our study was approximately 1.42 per 1000 population, which is similar to birth estimates reported of 2.11 per 1000 population [38] conditional on surviving to 10 years. We would also expect there to be 2276 (i.e., 6.2 times as many) people with cerebral palsy in the entire population sample, which would equate to 29% of people with cerebral palsy having intellectual disabilities. This is within the range reported in the literature, which cites 22–40% of individuals with cerebral palsy having cognitive impairment (IQ < 70) [39], although some studies report figures closer to onehalf [40]. It is worth emphasising, however, that many—if not most—people with cerebral palsy do not have intellectual disabilities and it is important to make sure that their needs are adequately met. The prevalence of severe mobility difficulties (10.5%) in people with intellectual disabilities is similar to previous estimates of 9.2% for being 'non-mobile' [41], but it is hard to determine the prevalence in the general population owing to the recognised variation in thresholds for reporting mobility disabilities [42].

#### *4.3. Recommendations*

Given that this descriptive study did not seek to control for other contributing factors, we are nonetheless able to make some broad recommendations. First, it is clear from our findings that health needs are a significant problem for people with intellectual disabilities and that, with the exception of severe hearing impairments, they play a key role in shortening life expectancy. More effective management and treatment of these health needs, including regular assessment of associated care requirements, have the potential to improve outcomes and quality of life for those affected. Many of these health needs are relatively rare in the general population, so the development of tailored care pathways for people with intellectual disabilities, based on national guidelines and policies where available, is likely to be a priority. Such pathways may include monitoring medication (e.g., epilepsy—with a focus on epilepsy syndromes and tuberous sclerosis), provision of specialist support (e.g., visual impairment and hearing impairment), communication plans (e.g., cerebral palsy), pain management (e.g., severe mobility difficulties), prevention strategies (e.g., incontinence) and oral care (e.g., PEG feeding). All pathways should include mechanisms for the provision of coordinated care between health, social care and voluntary services so that unnecessary burden is not placed on carers. They should also be adequately flexible to allow for individuals' differences and needs.

#### **5. Conclusions**

We conclude that differential life expectancy in people living with intellectual disabilities compared to the general population is not wholly attributable to increased prevalence of severe health needs. Our findings highlight the need to continue to find ways to improve health outcomes and quality of life for people living with intellectual disabilities so that they can be supported to lead long and fulfilling lives.

**Supplementary Materials:** The following supplementary information can be downloaded at https: //www.mdpi.com/article/10.3390/ijerph19116602/s1, Table S1: RECORD checklist; Table S2: Diagnostic and classification codes for intellectual disabilities, ethnicity and severe health needs investigated; Figure S1: Data flow diagram of individuals included in the study population from original extracted data; Table S3: Characteristics of individuals with specific health needs under investigation.

**Author Contributions:** Conceptualisation, F.T. and M.J.R.; data curation, F.T. and M.J.R.; methodology, F.T., M.J.R., R.M., R.K. and S.K.G.; validation, M.J.R.; formal analysis, F.T.; investigation, F.T., M.J.R., R.M., R.K., H.K. and S.K.G.; resources, F.T. and M.J.R.; writing—original draft preparation, F.T.; writing—review and editing, F.T., M.J.R., R.M., R.K., H.K. and S.K.G.; visualisation, F.T. and M.J.R.; supervision, M.J.R. and R.M.; project administration, F.T. and M.J.R.; funding acquisition, F.T. and M.J.R. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded from a Baily Thomas Doctoral Fellowship award (TRUST/VC/AC/ SG/5366-8393). The funders had no role in study design, data collection and analysis, the decision to publish or the preparation of the manuscript. The study is based in part on data from the CPRD GOLD database obtained under licence from the UK Medicines and Healthcare products Regulatory Agency. The provision of CPRD and linked data was through Leicester Real World Evidence (LRWE)

Unit, which is funded by University of Leicester, National Institute for Health Research (NIHR) Applied Research Collaboration (ARC) East Midlands and Leicester NIHR Biomedical Research Centre. The interpretation and conclusions contained in this article are those of the authors alone and not necessarily those of the LRWE Unit, the NHS, the NIHR or the Department of Health and Social Care.

**Institutional Review Board Statement:** The CPRD has Health Research Authority (HRA) approval for all studies using anonymised data for observational research (East Midlands Research Ethics Committee [REC] No. 05/MRE04/87). Research using the CPRD is also subject to regulatory approval from the UK Medicines and Healthcare products Regulatory Agency (MHRA) Independent Scientific Advisory Committee (ISAC); the approved protocol reference no. for this study is: 19/267RA3.

**Informed Consent Statement:** The CPRD has Health Research Authority (HRA) approval for all studies using anonymised data for observational research (East Midlands Research Ethics Committee [REC] No. 05/MRE04/87). Consent was not obtained for the use of anonymised data—approval for the use of the CPRD (data controller) was through the UK MHRA Independent Scientific Advisory Committee (ISAC) (approved protocol no. 19/267RA3).

**Data Availability Statement:** Data for this study were obtained from the Clinical Practice Research Datalink (CPRD), provided by the UK MRHA. The authors' licence for using these data does not allow sharing of raw data with third parties. Information about access to CPRD data is available here: https://www.cprd.com/research-applications (accessed on 20 May 2022). Researchers should contact the ISAC Secretariat at isac@cprd.com for further details.

**Acknowledgments:** The authors gratefully acknowledge support from people with intellectual disabilities and their family carers for relating their own health-related experiences, health needs and support that they received with their health and social care. In particular, we would like to thank: the Talk & Listen group (Leicester, UK), ably facilitated by Pauline Ndigirwa; the Charnwood Action Group (Leicestershire, UK); Gill Huddleston (Carers' UK); Sarah Stanyer; Amy Stanway and Kate Dolan.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


## *Review* **The Association between Physical Environment and Externalising Problems in Typically Developing and Neurodiverse Children and Young People: A Narrative Review**

**Alister Baird 1,\*, Bridget Candy 1, Eirini Flouri 2, Nick Tyler <sup>3</sup> and Angela Hassiotis <sup>1</sup>**


**Abstract:** The physical environment is of critical importance to child development. Understanding how exposure to physical environmental domains such as greenspace, urbanicity, air pollution or noise affects aggressive behaviours in typical and neurodiverse children is of particular importance given the significant long-term impact of those problems. In this narrative review, we investigated the evidence for domains of the physical environment that may ameliorate or contribute to the display of aggressive behaviours. We have considered a broad range of study designs that include typically developing and neurodiverse children and young people aged 0–18 years. We used the GRADE system to appraise the evidence. Searches were performed in eight databases in July 2020 and updated in June 2022. Additional articles were further identified by hand-searching reference lists of included papers. The protocol for the review was preregistered with PROSPERO. Results: We retrieved 7174 studies of which 67 are included in this review. The studies reported on green space, environmental noise and music, air pollution, meteorological effects, spatial density, urban or rural setting, and interior home elements (e.g., damp/sensory aspects/colour). They all used well validated parent and child reported measures of aggressive behaviour. Most of the studies were rated as having low or unclear risk of bias. As expected, noise, air pollution, urbanicity, spatial density, colour and humidity appeared to increase the display of aggressive behaviours. There was a dearth of studies on the role of the physical environment in neurodiverse children. The studies were heterogeneous and measured a range of aggressive behaviours from symptoms to full syndromes. Greenspace exposure was the most common domain studied but certainty of evidence for the association between environmental exposures and aggression problems in the child or young person was low across all domains. We found a large knowledge gap in the literature concerning neurodiverse children, which suggests that future studies should focus on these children, who are also more likely to experience adverse early life experiences including living in more deprived environments as well as being highly vulnerable to the onset of mental ill health. Such research should also aim to dis-aggregate the underlying aetiological mechanisms for environmental influences on aggression, the results of which may point to pathways for public health interventions and policy development to address inequities that can be relevant to ill health in neurodiverse young people.

**Keywords:** physical environment; conduct disorders; intellectual disabilities; aggression; review

#### **1. Introduction**

The physical environment encompasses all aspects of a child's physical world and may be defined as objective characteristics of the physical context in which children spend

**Citation:** Baird, A.; Candy, B.; Flouri, E.; Tyler, N.; Hassiotis, A. The Association between Physical Environment and Externalising Problems in Typically Developing and Neurodiverse Children and Young People: A Narrative Review. *Int. J. Environ. Res. Public Health* **2023**, *20*, 2549. https://doi.org/10.3390/ ijerph20032549

Academic Editor: Shoumitro Deb

Received: 21 November 2022 Revised: 28 January 2023 Accepted: 28 January 2023 Published: 31 January 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

13

their time (e.g., home, neighbourhood, school). The influence of children's physical exposures has been summarised differentially by various models, theorems, and theorists over the previous century. Notably, these include the physical environmental elements of children's exposome (a term introduced by Wild [1,2] regarding the non-genetic influences on outcomes across the lifespan) and Bronfenbrenner's bioecological model [3–5], proposing that children develop within an environmental milieu of five interconnected systems, spanning aspects from urban design (e.g., presence and structure of sidewalks), traffic density, and design of venues for physical activity (e.g., playgrounds, parks, and school yards), to biologically active chemicals, radiation, the internal chemical environment, and psychosocial aspects [6]. The difficulty with these conceptualisations of child development is that they include both physical environmental and (psycho)social influences. As exemplified in a review of the influence of interior hospital environmental interior conditions, Harris [7] segmented the environment into distinct physical exposure categories: ambient, architectural, and interior design.

In this work, an operationalised definition of "physical environment" was incorporated to identify eligible environmental exposures. This classification was derived from a coalescence of Harris's [7], Bronfenbrenner's [3–5] and Wild's [1,2] theorems. This resulted in the inclusion of a diverse array of domains, from ambient exposures (sunlight, sound, meteorology), interior design elements (colour, lighting), architectural features (space/spatial crowding), and biological active agents (i.e., air particulate pollutants), to physical aspects of children's microsystem (i.e., home, school, and neighbourhood characteristics).

A variety of theories have attempted to explain the mechanisms via which environmental domains influence physical and mental health. Although none of these mechanistic models have been fully proven, there are suggestions that positive effects may be the end product of pathways that link several elements, such as mitigation (reduction in air pollution or traffic noise), restoration (stress reduction and attention restoration in alignment with what the Attention Restoration Theory posits) and instoration, whereby attributes of the physical environment, such as greenness in particular, may promote physical activity and social capital and cohesion [8–10].

Previous theories have primarily focused on the stress-reducing effects of greenspace, either via a protective influence from harmful environmental stimuli (noise and air pollution) [11–13], or via the restoration of attentional resources [14,15]. Recently, it has been posited that greenspaces may provide more direct physiological benefits via increased exposure to phytoncides (plant-derived antimicrobial volatile organic compounds) [16]. Whilst preliminary research into the effects of phytoncide exposure is positive, it is currently inconclusive and additional studies are required [17]. Neuroimaging studies are also shedding insight into potential mechanisms for greenspace exposures potential mechanisms, with one study [18] showing that it can beneficially deactivate the prefrontal cortex in regions linked to depression and rumination.

The literature also indicates that aspects such as ambient air particulate matter exposure may negatively impact development via neuroinflammatory pathways [19–24]. Noise pollution may also have detrimental effects via contributions to subjective annoyance and irritation; whilst not necessarily directly causing aggression, noise exposure in those with low threshold for expressing anger may increase its severity [25,26] via draining of attentional and cognitive resources and subsequently leading to increased self-regulatory difficulties [27]. Social-behavioural mechanisms may explain the relationship between behaviour and fluctuations in meteorological effects (such as temperature), e.g., the routine activity theory that proposes that warmer temperatures facilitate more frequent social interaction, increasing opportunity for aggression [28] or that heat increases hostility and physiological arousal and consequently to aggressive behaviour [29]. Theories have posited that high spatial density triggers perceptions of crowding and a subsequent physiological stress arousal response [30–32]. Why proximity elicits these responses is still unclear and has been linked to competition for resources and invasion of personal space [33]. Baird et al. [34] reported a beneficial association between household crowding and reduced

conduct problems in children with intellectual disabilities. The authors propose several theories about these potentially counterintuitive findings, suggesting that increased availability of and proximity to family members, in intergenerational households, and parental habituation to problematic conduct behaviours are all potential mechanisms underpinning this finding. Using a sensory room unaccompanied may be associated with a sense of autonomy in children and young people which in turn reduces distress [35]. Other pathways may contribute to the impact that music listening has on a broad range of psychological and physiological benefits [36–41].

As discussed, social-behavioural mechanisms may explain the relationship between aggression and climate effects, for example the routine activity theory proposes that warmer temperatures facilitate more frequent social interaction, increasing opportunity for aggression [28]. Alternatively, the general aggression model (GAM) is more grounded in a physiological aetiology of aggression, suggesting that heat increases hostility and physiological arousal and consequently aggressive behaviours [29].

From the evidence presented so far, it appears that both physical and social environments, in addition to genetic and epigenetic influences, shape the developmental trajectories of children [42–46]. However, in the main, published research is focused on typically developing rather than neurodiverse children [47]. Previous work has evidenced disproportionate influence of children's early environmental milieu in shaping a range of socio-emotional and cognitive developmental outcomes. Specifically, learning disabled children are more likely to be affected by social adversity, poor housing, and poverty [48]. These children are also exponentially more likely to be exposed to negative environmental exposures such as air pollution [49]. To address failings in supporting these children and their families, an important element is to reduce socioeconomic inequality and improve residential conditions [50]. Furthermore, children with complex neurodisabilities have increased barriers to accessing potentially therapeutic aspects of both the physical and social early environments [51]. Disabled child access to urban greenspaces, for example, is not only infrequent in comparison to their typically developing peers [52], but when significant resources are employed to facilitate access for neurodisabled children, the high-risk nature of visiting these spaces requires rigid structure, impacting on the quality of nature experiences when they do occur [53]. This is one example of the health inequities and disparities experienced by neurodiverse children in comparison to their peers, exemplifying the need for additional research in these domains.

Externalising disorders are characterised by display of a range of behaviours which are associated with poor impulse-control, and include rule breaking, impulsivity, and inattention; in addition, a core component of these conditions is the presence of heightened aggression.

Specific child and adolescent externalising disorders include conduct disorder (CD), oppositional defiant disorder (ODD), and attention- deficit-hyperactivity disorder (ADHD). Of particular concern is this repeated presence of aggressive behaviour in these disorders as it is often associated with referral to services and application of a range of restrictive practices, most commonly antipsychotic medications but also inpatient admissions.

Aggressive behaviours and general behavioural problems such as destructive behaviours have an overall negative influence on carers due to stress and negative interactions between carers and the person they care for, likely resulting in a deterioration of the quality of care [54]. Moreover, behavioural problems are associated with increased service costs because of the impact of behaviours on staff and need for high support levels [55]. Aggressive episodes also provoke concerns about threat to personal safety as well as cause panic and upset [56,57].

These behaviours in both typically developing and neurodiverse children compound societal and educational limitations [58–61]. They reduce life satisfaction via degradation of social and familial relationships [62], increase economic costs [63], require higher use of physical restraints [64] and restrictive environmental placements [65,66], limit access to support services [67], impair caregiver functioning [68,69], reduce educational opportunities due to teacher burnout [70] and encourage use of restrictive practices including psychotropic medication use [71,72].

Neurodevelopmental disorders (NDDs) are a category of "etiologically diverse conditions" with onset during the developmental period and are characterised by below average intellectual functioning and adaptive behaviour [73]. This classification includes disorders such as intellectual disability (also called learning disability in the UK), autism spectrum disorders (ASD), and other developmental delays (DD). Whilst we appreciate the nuances of the definitions for brevity and clarity, we will refer to those children with NDDs as neurodiversity in this context.

About one in one hundred individuals has a neurodevelopmental disorder and there are about 351,000 children with intellectual disability in the UK, often coexisting with other neurodevelopmental disorders [74]. Prevalence of aggressive behaviours in NDDs appears to fluctuate depending on sampling methods and assessment strategies, ranging from 8.3% in community samples [75] to 64% in inpatient care [76,77]. Children with intellectual disability were six times more likely to have conduct disorder measured by the Strengths and Difficulties Questionnaire compared to their typically developing peers [78]. Aggressive behaviours are persistent over time [79], with displays of aggression being consistently linked with neurodiversity [57,80–85] though prevalence rates reported can be inconsistent.

Whilst previous research has examined predictors of broadly defined challenging behaviour in children with intellectual disability [86–88], none of the studies has included examination of the influence of the physical environment specifically on such behaviours to date. Here, we build on previous work examining the influence of single domains of the physical environment on aggressive behaviour of typically developing and neurodiverse children by including (1) children across the spectrum of ability and (2) all available objective domains of the physical environment.

Therefore, in this narrative review, we examine the certainty of evidence of the impact of the physical environment on typically developing and neurodiverse children's aggressive behaviours. The outcome of interest was either psychological or biological proxies of aggressive behaviour, annoyance and irritability measured by validated psychometric questionnaires (measures or outcomes which have been empirically evaluated for reliability) or biological markers such as blood pressure, heart rate and skin conductance. The findings are presented by environmental domain (Greenspace, noise pollution, air pollution, meteorology, spatial density, rurality of residence, interior design, and music) and separately for typically developing and neurodiverse children.

#### **2. Materials and Methods**

#### *2.1. Search Strategy*

We adhered to the Preferred Reporting Items of Systematic reviews and Meta-analyses (PRISMA) statement checklist [89] in conducting the review, as well as guidance from the Synthesis Without Meta-analysis [90], and the Meta-analysis of Observational Studies in Epidemiology [91] to improve the precision of our reporting. The study protocol was preregistered on PROSPERO (CRD42020160251). Because of the heterogeneity in outcome used and the variation in exposure measures, we were unable to perform a meta-analysis. Instead, we reported the degree of certainty of the evidence available in terms of protective/detrimental, inconclusivity, or no association for each outcome and exposure metric across each domain of the physical environment.

The electronic search strategy comprised 8 bibliographic databases (MEDLINE, Psych-INFO, Web of Science, CHINAHLplus, Embase, Cochrane library, EThOS and ProQeust dissertations and theses) and two grey literature sources (NICE evidence search and Google scholar). The inclusion of the latter sources facilitated the retrieval of additional studies from a more diverse range of sources (including policy and public health), whilst mitigating publication bias and increasing the comprehensiveness of the review [92,93]. The search was carried out in July 2020, and replicated in the update to June 2022 with no year of publication limit. Bibliographies of retrieved articles were searched to maximise retrieval of relevant articles. The search strategy was overseen by a specialist librarian (see Supplementary Materials).

#### *2.2. Selection Criteria*

Studies were included if they (a) reported primary research, (b) were written in English, French, German, Mandarin Chinese and Spanish which were languages spoken by fellow researchers and therefore could be translated, (c) included human participants aged between 0–18 years, (d) contained a psychometrically valid parent or child reported outcome measure of aggressive behaviours or physiological measures of arousal (identified as a proxy measure of aggressive behaviour) and (e) examined exposure to domains of the physical environment.

#### *2.3. Screening and Appraisal Process*

All retrieved articles were screened by the first author (A.B.). A sub-sample of titles and abstracts (10%) were co-screened by a senior researcher (A.H.) and a post-doctoral researcher (R.R.). Inter-rater reliability for this initial screening was 87% (0.868). Full text data extraction was conducted by the main author (A.B.) using a modified flexible data extraction template used for non-Cochrane reviews [94] with co-screening conducted for a proportion of studies (59%) by independent researchers (see acknowledgments). Substantial agreement between the primary author and co-screeners was reported (83%, κ = 0.6126) with disagreements resolved by the senior researcher (A.H.) who also crosschecked the extraction table for any inconsistencies.

Risk of bias assessment (RoB) and GRADE protocol were adapted from a systematic review by Clark, Crumpler, and Notley [95] on the evidence relating to effects of environmental noise pollution on mental and physical health outcomes. Four items from this review were used to assess the bias for each paper:


One measure of RoB that was not included in this review was "due to blinding to exposure outcome" as it was not considered appropriate for the methodology of the majority of the retrieved studies which infrequently blind outcome assessors. Overall RoB ratings for each study were aggregates of high, low or unclear across the four domains. We adopted a conservative rating strategy where studies that had equal reports of low and high risk of bias were classified as high.

The GRADE system [96] is a widely used tool recommended by The Cochrane collaboration [97] which provides a ranking of quality for evidence on interventions and relevant outcomes. The modified GRADE approach assigns a priori the highest quality of evidence to longitudinal or intervention studies, and the lowest to cross-sectional studies, subsequently up- or down-grading evidence dependent upon various methodological factors such as RoB, studies not comparing the same variables, inconsistency of findings

between studies, imprecision (effect estimate confidence interval containing 25% harm or benefit), publication bias of funnel plot reported, and other considerations (large effect RR > 2, adjustment for all plausible confounding, dose response gradient). As we did not carry out a meta-analysis assessment of GRADE criteria such as precision or publication bias was not possible.

#### *2.4. Measures of Environmental Exposure*


#### *2.5. Measures of Aggressive Behaviours*

The studies utilised a number of psychometrically valid parent and child reported measures of aggressive behaviour, as well as observer ratings. These comprised the full instrument or conduct, aggression, and externalising behaviour domains as follows:


#### **3. Results**

The two searches retrieved 7434 records. After deduplication, 7174 were screened of which 257 underwent full-text assessment, resulting in the inclusion of 67 papers (details are shown in the PRISMA flow diagram, Figure 1). Six of which reported on the physical environment and aggressive behaviours in neurodiverse participants.

We report RoB separately for studies carried out with typically developing (Table 1) and neurodiverse populations (Table 2). We follow the same format for the GRADE evidence summaries for the environmental exposures on outcomes of aggressive behaviours for typically developing and neurodiverse children (Tables 3 and 4).

**Figure 1.** PRISMA flow diagram of the included studies.


environmental



**Table 1.** *Cont.*



**Table 1.** *Cont.*


**Table 1.** *Cont.*


**Table**

**1.**

*Cont.*


was reported.



**Table 3.** GRADE summary of quality of evidence for typically developing

children.


8 Downgraded due to inability to assess consistency.


**Table 3.** *Cont.*





g Baird et al., 2022 [34]: Parent-reported Strengths and Difficulties Questionnaire (SDQ) conduct problems subscale scores [98]).

7 Downgraded due to inability to assess consistency.

#### *3.1. Typically Developing Children*

#### 3.1.1. Greenspace

Eleven longitudinal and seven cross-sectional studies (~46,684 participants) examined associations between greenspace exposure and childhood aggression [34,106–122]. Five studies were carried out in the UK, four in the USA, two in Belgium, with the remaining in Australia, Korea, Lithuania, Germany, Spain and China. All greenspace studies were classified as low RoB.

Inconsistent evidence for harms or benefits was reported across eight studies [106–109,112,113,117,121] that examined associations between satellite derived neighbourhood greenspace (NDVI) and parental-reported child aggression related outcomes. Two studies [101,109] examining the association between parental-reported child aggression and conduct problems and percentage of land designated as natural land, reported high-quality evidence. Proximity of the child's residence to greenspace was inconsistently associated with parent reported conduct problems across three studies [106,108,114]. Very low-quality evidence [111,116,120] reported no relationship between percentage of neighbourhood greenspace and both child and parent-reported conduct problems. Moderatequality evidence from three studies [34,111,120] reported inconsistent beneficial effects of access to private garden space on parent-reported conduct problems.

#### 3.1.2. Environmental Sound and Noise

Three longitudinal and eight cross-sectional studies (*n* = 23,665) assessed the association between environmental noise pollution including road traffic, construction noise, aircraft noise and aggression outcomes [123–133]. These studies were primarily conducted in the UK, Spain, Germany, and the Netherlands, and one study in China. Three of these studies [124,131,132] used data from the multi-national RANCH study examining the influence of high and low road and aircraft noise on the behaviour of pupils who attended schools that were close to main roads or under flypaths. Two studies were judged to be of unclear RoB [126,130], with the majority being rated as low RoB. A very low-quality evidence for harmful association [130] between residential aircraft noise exposure and increased child annoyance was reported. Similarly, low- and very low-quality evidence was found for associations between increased residential noise [126], predicted air and road traffic noise [131], and heightened self-reported child annoyance. Schools located in areas of high aircraft noise were associated with increased child-reported annoyance [127–129], but inconsistently correlated with parent-reported child conduct problems ([127,129], both very low quality). Two studies [124,132] examining the role of residential aircraft noise on the parent-administered conduct problems subscale of the SDQ reported no association (low quality). Five studies [123–125,133,185] reported very low quality inconsistent evidence for estimated noise exposure effects on parent-reported child aggression.

Two studies (longitudinal and within-group repeated measures) from the USA (*n* = 658) assessed the association of music on childhood aggression [183,184]. Both studies were rated as high RoB. Aggressive or sexual music content was associated with increased self-reported aggressive behaviour in adolescents ([183], very low quality). Low-quality evidence reported no association between alternating periods of instrumental music and observer rated aggressive behaviours [184]).

#### 3.1.3. Air Pollution

Eight longitudinal and six cross-sectional studies from Lithuania, China, Korea, Iran, Canada, USE, and the UK (*n* = 45,607) explored the influence of air particulate matter on aggressive behavioural outcomes in typically developing children and young people [34,107,116,123,135,136,138,141,142,144–149]. One study was rated as high RoB [146], one as unclear RoB [136], and the remaining as low RoB.

Five studies [135,136,146,147] provided either low- or very low-quality evidence supporting the harmful influences of tobacco smoke exposure across various aggressive behavioural questionnaires. Very Low-quality evidence for a harmful association [132] between active or passive tobacco exposure and child self-reported anger and aggressive behaviour was found.

Three studies [116,141,149] examined the relationship between Nitrogen Dioxide (NO2) exposure and child self-reported conduct problems symptoms and reported inconsistent evidence for a harmful association (Very Low quality). No effect of Elemental Carbon Attributed to Traffic (ECAT) on parent-reported externalising behaviours (BASC-2) was found ([145], Moderate quality).

In addition, there was inconsistent evidence for an association between exposure to particulate matter less than 2.5 microns (PM2.5), and child self-reported conduct problems [141,149]. No effect was found in a study that examined the influence of PM2.5 on parent reported conduct problem scores [107]. Another study by Loftus et al., 2020 [144] explored the influence of exposure to particulate matter less than 10 microns (PM10) on parent reported child aggressive behaviours but it did not show a significant association (Very Low quality). Ambient air lead exposure (PbA)) was associated with high parent-reported aggressive behaviour ([148], Very Low quality).

#### 3.1.4. Meteorological Exposure

Five longitudinal and two cross-sectional studies (approximately = 6314) from Chile, Canada, the Netherlands, USA, and Italy, assessed associations between meteorological variables and child aggression outcomes [151–159]. One study was rated as high RoB [158] with the remaining studies rated as low RoB.

The study by Muñoz-Reyes et al. [158] contrasted the frequency of observed aggressive behaviours during the warm season (summer/spring) with the frequency of such behaviours during the cold season (autumn/winter), reporting Very Low-quality evidence for harmful effect of warm seasonality. Low-quality evidence associated increased humidity with harmful increases in teacher-reported child aggressive behaviours [151,156]. Studies examining the effects of sunlight exposure on teacher reported [151,156] and child self-assessment [152] behavioural outcomes reported inconsistent or no evidence, respectively (very low quality). Low- and Moderate-quality evidence for the harmful influence of increased temperature on teacher and parent-reported child aggression symptoms was reported in three studies [151,156,159]. However, we found one Very Low-quality study that provided evidence for beneficial effect of temperature on children's self-reported anger [152]. Aggression during summer recess was lower compared with aggression during the school year ([154]; Low quality). No association between hours of precipitation per day and children's self-reported anger was found ([152], Very Low-quality evidence). Finally, a study carried out by Lochman et al. [153] examined longitudinal associations between tornado exposure and externalising symptoms, and reported a harmful associations of Moderate quality.

#### 3.1.5. Spatial Density and Interior Design

Four observational and two longitudinal studies [34,160–163,165] (*n* = 8568) from the USA and the UK examined spatial density and architectural design in relation to childhood aggression. RoB was judged as high in all studies except one rated as unclear [163] and one rated as low [34]. A study [165] reported a beneficial effect of increased playroom openness, but no effect of space per child or room group size on observed aggressive behaviours. Low-quality evidence assessing the association between high density (in comparison to low density) child playrooms and frequency of aggressive behaviours reported inconsistent results [160–162]. Moderate-quality evidence examining the effect of overcrowding in the home [34,163] reported inconsistent associations with parent-reported conduct problems but was associated with reduced teacher-reported externalising behaviours.

Three studies, two quasi-experimental and one longitudinal (*n* = 8257) conducted in Iran, the UK, and the USA examined the associations between interior design features and childhood aggression [34,179,181]. Low-quality evidence of association ([181] unclear RoB) between red painted classroom walls and increased self-reported aggression was found. In-patient psychiatric ward sensory room modifications were correlated with beneficial reductions in observer rated aggressive behaviour ([179] unclear RoB Moderate quality). Additionally, presence of damp in the house was associated with elevated trajectories of conduct problems in children ([34], Moderate quality).

#### 3.1.6. Urbanicity and Rurality

Three longitudinal and three cross-sectional studies (*n* = 17,630) from the USA, the Netherlands, and Thailand explored the influence of urbanicity and rurality of residence on children's aggressive behavioural outcomes [34,164,168,170,172,176]. One study was rated as high RoB [168] with the remaining assessed as low or moderate RoB. One study [176] reported inconsistent associations between the location of the participants and scores across three self-reported aggression outcomes (Very Low quality). Moderate-quality inconsistent evidence [34,172] was reported for the effect of urban residence on child conduct problems and aggressive behaviour in parent-reported questionnaires, whilst evidence for a lack of association was found for teacher-completed aggression outcomes [172]. Another study [170] examined the effects of urban or rural settings on aggressive behaviours in schoolchildren attending schools from either setting. It reported no association of setting with parentreported behaviours, but a harmful effect of urban school location on teacher-assessed behaviours (both Very Low quality). Very Low-quality evidence reported no association between children recruited from rural or urban Head Start centres and teacher-reported anger ratings ([168]: AML Behaviour Rating Scale). Neighbourhood urbanicity (mean number of addresses within a 1 km radius of participant's residence) was associated with increased teacher-reported child problem behaviours ([166] Low quality).

#### *3.2. Neurodiverse Children*

Six studies (*n* = 79,249) from the USA, Pakistan, the UK, and Australia included neurodiverse participants exclusively [34,188,190–193]. The studies are heterogenous utilising a variety of designs including longitudinal, cross-sectional, quasi-experimental, interventional, including two case studies. Two studies were judged to be of high RoB [190,192], one unclear [193] and the remaining three of low RoB.

Baird et al. [34] explored interaction effects between a sub-sample of children with intellectual disability (assessed via cognitive measures) from the Millennium Cohort Study (MCS) and various physical environmental exposures (neighbourhood greenspace: NDVI, access to a private garden, air pollution: NO2, urban or rural residence, household density, presence of damp. The authors reported no mediating influence of intellectual disability on the association between environmental exposures and children's conduct problem trajectories, except for household density (beneficial effect, moderate quality). Another study [188] reported no correlation between urban tree canopy coverage and frequency of aggressive behaviours in children with ASD but found an association between residing in lower urban tree canopy areas with increased parent-reported conduct problem severity. However, the evidence was deemed to be of low quality in both studies. The case study by Durand and Mapstone [190] examined the impact of fast and slow beat music on a child with intellectual disability, reporting reductions in observed frequency of aggressive behaviour during the fast beat condition and increases during the slow beat condition in comparison to a no-music baseline (Low quality). Additionally, a clinical trial of new age and classical music [191] provided Moderate-quality evidence for the beneficial effects of music on self-reported aggression in children with intellectual disabilities. A case study [192] assessing the impact of spatial proximity between an adolescent girl with intellectual disability and the therapist, provided a Very Low-quality evidence for a correlation between closer proximity and increased duration of observed aggressive behaviours. Finally, a study [193] examined the efficacy of modified sensory rooms in reducing distress in adolescent psychiatric inpatients, reporting additional benefits for individuals who had a history of aggression (Moderate quality).

#### **4. Discussion**

This is the first narrative review that updates previous literature across several environmental domains as well as including neurodiverse children, a previously under reported population in other reviews.

#### *4.1. Physical Environmental Domains*

#### 4.1.1. Greenspace

We found evidence that supports the therapeutic benefits of increased natural land and greenness surrounding child residences. Previous reviews have also shown associations between greenspace exposure and reductions in violent behaviours [194,195].

The greenspace evidence synthesised primarily supports the therapeutic influence of neighbourhood nature exposure on child aggressive behavioural outcomes. These effects, at least partially, were also present in NDDs populations. Whilst more epidemiological and experimental research paradigms are required to solidify the evidence for this therapeutic relationship and understand its underlying mechanistic pathways, we provide initial evidence for the role of nature in reducing aggression in neurotypical and diverse children. Initial attempts at establishing guidelines for integration and therapeutic adoption are beginning to be developed [196]. Studies examining socio-cultural barriers to children accessing urban greenspaces [197] are of crucial importance, but these findings need to be communicated to institutions and policy decision makers. We also recommend future experimental studies that aim to elucidate the underlying (neuro)mechanistic pathways via which nature exposure conveys these potential benefits. Advances in this regard would drastically redefine architectural and urban design for physical and mental health.

#### 4.1.2. Noise Pollution

Children appear to consistently self-report higher aggressive and annoyance related behaviours related to environmental noise, whereas parent reported outcomes either show a lack of association or inconsistent associations both for harm and benefit. This may suggest that noise exposure operates on pathways involving subjective annoyance and irritation which may not translate into objective longer-term increases in aggression problems. Additionally, although noise annoyance may not play a direct role in the aetiology of those problems, noise exposure of individuals who experience frustration or irritable mood has been shown to increase its severity [25,26]. Noise pollution, therefore, may not operate as a causal mechanism of aggression, but exacerbate pre-existing manifestation, potentially via draining of attentional and cognitive resources, leading to increased self-regulatory difficulties [27].

#### 4.1.3. Air Pollution

We found absent and inconsistent associations between ECAT, particulate matter less than PM2.5, particulate matter less than PM10 and NO2 exposure and childhood aggression problems. Tobacco smoke exposure showed a harmful association with aggressive behavioural outcomes irrespective of who was the outcome assessor. We also found this harmful association for childhood exposure to ambient air lead exposure (PbA). The lack of association of PM2.5 and PM10 with these behaviours is potentially anomalous when considering research that has linked air pollution with increased risk of mental health disorders [198]. The harmful effects of tobacco smoke and ambient lead exposure may increase the risk of neuropsychiatric disorders and violent crime, possibly via neuroinflammation [19–24].

Whilst none of the retrieved articles examined the effects of air pollution on neurodiverse children, it was shown that families of these children disproportionately reside in areas of higher particulate concentration than those of typically developing children [49], as well as exhibiting elevated rates of aggressive behaviour [199,200].

#### 4.1.4. Meteorological Effects

Summer seasonality, humidity, temperature, and previous tornado exposure were consistently correlated with increased childhood aggressive behaviours. We found little evidence for either harmful or beneficial effects of ambient temperature and seasonality. Previous studies suggest that humidity compounds the negative effects of heat on mental health [201], as well as being associated with increased emergency department visits for mental health problems [202]. Elevated temperature has also been associated with increased violent crime [203]; however, those associations warrant further examination.

#### 4.1.5. Spatial Density

The negative impact of high spatial density on aggression in young people [204] and inpatients in psychiatric wards has been highlighted previously [205–207]. Notwithstanding the beneficial effects of increased playroom openness, inconsistent influences for other spatial characteristics prevent a firm explanation of findings. Theories have posited that high spatial density triggers perceptions of crowding and a subsequent physiological stress arousal response [30–32]. Further studies on possible mechanistic pathways between high spatial density and aggression in children could lead to therapeutic adaptations in clinical and residential spaces [208].

#### 4.1.6. Urbanicity and Rurality of Residence

Due to the quality of retrieved evidence, we were unable to extricate any definitive conclusions for associations between urban or rural residence and childhood aggressive behaviours. This is potentially anomalous considering that children residing in rural areas are exposed to more greenspace which generally appears to have calming effects [209–214]. Rurality, however, is only one factor in a great number of confounders on childhood aggression. Furthermore, studies do not often use operationalised definitions of "rural" or "rurality" [215], potentially leading to heterogeneity in the underlying conceptual constructs being examined, limiting the replicability and specificity of results.

#### 4.1.7. Interior Design and Housing Quality

Previous work has associated damp problems with increased toxic mould, contributing to poor air quality [216] and/or potential neuroinflammatory and/or neurotoxic responses [20,22]. Damp in a house may also be associated with other adversities such as low socio-economic status and household disruption [217] exemplified by previous research linking poor household conditions to psychological distress [218].

Whilst preliminary evidence from this review supported the positive impact of modified sensory rooms to de-escalate aggression, it is very limited in scope. One study [35] suggested that the increased reduction in distress related to sensory deficits may be attributable to a sense of autonomy children and young people may gain by using the room unaccompanied.

#### 4.1.8. Music

We found preliminary evidence for the therapeutic potential of music in neurodiverse children which is similar with findings reported in adults [219]. Music listening has been associated with a broad range of psychological and physiological benefits [38–40]. Some [36,37] have stated that the therapeutic influences of music may operate mechanistically via enhancing emotional regulation, but such evidence is not yet available [41]. Music is a complex physical phenomenon, which requires additional targeted research to examine its effects on aggressive behaviours in typically developing and neurodiverse young people.

#### *4.2. Strengths and Limitations*

This review is comprehensive and has examined the evidence of a wide range of environmental exposures in relation to the display of aggressive behaviours in typical and neurodiverse children. To the best of our knowledge, this is the first review that comparatively examines available research on environmental determinants of aggression in these two groups. The review shows clearly the disproportionately sparse literature relating those children and the physical environment despite the fact that they are more likely to be affected by social adversity, poor housing, air pollutants, and poverty [48–50,220,221].

The incorporation of GRADE to assess the quality of evidence in this review may well be simultaneously both a strength and a limitation. Whilst it facilitated the examination of the certainty of included evidence, the adaptation of GRADE for use in a non-metaanalytic review including epidemiological studies, may, as highlighted previously [95], inadvertently result in downgrading of evidence irrespective of study quality. We also adopted a modified risk of bias protocol which may have impacted the RoB assessments of included studies. There may also have been potential conflicts of interest based on the source of funding which we did not consider in this review.

A final limitation of this evidence synthesis is the inclusion of studies that adopt a diverse range of heterogenous physical environmental exposures and metrics. As has been highlighted previously by experts in physical environmental epidemiological analysis on child socio-cognitive outcomes [116], further research is needed on improving environmental measures of aspects such as air pollution exposure, and access to and quality of children's greenspaces. Developing more holistic, accurate, and reliable measures of environmental exposures will facilitate novel research paradigms (computational, simulatory and experimental) that can elucidate the influences of these aspects, reciprocally informing direction for future research into (neurobiological)mechanistic pathways.

#### **5. Conclusions**

Physical environmental exposures sit at the intersection of social, biochemical, and (epi)genetic aetiological influences on the development and progression of a spectrum of physical and mental health outcomes. Further research can support stakeholders, ranging from city planners and environmental legislators to politicians and clinicians, in considering the role of the physical environment in the context of adverse impact on child (neuro)development. Whilst there is obvious need to further examine environmental and climate influences on mental health of all children, particular attention must be paid to neurodiverse children and their families. A recent report recommended that in order to pursue and achieve health parity for those children, we must "reduce poverty and improve living environments" [50]. Research focusing on that population will help to bridge the equity gap that has significant therapeutic and health implications for all citizens.

**Supplementary Materials:** The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/ijerph20032549/s1, Table S1: search strategy.

**Author Contributions:** Conceptualization: E.F., A.H., N.T. and A.B.; methodology, A.H., A.B. and B.C.; writing—original draft preparation, A.B.; writing—review and editing, N.T., B.C. and A.H. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** We thank Nancy Kouroupa, Steven Naughton, Laura Paulauskaite, Peiyao Tang and Rachel Royston for assisting in co-screening studies; Bori Vegh for support with preparation of the manuscript; Louise Marston, for guidance on study heterogeneity and narrative synthesis reporting; Deborah Marletta for assistance with the electronic database protocol development.

**Conflicts of Interest:** Multiple studies included in this review involved the authorship of Eirini Flouri. Flouri had no influence/involvement in the selection or appraisal of these studies. No other authors report any potential conflict of interest.

#### **References**


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## *Review* **Developmental Delays in Socio-Emotional Brain Functions in Persons with an Intellectual Disability: Impact on Treatment and Support**

**Tanja Sappok 1,\*, Angela Hassiotis 2,3, Marco Bertelli 4, Isabel Dziobek <sup>5</sup> and Paula Sterkenburg 6,7**


**Abstract:** Intellectual disability is a neurodevelopmental disorder with a related co-occurrence of mental health issues and challenging behaviors. In addition to purely cognitive functions, socio-emotional competencies may also be affected. In this paper, the lens of developmental social neuroscience is used to better understand the origins of mental disorders and challenging behaviors in people with an intellectual disability. The current concept of intelligence is broadened by socio-emotional brain functions. The emergence of these socio-emotional brain functions is linked to the formation of the respective neuronal networks located within the different parts of the limbic system. Thus, high order networks build on circuits that process more basic information. The socio-emotional skills can be assessed and complement the results of a standardized IQ-test. Disturbances of the brain cytoarchitecture and function that occur at a certain developmental period may increase the susceptibility to certain mental disorders. Insights into the current mental and socio-emotional functioning of a person may support clinicians in the calibration of treatment and support. Acknowledging the trajectories of the socio-emotional brain development may result in a more comprehensive understanding of behaviors and mental health in people with developmental delays and thus underpin supports for promotion of good mental health in this highly vulnerable population.

**Keywords:** developmental neuroscience; emotional functioning; intellectual disability; intervention mental health; limbic system; social brain network

#### **1. Introduction**

According to a nationwide US survey, one in six persons has a developmental disability, with most suffering from neurodevelopmental disorders, such as attention-deficit/hyperactivity disorder (ADHD) (9.5%), autism spectrum disorders (2.5%), learning disability (7.9%), or intellectual disability (1.2%) [1]. During the past decade, these prevalence rates have increased, e.g., from 1.1% to 2.5% for autism and from 0.9% to 1.2% for intellectual disability [1,2] as a result of better assessment and diagnosis. According to the WHO Global Health metrics, there are about 100 million people with an intellectual disability world-wide [3].

People with an intellectual disability are more vulnerable to physical or mental disorders [4–7]. According to the recent meta-analysis of Mazza [4], 33,6% suffer from a mental disorder, which is about double of the prevalence rates in the general population. In 2018,

**Citation:** Sappok, T.; Hassiotis, A.; Bertelli, M.; Dziobek, I.; Sterkenburg, P. Developmental Delays in Socio-Emotional Brain Functions in Persons with an Intellectual Disability: Impact on Treatment and Support. *Int. J. Environ. Res. Public Health* **2022**, *19*, 13109. https:// doi.org/10.3390/ijerph192013109

Academic Editor: Paul B. Tchounwou

Received: 8 September 2022 Accepted: 10 October 2022 Published: 12 October 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

one in three persons with a cognitive disability experienced more than 50% physically unhealthy days, and one in two persons reported more than 50% mentally unhealthy days [7]. Furthermore, approximately one in two persons with a cognitive disability slept less than 6 h a night, had experienced depression, and rated their health as fair to poor [7]. Especially these chronic and secondary health conditions decrease the life expectancy of persons with an intellectual disability by around 20 years compared to the general population [8,9]. Factors associated with death in people with an intellectual disability are mental and physical illnesses (e.g., cancer, heard, pulmonary and renal diseases) and physical disabilities such as cerebral palsy and epilepsy [10]. More than a third of those deaths are potentially amenable to healthcare interventions [11,12]. Due to the poorer management of chronic health conditions in primary healthcare, application of reasonable adjustments in services and awareness training have to be expanded to meet the needs of people with developmental disabilities [12].

People with an intellectual disability face various barriers to receiving adequate healthcare. Hence, person-related factors, such as lack of information and health literacy or communication difficulties, and system-related aspects, such as insufficient knowledge or even discriminatory attitudes among practitioners and service providers, have to be considered [10]. Health impairments lead to a significant emotional, social, and financial burden on the patients and on their social networks. In the European Union, intellectual disability was amongst the top ten most expensive diseases of the brain [13], requiring an annual expenditure of 43.3€ billions in 2010. In a Canadian study, adults with an intellectual disability were nearly four times more likely to incur high annual healthcare costs than those without an intellectual disability [14]. An Australian study demonstrated the considerable economic impact of intellectual disability on families, governments, and broader society [15], and a study on health-service use and the costs of Americans with an intellectual disability revealed that the presence of chronic medical conditions and poor mental health status predicted high expenses across various types of healthcare [16]. Taken together, all the evidence points to the urgent need for public health to focus on effective interventions for and the holistic management of secondary disorders in people with an intellectual disability.

The present paper develops five main themes. First, the current understanding of intelligence and the options of broadening the concept by integrating socio-emotional competencies will be outlined. Second, the development of socio-emotional brain functions will be linked to the maturation of the socio-emotional brain networks. Third, options to systematically assess socio-emotional brain functions will be offered. Fourth, the relatedness of developmental neuroscience and mental health in persons with an intellectual disability will be addressed. Finally, the implications of the developmental approach to treatment and support will be posed.

The lens of developmental neuroscience provides insights into the co-regulating processes of emotion regulation, social interaction and adaptation and may serve as a window into general psychological mechanisms. In a translational pathway, the underlying processes may have a broad impact on our understanding of human behavior [17].

#### **2. Intellectual Disability Revisited: About the Current Understanding of Intelligence and Why There Is a Need for Broadening the Concept towards the Social Realm**

In Western societies, Descartes [18] laid the foundation for continental rationalism: "Je pense, donc je suis" ['I think therefore I am']. Pioneers such as Damasio [19] overcame the dualistic body-mind distinction and delineated the importance of emotion and the sensorial body within cognitive science approaches. Socio-emotional and cognitive processes have been proposed to be highly intertwined and overtly present in all physiological and pathological mental activities. Ciompi [20] and the RDoC (Research Domain Criteria) framework [21] provided well-known examples. In the International Classification of Diseases, ICD-11, disorders of the intellectual development (also termed "intellectual disability" in DSM-5) are counted among the neurodevelopmental disorders that "arise

during the developmental period" and "involve significant difficulties in the acquisition and execution of specific intellectual, motor, language, or social functions" [22]. As such, in addition to poor cognitive functions, social, affective, and adaptive functions are also affected. However, the concept of "intelligence" is still dominated by Descartes' rationalism, and the diagnosis of an intellectual disability is still centred on general IQ measures, academic learning, and complex logical-deductive executive functions, such as working memory, processing speed, attention, encoding, verbal comprehension and expression, abstract reasoning, and problem solving.

However, emotional and social intelligence differ from cognitive intelligence and require different neural circuitries [23]. Socio-emotional brain functions refer to the ability to regulate one's own emotional expression, to identify the emotional expressions of others, to interpret emotional cues, to respond accordingly, and to self-soothe and manage emotional outbursts. Emotional intelligence is therefore essential for the quality of relationships with the self and with other people, the ability to adapt, to cope with stress and to communicate and interact appropriately [24]. A functional account of emotions posits that emotions are mental activities that respond to environmental stimuli, such as a social or physical challenge, and determine in turn physical and behavioral reactions. Emotional brain functions also influence cognitive processes, including perception, attention, learning, memory, reasoning, and problem solving and vice-versa. A detailed knowledge about emotional competencies such as emotional awareness, managing of own emotions and emotions of other people, self-motivation, impulse control and empathy may support caregivers, clinicians, and therapists to get an insight into the mental processes and needs of persons with low cognitive abilities [23,24].

In this theoretical paper, we aim to integrate knowledge from developmental neuroscience to expand our understanding of intellectual disability. As intellectual disability is a disorder of the brain that manifests during the developmental period, the stepwise acquisition of the different emotional and social skills can be depicted alongside the developmental trajectories of typically developing children [25,26], c.f. Table 1.


**Table 1.** Development of socio-emotional brain functions [26].

#### **3. Linking the Socio-Emotional Brain Functions with the Maturation of the Socio-Emotional Brain Networks**

Depending on the functionality of the respective brain networks, different ways of thinking and developmental tasks, needs, and skills can be learned [25,26]. Knowledge of the socio-emotional brain network functions may provide the clinician with insights into the "inner world" of people who experience difficulties expressing their own thoughts/feelings, and it could increase the understanding of their behaviors [25–27]. We therefore wish to outline the developmental milestones of brain development and link it to the respective socio-emotional functions. Persons with a developmental delay principally follow the same trajectories as people with a neurotypical development; however, the developmental milestones may be reached later or incompletely.

The brain architecture is scaffolded prenatally and early in life, followed by an extended period of differentiation of the cytoarchitecture by dendritic growth and the formation, pruning, and stabilization of synapses. While short-range connectivity predominates in infancy, there is a shift towards long-range networks in adolescents and adults [25]. The developmental changes of structural brain connectivity result from a sequence of genetic and epigenetic mechanisms at key developmental stages [25,28–30]. Environmental factors and early life experiences in social interactions play a crucial role in the coordination and timing of the specific neuronal patterning [25,31,32].

At birth, the neuronal networks are already at a certain stage of maturity. However, functional magnetic resonance imaging studies showed that local brain activity and functional connectivity differ between neonates and adults. While in the neonatal brain, for example, sensorimotor, visual and auditory areas were most active, other frontal brain regions, the basal ganglia and limbic/paralimbic areas showed lower dynamic connections than adult brains [28]. The emergence of the various socio-emotional skills is linked to the formation of the respective brain networks located within the different parts of the limbic system [33]. Thus, higher order networks build on circuits that process more basic information [25]. The recognition of emotional-communicative signals, for example, is a prerequisite for the proper functioning of the Theory of Mind network, or stress and emotion regulation abilities are necessary for successful impulse control.

The different steps (Figure 1) provide an insight into the stepwise emerging mentalization abilities. Depending on the respective developmental stage, different ways of thinking occur [32]:


Knowledge of the development of the mentalization abilities is supportive for a proper understanding of a person's mental framework, especially in the case of the nonmentalizing ways of thinking.

Figure 1 exemplifies the stepwise development of the Theory of Mind network.

**Figure 1.** Milestones of development of the Theory of Mind network: Teleological thinking (0–15 months); concrete thinking (15–24 months); Pseudomentalization (24–48 months); Theory of Mind network (>48 months). Details c.f. [32,34].

Depending on a variety of factors, including specific brain alterations and their time course, in persons with an intellectual disability, the formation of the socio-emotional brain networks may differ from the pattern that can be observed in typical development [35,36]. According to the definition in the ICD-11/DSM-5, intellectual disability begins during the developmental period and is associated with impairments of the different brain functions, which will be related to the different neural networks in the following stage.

However, when the developmental delay is severe, the *deep limbic system* drives most emotional and relational acts. This part of the limbic system develops prenatally and during the very first months after birth and includes the central nucleus of the amygdala, the hypothalamus, and parts of the brain stem including the periventricular grey and the vegetative nuclei. This first step of brain development is accompanied by an action-oriented *way* of thinking with an inability to express feelings and thoughts with words [32]. Feelings and thoughts cannot yet be expressed with words but involve goal-oriented actions. The autonomic and the stress-regulation systems process basal functions for survival, such as heart rate and temperature control, feeding, sexuality, territoriality, and stress responses including fight-flight reactions (see Figure 2) [32]. These mostly unconscious processes are genetically-epigenetically determined and influenced by early life experiences [37].

In moderate to severe forms of developmental delay, the functions located within the *mesolimbic system* determine the way of thinking and social interaction. This part of the limbic system is located in the basolateral amygdala, the ventral tegmental area, and the nucleus accumbens/ventral striatum and is the seat of the reward and the reward expectation system where emotional conditioning and emotion regulation are processed. Hence, basic emotional functions, such as fear, sadness, disgust, happiness, and anger, are determined [31,38]. The basic needs are safety and security [25,26]. In this stage of brain

development, the person is learning to build up an inner picture of the outside environment (object permanence) and to experience his/her own thoughts as reality (concrete thinking) [39]. This may result in misunderstandings, as facts are not differentiated from convictions [32]. In the next step, accompanied by the ability to differentiate between the self and the other, the pretend mode of thinking 'pseudo-mentalization' arises [32]. This can lead to meaningless conversations, such as repetitive questioning, and in the case of trauma, may result in dissociation [32]. The mesolimbic system develops within the first months and years of life and operates predominantly unconsciously (cf. Figure 2) [33].

**Figure 2.** The development of the different parts of socio-emotional brain networks. Details about the different parts and functions of the limbic system c.f. [33]. Socio-emotional brain functions rely on a proper formation of the respective brain areas of the limbic system. Depending on the severity of brain damage, also socio-emotional competencies are affected accordingly. Abbreviations: PFC: Prefrontal Cortex; IC: Insular Cortex; Ant.: Anterior; ACC: Anterior Cingulate Cortex; Bl.: Basolateral; AM: Amygdala; Basal Gang.: Basal Ganglia; VS: Ventral Striatum; VTA: Ventral Tegmental Area.

In milder forms of developmental delays, the *upper limbic system* dominates social cognition and adaptive behaviors. It is composed of a group of tightly interconnected cortical brain areas including the prefrontal, the orbitofrontal, the ventromedial frontal, the anterior cingulate, and the insular cortex. It comprises the neural activity that controls the Theory of Mind, different aspects of executive functions, risk assessment, and reality awareness [40–42]. In a top-down mechanism, these neocortical networks attenuate the emotional responses of the lower-order brain circuits located within the mesolimbic and deep limbic systems [43]. Logical thinking, impulse control, delayed gratification, and affect regulation are important for pro-social behaviors [44]. Concomitantly, emotional states, such as empathy, friendship, loyalty, and moral thinking, may be observed [27,45,46]. The upper limbic system evolves in late childhood and adolescence and can be partly modulated by learning [33].

A variety of conditions associated with an intellectual disability, such as ASD, meningoencephalitis, or genetic syndromes, may cause impairments of the early wiring within the limbic system and the associated brain functions [25,42,45,47,48]. Therefore, the socioemotional brain functions, e.g., perspective-taking skills, may differ in persons with different syndromes (Cornelia de Lange syndrome vs. William syndrome) or comorbidities such as ASD or attention-deficit-hyperactivity disorders (ADHD) [34,49]. Furthermore, stress and trauma can influence social brain functions in general, and specifically for persons with intellectual disabilities [25,26,50].

So far, there is a lack of assessment instruments for emotional and social competencies. Thus, incorporating structured information about the social, emotional, and practical skills into the assignment to the different levels of intellectual disability may be supportive for clinical care, especially when it comes to the more severe forms where classical IQ-tests cannot be applied.

#### **4. Assessment of Socio-Emotional Functioning**

Depending on the individual pattern of developmental delay, also in adults with an intellectual disability, socio-emotional brain functions may be delayed. For a comprehensive evaluation of the mental abilities of a person, we propose integrating the assessment of the different emotional and social skills located in the respective brain network, as these are crucial for perception, the way of thinking, and adaptive behaviors outcomes. Currently, IQ tests focus on logical-deductive academic skills [23,24,51]. However, the IQ score does not always relate to the individual's functioning at a specific point in time, and emotional competences, such as affect regulation, risk assessment, delayed gratification, impulse control, mentalizing abilities, and reality awareness, must also be taken into account [24,46]. Structured assessments addressing these abilities may be helpful to further ascertain this population and support clinicians in the calibration of treatment and support.

Being aware that development is a continuous process, for an assessment of the functional skills, a stepwise model is necessary. Researchers have developed assessment instruments to determine the socio-emotional functioning of a person with an intellectual disability [52,53]. In particular, the Scale of Emotional Development-Short (SED-S) is based on the normative developmental trajectory of the social brain network to define the central characteristic of socio-emotional functioning in a certain age group [35]. The instrument was tested for proof of evidence for criterion validity on item, domain, and scale level by applying the scale to a sample of typically developing children [54]. For the majority of items, the expected response pattern emerged, showing the highest response probabilities in the respective target age groups. Agreement between the classification of the different SED-S domains and the chronological age of children with normative development was high (*κw* = 0.95; exact agreement = 80.6%) [54]. Interrater reliability at domain level ranged from *κw* = 0.98 to 1.00, and internal consistency was high (α = 0.99) [54]. The SED-S is applicable and valid in children [55] and adults with ID [34]. Lower levels of socioemotional development are associated with more severe forms of challenging behaviors [49]. Mentalization abilities can be assessed using the Reflective Functioning Questionnaire– Mild to Borderline intellectual Disabilities *+* (RFQ-MBID) [56]. Depending on the pattern of brain alterations, in persons with an intellectual disability, the intellectual reference age is likely to be distinct from the emotional age [49]. Therefore, we argue that the socioemotional brain functions should be evaluated separately, and specific instruments should be added to those already in use to measure the IQ itself. The utility of the comprehensive assessment of the level of socio-emotional brain functions should be viewed as paramount in supporting clinicians in personalizing treatment and care in the clinical setting. A person's social, emotional, and practical abilities are central for the adaptive behavior, emotional well-being, and mental health.

#### **5. Mental Disorders and Developmental Neuroscience in Persons with an Intellectual Disability**

Mental health and emotional functioning in a particular social environment are strongly interrelated. Persons with an intellectual disability are highly vulnerable to mental disorders [4–6]. The conceptualization of psychopathology and mental disorders relies on the grouping of defined symptoms into syndromes that yield a psychiatric diagnosis. The co-occurrence of certain developmental disorders and intellectual disability may suggest a common underlying neurobiology at an early stage of brain development. The increasing evidence for shared genetic etiology across different psychiatric disorders and intellectual disability suggests a continuum of neurodevelopmental causality that includes both the heterogeneity and the overlap of risk factors and disease mechanisms [57]. The developmental miswiring within the social brain networks at sensitive periods may be associated with mental disorders that occur at a certain point of brain development [45,58]. Hence, certain disorders such as autism spectrum disorders (ASD) may be more prevalent in people with more severe forms of intellectual disability while other disorders such as social anxiety disorders may be more often seen in milder forms of intellectual disability.

In ASD, for example, core symptoms, such as perspective-taking skills, are rooted in developmental delays of the brain circuits related to social cognition [59]. In ADHD, widespread alterations of structural and functional brain connectivity are described [60]. Insecure attachment appears to be linked to social experiences that occur during critical periods of development which affect the architecture of the limbic and stress regulation system and have an impact on emotion processing, emotion regulation, and risk assessment [23,25,61]. Alterations in specific neural circuits that develop prenatally or very early in life are also often reported in persons with an intellectual disability, especially when the developmental delay is severe [45,58].

However, other psychiatric disorders, such as social anxiety disorders, dissociative disorders, or personality disorders, may require the maturation of higher-order social brain networks and so cannot be found earlier than age 5 years [62–64]. Social anxiety disorders require perspective-taking skills located in the Theory of Mind network [62]. Dissociative disorders are associated with subcortical white matter alterations within the higher limbic system [63,64]. Conduct disorders may progress to antisocial personality disorders during adolescence/early adulthood [65]. Social anxiety, dissociative disorders, or personality disorder can be linked to disturbances of higher-order brain circuits and typically arise concomitantly to the formation of the respective neural networks during childhood and adolescence. These mental disorders are rarely observed in severe forms of intellectual disability and are more prevalent in persons with borderline intellectual functioning or mild cognitive impairments [5].

Therefore, it can be argued that disturbances of the brain cytoarchitecture and function that occur at a certain developmental period may increase the susceptibility to certain mental disorders. This is supported by research examining emotional intelligence and psychopathy [66,67]. The developmental approach for socio-emotional brain functions in persons with an intellectual disability offers a fundamental perspective in mental health and opens up new treatment options [45].

#### **6. Impact of the Social Brain Development on Treatment and Support**

The quantity and quality of studies evaluating the efficacy of psychological therapies in persons with an intellectual disability and mental ill-health are still limited, especially in those with severe to profound intellectual disabilities [68]. Some studies tested commonly used psychosocial interventions, such as cognitive behavioral therapy, and there are valuable efforts to adapt the methods to the level of cognitive functioning; however, treatment manuals for severe and profound levels are still scarce [49,69]. In addition, effectiveness studies often exclude persons with multiple disabilities and comorbidities which is the clinical reality we are faced with [49,68].

With regard to treatment and care, aspects such as the level of socio-emotional functioning and the associated mental competencies and possibilities for reflection may support the decision for or against a certain therapeutic approach. Well-developed perspective-taking skills, for example, may increase the probability of the individual deriving benefit from cognitive behavioral therapy or mentalization-based treatment, while individuals with limited stress regulation abilities may be more likely to respond to bodily and experience-based treatment methods, such as attachment-based behavioral therapy or dance and movement therapy [48,70–72]. Targeting evidence-based treatment programs that are personalized and in line with the individual's abilities and goals is particularly vital in persons with developmental disabilities [49,73]. The 'social information processing model', for example, aims to choose the type of intervention according to the mental state of a person during a social interaction [74]. Moreover, knowledge of the emotional reference age of the individual may enable caregivers to be more attuned to his/her emotional needs and, therefore, promote and maintain good mental health. Finally, the awareness of the socio-emotional functioning of persons with an intellectual disability at that time point may enhance the diagnostic process of ascertaining co-occurrent psychiatric disorders. Externalizing behaviors or observable psychological distress may be interpreted as psychopathological symptoms but could be better explained as a mismatch between the level of individual development expected for the chronological age and the level of actual individual functioning [56,75]. This is particularly useful in persons with low or absent verbal communication skills, in whom key elements of psychiatric disorders, such as delusions, hallucinations, or suicidal ideation, are often very hard to recognize and may only be expressed by changes in behavior [76]. Matson et al. [77] claimed that "accurately identifying the causes of adaptive skill deficits will likely result in more precise and effective treatment" (p. 1317). Therefore, disturbances of the socio-emotional brain networks at a certain developmental period may increase the susceptibility to certain mental disorders. Aligning treatment options according to the level of socio-emotional functioning may strengthen the efficacy and increase the outcome of treatment of certain mental disorders. Furthermore, teaching emotional competencies may further improve skills such as emotional awareness, managing of own emotions and emotions of other people, self-motivation and empathy [78].

#### **7. Discussion**

The developmental perspective on the socio-emotional brain network may give insights into their own perspective and experiences, especially in people who experience difficulties expressing their own thoughts and feelings, and it may support clinicians to better understand the shown behaviors [25–27]. Therefore, the linkage of the developmental milestones of brain development with the respective socio-emotional functions may help adapt treatment and support accordingly. We are aware that the staged limbic-structure theory is simplifying the complexity of human brain development [79,80]. This perspective or framework opens up the road for rolling out and promoting early intervention strategies that impact both behavior and adaptive skills as these appear to be likely modifiable factors that can improve longer term outcomes. Further in-depth insights into the perceptual, cognitive, and social-communicative functions in specific syndromes like Downs syndrome or Williams syndrome need to be considered [81,82].

#### **8. Conclusions**

The focus of this article is to connect recent knowledge from developmental neuroscience with clinical research in persons with an intellectual disability with the aim of deducing the implications for treatment and support. Despite the given limitations of the broad-brush description of the stepwise development of the brain, specifically of the different parts of the limbic system and its associated functions, a developmental neurobiological basis may offer an additional perspective in our understanding and conceptualization of psychopathology and mental health in persons with developmental delays. The developmental miswiring within the socio-emotional brain networks at sensitive periods may be associated with mental disorders that occur at a certain point of brain development [45,58]. A common underlying neurobiology at an early stage of brain development may cause an association of certain disorders with different severities of intellectual disability. This synthesis offers relevant evidence about the necessity to integrate developmental neuroscience into clinical practice and care for persons with an intellectual disability to further promote mental health in this highly vulnerable population. Knowledge of development of the socio-emotional brain is important in the clinical and daily work context, as it provides insights into the inner world of persons who may have difficulties in reporting about their own thoughts and needs. Accordingly, this article aims to cross the bridge from basic neuroscience to the practical work with persons with developmental disabilities. A comprehensive assessment of intellectual functioning including socio-emotional functioning is important in treatment provision that is personalized and addresses individual goals and deficits. Therapeutic considerations should not only contribute to increased well-being but should also be consistent with the person's emotional status and congruent with the social environment (cf. Figure 1). This extended understanding of how people with intellectual disability function and how they participate in society may enable persons with developmental disabilities to "participate in every aspect of life to the best of their abilities and desires" [7]. We assert that it is only in this way that the person can be supported to fully realize his/her potential and prevent new onset or exacerbations of a mental disorder.

**Author Contributions:** The article was conceptualized and the original draft written by T.S., A.H., M.B., I.D. and P.S. substantially contributed in discussing the outline, writing certain paragraphs, reviewing and editing the whole manuscript. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was supported by funds of the v. Bodelschwinghsche Stiftungen Bethel (c.f. Board Meeting Protocol from 19.1.2016). P.S. was funded by the Bartiméus Fund (reference number P00238).

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** This analysis of the development of the social brain functions and its impact on the needs of persons with an intellectual disability would not have been possible without the work of the founding father of the dynamic developmental approach, Anton Došen. In 2015, Došen, together with clinicians and scientists of different professions from all over Europe, founded an international working group, the *Network of Europeans on Emotional Development* (NEED), which meets annually in different European cities. The ideas and fruitful discussion of this group contributed greatly to the content of the article. We thank Filip Morisse for his valuable comments and suggestions on the manuscript.

**Conflicts of Interest:** T.S. receives royalties from different publishers (esp. Hogrefe, Kohlhammer) for various books and funds of the v. Bodelschwinghsche Stiftungen Bethel. No conflict of interest is declared for M.B., A.H., I.D. and P.S. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

#### **References**


## *Article* **More than a Physical Problem: The Effects of Physical and Sensory Impairments on the Emotional Development of Adults with Intellectual Disabilities**

**Paula S. Sterkenburg 1,2,\*, Marie Ilic 3, Miriam Flachsmeyer <sup>4</sup> and Tanja Sappok <sup>4</sup>**


**Abstract:** With the introduction of the ICD-11 and DSM-5, indicators of adaptive behavior, including social–emotional skills, are in focus for a more comprehensive understanding of neurodevelopmental disorders. Emotional skills can be assessed with the Scale of Emotional Development-Short (SED-S). To date, little is known about the effects of physical disorders and sensory impairments on a person's developmental trajectory. The SED-S was applied in 724 adults with intellectual disabilities, of whom 246 persons had an additional physical and/or sensory impairment. Ordinal regression analyses revealed an association of movement disorders with more severe intellectual disability and lower levels of emotional development (ED) on the overall and domain levels (*Others*, *Body*, *Material*, and *Communication*). Visual impairments predicted lower levels of ED in the SED-S domains *Material* and *Body*, but not the overall level of ED. Hearing impairments were not associated with intellectual disability or ED. Epilepsy correlated only with the severity of intellectual disability. Multiple impairments predicted more severe intellectual disabilities and lower levels of overall ED. In conclusion, physical and sensory impairments may not only affect physical development but may also compromise intellectual and emotional development, which should be addressed in early interventions.

**Keywords:** emotional development; intellectual disability; visual impairment; hearing impairment; physical disability; sensory impairments

#### **1. Introduction**

People with intellectual disabilities have a higher risk of developing psychological stress than people without intellectual disabilities [1]. Possibly contributing to this, people with intellectual disabilities have difficulty assessing and processing information [2], they need predictable environments [3], and they have poor coping mechanisms [4]. Furthermore, due to affected children's limited behavioral repertoires, parents and caregivers need to have a high level of sensitivity and responsiveness to signals and react adequately to the behavior, needs, and wishes of the person with an intellectual disability [4,5]. Consequently, there is a higher risk of disturbed attachment and emotional and behavioral problems [6,7].

According to the American Association on Intellectual and Developmental Disabilities (AAIDD), people are classified as having an intellectual disability when they have an IQ score below 70 and/or a significant limitation in their adaptive behavior [8]. The need for support for conceptual, social, and practical skills starts before the age of 22 [8]. Likewise, the classification systems DSM-5 and ICD-11 also include limitations in adaptive

**Citation:** Sterkenburg, P.S.; Ilic, M.; Flachsmeyer, M.; Sappok, T. More than a Physical Problem: The Effects of Physical and Sensory Impairments on the Emotional Development of Adults with Intellectual Disabilities. *Int. J. Environ. Res. Public Health* **2022**, *19*, 17080. https://doi.org/10.3390/ ijerph192417080

Academic Editor: Paul B. Tchounwou

Received: 14 October 2022 Accepted: 7 December 2022 Published: 19 December 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

behavior and social skills in the diagnostic criteria for intellectual disability/disorders of intellectual development, respectively. Intellectual disability is often associated with a delay in emotional development [9]. Delayed social–emotional development and associated neglect of basic emotional and support needs result in stress and consequently possibly challenging behavior [7]. To provide adequate care matching the emotional functioning and needs of persons with intellectual disability, the Scale for Emotional Development-Short (SED-S) has been developed and studied in children with and without intellectual disabilities [9–11] as well as in adults [12–15]. The SED-S is based on the Scheme for Appraisal of Emotional Development (SAED) [16], the Scale for Emotional Development– Revised (SED-R) [17], and the SED-R2 [18]. Adequate psychometric properties are reported for the SED-S [9,10].

The prevalence of co-occurring impairments (such as physical, visual, and hearing impairments) is higher among persons with intellectual disability than in those without [19,20]. In studies conducted in the Netherlands among 1598 persons with intellectual disability who were older than 18 years of age, the following prevalence rates were reported: visual impairment, 14%; blindness, 5%; mild hearing loss, 30%; moderate to severe hearing loss, 15%; and dual impairments (visual and hearing impairments), 5% [20–22]. What is more, in a Finnish study among 461 persons with profound to severe intellectual disability, the prevalences of motor impairments and epilepsy were, respectively, 35% and 51% [23]. These impairments in addition to intellectual disability may affect emotional functioning.

Auditory sensory loss is, for example, of interest when studying social–emotional development in people with intellectual disabilities. In studies conducted before the implementation of neonatal hearing screening programs, results indicated that children over the age of 4 with hearing loss had more social–emotional difficulties than did children without hearing loss [24]. An uncompensated hearing impairment also affects communication in a negative way in adulthood [25,26]. However, the results of a study conducted in 18-month-old children with hearing loss found no apparent difficulties in social–emotional functioning [27]. Additionally, Lederberg and Mobley [28] found no difference in the quality of attachment of children with and without hearing impairments. This could be thanks to the ability of parents and children to communicate nonverbally during the child's first years, with children with a hearing impairment being able to adequately imitate facial expressions and hand and body movements, in addition to using gestures and pointing [29]. Moreover, parents put much effort into early communication, such as trying to establish (eye) contact or elicit a response through manifesting exaggerated facial expressions, waving their hands, and moving objects or people into the child's line of sight [29]. Although parents and children have compensatory communication in place, Dirks et al. [30] did report that children with a hearing impairment are at risk for social–emotional difficulties. Adding to this, Sterkenburg et al. [9] reported that children with an intellectual disability and a hearing-and/or visual impairment (n = 9) showed lower emotional functioning than children with intellectual disabilities without these sensory impairments (n = 108). These results were found on the SED-S overall score and on the domain *Others* (meaning "relating to significant others"). However, due to the small sample size in this study, people with visual or hearing impairments were combined into one group. Consequently, it is unclear whether emotional functioning is lowered by the separate sensory impairments.

Regarding the emotional development of persons with visual disabilities, the physical, cognitive, and social development of a child are affected by visual impairment [31]. Urqueta Alfaro et al. [32] confirmed that, compared with children without visual impairment, the overall development of children with visual disabilities is delayed. To be precise, the visual impairment hinders their social development, as social behavior and communication mostly develop through eye contact and observation [31]. Zooming in on the emotional development of children with visual impairment, Fraiberg [33] reported that blind children show more fear of strangers than sighted peers and that their facial expressions are frequently indistinct. Additionally, their nonverbal expressions are sometimes different and very subtle [34]. The findings of Fraiberg [33], suggested that children with a visual

impairment do develop mental representations of their attachment figures, but that these representations start at a later age and/or show different characteristics than in sighted peers. This delay may affect their emotional functioning. Furthermore, infants with visual impairments need more help and encouragement to become aware of their range of motion. This help prevents them from remaining in their natural passive state, which could hinder their physical development, including posture and mobility [35], and affect their exploration and social and emotional development.

Next to the influence of a hearing or visual impairment, a child's physical development may also impact their emotional development. Persons with an intellectual disability have an increased risk for physical disabilities and epilepsy [19,36]. Vandesande et al. [37] conducted a study among children with severe and profound intellectual disabilities during a stressful situation, where the child's parents and a stranger were present. Interestingly, the child's differentiated responses to comfort seemed to be related to their fine motor skills [37]. Therefore, to adequately support persons with intellectual and physical disabilities, it is important to examine the effects of the disabilities on the different domains of emotional development.

According to Došen [38], the social–emotional development of a neurotypical child goes through several stages, and these stages are linked to social–emotional developmental milestones [38–40]. For children with intellectual disabilities and sensory, physical, or multiple impairments, reaching these milestones requires more effort than it does for children without these impairments. Up to now, to our knowledge, no studies have been conducted among adults with intellectual disability to examine the effect of visual, hearing, or physical impairments on emotional functioning. Therefore, the aim of this study was to examine whether physical or sensory impairments of adults with intellectual disabilities can predict their level of social–emotional functioning.

#### **2. Materials and Methods**

#### *2.1. Setting and Design*

The study was conducted from May 2016 to November 2020 in three hospitals and five home care facility centers in Belgium, the Netherlands, and Germany. Inclusion criteria were age >18 years and a diagnosis of intellectual disability. There were no exclusion criteria within this respective population. A sample of 724 adults with intellectual disabilities was recruited, among which 246 persons (34%) had an additional physical disorder and/or sensory impairment such as a hearing and/or visual impairment, movement disorder, and/or epilepsy.

The participating organizations were Tordale in Torhout (Belgium), Cordaan in Amsterdam (Netherlands), ORO in Helmond (Netherlands), De Twentse Zorgcentra in Losser (Netherlands), Bartiméus in Doorn (Netherlands), the Evangelisches Krankenhaus Königin Elisabeth Herzberge in Berlin (Germany), Klinikum München Oberbayern in München (Germany), and St. Lukas-Klink in Liebenau (Germany). The persons themselves or their legal guardians gave their informed consent for participation in this study.

#### *2.2. Participants*

The total study sample consisted of 724 participants with intellectual disabilities. Due to missing information about the researched impairments, two persons were omitted from the analyses, leaving a total sample of 722 participants. The average participant age was 37.4 years (18–76 years, *SD* = 13.3) and males were slightly in the majority (56.4%). The degree of intellectual disability ranged from mild (IQ 50–55 to 70: 28.2%), moderate (IQ 35–40 to 50–55: 37.4%), and severe (IQ 20–25 to 35–40: 26.8%), to profound (IQ < 20–25: 7.6%).

The age of the 246 (34%) participants with sensory impairments ranged from 18 to 76 years, and the average age was 39.9 years (*SD* = 13.7). This sample included more males (60.2%) than females. All levels of intellectual disability were represented; most of the participants had moderate intellectual disabilities (38.2%), followed by severe intellectual disabilities (28.5%), mild intellectual disabilities (19.5%), and profound intellectual disabilities (13.8%). In this group with sensory impairments, 44 persons (17.9%) had hearing impairments and 64 persons (26%) had visual impairments. In the sample with sensory impairments, 87 persons (35.4%) had a movement disorder. Epilepsy was reported in 130 persons (52.8%).

#### *2.3. Assessment*

The level of emotional development (ED) was assessed using the SED-S [10]. The SED-S is a semi-structured interview consisting of 200 binary items in eight domains, concerning different aspects of daily life behaviors. The scale assesses five developmental stages with reference ages ranging from 0 to 12 years of age. Each level of ED is assessed by five items per domain. The eight domains are: (1) *Body* (Relating to His/Her Own Body), (2) *Others* (Relating to Significant Others), (3) *Object* (Dealing with *Change*: Object Permanence), (4) *Emotions* (Differentiating Emotions), (5) *Peers* (Relating to Peers), (6) *Material* (Engaging with the Material World), (7) *Communication* (Communicating with Others), and (8) *Affect* (Regulating Affect).

Within the SED-S items, behaviors for a certain level of ED are described, which are either typical in the respective person ("yes" answers) or not typical ("no" answers). To determine the level of ED in a certain domain, the number of "yes "answers is counted. The level with the most "yes "answers is the domain-wise level of ED. Estimating the overall level of ED, these domain-specific results are ordered from low to high, and the four lowest domains determine the overall result. Trained psychologists, psychiatrists, developmental psychologists, or ortho-pedagogues conducted the interview with two to five informants, such as family members or close caregivers. The assessment relied on behaviors displayed during the previous 2 weeks.

Expert validity can be taken as given, as the scale is based on a survey of developmental psychology experts and their assessments of behaviors typical for specific levels of development, [10]. Validation against a group of 160 typically developed children showed a high degree of correspondence (81% exact agreement; 0.95 weighted kappa value) [11]. An exploratory factor analysis provided a one-factor model with a good model fit in 724 adults with ID, most of them having additional mental health problems [15,41], in 118 children with ID and mental health problems [9] and in 83 healthy adults with ID [14,41]. Divergent validity was found for chronological age in children with ID [9] and in healthy adults with ID [14,41]. Convergent validity with the Vineland Adaptive Behavior Scale could be seen in the children's sample (r = 0.642, *p* < 0.001; [9]). Strong negative associations with the severity of ID could be shown in 327 adults with ID and mental health problems (r = −0.654, *p* < 0.001; [11]), in 83 adults with ID without mental health problems (−0.753, *p* < 0.001; [14,41]) and in 118 children with ID (G = −0.69; *p* < 0.001; [9]). Inter-rater reliability for 25 typically developed children was 1.0 (Cohen's kappa). Internal consistency as measured by Cronbach's alpha was 0.99 in typically developing children [11], 0.94 in 118 children with ID [9] and 0.92 in 83 adults with ID without mental health problems [14,41].

The degree of intellectual disability was diagnosed using the Disability Assessment Schedule (DAS), which is an informant-based structured interview [41]. It poses several questions about adaptive behaviors in four parts: continence, self-help skills, communication, and (cognitive) skills. Depending on the presence of these behaviors, points are given and summed to a total score (minimum 15 points; maximum 71). The total score corresponds with the levels of ID (mild, moderate, severe, profound). The DAS is a reliable measure when applied by trained professionals [42]. Evidence pertaining to its validity in people with ID is provided by correlation analysis with the Colored Progressive Matrices and the Columbia Mental Maturity Scale [43].

The data regarding hearing and visual impairment, movement disorders, and epilepsy were systematically recorded upon the assessment of the SED-S.

#### *2.4. Statistical Analysis*

The statistical analyses were conducted using IBM SPSS 27 Statistics for Windows, USA. Associations of hearing and/or visual impairment, and movement disorder and/or epilepsy, with the severity of the intellectual disability and the level of ED (overall and domain wise) were examined by applying an ordinal logistic regression analysis. The ordinal logistic regression model was chosen because of the dichotomous variable structure of the impairments and because the severity of the intellectual disability and level of ED were ordinal variables [44]. A further key assumption of ordinal logistic regression analysis is that of assumption of proportional odds, which in SPSS is examined with the test of parallel lines. Chi-square was used to determine whether the assumed model with an explanatory variable was improved in comparison with the baseline model without this explanatory variable.

A significant *p*-value indicates an improved fit to the data. Nagelkerke *R*<sup>2</sup> is reported as a pseudo *R*<sup>2</sup> value, indicating the proportion of variation in the outcome that can be accounted for by the explanatory variables. To specifically analyze the relationship between the sensory impairments and the intellectual disability and ED, odds ratios and the Wald χ<sup>2</sup> were calculated to investigate whether a significant impact of the explanatory variables existed.

#### **3. Results**

Assumptions of parallel lines were met for all our analyses (*p* > 0.05) with one exception: for the regression of the domain *Others* on the four impairments, it was significant with *p* = 0.044, meaning these results should be interpreted cautiously.

#### *3.1. Number of Impairments as a Predictor of Intellectual Disability and ED*

Since many participants had more than one reported impairment, the number of impairments (e.g., visual, hearing) was analyzed as a predictor of the intellectual disability and ED. For intellectual disability, ordinal regression analysis revealed that higher numbers of co-occurrent physical impairments were related to more severe intellectual disability (Δχ<sup>2</sup> = 37,85, *df* = 4, *p* < 0.001; Nagelkerke *R*<sup>2</sup> = 0.055). The individual odds ratios were nonsignificant. Additionally, the level of ED improved the model fit of the regression analysis when the number of impairments was used as a predictor to explain the level of ED (Δχ<sup>2</sup> = 11.56, *df* = 4, *p* < 0.021; Nagelkerke *R*<sup>2</sup> = 0.017). Again, the individual odds ratios were nonsignificant.

#### *3.2. Different Forms of Impairments as Predictors of Intellectual Disability and ED*

Looking at the frequency of the different levels of intellectual disability and ED for the different groups of impairments (reported in Tables 1 and 2), not only the presence or absence of physical or sensory impairments, but also the type of impairment was relevant. For an overview of the results, see Table 3.


**Table 1.** The Different Impairments and Severities of Intellectual Disability.

Note. In parentheses are percentages per column. Regression analyses for the impairments marked with \* showed a significant association with the severity of intellectual disability.


**Table 2.** The Different Impairments and Levels of Emotional Development.

Note. In parentheses are percentages per column. Regression analyses for the impairments marked with \* showed a significant association with level of ED.

**Table 3.** The associations between sensory impairments, ID, and ED.


Hearing impairment. Hearing impairments were not associated with the severity of intellectual disability or the level of ED in any of the ten analyses (Details for the nonsignificant analyses are available from the authors upon request).

Visual impairment. Having a visual impairment was related neither to the intellectual disability nor to the level of overall ED. However, visual impairments significantly predicted lower levels of ED on the domains of *Body* (odds ratio 1.65, 95% CI 1.022–2.68; Wald *χ*2(1) = 4.082, *p* = 0.043) and *Material* (odds ratio 1.71, 95% CI 1.06–2.72, *Wald χ*2(1) = 4.823, *p* = 0.028).

Movement disorder. A movement disorder was related to more severe forms of the intellectual disability (odds ratio 0.28, 95% CI 0.18–0.43; Wald *χ*2(1) = 33.446, *p* < 0.001). Furthermore, the presence of a movement disorder was related to lower levels of ED in general (odds ratio 1.59, 95% CI 1.05–2.42; Wald *χ*2(1) = 4.815, *p* = 0.028) and for the domains of *Body* (odds ratio 2.25, 95% CI 1.47–3.45; Wald *χ*2(1) =13.988, *p* < 0.001), *Others* (odds ratio 1.66, *95% CI* 1.06–2.72; Wald *χ*2(1) = 5.591, *p* = 0.018), *Material* (odds ratio 1.66, 95% CI 1.10–2.50; Wald *χ*2(1) = 5.821, *p* = 0.016), and *Communication* (odds ratio 2.14, 95% CI 1.41–3.24; Wald *χ*2(1) = 12.964, *p* < 0.001).

Epilepsy. Epilepsy was associated with more severe forms of intellectual disability (odds ratio 0.65, 95% CI 0.46–0.93; Wald *χ*2(1) = 5.590, *p* = 0.018), but not with the level of ED (neither overall nor domain wise).

#### **4. Discussion**

The aim of this study was to examine if adults with intellectual disability and physical and/or sensory impairments score lower on the SED-S than adults with intellectual disability but without these additional impairments. At first, the results indicated that an accumulation of impairments predicts lower emotional functioning. This could be explained by one impairment significantly affecting the other. For example, as Fraiberg [35] reported, a visual impairment may influence physical development. This in turn may shape emotional development. What is more, persons with a disability are unable to compensate

for the co-occurrent impairment. For instance, Gunther [45] reported that the presence of a visual impairment in addition to an intellectual disability means that vision cannot be used to compensate for the intellectual disability, and vice versa. Therefore, people with visual and intellectual disabilities find it is even more difficult to understand social relationships than do people with only intellectual disabilities [46]. Additionally, as found in this study, in persons with a visual and intellectual disability as well as an added hearing impairment, emotional functioning is significantly lower than it is in adults with intellectual disabilities with either a hearing or a visual impairment (not having both impairments).

A second finding of this study is that hearing impairments seem not to be associated with intellectual disability or emotional development. These findings indicate that although there is a risk for social–emotional difficulties in children [30], the focus on learning to communicate [29] and socially interact may eventually buffer the effect of the hearing impairment on emotional functioning. Early intervention programs focusing on joint engagement and emotional availability can be used for this purpose [47,48].

Third, in this study, no significant effects of visual impairment and intellectual disability on the total score for emotional development were found. However, it is important to note that there were domain-specific outcomes, namely in the domains *Relating to His/Her Own Body* and *Engaging with the Material World*. Zooming in on the items of these domains, the hindering effect of the visual impairment becomes more clear: for example, in the use of tactile senses to explore the world, the need to feel safe in an open space, and requiring more time to explore materials, while contact with others is less evident. This may confirm what Fraiberg [33] suggested, namely that emotional development could be delayed and/or show different characteristics than it does in sighted peers. These outcomes are presumably of great importance for (early) intervention programs, which it seems should be more focused on these aspects of socio-emotional development. Additionally, as for all persons, disharmonious emotional development may affect well-being, and therefore should be noticed [49].

A fourth finding of this study is that having a physical disability was associated with more severe forms of intellectual disability and lower levels of emotional functioning. These results indicate that a tailored approach is needed for these persons. Due to the severe or profound disability, repetition, patience, and interaction are needed for emotional development. Nowadays, technology can also be used in daily care to support emotional development [50] and communication. The results of this study stress the importance of addressing these caregiving and assistive technology needs in interventions.

Fifth, epilepsy was related to intellectual disability but could not be linked to emotional development. Thus, epilepsy does not seem to directly obstruct emotional functioning, although adequate care and support for emotional and physical needs is required.

Sterkenburg et al. [9] found a significant relation between visual and hearing senses and emotional development in children. However, in this study the focus was on adults with a mean age of 37.4 years and less-significant links were found. Matching the findings reported by Fraiberg [33] for children with a visual impairment, there was a delay in development, but there seems to be a catching up later in life. However, accumulated impairments did show significant relations with emotional development. Thus, (early) intervention programs are essential and should consider the different co-occurring impairments. There are programs such as: "Development of an attachment relationship" [51]; "Learning together" [52]; "Little room" [53]; "Barti-mat" [54], and the Light Curtain [55]. These results may encourage the application of early interventional strategies that impact both physical and social–emotional skills in people with intellectual and additional disabilities. Hereby, longer-term outcomes, quality of life, and social participation may be improved substantially. Therefore, we recommend continued investment in and provision of (early) intervention programs for parents of infants with intellectual disability and sensory impairment. Additionally, there is a need for more projects focusing on parent–child interaction and the use of technology in supporting the social and emotional development of persons with intellectual disability and sensory impairment.

#### *Limitations*

During the assessment, the data regarding visual and hearing impairments, physical disabilities, and epilepsy were reported based on participants' records. However, on-the-spot assessments were not conducted. Thus, the data may be incomplete or not adequately reported in the records and may, therefore, be biased. However, comparing the prevalence of the impairments reported in this study to the prevalence mentioned in the literature [20–23], this does not seem to be the case.

The reported results are based on cross-sectional data, so causal interpretations need to be made with caution. A longitudinal study that follows the development of children with and without intellectual disabilities and physical impairments would be required to be able to fully understand how these factors influence each other and social–emotional development.

The study was conducted in three Western European countries. Due to the small sample size for each of the studied impairments, comparisons between countries were not possible. There may be differences that we cannot now report and that need to be studied in future research. Furthermore, the (early) interventional care in the studied countries may explain the possible catching up when people have reached adulthood; such catching up may not occur in other parts of the world. Replication of this study is therefore needed, covering a broader spectrum of the world population.

#### **5. Conclusions**

In summary, higher numbers of co-occurrent physical and/or sensory impairments were related to more severe intellectual disability and lower levels of emotional development (ED). Interestingly, movement disorders affected intellectual and ED, while auditory impairment did not affect ED. Epilepsy correlated only with the degree of intellectual disability but not with the level of ED. On the domain level, *Relating to His/Her Own Body* and *Engaging with the Material World* showed associations with visual impairments and movement disorder, the latter disorder also predicting lower levels of ED in the domains *Relating to Significant Others* and *Communicating with Others.* Considering these overall and specific effects of different impairments on the intellectual and emotional functioning of people with multiple disabilities may align early interventions and thereby further improve long-term outcomes.

**Author Contributions:** M.I. and M.F. conducted the analyses, P.S.S. wrote the introduction and discussion, and T.S. finalized the paper and coordinated the study. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was supported by funds of the v. Bodelschwinghsche Stiftungen Bethel (c.f. Board Meeting Protocol from 19.1.2016). PSS was funded by the Bartiméus Fund (reference number P00238).

**Institutional Review Board Statement:** The study was conducted according to the ethical principles of the 1975 Declaration of Helsinki. All organizations acquired ethical approval separately. For Belgium, the University of Ghent ethics commission of the Faculty of Psychology and Pedagogic Science gave their permission. The ethics board in each Dutch organization gave approval. For Germany, the Charité University Hospital in Berlin (Ethics vote: EA2/193/16) gave their permission; additionally, every hospital received ethical approval from its own ethics commission.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** On request.

**Acknowledgments:** We thank all the participants, their parents or relatives, and the caregivers who contributed to this study. We thank the caregiving organizations for facilitating the study. Thanks also to Paula Verbon-Dekkers for providing feedback on the manuscript. Great appreciation goes all the members of the Network of Europeans on Emotional Development (NEED) who participated in the data collection.

**Conflicts of Interest:** T.S. receives royalties from different publishers (esp. Hogrefe, Kohlhammer) for various books and scales and funds of the v. Bodelschwinghsche Stiftungen Bethel.

#### **References**


## *Article* **Intellectual Disability Profiles, Quality of Life and Maladaptive Behavior in Deaf Adults: An Exploratory Study**

**Johanna Eisinger 1, Magdalena Dall 1,\*, Jason Fogler 1,2,3, Daniel Holzinger 1,4,5 and Johannes Fellinger 1,4,6**

	- Medical University of Vienna, 1090 Vienna, Austria

**Abstract:** Individuals who are prelingually deaf and have intellectual disabilities experience great challenges in their language, cognitive and social development, leading to heterogeneous profiles of intellectual and adaptive functioning. The present study describes these profiles, paying particular attention to domain discrepancies, and explores their associations with quality of life and maladaptive behavior. Twenty-nine adults with prelingual deafness (31% female) and mild intellectual functioning deficits (mean IQ = 67.3, SD = 6.5) were administered the Vineland Adaptive Behavior Scales-II (VABS-II) and an adapted sign language version of a quality of life scale (EUROHIS-QOL 8). Intellectual disability domain discrepancies were characterized as at least one standard deviation difference between the social domain and IQ and the practical domain and IQ, and a significant difference, according to the VABS-II manual, between the social and practical domains. Domain discrepancies were found between intellectual functioning and both the practical (58.6%) and social domain (65.5%). A discrepancy between intellectual and social functioning was significantly associated with a higher level of internalizing maladaptive behavior (T = 1.89, *p* < 0.05). The heterogeneous profiles highlight the importance of comprehensive assessments for adequate service provision.

**Keywords:** intellectual disability; deaf; adaptive behavior; intellectual functioning; domain discrepancy; maladaptive behavior; quality of life

#### **1. Introduction**

Deafness is a heterogeneous condition that can impact communication, social–emotional development and cognitive development [1]. Around 7 per 10,000 people have severe to profound hearing loss, with onset before language acquisition [2,3].

Approximately one-third to one-half of individuals who are prelingually deaf or hard of hearing have additional disabilities [4,5], most commonly intellectual disability [6]. Additive deprivation of language and communication, stemming from delayed identification, insufficient or late provision of hearing technology and little or no access to sign language, further impedes these individuals' community participation [7–10].

The diagnostic criteria for intellectual disability have been revised in the Diagnostic and Statistical Manual of Mental Disorder-Fifth edition (DSM-5; [11]) to encourage a more comprehensive patient assessment, with greater weight given to adaptive functioning than intellectual functioning for the purpose of ascribing intellectual disability severity [11]. Whereas intellectual functioning generally involves abilities such as reasoning, problem solving, knowledge and experience [12], adaptive functioning refers to the skills that are

**Citation:** Eisinger, J.; Dall, M.; Fogler, J.; Holzinger, D.; Fellinger, J. Intellectual Disability Profiles, Quality of Life and Maladaptive Behavior in Deaf Adults: An Exploratory Study. *Int. J. Environ. Res. Public Health* **2022**, *19*, 9919. https:// doi.org/10.3390/ijerph19169919

Academic Editor: Shoumitro Deb

Received: 14 July 2022 Accepted: 7 August 2022 Published: 11 August 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

learned and performed to meet the everyday demands of one's community or society [13], suggesting that adaptive behavior may be the more malleable (and hence important) intervention target to unlock an individual's full potential. Adaptive functioning includes three domains: the conceptual domain, including applied skills in language, reading, writing, math, reasoning, knowledge and memory; the social domain, referring to empathy, social judgment, interpersonal communication skills and the ability to make and retain friendships; and the practical domain, including self-management in areas such as personal care, job responsibilities, money management, recreation and organizing school and work tasks [11].

Intellectual and adaptive functioning, the two aspects of intellectual disability, are related but separate constructs [13]: a large meta-analysis of 148 samples containing a total of 16,468 participants showed a moderate relationship (r = 0.51) between intelligence and adaptive behavior, which is stronger in lower IQ groups [14].

With this more nuanced definition of adaptive functioning has come greater interest in intellectual disability domain discrepancy, in which one domain is markedly more deficient than another, as well as inquiry into whether different populations have unique, or at least specific, intellectual disability profiles. Sparrow, Cicchetti and Balla [15], authors of the Vineland Adaptive Behavior Scales-II (VABS-II), provide various adaptive functioning profiles based on pairwise comparison of the four adaptive behavior domains (communication, socialization, daily living skills and motor skills) outlined in the Vineland-II manual. When comparing the specific profile of individuals with hearing impairment with samples matched by age range and controlled for sex, ethnicity and education level, the researchers found that individuals with hearing impairment had lower levels of communication and daily living skills than the IQ-matched sample with typical hearing. The socialization scale appeared as a relative strength, though still lower than the non-clinical group [15].

There is a growing body of research on adaptive profiles in individuals with different neurodevelopmental disorders [16–22]. Tillmann et al. [23] examined how IQ and levels of ASD symptom and autistic trait severity are associated with adaptive functioning and suggested that core ASD-related social communication problems contribute both to adaptive functioning impairments and to the discrepancy between IQ and adaptive functioning. Further supporting this point, a discrepancy between intellectual functioning and adaptive skills was found to be significantly correlated with depression and anxiety in a sample of adults with ASD without intellectual disability, in which socialization was by far the largest weakness [24].

Studies correlating adaptive profiles with such clinically relevant variables as quality of life (QOL) and problem behavior (e.g., [13,25]) show divergent results. Tassé [13] and Simoes et al. [26] found a positive correlation between adaptive behavior and QOL in samples of individuals with mild-to-moderate intellectual disability, whereas Graves et al. [18] did not find significant associations between adaptive functioning and self-reported QOL in a sample of adults with Down syndrome. Jones et al. [27] found higher levels of problem behavior to be associated with more severe degrees of intellectual disability. Curiously, Balboni et al. [25] found that a subgroup of individuals with intellectual disability with the highest levels of problem behavior also had higher levels of adaptive behavior, explaining that a basal level of adaptive skills appears to be necessary for the person to be able to engage in their environment, positively or negatively.

No research to date has investigated the intellectual disability profiles and the relationships between intellectual disability domain discrepancies, QOL and maladaptive behavior in a population with prelingual deafness and intellectual functioning deficits. Hence, the main aim of this study is twofold: (a) to describe the intellectual disability profiles and potential intellectual disability domain discrepancies in a sample of adults who are deaf with borderline and mild cognitive functioning impairment and (b) to explore how these intellectual disability profiles and domain discrepancies are related to maladaptive behavior and self-reported QOL in this population. We explored whether expressed intellectual disability domain discrepancies between cognitive potential and lower social and practical

abilities are experienced as stressful barriers to unlock one's potential and therefore may be linked with lower quality of life and increased rates of maladaptive behavior.

#### **2. Materials and Methods**

#### *2.1. Participants*

This cross-sectional exploratory study was conducted within three therapeutic living communities (Lebenswelt) specifically developed to accommodate the needs of individuals with deafness and additional disabilities, focusing on supporting communication, social relationships, conflict resolution and work satisfaction. They are characterized by the constant use of sign language; one-quarter of the staff members are deaf themselves [7].

We recruited 29 individuals (9 women and 20 men) who met the inclusion criteria of having at least moderate hearing impairment and an IQ score between 50 and 85 (see Table 1). Of these participants, 93% were profoundly deaf and 7% had moderate hearing loss. Nearly all the participants joined their therapeutic communities with lifetime histories of potentially traumatic events—a sadly common finding among members of the deaf community [28,29]—and about 38% had experienced at least one depressive episode [30]; however, no participant was experiencing an active depressive episode during the time of data collection. Their length of enrollment in the therapeutic living communities ranged from 6 months to 20 years. Most of the participants (n = 23; 79.3%) lived and worked in these communities, and the remaining participants (n = 6; 20.7%) only took part in the workshop facilities. Their mean age was 46.89 years (SD = 16.42, range 20–73 years), and their mean IQ score was 67.31 (SD = 6.49, range 57–82). Based on the ICD-10/WHO criteria, the majority (72.4%) were classified as having mild deficits indicated by an IQ score between 50 and 69 [31]. In addition, half (51.7%) of the participants were currently diagnosed with intellectual disability with challenging behavior (F70.1 (ICD-10)), 20.7% with cerebral palsy, 13.8% with epilepsy and 13.8% with autism. Table 1 displays the sample characteristics in detail.


**Table 1.** Sample characteristics.

This study was approved by the ethical committee of the hospital St. John of God in Linz, Austria. Consent was given by the participants themselves and/or by their legal guardians (if applicable).

#### *2.2. Instruments*

2.2.1. Intellectual and Adaptive Functioning

The Vineland Adaptive Behavior Scales-II [15] is a comprehensive measure of adaptive behavior. This standardized norm-referenced assessment instrument provides information on an individual's adaptive behavior from birth to 90 years of age across motor, communication, daily living and socialization skills. A standard score (M = 100, SD = 15) for each domain is calculated as well as a summary adaptive behavior composite score. The subscales of the Vineland-II do not perfectly align with the current tripartite model of adaptive behavior described in the DSM-5 s definition of intellectual disability. Tassé and Mehling [12] proposed the following alignment or "cross-walking" of the VABS-II domains with the three domains of adaptive functioning identified in DSM-5: communication = conceptual skills; socialization = social skills; and daily living skills = practical skills. Accordingly, the socialization and daily living skills subscales of the Vineland-II were used to address the social and practical domains. However, two of the three sections of the communication subscale relate to the comprehension and production of spoken language. After adapting comprehension items to a visual modality, many items specifically referring to the structure of spoken language (e.g., intonation, verb inflection, prepositions, pronunciation, pronouns) had to be replaced by Austrian sign language items estimated to be functionally equivalent and of a comparable level of complexity. This non-validated adaptation resulted in significant floor effects that strongly weighed against its being considered for measuring the conceptual domain in this group of adults who are deaf with intellectual disability (see Figure 1).

**Figure 1.** Boxplots of the domains of intellectual disability (standard scores of Vineland-II domains and SON-R 6-40).

To assess participants' intellectual functioning, we administered the Snijders-Oomen Non-verbal Intelligence Scale for individuals (SON-R 6-40; [32]). The SON-R 6-40 assesses the participant's non-verbal cognitive developmental level and provides a standard IQ score (M = 100, SD = 15), making it relatively easy to compare with the standard scores derived from the two VABS-II subscales.

#### 2.2.2. QOL

The EUROHIS-QOL 8-item index (European Health Interview Surveys) is a short version of the WHOQOL-BREF. It consists of 8 questions that are also included in the 26 questions of the WHOQOL-BREF [33]. All four domains (physical, psychological, social and environmental) are represented, each with two questions. A normative study in Germany showed good construct validity and reliability [34]. An adapted, easy-tounderstand sign language version of the EUROHIS-QOL 8-item index was administered to assess participants' self-rated QOL [35]. Fellinger et al. (2021) [35] demonstrated that reliable and valid self-reports of QOL can be obtained from adults who are deaf with mildto-moderate intellectual disability using standard inventories such as the EUROHIS-QOL adapted to the linguistic and cognitive levels of these individuals. The EUROHIS-QOL 8-item index score was computed as the mean score across the eight items, ranging from 1 (worst QOL) to 5 (best QOL). The test–retest reliability was good (0.75), and internal consistency showed a Cronbach's Alpha of 0.78.

#### 2.2.3. Maladaptive Behavior

The VABS-II includes two subscales for internalizing and externalizing maladaptive behavior. The two subscales are reported as v-scale scores. A v-scale score below 18 indicates a non-clinical level of maladaptive behavior; a score between 18 and 20 indicates an elevated level; and a score between 21 and 24 indicates a clinically significant level of maladaptive behavior [15].

#### *2.3. Data Collection*

Data collection took place between September 2017 and March 2018. Participants' clinical characteristics (i.e., type and degree of hearing loss; psychiatric, behavioral and neurological diagnoses) were extracted from the medical records of the individuals at the hospital St. John of God. The QOL self-reports were gathered through a structured interview between the resident and a sign language-competent staff member who was not directly involved in the care of the residents (non-involvement in direct care was considered important in order for the participants not to feel pressured to give answers that they thought would be preferred by the interviewer).

VABS-II data were collected for each participant by the staff psychologist in consultation with either a family member or the participant's primary caregiver. Primary caregivers serve the roles of coach, case manager, advocate and personal assistant for residents and were therefore thought to be particularly well-qualified to serve as informants for this study.

#### *2.4. Computing Intellectual Disability Domain Discrepancies*

Within the context of this paper, we use the term *intellectual disability domain discrepancy* to indicate that there is a substantial difference between the level of intellectual, social and/or practical adaptive functioning. For the purpose of this study, when comparing intellectual functioning with the social or practical domain, a difference of at least 15 points (=1 SD) between the IQ score (SON-R 6-40) and the socialization and daily living skills (DLS) standard scores indicates an intellectual disability domain discrepancy. When comparing the social and practical domains, a difference between the socialization and the DLS standard scores with a significance level of 0.05 according to the VABS-II manual indicates a domain discrepancy between these two domains.

#### *2.5. Statistical Analysis*

First, univariate analysis of the key variables was applied to describe intellectual disability domains, QOL and maladaptive behavior, as well as domain discrepancies. Next, Spearman's correlation was performed to test for a correlation between intellectual disability domains (social, practical and intellectual functioning), QOL and maladaptive behavior. To investigate whether there were significant differences in the means of selfreported QOL and internal and external maladaptive behavior with and without intellectual disability domain discrepancies, an independent samples *t*-test was performed.

#### **3. Results**

#### *3.1. Intellectual Disability Domains, QOL and Maladaptive Behavior*

Figure 1 shows the distribution of the median standard scores of (a) SON-R 6-40 intellectual functioning and (b) the three domains of Vineland-II adaptive functioning (practical, social and communication). Intellectual functioning emerged as the strongest domain, with a mean standard score of 67.31 (SD = 6.49) and no standard scores lower than 57 (see Table 2). The individuals also demonstrated a low level of practical functioning with a mean score of 48.97 (SD = 17.41), with more than half of the sample classified as having moderate or severe deficits. The social domain was the weakest domain with a mean score of 41.45 (SD = 19.66), indicating a moderate level of impairment according to the classification of the ICD-10 [31], and 12 (41.4%) individuals can be classified as having severe deficits in this domain. The communication domain of the Vineland-II, with a median standard score of 22, emphasizing the floor effect described earlier, was impossible to use as a proxy for the conceptual domain.

**Table 2.** Descriptive results for intellectual disability domains, QOL and maladaptive behavior.


*3.2. Correlations between the Intellectual Disability Domains and QOL and Maladaptive Behavior*

Table 3 shows the Spearman's correlation coefficients between the three domains. The social and practical domains are significantly positively correlated (r = 0.783, *p* = 0.000), as are the practical domain and intellectual functioning (r = 0.453, *p* < 0.05). The social domain and intellectual functioning are not significantly correlated (see Table 3). There are neither significant correlations between adaptive behavior and self-reported QOL nor significant relationships between adaptive behavior and maladaptive behavior, although correlations with social functioning approached the trend level of significance (*p* < 0.1).


**Table 3.** Zero-order correlation matrix among intellectual, social and practical functioning variables; quality of life; and maladaptive behavior (N = 29).

Spearman's correlation coefficient: † *p* < 0.1; \* *p* < 0.05, \*\* *p* < 0.001.

#### *3.3. Intellectual Disability Domain Discrepancies*

Almost two-thirds of the individuals had an intellectual disability domain discrepancy between their intellectual functioning level and the social domain (n = 19, 65.5%), and more than half had an intellectual disability domain discrepancy between their intellectual functioning and the practical domain (n = 17, 58.6%). About one-quarter of the individuals had an intellectual disability domain discrepancy between the social and the practical domains (n = 7, 24.1%), where in all cases the social domain was the weaker domain. Thus, participants' social adaptive skills were often poorer than their intellectual functioning and practical adaptive skills.

#### *3.4. Associations between Intellectual Disability Domain Discrepancies and Self-Reported QOL as Well as Maladaptive Behavior (Independent Samples t-Tests)*

When comparing participants with and without intellectual disability domain discrepancies, high mean QOL was endorsed across both groups, and no significant differences were found (see Table 4). Participants with a discrepancy between intellectual functioning and social domain had significantly higher levels of internalizing maladaptive behavior than the other groups (T = 1.889, *p* < 0.05).

**Table 4.** Mean differences in self-reported QOL and internal and external maladaptive behavior with and without intellectual disability domain discrepancies (independent samples *t*-test).


Self-reported QOL is indicated by a 5-point scale; \* = *p* < 0.05; maladaptive behavior is reported as v-scale scores: <18 indicates average level, 18–20 indicates elevated level and 21–24 indicates a clinically significant level.

#### **4. Discussion**

The aim of this study was to describe profiles of intellectual disability and domain discrepancies in a sample of adults who are prelingually deaf with mild and borderline cognitive impairment and to explore how these domains of intellectual disability are related with each other and associated with self-reported QOL and maladaptive behavior. Our findings provide a first indication of possible intellectual disability domain discrepancies among individuals with deafness and intellectual disability and highlight the value—as well as potential challenges or limitations—of DSM-5 s definition of intellectual disability for the deaf population. Furthermore, we investigated differences between those with and without domain discrepancies with respect to QOL and internalizing and externalizing maladaptive behavior.

Heterogeneous intellectual disability profiles were highly common among our participants, with only 24% showing no discrepancy between intellectual and adaptive functioning. In nearly two-thirds of the sample, intellectual disability domain discrepancies could be observed between intellectual functioning (65.5%) and both the practical (58.6%) and the social domain (65.5%). Domain discrepancy between the practical and social domain occurred in about one-fourth of cases (24.1%). Less than half of the sample had adaptive functioning levels in the practical and social domains that corresponded to their level of mild intellectual impairment, whereas severe levels of impairment were evident in the practical domain in 28% of the sample and in the social domain in 41%.

In our sample, the results of the communication subscales of the VABS-II, which were adapted but not originally designed for use in deaf populations, indicated severe deficits in 65.5% of the sample. Due to pronounced floor effects, the values of this domain were used neither as an equivalent for the conceptual domain nor for further calculations. Language is an important driver of acquiring social and practical skills above a rudimentary basal level [36], and the huge discrepancies seen in our sample with cognitive impairments may be due to the force multiplier effect of communication deprivation on the development of adaptive skills in this vulnerable population. These findings underscore how severe early childhood language deprivation impacts communication skills [10], even in our population where great effort has been taken to optimize access to communication through sign language in adult life. Other research in individuals with intellectual disabilities could show a strong association between communicative competences and QOL [37], which highlights the importance of access to language and communication. In contrast to the findings of Sparrow et al. 2005, in the present study with a sample who is prelingually deaf with mild cognitive deficits, the socialization domain appeared to be the weakest [15].

The relationship between intellectual functioning and the practical domain in our sample was moderately significant (r = 0.453, *p* < 0.05) and in line with the results of the meta-analysis of Alexander and Reynolds [14], whereas no significant correlations between intellectual functioning and the social functioning domain could be found in our sample.

Tassé [13] and Simoes et al. [26] both found a positive correlation between adaptive behavior and QOL in samples with mild-to-moderate intellectual disability. A similar effect is hinted at in our sample, with correlations trending toward statistical significance between social functioning and self-reported QOL (r = 0.354, *p* < 0.1), as well as a negative correlation between social functioning and internalizing maladaptive behavior (r = −0.351, *p* < 0.1). Conversely, neither intellectual functioning nor adaptive functioning in the practical domain were correlated with QOL or maladaptive behavior, a comparable finding to that observed by Graves et al. [18], who found no correlation between adaptive behavior and quality of life in adults with Down syndrome.

Having a statistically significant adaptive domain discrepancy between intellectual and social functioning was significantly correlated with higher levels of internalizing maladaptive behavior, a phenomenon that has also been observed in Autism Spectrum Disorder (e.g., [24,38]). Pending replication, one is tempted to query whether social connection is the critical ingredient in the positive adjustment and emotional well-being of individuals who are deaf (see, e.g., [39,40]), as well as individuals who are deaf and have intellectual disabilities, and we will pursue and welcome further inquiry in this area.

#### *Limitations*

We must also note this study's limitations. First and foremost, this is a small sample drawn from a highly enriched therapeutic residential care setting for adults who are deaf and have intellectual disabilities. Since this sample has only borderline-to-mild cognitive impairment, we make no claim to generalizability to the larger population of adults who are deaf with intellectual disability; much larger replication trials are needed.

Second, we must query whether the VABS-II, widely regarded as the "gold standard" adaptive measure in the majority of cases, is the most appropriate measure for this population. We therefore encourage further research in the service of formulating an optimal assessment battery both to gauge and, we hope, discover how to unlock these individuals' full potential. We would emphasize the importance of developing and validating a communication scale that is independent of (or less conflated with) solely spoken and auditory modalities.

#### **5. Conclusions**

Clearly, the assessment of intellectual disability transcends IQ, and we hope to inspire efforts toward an even higher level of measure refinement and collaborative research between investigators and participants. Underscoring the DSM-5 s incorporation of adaptive functioning into its definition of intellectual disability, our population of participants who were prelingually deaf with mild cognitive impairments had a broad array of strengths and challenges. Intellectual functioning emerged as a relative strength, whereas almost half our participants had severe deficits in the social domain. Critically, a higher level of internalizing maladaptive behavior was observed in those participants with a domain discrepancy between their intellectual and social functioning. We must acknowledge that, even with our best efforts in providing accessible therapeutic communities in adulthood, deficits in the social domain could not be fully compensated after histories marked by severe trauma and deprivation. This finding constitutes a strong case for the early prevention of communicative and social deprivation by providing full access to spoken and/or signed communication. Nevertheless, nuanced measurement of adaptive skills gives us a good opportunity to identify and target malleable factors to improve QOL in individuals who are deaf and have intellectual disability more broadly.

**Author Contributions:** Conceptualization, J.F. (Johannes Fellinger) and M.D.; methodology, J.E.; validation, J.F. (Johannes Fellinger), D.H., J.F. (Jason Fogler), J.E. and M.D.; formal analysis, J.E.; investigation, M.D. and J.F. (Johannes Fellinger); data curation, M.D.; writing—original draft preparation, J.E., J.F. (Jason Fogler), M.D., D.H. and J.F. (Johannes Fellinger); writing—review and editing, J.E., J.F. (Jason Fogler), M.D., D.H. and J.F. (Johannes Fellinger); supervision, J.F. (Johannes Fellinger); project administration, M.D.; funding acquisition, J.F. (Johannes Fellinger). All authors have read and agreed to the published version of the manuscript.

**Funding:** Supported by Johannes Kepler Open Access Publishing Fund.

**Institutional Review Board Statement:** The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of the Hospital of St. John of God in Linz (approval number: 14-08).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study or their legal guardians.

**Data Availability Statement:** Data are not publicly available due to data protection issues.

**Acknowledgments:** We would like to thank Johannes Kepler Open Access Publishing Fund.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


## *Article* **Withdrawing Antipsychotics for Challenging Behaviours in Adults with Intellectual Disabilities: Experiences and Views of Prescribers**

**Gerda de Kuijper 1,2,\*, Joke de Haan 1, Shoumitro Deb <sup>3</sup> and Rohit Shankar <sup>4</sup>**


**Abstract:** International current best practice recommends the discontinuation of antipsychotics for challenging behaviours in people with intellectual disabilities (ID), due to lack of evidence of efficacy and risks of harmful side-effects. In clinical practice, discontinuation may be difficult. The aim of this study was to gain insight into prescribers' practice by investigating their experiences with the discontinuation of long-term antipsychotics for challenging behaviour. From professionals' associations thirty-four registered ID physicians, psychiatrists and specialist mental healthcare nurses were recruited who completed an online questionnaire in this survey–study. Almost all participants had attempted to deprescribe antipsychotics for their patients with ID. Sixty-five percent of participants achieved complete discontinuation in 0–25% of their patients, but none in over 50%. Barriers were a lack of non-pharmaceutical treatments for challenging behaviours and caregivers' and/or family concern. Seventy percent of participants indicated that their institutions had encouraged implementing their discontinuation policies in line with the new Dutch Act on Involuntary care and a new Dutch multidisciplinary guideline on problem behaviour in adults with ID. Support and facilitation of clinicians from institutions' managers and political and professional bodies may be helpful in further implementation of best practice in the treatment of challenging behaviour in people with ID.

**Keywords:** intellectual disabilities; antipsychotics; challenging behaviour; discontinuation; prescribers' policies; survey

#### **1. Introduction**

The rates of challenging behaviours displayed by people with intellectual disabilities (ID) vary from 18% in community populations to 85% in people with profound ID who live in institutions [1–3]. The onset and maintenance of challenging behaviours in individuals with ID are associated with biological, psychological and environmental factors [1,2,4–6]. Behaviours include outwardly directed behaviours like aggressive-destructive behaviour, inappropriate (sexual) behaviour and disruptive behaviours. It also includes hyperactivity, irritability, lethargy and self-injurious, stereotypic and withdrawn behaviours [2,7,8]. Challenging behaviours may vary in intensity and be persistent [9–12]. When individuals present with challenging behaviour, this may negatively influence their quality of life [13,14] and social participation [15]. Diagnosis and management require a multidisciplinary and integrative approach as the causes of these behaviours are multi-factorial (physical, genetic, psychiatric, psychological, social, environmental, etc.) [3,6,16].

**Citation:** de Kuijper, G.; de Haan, J.; Deb, S.; Shankar, R. Withdrawing Antipsychotics for Challenging Behaviours in Adults with Intellectual Disabilities: Experiences and Views of Prescribers. *Int. J. Environ. Res. Public Health* **2022**, *19*, 17095. https://doi.org/10.3390/ ijerph192417095

Academic Editor: Paul B. Tchounwou

Received: 11 October 2022 Accepted: 15 December 2022 Published: 19 December 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

Psychotropic drugs, especially antipsychotics, are often prescribed for the management of challenging behaviours [17–22]. Significantly higher levels of antipsychotic drug prescribing occur to manage challenging behaviour in people with ID and/or autism [23]. However, the effectiveness of psychotropic drugs for the treatment of challenging behaviours in people with ID has not been proven [24–27]. Moreover, in this population, the risk of side-effects like diabetes, cardio-vascular disorders, sedation and movement disorders is considerable, especially in the case of long-term use of antipsychotics [28–31]. It is recommended by all good practice guidelines that the treatment of challenging behaviours should be, in the first place, non-pharmacological, i.e., psychosocial and behavioural. Practitioners should only prescribe psychotropic drugs after careful weighing of the potential positive and negative effects of this medication and preferably just for the short-term (max. 6–12 weeks). For example, prescription may be beneficial to overcome crisis situations when the person or others are at risk of serious harm, or in conjunction with non-pharmacological interventions [16,32,33].

Although it is recommended that long-term off-label psychotropic drug prescription should be discontinued especially antipsychotics, they are still frequently prescribed for the treatment of challenging behaviours [34–36]. This may, at least partially be, because of failures of successful discontinuation of antipsychotics due to worsening of behaviour upon drug withdrawal [37]. Besides user-related factors, like the occurrence of withdrawal symptoms, symptoms of previously not-recognized mental or physical disorders or other health problems, and staff-related factors, are associated with unsuccessful withdrawal of antipsychotics [38]. For example, staff may experience difficulties in the management of changes in their clients' behaviour, may have negative feelings towards clients' behaviour or lack knowledge or have unrealistic expectations about the effects of psychotropic drugs [39,40]. The involvement of all stakeholders, including the patients and their relatives, seems a key-element in the achievement of successful changes in prescription policies [41].

In some countries, initiatives have been taken to facilitate the deprescribing of antipsychotics for challenging behaviours. For example, in the UK, the "stopping over medication of people with a learning disability, autism or both with psychotropic medicines" (STOMP) is now incorporated within the NHS England long-term plan [42]. The development of a structured pathway with the involvement of all stakeholders led to successful discontinuation in 46% of cases and dose reductions of over 50% in another 11% [43]. A survey among UK psychiatrists about changes in prescription policies as a result of the STOMP initiative showed that the prescriptions practice has changed. The UK psychiatrists are less likely to initiate new prescriptions of antipsychotics. However, complete antipsychotic discontinuation in over 50% of their patients was achieved by only 4.5% of responding psychiatrists [44].

In The Netherlands, Vilans, a knowledge centre on long-term care has conducted a project (2015–2019) to reduce inappropriate psychotropic prescribing in the elderly with dementia and in people with ID and high care needs. In this project, an e-learning on psychotropic drug use in people with ID for support professionals has been developed [45]. Moreover, in The Netherlands, in December 2019, a new multidisciplinary guideline on challenging behaviour [46] and, in January 2020, a new Dutch Act on Involuntary care was published. In both, the prescription of psychotropic drugs for challenging behaviours outside guideline recommendations is regarded as restricted practice. A study among Dutch ID physicians on their experiences with the guideline and new Act showed that they regarded the Act as supportive of reducing the off-label prescriptions of psychotropics. However, because of organisational difficulties, the feasibility of implementing the guideline and new Act is not always possible in practice [47].

In The Netherlands, there are 250 registered ID physicians. Most of them take care of people with ID and complex needs, including people with multiple disabilities and/or behavioural problems.

There are approximately 15–20 ID specialized mental healthcare outpatient clinics spread over The Netherlands. Psychiatrists in mainstream mental healthcare organizations or who have their own private practice may also be consultants at ID institutions. In Dutch mental healthcare, specialist nurses monitor the use of the psychotropic drugs and are authorized to stop or change a prescription in consultation with the psychiatrist who initiated the prescription. In community care, GPs may provide repeat prescriptions and/or the monitoring of psychotropic drug use; however, mostly, they refer to ID physicians or specialized ID mental healthcare when discontinuation or change in medication is necessary. The total number of mental healthcare professionals affiliated with the Dutch ID mental healthcare outpatient clinics, authorized to prescribe psychotropic medication, is unknown. We estimate 100–150 such prescribers based on the number of ID mental healthcare clinics and consultant -psychiatrists specializing in people with ID in The Netherlands.

The present study aimed to gather information about facilitators and barriers to the successful discontinuation of antipsychotic drugs when used for challenging behaviours in people with ID. We conducted a survey, similar to the UK survey [44], about experiences with antipsychotic drug discontinuation among ID physicians, psychiatrists and specialist nurses in The Netherlands who were responsible for the psychotropic drug prescriptions for their patients with ID. We also asked whether their antipsychotic prescribing practice had changed because of the new guideline and new Act.

#### **2. Materials and Methods**

#### *2.1. Design*

This was a cross-sectional study including a questionnaire survey among Dutch prescribers of psychotropic medications for people with ID.

#### *2.2. Participants and Settings*

Participants were registered ID physicians affiliated with ID institutions and institutions' outpatient clinics or having their own practice, and psychiatrists or specialist nurses affiliated with ID-specialized mental healthcare outpatient clinics or having their own practice.

#### *2.3. Materials*

The questionnaire items were adapted for the Dutch ID healthcare system from a survey which was developed in a recent study of UK psychiatrists' views on the rationalization of psychotropic use among people with ID [44]. The survey answer options of items were multiple choice with an open field for comments. Supplementary Materials shows the items of the questionnaire and corresponding answer options. The forty-two questionnaire items were grouped under five themes similar to those in the UK survey. These themes included:


#### *2.4. Procedures*

The participants were recruited from the ID physicians affiliated with the Dutch Intellectual Disabilities physicians' association (NVAVG), psychiatrists affiliated with the Dutch Psychiatrists Association (NVvP) and nurses affiliated with the Dutch specialist nurse care association (VenVNVS). We had to approach all the Dutch psychiatrists and specialist nurses as there is no Register of those who specifically specialize in ID mental healthcare.

The survey was open between 19 February and 1 May 2021. A reminder was sent three weeks before the closing date. A news item with the link to the questionnaire was also placed on the websites of the professionals' associations. Members of the professional organisations/potential responders received an explanatory letter with a link to the program Qualtrics where they could fill in the questionnaire. On average, it took participants 30–45 min to complete the questionnaire.

#### *2.5. Ethics*

All responders in the survey participated voluntarily. All data were collected, stored, and safeguarded anonymously, according to the European Act on Protection of Personal Information, in The Netherlands, which was ratified in 2018.

#### *2.6. Analyses*

SPSS 26 was used to analyse the survey data. Descriptive statistics were used to calculate frequencies of respondents' characteristics and answer categories as per the multiple-choice questions. Pearson Chi-Square was used to compare characteristics and answer categories between a group consisting of ID physicians on the one hand and psychiatrists and ID specialist mental healthcare nurses on the other.

#### **3. Results**

We present the results by the forming of two clusters encompassing the five themes of the questionnaire as described under Methods/Materials (themes 1 and 2, and themes 3, 4 and 5 respectively). The data and analyses of all the 42 questions and corresponding answers (see Supplementary Materials) are available on request.

#### *3.1. Participants and Prescription Patterns (Themes 1 and 2 of the Questionnaire)*

Twenty-one of the 250 ID physicians registered in The Netherlands and thirteen of the estimated 100–150 mental healthcare professionals prescribing psychotropics to patients with ID (i.e., psychiatrist or specialist mental healthcare nurse) completed the questionnaire (response rate of 8.5% and estimated response rate 8.6–13%, respectively). The exact response rate of the ID mental healthcare professionals could not be calculated because there are no data on the total number of those in ID mental healthcare in The Netherlands.

Twelve (35%) of the total 34 participants reported that their working experience in the field was for less than 10 years, 10 (30%) had worked in the field for 10–19 years, 11 (32%) 20–29 years, and 1 (3%) for more than 30 years. Five (15%) of the participants stated that 0–25% of their patients, 17 (50%) that 25–50%, 5 (14%) that 50–75% and 4 (12%) that 75–100% of their patients with ID were prescribed antipsychotics. Three participants (9%) could not provide the percentage.

#### *3.2. Participants' Policies and Experiences (Themes 3, 4 and 5 of the Questionnaire)*

Table 1 shows the results of participants' practice and experience regarding the deprescribing of antipsychotics in their patients with ID. Participants attempted to deprescribe antipsychotics in a variable part of their patients. In Table 1, the number and percentage of participants is shown who attempted to deprescribe antipsychotics in a certain proportion of their patients.

A considerable number of participants did not attempt to withdraw antipsychotics in their patients with ID and challenging behaviour when there was a clear diagnosis of a psychiatric disorder which justified the prescription. This diagnosis was confirmed recently (i.e., in the two preceding years) in more than half of the total number of respondents (55%). A significantly lesser proportion of ID physicians (38%) compared with ID mental healthcare professionals (ID psychiatrists and nurses) (83%) confirmed the psychiatric diagnosis (*p* = 0.01). Only eight (24%) prescribers confirmed psychiatric diagnosis themselves (ID physicians 10%, ID healthcare professionals 50%, the difference not significant). In addition, there were differences between these two groups with regard to the mean duration of the discontinuation trajectory, which was, on average, significantly longer in ID physicians (0–6 months, 9% in ID physicians versus 8% in ID mental healthcare professionals, 6–12 months, 24% versus 77%, 12–18 months, 47% versus 0%, and >18 months in 19% versus 15%, respectively, *p* = 0.01)

**Table 1.** Practice and experience of intellectual disability (ID) physicians and ID mental healthcare professionals # who completed the survey (N = 34 participants) in deprescribing antipsychotics for challenging behaviours.

