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Article

Frailty in Community-Dwelling Adults Aged 40 Years and over with Type 2 Diabetes: Association with Self-Management Behaviors

1
Department of Clinical Pharmacy and Pharmacy Administration, School of Pharmacy, Fudan University, Shanghai 201203, China
2
Minhang Hospital & School of Pharmacy, Fudan University, Shanghai 201199, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Int. J. Environ. Res. Public Health 2022, 19(15), 9092; https://doi.org/10.3390/ijerph19159092
Submission received: 19 May 2022 / Revised: 21 July 2022 / Accepted: 22 July 2022 / Published: 26 July 2022

Abstract

:
Background: Evidence is lacking on risk factors for frailty and prefrailty and their relationship with self-management behaviors in patients ≥40 years of age with type 2 diabetes. Methods: Participants were selected as a cross-sectional cohort at five communities in Shanghai, China during January–March 2021. The modified FRAIL scale and the Summary of Diabetes Self-Care Activities (SDSCA) measure were used. Results: Of the 558 participants, 10.2% were classified as frailty and 34.1% as prefrailty. The prevalence of frailty was higher in males than in females (p = 0.009), whereas females were associated with higher odds of prefrailty (aOR 1.67, 95% CI [1.08–2.60]). Multimorbidity, ≥3 chronic diseases, and hospitalization in the past year were considered risk factors for both frailty and prefrailty. Each point earned on SDSCA and physical activity were associated with lower odds of frailty (aOR 0.95, 95% CI [0.92–0.98]) and prefrailty (aOR 0.52, 95% CI [0.31–0.85]), respectively. Frail participants performed significantly worse self-care practice than prefrail and non-frail ones, especially on diet, physical activity, and medication adherence (p < 0.001). Conclusions: Frail patients ≥40 years of age with type 2 diabetes reported poorer self-care performance. Further interventional studies are warranted to clarify their causal relationship.

1. Introduction

Diabetes mellitus is a major public health issue across the world, which imposes a considerable socioeconomic burden worldwide [1]. China is now the world’s largest diabetes endemic country. An estimated 108 million people aged from 20 to 79 years in China had diabetes in 2021, by far the highest number of any country [2]. By 2045, the number is anticipated to reach 147 million [3]. The prevalence was even higher among the elderly at 22.5% [4]. Therefore, the care of patients with diabetes is of great importance with national-level prioritization.
Frailty is a status of decreased physiological reserve that is common among the middle-aged and elderly population [5]. Fried et al. described the most commonly used definition of frailty as the presence of three or more of the following characteristics: self-reported exhaustion, muscle weakness, slow walking speed, low physical activity, and unintentional weight loss [5,6]. Many studies have proven that frail people were at greater risk of disability, dependence, hospitalization and death [7,8,9,10]. Frailty is complex and multifaceted, often coexisting with other diseases, such as heart failure, that share common pathophysiological pathways and are associated with adverse outcomes that should be adequately assessed and comprehensively intervened [11,12]. Diabetes was considered one of the risk factors for frailty, the presence of which, in turn, was an important contributor to poor prognosis in older adults with diabetes [13,14]. Frail diabetic patients also appeared to have higher mortality rates than robust patients [15]. Although the prevalence of frailty increases with age, frailty can also affect younger people [16]. Studies have suggested that frailty was a preventable and reversible condition [6], particularly at an early stage [17,18], suggesting timely identification and management of frailty may be important for improving diabetes outcomes from the clinical point of view. Despite the potential importance of frailty in the middle-aged population, studies mostly relied on patients over 65 years old to complete the assessment. The prevalence of frailty and its subclinical state, prefrailty, in relatively young populations such as middle age remains to be determined. This is the first attempt to evaluate the frailty status of patients with diabetes dwelling in Chinese community, involving a much larger age range than previous studies.
Self-management behaviors refer to the actions taken by patients to deal with the disease based on their knowledge and skills [19]. This is especially vital for patients with chronic diseases such as hypertension and diabetes, because in addition to following their doctor’s orders, they must take personal responsibility toward their illnesses in daily lives. They are the real masters of their own health and well-being, and decide about whether to change lifestyles, exercise, eat healthy, and take medications [20]. Rigorous diabetes self-care practices have been shown to be effective in controlling blood glucose, preventing complications, and reducing long-term morbidity and mortality [21,22,23,24,25]. However, due to decline in self-control and memory, older adults often struggle to manage these tasks. They tend to cling to false beliefs and slip back into bad habits, making them particularly vulnerable to adverse health outcomes [26]. Their amount of self-care was significantly influenced by factors such as gender, education level, economic status, social support, and the duration of the disease [27]. On the other hand, although the evidence is scant, young adults with type 2 diabetes have been shown to perform worse than their older counterparts on some aspects of self-management, especially medication adherence [28,29]. Therefore, studies targeting younger patients are also warranted.
There is some evidence that high levels of self-care are associated with a lower incidence of frailty among older patients with cardiovascular conditions [30]. However, to the best of our knowledge, such correlation analysis is still lacking in diabetes. Given the rising prevalence of diabetes and the aging population in China, there is an urgent need to clarify it. The purpose of this study was to explore the prevalence and risk factors for frailty and prefrailty, and to evaluate the relationship between frailty and self-management behaviors in community-dwelling Chinese aged ≥40 years of age with diabetes.

2. Methods

2.1. Design, Setting, and Participants

This was a cross-sectional study and all participants were recruited through convenience sampling from the outpatient units of five community health centers in Shanghai, China, between January 2021 and March 2021. Experienced interviewers (i.e., general physicians, pharmacists, and nurses) administered questionnaires face-to-face to collect data on characteristics and medical history. Assistance (i.e., reading questions) was offered to participants who cannot fill out the questionnaire by themselves (i.e., having poor eyesight). The inclusion criteria were people ≥40 years of age, diagnosed with type 2 diabetes ≥3 months prior to the study, and able to provide informed consent. People with severe diabetes-unrelated organ damage, cognitive impairment, dementia, psychiatric disorders, and those unwilling to respond to the questionnaire were excluded. This study was approved by the Ethics Committee of Minhang Hospital (No. 2020-048-01K). Written informed consent was obtained from all participants.

2.2. Instruments for Data Collection

Frailty status was evaluated using a modified FRAIL scale in this study. The FRAIL scale is a time- and cost-effective frailty screening instrument with acceptable sensitivity and specificity compared to the commonly used screening tool, the frailty phenotype (FP) [5,31]. The scale contains five questions to assess the presence of fatigue, muscle resistance, ambulation, disease burden, and weight loss. Scoring is 0 for “no” and 1 for “yes”. Participants with a score ≥3 were classified as frail, those with a score of 1–2 as prefrail, and those with a score of 0 as non-frail [5].
The Chinese version of Summary of Diabetes Self-Care Activities (SDSCA) measure, a self-reported questionnaire with high reliability and validity, was employed to assess the frequency of performing self-care activities over the last seven days [32,33]. The SDSCA is one of the most common and widely used measures by clinicians [34]. The instrument consists of 12 items, covering six important domains of self-care practices: diet (general and special), physical activity, medication adherence, blood glucose monitoring, foot care, and smoking [33,35]. Except for a true-false question about smoking, each item scores on a scale of 0 to 7 with higher scores indicating better self-management. The total score of the questionnaire was 77. In order to help better describe the self-care performance, we defined a score ≥62 as “excellent”, 39–61 as “moderate”, and ≤38 as “poor” in this study. The Cronbach’s alpha coefficient (excluding the item on smoking) was 0.732, indicating acceptable internal consistency. The Kaiser-Meyer-Olkin value of 0.625 indicated an acceptable score with a significant Bartlett’s test of Sphericity (p < 0.001).
Copies of the modified FRAIL and SDSCA scale were distributed to diabetic patients who met inclusion criteria during outpatient encounters. The questionnaire survey was designed to obtain other self-reported information as well, including age, gender, height, weight, education level, socioeconomic, marital and cohabitation status, alcohol intake, smoking, duration of diabetes, medication use, and history of comorbidities and chronic diseases. Biochemical parameters such as HbA1c and fasting blood glucose (FBG) were directly retrieved from the hospital information system (HIS). All data were anonymized.

2.3. Statistical Analysis

The data were presented as number (percentage) or means (standard deviation). For categorical variables, the chi-square test and Fisher’s exact test were used to test the difference among non-frail, prefrail, and frail persons. For continuous variables, independent t-test and analysis of variance were used. A multinomial logistic regression model was used to compare sociodemographic characteristics and the SDSCA score of frail or pre-frail participants with non-frail participants. All significant variables in descriptive statistics were included in the final model. Adjusted odds ratios (aOR) and 95% confidence interval (CI) were calculated for the frail and prefrail groups, respectively, compared to the reference group (non-frail). The significance level was set at p < 0.05. All statistical analyses were performed by using the SPSS software, version 23 (IBM, Armonk, NY, USA).

3. Results

3.1. Characteristics of Study Sample and Prevalence of Frailty and Prefrailty

We included 558 participants with type 2 diabetes from the community. The majority (50.4%) were males, with a mean age of 69.1 ± 9.0 years. Most of them were unemployed or retired (91.4%), married (87.6%), and living with family or partners (95.0%); only 5.2% participants had a bachelor’s degree or higher. The mean duration of diabetes was 12.3 ± 7.8 years (Table 1).
The prevalence of frailty and prefrailty were 10.2% (n = 57) and 34.1% (n = 190), respectively. As shown in Table 1, the prevalence of frailty in men was more than twice that in women, but the prevalence of prefrailty was higher in women (p = 0.009). The proportion of frailty significantly increased with age, unemployment, HbA1c, number of comorbidities, chronic diseases and medications, and disease duration (p < 0.05). However, changes in the prevalence of prefrailty did not fully conform to this pattern. In addition, the frail group had markedly lower levels of physical activity, alcohol consumption, and hospitalization in the past year compared to other two groups.

3.2. Analysis of Self-Care Performance

Among the 558 participants, the mean SDSCA score was 39.03 ± 14.03, of which 54.8% (n = 306) had poor self-management, 36.2% (n = 202) had moderate self-management, and only 9.0% (n = 50) had excellent self-management. According to Table 2, participants were most likely to adhere to medication (5.34 ± 2.64), followed by diet (4.59 ± 1.51), and least likely to monitor blood glucose (1.91 ± 1.99). Compared with the prefrail and non-frail participants, the frail participants had a significantly lower mean SDSCA score of only 30.75 ± 8.60, indicating that their self-care performance was the least satisfactory, especially in diet, physical activity, and medication adherence (p < 0.001).
As shown in Table 3, females scored significantly higher than males (p = 0.018). In addition, those with higher education levels, lower HbA1c, and fewer comorbidities also had significantly higher SDSCA scores (p < 0.05). There were no differences when participants were stratified by any other variables.

3.3. Risk Factors for Frailty/Prefrailty and Their Relationship with Self-Management Behaviors

We then used multinomial logistic regression analysis to assess the relationship between frailty and self-management behaviors, as well as the risk of developing frailty and prefrailty (Table 4). Overall, patients with multimorbidity or ≥3 chronic diseases were more likely to be frail and prefrail compared to other groups, except for 1–2 vs. ≥3 chronic diseases that did not differ in the odds of prefrailty. Hospitalization in the past year was also of concern (frail: aOR 4.67, 95% CI [1.96–11.14]; prefrail: 4.27, [2.27–8.03], respectively). Female gender was considered another risk factor for prefrailty (aOR 1.67, 95% CI [1.08–2.60]). In contrast, physical activity worked as a protective factor for prefrailty (aOR 0.52, 95% CI [0.31–0.85]), and each point scored on the SDSCA scale was associated with lower odds of frailty (aOR 0.95, 95% CI [0.92–0.98]).

4. Discussion

In this cross-sectional study, we found that 10.2% and 34.1% of participants met the criteria for frailty and prefrailty, respectively, using the modified FRAIL scale. Although previous studies have noted that people with diabetes were more prone to frailty than those without diabetes, the reported prevalence in the diabetic population varied widely (ranging from 5% to 48%) [36,37]. In line with previous studies [38,39,40], our study showed that the prevalence of frailty significantly increased with age (p < 0.001). The mean age of our sample population was 69.1 ± 9.0 years. The correlation between frailty and age greatly heightened its importance in the context of an ageing global population [41]. Several studies also revealed that people with diabetes were more likely to become frail at a younger age [37,42]. In addition to age, Table 1 demonstrated that the prevalence of frailty also increased with unemployment, HbA1c, number of comorbidities, chronic diseases and medications, and disease duration (p < 0.05). These findings may help identify those at greatest risk and those most likely to benefit from optimization of treatment regimens [18,43].
In addition to the frail, individuals with prefrailty also accounted for a considerable proportion (34.1%) in this study. Since the transition between different frailty states was reversible, prefrailty, the subclinical phase of frailty, should be identified and intervened in as early as possible. The earlier screening and intervention begin, the greater the benefit to patients and healthcare systems [18]. Moreover, we noticed that the prevalence of prefrailty increased with age, unemployment, and number of comorbidities, chronic diseases, and medications such as frailty (Table 1). Previous studies revealed that risk factors such as older age, stroke, lower cognitive function, osteoarthritis, and hospitalizations were strongly associated with deterioration in frailty status among prefrail patients [42]. In support of this conclusion, our result showed that multimorbidity, ≥3 chronic diseases, and hospitalization in the past year were independent risk factors for both frailty and prefrailty (Table 4). An earlier meta-analysis of community-dwelling diabetic patients found that the pooled ORs for hospitalization due to frailty and prefrailty were 5.18 (95% CI 2.68–9.99) and 2.15 (95% CI 1.30–3.54), respectively [44], which was consistent with our results of 4.67 (95% CI 1.96–11.14) and 4.27 (95% CI 2.27–8.03). At the same time, although diabetes has been shown to be associated with fragility fractures in middle-aged men (relative risk [RR] 2.38, 95% CI [1.65–3.42]) and women (RR 1.87, 95% CI [1.26–2.79]) [45], in this study, being female was only considered a risk factor for prefrailty (aOR 1.67, 95% CI [1.08–2.60]), but not frailty (aOR 0.88, 95% CI [0.42–1.81]). Contrastingly, physical activity was related to lower odds of prefrailty (aOR 0.52, 95% CI [0.31–0.85]), which was also consistent with the literature [46,47].
In this study, the mean score of the SDSCA measure was 39.03 ± 14.03. Most of the participants had poor or moderate self-care performance; only 9.0% could be classified as excellent by our criteria. This finding was consistent with other research indicating that people with diabetes in many countries had poor self-care habits [48,49]. Not surprisingly, frail participants reported significantly worse self-care performance than those who were classified as prefrail and non-frail, especially in diet, physical activity, and medication adherence (p < 0.001, Table 2). This was also supported by the results of regression analysis shown in Table 4 (aOR 0.95, 95% CI [0.92–0.98]).
Of the five domains of SDSCA, BGM had the lowest mean score (1.91 ± 1.99), indicating it was the most difficult task for participants to accomplish. Similar findings have been documented [50,51,52,53]. Although self-management were already known to be particularly important for elderly diabetic patients, most Chinese patients did not perform BGM as recommended [54]. One explanation for this may be the cost of testing devices. The population included in our study had relatively low levels of education and employment, and may not recognize the importance of BGM nor afford the additional cost. However, despite having the lowest score, the frail and prefrail group showed a paradoxical, insignificant, but higher BGM score compared to the non-frail group (Table 2). This could be partly explained by the perceived support from family or cohabitants for handling testing tools.
Contrastingly, Gatt et al. [55] claimed that physical activity was the least self-care activity carried out by participants. The overall level of physical activity in this study was fine, probably because the rural population was more physically active on a daily basis, however it should be noted that frail participants scored significantly lower (p < 0.001). One possible reason for this contradiction is the inactivity of these patients caused by the COVID-19 quarantine and lockdown.
With regard to the domain where participants performed most satisfactorily, the findings varied considerably. Our results were consistent with most of the literature [50,52,53,55], which reported the highest score for medication taking, whereas Jackson et al. [51] declared that general diet was the most common self-care activity. Management of diabetes requires long-term compliance. However, according to our results, although the participants’ medication adherence was great overall with a highest mean SDSCA score of 5.34 ± 2.64, frail patients had poorer performance than other groups (p < 0.001). Similarly, although diet was the second-best self-management behavior overall (SDSCA score: 4.59 ± 1.51), frail patients had significantly worse eating habits than non-frail and prefrail ones (p < 0.001). Most participants reported that their meals were cooked at home. Frail people with difficulty getting out of the house were less likely to regularly purchase foods that are not easy to preserve, such as fruits or vegetables. This may be why the frail participants scored lower on diet. As shown in Table 3, sociodemographic and clinical characteristics including male gender, lower education level, higher HbA1c, and more comorbidities were significantly associated with poor self-care performance (p < 0.05). Similar findings have been observed in previous surveys [48,49,56,57]. This evidence provided references for individualized clinical, academic, and behavior interventions.
Our study assessed the frailty status and self-care performance in community-dwelling diabetic patients. To our knowledge, this is the first study to simultaneously explore the prevalence and risk factors of frailty and prefrailty in Chinese patients aged ≥40 years with type 2 diabetes, and to evaluate their association with self-management behaviors. On one hand, loss of self-efficacy may generally accelerate the transition to frailty [15]. The evidence is that diabetic patients with higher self-efficacy have demonstrated better self-management behaviors in diet, exercise, BGM, and taking medication [53]. On the other hand, frail patients may face great obstacles in performing self-care activities, for instance, disability, unexpected falls, fractures, worsening mobility, and cognitive decline [58]. Our findings suggested that good habits in diet, physical activity, and medication adherence may markedly help reduce possibility of frailty among diabetic patients, which should be emphasized in future management of diabetes. Our data were collected during the COVID-19 era when the public healthcare system was almost facing stagnation. Our results underscored the critical role of self-management behaviors in maintaining health and vitality in times of scarce community medical resources.
However, we do realize that our study has several limitations. First, the participants were selected from five community health centers in Shanghai by convenience sampling, which potentially reduced the representativeness of the sample population. Certain subgroups were underrepresented in this study, such as those with a bachelor’s degree or higher (only 5.2%), those who lived alone (5.0%), and those who received lifestyle interventions without taking any hypoglycemic drugs (3.4%). Thus, our findings should not be directly generalized to all patients with diabetes. Selection biases may also influence our conclusions as the participants may be more willing to engage in treatment and self-care than those who did not join the survey. Furthermore, as health authorities discouraged in-person visits during the COVID-19 pandemic, some eligible patients may be prevented from participating in the study, thus introducing sampling bias. Second, our findings were based on cross-sectional data. Therefore, causality could not be ascertained between frailty status and self-management behaviors. Although the Cronbach alpha coefficient was acceptable (0.732), the construct validity of the SDSCA measure used was not assessed considering the relatively low test-retest reliability [59]. Moreover, we neither recruited severely ill people nor compared the results to healthy people in this study, which may underestimate the prevalence of frailty as well as overestimate the overall self-care performance. Further prospective studies involving a larger and more general population are warranted.

5. Conclusions

This study provided epidemiological evidence for the prevalence of frailty and prefrailty among community-dwelling diabetic adults aged ≥40 years. Multiple sociodemographic and clinical variables have been proven to play key roles in the development of frailty and prefrailty. There was a significantly negative correlation between frailty and self-management behaviors. Further research should focus on identifying ways to enhance self-care activities in order to delay the onset of frailty, and clarifying possible causal relationships between them.

Author Contributions

Conceptualization: Z.T.; Data curation: C.S.; Formal Analysis: W.T. and Z.F.; Funding acquisition: Z.T. and X.X.; Investigation: C.S.; Methodology: Z.T. and Z.F.; Project administration: Z.T. and B.H.; Resources: Z.T. and X.X.; Software: Z.F.; Supervision: B.H.; Validation: B.H.; Writing—original draft: Z.F. and C.S.; Writing—review and editing: Z.T. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the start-up grant for Zhijia Tang by Fudan University (No. JIF301001Y) and the Key Innovative Team of Shanghai Top-Level University Capacity Building in Clinical Pharmacy and Regulatory Science at Shanghai Medical College, Fudan University (HJW-R-2019-66-19) from Shanghai Municipal Education Commission.

Institutional Review Board Statement

The study was approved by the Ethics Committee of Minhang Hospital (No. 2020-048-01K).

Informed Consent Statement

Written informed consent has been obtained from the patients to publish this paper.

Data Availability Statement

Data associated with the findings of this study are included in the article and are available from the author upon reasonable request.

Acknowledgments

We acknowledge all the participants in this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pena-Longobardo, L.M.; Oliva-Moreno, J.; Zozaya, N.; Aranda-Reneo, I.; Trapero-Bertran, M.; Laosa, O.; Sinclair, A.; Rodriguez-Manas, L. Economic evaluation of a multimodal intervention in pre-frail and frail older people with diabetes mellitus: The MID-FRAIL project. Expert Rev. Pharmacoecon. Outcomes Res. 2021, 21, 111–118. [Google Scholar] [CrossRef] [PubMed]
  2. Zhang, W. Estimated Number of People with Diabetes Mellitus in China in 2021, by Age Group. Available online: https://www.statista.com/statistics/1118008/china-diabetic-population-by-age-group/#statisticContainer (accessed on 13 July 2022).
  3. Thomala, L.L. Diabetes in China—Statistics & Facts. Available online: https://www.statista.com/topics/6556/diabetes-in-china/#dossierKeyfigures (accessed on 13 July 2022).
  4. Xu, Y.; Wang, L.; He, J.; Bi, Y.; Li, M.; Wang, T.; Wang, L.; Jiang, Y.; Dai, M.; Lu, J.; et al. Prevalence and control of diabetes in Chinese adults. JAMA 2013, 310, 948–959. [Google Scholar] [CrossRef] [PubMed]
  5. Thompson, M.Q.; Theou, O.; Tucker, G.R.; Adams, R.J.; Visvanathan, R. FRAIL scale: Predictive validity and diagnostic test accuracy. Australas. J. Ageing 2020, 39, e529–e536. [Google Scholar] [CrossRef] [PubMed]
  6. Fried, L.P.; Tangen, C.M.; Walston, J.; Newman, A.B.; Hirsch, C.; Gottdiener, J.; Seeman, T.; Tracy, R.; Kop, W.J.; Burke, G.; et al. Frailty in older adults: Evidence for a phenotype. J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56, M146–M156. [Google Scholar] [CrossRef] [PubMed]
  7. Umegaki, H. Sarcopenia and frailty in older patients with diabetes mellitus. Geriatr. Gerontol. Int. 2016, 16, 293–299. [Google Scholar] [CrossRef]
  8. Cesari, M.; Calvani, R.; Marzetti, E. Frailty in Older Persons. Clin. Geriatr. Med. 2017, 33, 293–303. [Google Scholar] [CrossRef] [PubMed]
  9. Soysal, P.; Veronese, N.; Thompson, T.; Kahl, K.G.; Fernandes, B.S.; Prina, A.M.; Solmi, M.; Schofield, P.; Koyanagi, A.; Tseng, P.T.; et al. Relationship between depression and frailty in older adults: A systematic review and meta-analysis. Ageing Res. Rev. 2017, 36, 78–87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Kojima, G.; Iliffe, S.; Walters, K. Frailty index as a predictor of mortality: A systematic review and meta-analysis. Age Ageing 2018, 47, 193–200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. de Sire, A.; Ferrillo, M.; Lippi, L.; Agostini, F.; de Sire, R.; Ferrara, P.E.; Raguso, G.; Riso, S.; Roccuzzo, A.; Ronconi, G.; et al. Sarcopenic Dysphagia, Malnutrition, and Oral Frailty in Elderly: A Comprehensive Review. Nutrients 2022, 14, 982. [Google Scholar] [CrossRef] [PubMed]
  12. Pandey, A.; Kitzman, D.; Reeves, G. Frailty Is Intertwined With Heart Failure: Mechanisms, Prevalence, Prognosis, Assessment, and Management. JACC Heart Fail. 2019, 7, 1001–1011. [Google Scholar] [CrossRef]
  13. Kitamura, A.; Taniguchi, Y.; Seino, S.; Yokoyama, Y.; Amano, H.; Fujiwara, Y.; Shinkai, S. Combined effect of diabetes and frailty on mortality and incident disability in older Japanese adults. Geriatr. Gerontol. Int. 2019, 19, 423–428. [Google Scholar] [CrossRef]
  14. Assar, M.E.; Laosa, O.; Rodriguez Manas, L. Diabetes and frailty. Curr. Opin. Clin. Nutr. Metab. Care 2019, 22, 52–57. [Google Scholar] [CrossRef]
  15. Yanase, T.; Yanagita, I.; Muta, K.; Nawata, H. Frailty in elderly diabetes patients. Endocr. J. 2018, 65, 1–11. [Google Scholar] [CrossRef] [Green Version]
  16. Barnett, K.; Mercer, S.W.; Norbury, M.; Watt, G.; Wyke, S.; Guthrie, B. Epidemiology of multimorbidity and implications for health care, research, and medical education: A cross-sectional study. Lancet 2012, 380, 37–43. [Google Scholar] [CrossRef] [Green Version]
  17. Gill, T.M.; Gahbauer, E.A.; Allore, H.G.; Han, L. Transitions between frailty states among community-living older persons. Arch. Intern. Med. 2006, 166, 418–423. [Google Scholar] [CrossRef]
  18. Hanlon, P.; Nicholl, B.I.; Jani, B.D.; Lee, D.; McQueenie, R.; Mair, F.S. Frailty and pre-frailty in middle-aged and older adults and its association with multimorbidity and mortality: A prospective analysis of 493 737 UK Biobank participants. Lancet Public Health 2018, 3, e323–e332. [Google Scholar] [CrossRef]
  19. Yang, J.; Zhang, Z.; Zhang, L.; Su, Y.; Sun, Y.; Wang, Q. Relationship Between Self-Care Behavior and Cognitive Function in Hospitalized Adult Patients with Type 2 Diabetes: A Cross-Sectional Study. Diabetes Metab. Syndr. Obes. 2020, 13, 207–214. [Google Scholar] [CrossRef] [Green Version]
  20. Ebrahimi Belil, F.; Alhani, F.; Ebadi, A.; Kazemnejad, A. Self-Efficacy of People with Chronic Conditions: A Qualitative Directed Content Analysis. J. Clin. Med. 2018, 7, 411. [Google Scholar] [CrossRef] [Green Version]
  21. Funnell, M.M.; Brown, T.L.; Childs, B.P.; Haas, L.B.; Hosey, G.M.; Jensen, B.; Maryniuk, M.; Peyrot, M.; Piette, J.D.; Reader, D.; et al. National standards for diabetes self-management education. Diabetes Care 2012, 35 (Suppl. 1), S101–S108. [Google Scholar] [CrossRef] [Green Version]
  22. Dong, Y.; Wang, P.; Dai, Z.; Liu, K.; Jin, Y.; Li, A.; Wang, S.; Zheng, J. Increased self-care activities and glycemic control rate in relation to health education via Wechat among diabetes patients: A randomized clinical trial. Medicine 2018, 97, e13632. [Google Scholar] [CrossRef]
  23. Song, M.; Ratcliffe, S.J.; Tkacs, N.C.; Riegel, B. Self-care and health outcomes of diabetes mellitus. Clin. Nurs. Res. 2012, 21, 309–326. [Google Scholar] [CrossRef] [PubMed]
  24. Laxy, M.; Mielck, A.; Hunger, M.; Schunk, M.; Meisinger, C.; Ruckert, I.M.; Rathmann, W.; Holle, R. The association between patient-reported self-management behavior, intermediate clinical outcomes, and mortality in patients with type 2 diabetes: Results from the KORA-A study. Diabetes Care 2014, 37, 1604–1612. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Norris, S.L.; Nichols, P.J.; Caspersen, C.J.; Glasgow, R.E.; Engelgau, M.M.; Jack, L.; Snyder, S.R.; Carande-Kulis, V.G.; Isham, G.; Garfield, S.; et al. Increasing diabetes self-management education in community settings. A systematic review. Am. J. Prev. Med. 2002, 22, 39–66. [Google Scholar] [CrossRef]
  26. Qi, X.; Xu, J.; Chen, G.; Liu, H.; Liu, J.; Wang, J.; Zhang, X.; Hao, Y.; Wu, Q.; Jiao, M. Self-management behavior and fasting plasma glucose control in patients with type 2 diabetes mellitus over 60 years old: Multiple effects of social support on quality of life. Health Qual. Life Outcomes 2021, 19, 254. [Google Scholar] [CrossRef]
  27. Bai, Y.L.; Chiou, C.P.; Chang, Y.Y. Self-care behaviour and related factors in older people with Type 2 diabetes. J. Clin. Nurs 2009, 18, 3308–3315. [Google Scholar] [CrossRef] [PubMed]
  28. Nanayakkara, N.; Pease, A.J.; Ranasinha, S.; Wischer, N.; De Courten, B.; Zoungas, S. Younger Patients with Type 2 Diabetes Have Poorer Self-Care Practices Compared with Older Patients: Results from the Australian National Diabetes Audit. Diabet. Med. 2018, 35, 1087–1095. [Google Scholar] [CrossRef]
  29. Afaya, R.A.; Bam, V.; Azongo, T.B.; Afaya, A.; Kusi-Amponsah, A.; Ajusiyine, J.M.; Abdul Hamid, T. Medication adherence and self-care behaviours among patients with type 2 diabetes mellitus in Ghana. PLoS ONE 2020, 15, e0237710. [Google Scholar] [CrossRef]
  30. Uchmanowicz, I.; Wleklik, M.; Gobbens, R.J. Frailty syndrome and self-care ability in elderly patients with heart failure. Clin. Interv. Aging 2015, 10, 871–877. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Aprahamian, I.; Cezar, N.O.C.; Izbicki, R.; Lin, S.M.; Paulo, D.L.V.; Fattori, A.; Biella, M.M.; Jacob Filho, W.; Yassuda, M.S. Screening for Frailty With the FRAIL Scale: A Comparison With the Phenotype Criteria. J. Am. Med. Dir. Assoc. 2017, 18, 592–596. [Google Scholar] [CrossRef]
  32. Yin, X.; Savage, C.; Toobert, D.; Wei, P.; Whitmer, K. Adaptation and testing of instruments to measure diabetes self-management in people with type 2 diabetes in mainland China. J. Transcult. Nurs. 2008, 19, 234–242. [Google Scholar] [CrossRef] [PubMed]
  33. Yang, H.; Gao, J.; Ren, L.; Li, S.; Chen, Z.; Huang, J.; Zhu, S.; Pan, Z. Association between Knowledge-Attitude-Practices and Control of Blood Glucose, Blood Pressure, and Blood Lipids in Patients with Type 2 Diabetes in Shanghai, China: A Cross-Sectional Study. J. Diabetes Res. 2017, 2017, 3901392. [Google Scholar] [CrossRef] [PubMed]
  34. Lin, K.; Yang, X.; Yin, G.; Lin, S. Diabetes Self-Care Activities and Health-Related Quality-of-Life of individuals with Type 1 Diabetes Mellitus in Shantou, China. J. Int. Med. Res. 2016, 44, 147–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Kamradt, M.; Bozorgmehr, K.; Krisam, J.; Freund, T.; Kiel, M.; Qreini, M.; Flum, E.; Berger, S.; Besier, W.; Szecsenyi, J.; et al. Assessing self-management in patients with diabetes mellitus type 2 in Germany: Validation of a German version of the Summary of Diabetes Self-Care Activities measure (SDSCA-G). Health Qual. Life Outcomes 2014, 12, 185. [Google Scholar] [CrossRef] [PubMed]
  36. Li, G.; Prior, J.C.; Leslie, W.D.; Thabane, L.; Papaioannou, A.; Josse, R.G.; Kaiser, S.M.; Kovacs, C.S.; Anastassiades, T.; Towheed, T.; et al. Frailty and Risk of Fractures in Patients With Type 2 Diabetes. Diabetes Care 2019, 42, 507–513. [Google Scholar] [CrossRef] [Green Version]
  37. Perkisas, S.; Vandewoude, M. Where frailty meets diabetes. Diabetes Metab Res. Rev. 2016, 32 (Suppl. 1), 261–267. [Google Scholar] [CrossRef] [Green Version]
  38. Collard, R.M.; Boter, H.; Schoevers, R.A.; Oude Voshaar, R.C. Prevalence of frailty in community-dwelling older persons: A systematic review. J. Am. Geriatr. Soc. 2012, 60, 1487–1492. [Google Scholar] [CrossRef] [PubMed]
  39. Joosten, E.; Demuynck, M.; Detroyer, E.; Milisen, K. Prevalence of frailty and its ability to predict in hospital delirium, falls, and 6-month mortality in hospitalized older patients. BMC Geriatr. 2014, 14, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Xu, L.; Zhang, J.; Shen, S.; Liu, Z.; Zeng, X.; Yang, Y.; Hong, X.; Chen, X. Clinical Frailty Scale and Biomarkers for Assessing Frailty in Elder Inpatients in China. J. Nutr. Health Aging 2021, 25, 77–83. [Google Scholar] [CrossRef] [PubMed]
  41. Dent, E.; Martin, F.C.; Bergman, H.; Woo, J.; Romero-Ortuno, R.; Walston, J.D. Management of frailty: Opportunities, challenges, and future directions. Lancet 2019, 394, 1376–1386. [Google Scholar] [CrossRef]
  42. Lee, J.S.; Auyeung, T.W.; Leung, J.; Kwok, T.; Woo, J. Transitions in frailty states among community-living older adults and their associated factors. J. Am. Med. Dir. Assoc. 2014, 15, 281–286. [Google Scholar] [CrossRef] [PubMed]
  43. Turner, G.; Clegg, A.; British Geriatrics, S.; Age, U.K.; Royal College of General, P. Best practice guidelines for the management of frailty: A British Geriatrics Society, Age UK and Royal College of General Practitioners report. Age Ageing 2014, 43, 744–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Ida, S.; Kaneko, R.; Imataka, K.; Murata, K. Relationship between frailty and mortality, hospitalization, and cardiovascular diseases in diabetes: A systematic review and meta-analysis. Cardiovasc. Diabetol. 2019, 18, 81. [Google Scholar] [CrossRef] [PubMed]
  45. Holmberg, A.H.; Johnell, O.; Nilsson, P.M.; Nilsson, J.; Berglund, G.; Akesson, K. Risk factors for fragility fracture in middle age. A prospective population-based study of 33,000 men and women. Osteoporos. Int. 2006, 17, 1065–1077. [Google Scholar] [CrossRef] [Green Version]
  46. Lenardt, M.; Sousa, J.; Carneiro, N.; Betiolli, S.; Ribeiro, D.K. Physical activity of older adults and factors associated with pre-frailty. ACTA Paulista de Enfermagem 2013, 26, 269–275. [Google Scholar] [CrossRef]
  47. Haider, S.; Grabovac, I.; Dorner, T.E. Effects of physical activity interventions in frail and prefrail community-dwelling people on frailty status, muscle strength, physical performance and muscle mass-a narrative review. Wien. Klin. Wochenschr. 2019, 131, 244–254. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Modarresi, M.; Gholami, S.; Habibi, P.; Ghadiri-Anari, A. Relationship between Self Care Management with Glycemic Control in Type 2 Diabetic Patients. Int. J. Prev. Med. 2020, 11, 127. [Google Scholar] [CrossRef]
  49. Ayele, K.; Tesfa, B.; Abebe, L.; Tilahun, T.; Girma, E. Self care behavior among patients with diabetes in Harari, Eastern Ethiopia: The health belief model perspective. PLoS ONE 2012, 7, e35515. [Google Scholar] [CrossRef] [Green Version]
  50. Kav, S.; Yilmaz, A.A.; Bulut, Y.; Dogan, N. Self-efficacy, depression and self-care activities of people with type 2 diabetes in Turkey. Collegian 2017, 24, 27–35. [Google Scholar] [CrossRef]
  51. Jackson, I.L.; Onung, S.I.; Oiwoh, E.P. Self-care activities, glycaemic control and health-related quality of life of patients with type 2 diabetes in a tertiary hospital in Nigeria. Diabetes Metab. Syndr. 2021, 15, 137–143. [Google Scholar] [CrossRef]
  52. Wu, S.F.; Huang, Y.C.; Liang, S.Y.; Wang, T.J.; Lee, M.C.; Tung, H.H. Relationships among depression, anxiety, self-care behaviour and diabetes education difficulties in patients with type-2 diabetes: A cross-sectional questionnaire survey. Int. J. Nurs. Stud. 2011, 48, 1376–1383. [Google Scholar] [CrossRef]
  53. Al-Khawaldeh, O.A.; Al-Hassan, M.A.; Froelicher, E.S. Self-efficacy, self-management, and glycemic control in adults with type 2 diabetes mellitus. J. Diabetes Complicat. 2012, 26, 10–16. [Google Scholar] [CrossRef] [PubMed]
  54. Wang, X.; Luo, J.F.; Qi, L.; Long, Q.; Guo, J.; Wang, H.H. Adherence to self-monitoring of blood glucose in Chinese patients with type 2 diabetes: Current status and influential factors based on electronic questionnaires. Patient Prefer. Adherence 2019, 13, 1269–1282. [Google Scholar] [CrossRef] [Green Version]
  55. Gatt, S.; Sammut, R. An exploratory study of predictors of self-care behaviour in persons with type 2 diabetes. Int. J. Nurs. Stud. 2008, 45, 1525–1533. [Google Scholar] [CrossRef] [PubMed]
  56. Ahmad Sharoni, S.K.; Shdaifat, E.A.; Mohd Abd Majid, H.A.; Shohor, N.A.; Ahmad, F.; Zakaria, Z. Social support and self-care activities among the elderly patients with diabetes in Kelantan. Malays. Fam. Physician 2015, 10, 34–43. [Google Scholar]
  57. Shrivastava, S.R.; Shrivastava, P.S.; Ramasamy, J. Role of self-care in management of diabetes mellitus. J. Diabetes Metab. Disord. 2013, 12, 14. [Google Scholar] [CrossRef] [Green Version]
  58. Hoogendijk, E.O.; Afilalo, J.; Ensrud, K.E.; Kowal, P.; Onder, G.; Fried, L.P. Frailty: Implications for clinical practice and public health. Lancet 2019, 394, 1365–1375. [Google Scholar] [CrossRef]
  59. Toobert, D.J.; Hampson, S.E.; Glasgow, R.E. The summary of diabetes self-care activities measure: Results from 7 studies and a revised scale. Diabetes Care 2000, 23, 943–950. [Google Scholar] [CrossRef] [Green Version]
Table 1. Sociodemographic and clinical characteristics of participants, and prevalence of frailty and prefrailty in different subgroups (n = 558).
Table 1. Sociodemographic and clinical characteristics of participants, and prevalence of frailty and prefrailty in different subgroups (n = 558).
CharacteristicsFrailty Status, n (%)p Value
AllNon-Frail
(n = 311)
Prefrail
(n = 190)
Frail
(n = 57)
GenderFemale277 (49.6)155 (56.0)104 (37.5)18 (6.5)0.009
Male281 (50.4)156 (55.5)86 (30.6)39 (13.9)
Age (years)40–65135 (24.2)99 (73.3)31 (23.0)5 (3.7)<0.001
65–75278 (49.8)146 (52.5)100 (36.0)32 (11.5)
>75130 (23.3)59 (45.4)55 (42.3)16 (12.3)
Body mass index (kg/m2)<25337 (60.4)187 (55.5)112 (33.2)38 (11.3)0.424
25–29.9185 (33.2)103 (55.7)68 (36.8)14 (7.6)
≥3023 (4.1)13 (56.5)6 (26.1)4 (17.4)
Education levelSecondary or lower283 (50.7)155 (54.8)96 (33.9)32 (11.3)0.129
High school/associate246 (44.1)133 (54.1)89 (36.2)24 (9.8)
Bachelor or over29 (5.2)23 (79.3)5 (17.2)1 (3.4)
Socioeconomic statusEmployed/self-employed48 (8.6)40 (83.3)8 (16.7)0 (0)<0.001
Unemployed/retired510 (91.4)271 (53.1)182 (35.7)57 (11.2)
Marital statusSingle/divorced/widowed69 (12.4)31 (44.9)31 (44.9)7 (10.1)0.112
Married489 (87.6)280 (57.3)159 (32.5)50 (10.2)
Cohabitation statusSolitude28 (5.0)13 (46.4)12 (42.9)3 (10.7)0.530
Cohabitated530 (95.0)298 (56.2)178 (33.6)54 (10.2)
HbA1c (%)≤6.5120 (21.5)71 (59.2)46 (38.3)3 (2.5)0.003
>6.5394 (70.6)205 (52.0)135 (34.3)54 (13.7)
FBG (mmol/L)≤7.0319 (57.2)174 (54.5)107 (33.5)38 (11.9)0.299
>7.0229 (41.0)129 (56.3)82 (35.8)18 (7.9)
No. of comorbidities0300 (53.8)211 (70.3)79 (26.3)10 (3.3)<0.001
1–2177 (31.7)86 (48.6)71 (40.1)20 (11.3)
≥381 (14.5)14 (17.3)40 (49.4)27 (33.3)
No. of chronic diseases0145 (26.0)107 (73.8)32 (22.1)6 (4.1)<0.001
1–2363 (65.1)196 (54.0)133 (36.6)34 (9.4)
≥350 (9.0)8 (16.0)25 (50.0)17 (34.0)
No. of medications019 (3.4)14 (73.7)4 (21.1)1 (5.3)0.001
1–2239 (42.8)157 (65.7)72 (30.1)10 (4.2)
≥379 (14.2)33 (41.8)37 (46.8)9 (11.4)
Duration of diabetes (years)<10237 (42.5)147 (62.0)76 (32.1)14 (5.9)0.001
10–20213 (38.2)111 (52.1)79 (37.1)23 (10.8)
>2098 (17.6)45 (45.9)33 (33.7)20 (20.4)
Physical activity, yes146 (26.2)104 (71.2)37 (25.3)5 (3.4)<0.001
Smoking, yes73 (13.1)48 (65.8)20 (27.4)5 (6.8)0.171
Regular alcohol consumption, yes40 (86.9)27 (67.5)13 (32.5)0 (0)0.033
Cardiovascular disease, yes348 (62.4)185 (53.2)122 (35.1)41 (11.8)0.166
Hospitalization in the past year, yes89 (15.9)23 (25.8)50 (56.2)16 (18.0)<0.001
Emergency department visits in the past year, yes34 (6.1)14 (41.2)13 (38.2)7 (20.6)0.072
Abbreviation: FBG fasting blood glucose.
Table 2. Scores of the Summary of Diabetes Self-Care Activities (SDSCA) measure of participants (n = 558).
Table 2. Scores of the Summary of Diabetes Self-Care Activities (SDSCA) measure of participants (n = 558).
DomainsNo. of ItemsMean Score ± SDp Value
AllFrail
(n = 57)
Prefrail
(n = 190)
Non-Frail
(n = 311)
Diet44.59 ± 1.513.71 ± 1.644.57 ± 1.524.77 ± 1.42<0.001
Physical activity23.08 ± 2.081.92 ± 1.682.97 ± 2.183.36 ± 2.00<0.001
Blood glucose monitoring21.91 ± 1.991.93 ± 1.432.02 ± 2.021.84 ± 2.070.611
Foot care22.72 ± 2.752.11 ± 1.782.72 ± 2.752.84 ± 2.880.186
Medication adherence15.34 ± 2.644.11 ± 2.515.68 ± 2.305.36 ± 2.80<0.001
Total1239.03 ± 14.0330.75 ± 8.6039.27 ± 15.2040.40 ± 13.60<0.001
Table 3. Univariate analysis of the Summary of Diabetes Self-Care Activities (SDSCA) measure stratified by characteristics.
Table 3. Univariate analysis of the Summary of Diabetes Self-Care Activities (SDSCA) measure stratified by characteristics.
VariablesMean Scorep Value
GenderFemale40.45 ± 13.800.018
Male37.63 ± 14.14
Age (years)40–6437.90 ± 12.350.273
65–7540.09 ± 14.96
>7538.38 ± 13.92
Body mass index (kg/m2)<2539.17 ± 13.830.951
25–29.939.18 ± 14.45
≥3038.22 ± 14.86
Education levelSecondary or lower36.75 ± 12.87<0.001
High school/associate/bachelor or over41.38 ± 14.79
Socioeconomic statusEmployed/self-employed35.90 ± 11.680.061
Unemployed/retired39.33 ± 14.20
Marital statusSingle/divorced/widowed39.42 ± 12.560.805
Married38.98 ± 14.23
Cohabitation statusSolitude38.86 ± 14.190.947
Cohabitated39.04 ± 14.03
HbA1c (%)≤6.542.70 ± 16.570.002
>6.537.44 ± 12.72
FBG (mmol/L)≤7.039.03 ± 14.050.941
>7.039.12 ± 14.17
No. of comorbidities041.07 ± 14.41<0.001
1–237.82 ± 13.55
≥334.12 ± 12.10
No. of chronic diseases040.18 ± 12.450.074
1–239.13 ± 14.80
≥334.96 ± 11.96
No. of medications034.16 ± 9.290.156
1–240.64 ± 15.11
≥341.10 ± 13.78
Duration of diabetes (years)<1040.19 ± 15.100.161
10–2037.77 ± 13.56
>2038.12 ± 12.31
Smoking, yes37.84 ± 15.420.436
Regular alcohol consumption, yes40.40 ± 14.580.540
Cardiovascular disease, yes38.35 ± 14.160.142
Hospitalization in the past year, yes37.78 ± 14.630.358
Emergency department visit in the past year, yes40.32 ± 14.030.580
Abbreviation: FBG fasting blood glucose.
Table 4. Odds ratios from multinomial logistic regression for frailty and prefrailty.
Table 4. Odds ratios from multinomial logistic regression for frailty and prefrailty.
VariablesaOR (95% CI)
Frail vs. Non-FrailPrefrail vs. Non-Frail
GenderFemale0.88 (0.42–1.81)1.67 (1.08–2.60)
Male1 (reference)1 (reference)
No. of comorbidities00.10 (0.04–0.29)0.18 (0.09–0.39)
1–20.24 (0.10–0.63)0.36 (0.17–0.75)
≥31 (reference)1 (reference)
No. of chronic diseases00.18 (0.04–0.72)0.29 (0.11–0.80)
1–20.25 (0.08–0.73) 0.43 (0.17–1.07)
≥31 (reference)1 (reference)
Physical activity, yes0.42 (0.14–1.24)0.52 (0.31–0.85)
Hospitalization in the past year, yes4.67 (1.96–11.14)4.27 (2.27–8.03)
SDSCA score0.95 (0.92–0.98) 1.00 (0.99–1.02)
The reference category was the non-frail group. Results were presented as adjusted OR (95% CI). The model was adjusted for gender, age, employment status, HbA1c, number of comorbidities, chronic diseases and medications, duration of diabetes, physical activity, history of hospitalization (categorical), and SDSCA scale score (continuous). Numbers in bold indicated significant findings. Abbreviations: aOR adjusted odds ratio; CI confidence interval; SDSCA Summary of Diabetes Self-Care Activities.
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Tang, Z.; Shen, C.; Tong, W.; Xiang, X.; Feng, Z.; Han, B. Frailty in Community-Dwelling Adults Aged 40 Years and over with Type 2 Diabetes: Association with Self-Management Behaviors. Int. J. Environ. Res. Public Health 2022, 19, 9092. https://doi.org/10.3390/ijerph19159092

AMA Style

Tang Z, Shen C, Tong W, Xiang X, Feng Z, Han B. Frailty in Community-Dwelling Adults Aged 40 Years and over with Type 2 Diabetes: Association with Self-Management Behaviors. International Journal of Environmental Research and Public Health. 2022; 19(15):9092. https://doi.org/10.3390/ijerph19159092

Chicago/Turabian Style

Tang, Zhijia, Chunying Shen, Waikei Tong, Xiaoqiang Xiang, Zhen Feng, and Bing Han. 2022. "Frailty in Community-Dwelling Adults Aged 40 Years and over with Type 2 Diabetes: Association with Self-Management Behaviors" International Journal of Environmental Research and Public Health 19, no. 15: 9092. https://doi.org/10.3390/ijerph19159092

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