Next Article in Journal
Association between Antihypertensive Therapy and Risk of Acute Lower Respiratory Infections (ALRI): A Retrospective Cohort Study
Previous Article in Journal
Serostatus and Epidemiological Characteristics for Atypical Pneumonia Causative Bacteria among Healthy Individuals in Medina, Saudi Arabia, a Retrospective Study
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Might Dog Walking Reduce the Impact of COPD on Patients’ Life?

1
Respiratory Unit for Continuity of Care, IRCCS, Ospedale Policlinico San Martino, Department of Internal Medicine (DiMI), University of Genova, 16126 Genova, Italy
2
Institute of Translational Pharmacology, National Research Council, 90146 Palermo, Italy
3
Medical Affairs Boehringer Ingelheim, 20139 Milan, Italy
*
Author to whom correspondence should be addressed.
Healthcare 2022, 10(11), 2317; https://doi.org/10.3390/healthcare10112317
Submission received: 13 October 2022 / Revised: 13 November 2022 / Accepted: 14 November 2022 / Published: 18 November 2022
(This article belongs to the Topic Healthy, Safe and Active Aging)

Abstract

:
Low levels of physical activity (PA) lead to a worsening of physical condition and contributes to multimorbidity in Chronic Obstructive Respiratory Disease (COPD). Unsupervised PA related to dog ownership may contribute to reducing sedentary behavior. We aimed to investigate the relationship between dog walking, patient-reported outcomes (PROs) and exacerbations in COPD. A pre-defined sample of 200 COPD patients (dog owners and non-dog owners) with symptomatic COPD was sourced from a database representative of the Italian population. A computer-assisted personal interview was used to assess health status impairment (CAT), fatigue (FACIT), health-related quality of life (HRQoL) (EQ-5D), and PA frequency. In the whole sample, PA was associated with better CAT, EQ-5D, VAS, FACIT scores and reduced number of exacerbation (p < 0.001). Under the same CAT scores, dog-walking duration was associated with a better HRQoL (EQ5D, p = 0.015) and less fatigue (FACIT, p = 0.017). In an adjusted regression model, walking dogs >30 min was associated with lower fatigue (FACIT) than having no dogs and walking dogs <15 min (p = 0.026 and p = 0.009, respectively). Motivation related to dog walking could modify patients’ tendency to focus on symptoms during PA and, therefore, to perceive the fatigue. Dog walking may be effective for increasing and maintaining regular PA, reducing the subjective impact of COPD.

1. Introduction

The difficulty in keeping active is a common feature of Chronic Obstructive Respiratory Disease (COPD) depending on symptoms of breathlessness, fatigue and muscle deconditioning [1,2]. It begins in the early stages of the disease and gradually increases over time to a greater extent than in non-COPD subjects [3,4]. Lower levels of PA leads to a further worsening of the physical condition, lung function decline, and contributes to multimorbility [5]. This leads to a downward spiral of inactivity that impairs health outcomes and represents an independent risk factor for COPD-related hospital admissions and worst prognosis [6,7,8,9,10].
Physical activity (PA), defined as “any bodily movement produced by skeletal muscles resulting in an increase in energy expenditure of the body” [11], refers to the overall level of PA carried out by a person at work, at home, for commuting, and during leisure-time. The World Health Organization (WHO) 2020 recommendations [12] are to perform at least 150 min per week of moderate-intensity PA, or at least 75–150 min of vigorous-intensity PA, or an equivalent combination of moderate- and vigorous-intensity activity. The benefits of following these recommendations have been well established: PA is associated with a lower all-cause mortality and cardiovascular disease, morbidity, and disability [13,14]. In addition, there is increasing evidence that engaging in regular PA is associated with better patient-reported outcomes (PROs) such as health-related quality of life (HRQoL), symptoms, and mood [12,15].
However, despite converging evidence for the beneficial effects of being active, it is often challenging to increase engagement with PA in people with COPD [2,16]. Key barriers to maintain exercise behaviors are disease-specific problems (i.e., symptoms, functional limitations, comorbidities) [17,18], psychological factors (i.e., depression, disease-specific anxiety, fear avoidance behaviors [19,20], health attitudes toward fitness and strength [21], lack of motivation [16], shame [22]), in addition to practical difficulties (i.e., lack of transportation) [2] and limited access to interventions for improving PA [23].
Some of these barriers might be overcome through activities that can be easily integrated in individuals’ daily routine, without supervision, and using resources that are available at home (i.e., walking, climbing the stairs, exercises using water bottles as weights).
Recently, a systematic review and meta-analysis, highlighted that unsupervised PA interventions in people with COPD have a positive impact on dyspnea and exercise capacity; such interventions are safe and show a high adherence rate [24].
Unsupervised PA related to dog ownership may also contribute to reduce sedentary behavior. People owning dogs have been observed to be more physically active that non-owners [25,26] and, therefore, they are more likely to meet the recommended level of 150 min per week [26,27] and to engage in PA during leisure time [27].
The association between dog ownership and increased PA, primarily through dog walking, has been also confirmed in subjects with diabetes [28], cardiovascular diseases [29], breast cancer [30], in chronic hemodialysis patients [31] and in obese people who have undergone a gastric banding procedure [32].
Exploring if having a dog is associated with outcomes that are relevant to the experience of COPD patients will help to identify new insights into PA interventions in clinical practice.
The aim of this study is therefore to investigate if dog ownership is associated with PROs (such as health status, HRQoL and fatigue) and exacerbations in patients with COPD.

2. Materials and Methods

A cross-sectional survey was carried out between 7–18 March 2019. Trained research staff administered the survey using a computer-assisted personal interviewing (CAPI), a technique employed for data collection on a portable device. The study sample was sourced from the Doxa Population Panel, a proprietary quality-checked database representative of the general Italian population on several key socio-demographic variables. All procedures were in accordance with both international (ESOMAR and EphMRA) and national (FarmIndustria) ethical standards as well as with the 1964 Helsinki Declaration, its later amendments or comparable ethical standards. According to Italian law, when anonymous surveys are conducted without the use of clinical data, ethics approval from the IRB/local ethics committee is not required. Informed consent was obtained from all individual participants involved in the present study.
A pre-defined sample of 200 patients was recruited from a quality-checked database representative of the general Italian population. Inclusion criteria were symptomatic COPD and a COPD Assessment Test (CAT) [33] ≥ 10 (the threshold indicated by GOLD) [34]. Non exclusion criteria have been considered.
The CAPI system was used to administer the following PROs at the responder home:
  • CAT [33] an 8-item unidimensional measure of health status impairment in COPD. The score ranges from 0 to 40, with higher scores representing worse health.
  • EuroQol-5D (EQ-5D), developed in 1990, is a most widely used generic questionnaire to assess HRQoL [35]. It is applicable to the general population as well as a wide range of health conditions including COPD [36]. It consists of five questions assessing whether subjects were experiencing problems (no, some/moderate, or severe/extreme) in 5 dimensions of health (mobility, self-care, usual activities, pain/discomfort and anxiety/depression). It also includes a vertical visual analogue scale (VAS) asking subjects to rate their overall health on a scale from 0 (the worst imaginable health) to 100 (the best imaginable health).
  • Functional Assessment of Chronic Illness Therapy Fatigue Scale (FACIT-Fatigue), a 13-item questionnaire to assess fatigue and its impact on daily activities and functioning [37], which has been previously used in COPD [38,39,40]. The total score ranges from 0 to 52, with higher scores indicating less fatigue [41].
Socio-demographic characteristics (age, gender, education, employment status, family support), clinical features (CAT score and exacerbations defined as an cute worsening of respiratory symptoms that result in additional therapy, according to GOLD document) [34], self-reported frequency of PA, and dog-walking duration were recorded using an ad-hoc questionnaire.
Subject characteristics were summarized through the mean and standard deviation (SD) for quantitative variables and through absolute (percentage) frequencies for categorical variables. Comparisons among groups were carried out using one-way ANOVA (which reduces to the t-test in the case of comparison between two groups) for quantitative variables and the chi-square test for categorical variables.
An exploratory analysis was carried out to compare the distribution of questionnaire scores (CAT, EQ5D, VAS, and FACIT) and exacerbations in the last year (>1 vs. 1) by physical activity frequency (categorized as “never/hardly ever”, “<1 times/week”, “1–2 times/week”, “3–4 times/week”, “almost every day”), dog-ownership duration (“non-dog owner”, “0–2 years”, “3–5 years”, “>5 years”), and dog-walking duration (“non-dog owner”, “<15 min”, “15–30 min”, “>30 min”). For significant associations, pairwise comparisons between groups were carried out using the Holm’s method for addressing the aspect of multiplicity. Non-significant associations were not investigated further in subsequent analyses.
Linear regression models were estimated to formally investigate the association between dog-ownership categories (dog-ownership, dog-ownership duration, and dog-walking duration) and questionnaire scores. Both unadjusted models and models adjusted for age, gender, education level (lower than or at least 8 years), occupational status (retired or not), cohabitation status (living alone or not), and physical activity frequency were estimated. Since the dog-ownership duration and the dog-walking duration were structurally missing in non-dog owners, ad-hoc dummy variables were used if these variables were both included in regression models [42]. Similarly, logistic regression models were estimated using the frequency of exacerbations in the last year (>1 vs. 1) as the outcomes. Associations were reported as mean differences (β coefficients) and 95% confidence intervals for linear regression, and odds ratios (OR) and 95% confidence intervals for logistic regression. Since the distribution of EQ5D was negatively skewed, bootstrap confidence intervals were derived in the relevant linear regression model.
Analyses were carried out using the R statistical software, version 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria). Statistical significance was set at p < 0.05.

3. Results

A total of 200 subjects were included in this study, of which 99 were dog-owners and 101 were not (Table 1). On average, dog-owners were 3 years younger than non-dog owners (p = 0.038). About 50% of the subjects were females, 44% were retired, and 16% were living alone.
Physical activity frequency was not significantly associated with dog ownership (p = 0.071) despite somewhat larger frequencies of classes “3–4 times/week” and “almost every day” observed among dog-owners (18% and 27%, respectively). Mean dog-ownership duration was >5 years for 50% of dog-owners. Dog-walking duration was more than 30 min for 13% of dog-owners.
Questionnaire scores and the frequency of exacerbations were significantly associated with PA frequency in the whole sample (Table 2). Subjects who reported doing PA never/hardly ever had a higher mean CAT score and lower mean EQ5D, VAS, and FACIT scores than other physical activity groups (p < 0.001) (Table 2). Subjects who reported doing PA never/hardly ever or <1 times/week had more frequently multiple (>1) exacerbations in the last year than in other groups (p < 0.001) (Table 2). Dog-ownership duration was not associated with questionnaire scores and disease outcomes. No difference in CAT score emerged among non-dog owners and dog-owners walking for <15, 15–30, and 30 min. Dog-walking duration was significantly associated with EQ5D (p = 0.015) and FACIT scores (p = 0.017) (Table 2). In particular, mean scores were the lowest in subjects walking dogs for less than 15 min. Questionnaire scores were similar between non-dog owners and dog owners walking dogs for 15–30 min, while scores were the highest in subjects walking dogs for more than 30 min (Table 2, Figure 1).
Following this exploratory analysis, dog-ownership duration was not included in regression models. Physical activity frequency was categorized as “physical activity” and “no physical activity” (“never/hardly ever”) in linear regression models (Table 3), and as “regular physical activity” (at least once a week) and “others” in logistic regression models (Table 4). For dog-walking, “>30 min” was used as the reference (Table 3 and Table 4).
In unadjusted models, having no dogs was associated with lower EQ5D (β = −0.09, p = 0.043) an FACIT (β = −7.64, p = 0.011) scores than walking dogs >30 min, while walking dogs <15 min was associated with lower EQ5D (β = −0.14, p = 0.004) an FACIT (β = −9.89, p = 0.002) scores than walking dogs >30 min (Table 3). After adjusting PA and other potential confounders, the aforementioned EQ5D differences were attenuated, and having no dogs was not any more associated with a significantly lower EQ5D than walking dogs >30 min. Female gender was associated with lower VAS scores (β = −6.63, p < 0.001). Retired subjects and those living alone had somewhat worse questionnaire scores. Physical activity was significantly associated with better questionnaire scores (Table 3). In logistic regression models, no significant associations with dog-walking duration were found. Retired subjects were significantly associated with a higher risk of multiple exacerbations in the last year. Regular physical activity was significantly associated with a lower risk of multiple exacerbations in the last year (Table 4).

4. Discussion

Dog walking has been proposed as a purposeful and feasible opportunity for dog owners seeking to maintain regular PA [25,43]. At present, the few available data in patients with COPD have identified dog walking as a socio-environmental factor related to PA [44]. In this study, we assessed the relationship of dog ownership with PROs, self-reported PA and exacerbations in a pre-defined sample of subjects with moderate COPD.
Our first finding is that having a dog is not significantly associated to the level of PA. Second, PA frequency of COPD patients was significantly associated with questionnaire scores and frequency of exacerbations in the whole sample. Third, a significant association of dog-walking duration with PROs and exacerbations was found.
The positive association between dog ownership and levels of PA, detected in various populations [28,43], is only a non-significant tendency in our sample, although we found a higher percentage of subjects doing regular PA (3–4 times/week or almost every day) in dog owners (45% vs. 27%). Indeed, dog ownership may not modify habits by itself, as observed in a previous study assessing changes in PA following dog acquisition [45]. This may depend on factors related with both patients (i.e., comorbidities) and dogs (i.e., breed, size, age, health status) that we have not evaluated.
Our results are in line with previous studies that have highlighted the benefits of PA, assessed by a self-report measure, on PROs both in the general population and in patients with chronic diseases and disabilities [46,47,48]. In fact, the effect of PA is also perceived by patients with COPD in terms of health status, HRQoL, and fatigue. Overall, these results indicate that, for patients who spend time in physical exercise, the impact of the disease from a subjective viewpoint is less severe. PA levels were also associated with a higher number of exacerbations, in line with previous studies that have identified physical inactivity as a risk factor in the exacerbation of COPD [40,41,42,43,44,45,46,47,48,49,50,51]. Some mechanisms underlying the potential beneficial impact of PA on exacerbations may be hypothesized. One possible explanation is that a better conditioned cardiovascular system would fit better to the increased oxygen intake in respiratory muscles during COPD exacerbation [52]. Moreover, a reduction of induced lactic acidosis and improvement of the muscular oxidative capacity would lead muscles to better tolerate a COPD exacerbation [53]. Finally, the anti-inflammatory and anti-oxidant effects of PA [54] should have a role.
An interesting result of this study was the positive association of dog-walking duration with better HRQoL and less fatigue, regardless of the extent to which COPD affects patients’ lives. In fact, although non-dog owners and dog-owners walking for <15 and 15-min have no significant difference in CAT scores, subjects walking dogs for more than 30 min have better EQ5D and FACIT scores (Table 2). These results suggest that, even if significant COPD symptoms are present, it is possible to maintain regular activity and to improve HRQoL and fatigue as a function of PA levels.
Linear regression models confirmed the results of the exploratory analysis, highlighting the potential benefits of dog walking in patients with COPD. In unadjusted models, walking dogs >30 min was associated with higher HRQoL (EQ5D) and lower fatigue (FACIT) than having no dogs and walking dogs <15 min.
After adjusting for PA, age, gender, education level, occupational and cohabitation status, HRQoL differences were attenuated. Conversely, also in adjusted models, walking dogs >30 min was associated with a significantly lower fatigue than having no dogs and walking dogs <15 min. In this regard, it may be assumed that motivation plays a role in perception of effort. According to the psychobiological model of endurance performance based on motivational intensity theory [55], the experience of fatigue may be explained as a form of task disengagement rather than just as a worse COPD status. Dog owners who regularly walk their dog for more than 30 min could be motivated by strong attachment and responsibility toward the dog, as previously found in community samples [56,57] or by considering dog walking as an enjoyable activity. Such motivations may have modified patient’s tendency to focus on symptoms during PA and, therefore, to perceive the fatigue.
Moreover, in line with previous research, female gender [58,59] and retirement [60] were associated with lower overall HRQoL scores and suggest that health managers and clinicians should consider these features in the management of COPD with the ultimate aim of meeting the specific needs of their patients and increasing their HRQL. A significant association with living condition has been found for CAT and FACIT: in patients who live alone, PA (both in dog owners and non-owners) was significantly associated with worse PROs scores.
To the best of our knowledge, the relationship between PA, PROs and exacerbations, already known in other diseases, had never been investigated in COPD. However, there are also several limitations that have implications for future research and for the interpretation of our findings. First, it is a retrospective observational study carrying out the limitations of this kind of data, and the results should be considered as hypothesis-generating. Secondly, an objective evaluation of PA was difficult to obtain due to the study design that is based on patient reported outcomes. All information are based on self-reports which may be influenced by potential recall bias: the possibility that data could be under or over reported should be taken into account. The availability of devices to monitor PA and the increase in exercise tolerability may be used in longitudinal studies to obtain objective data. Thirdly, data and adherence concerning specific types of inhaler medications were not available; nor was a more complete staging of COPD. Finally, this study presents limitations in the generalizability of the results to populations outside of Italy.

5. Conclusions

In conclusion, the study results highlight the potentially important role that regular PA with a dog could play in reducing the burden of COPD on a patient’s life. Promoting dog walking among dog owners who do not routinely walk their dogs may be an effective strategy for increasing and maintaining regular PA and, consequently, for reducing the impact of COPD on clinical and patient-reported outcomes. Our results should be useful to develop and disseminate public education campaigns to promote PA in COPD patients. Moreover, the pet industry (food, treats, wellness, health) may identify COPD patients as a new target.

Author Contributions

Conceptualization, I.B., F.B. and C.S.; methodology, I.B., F.B., S.F. and S.L.G.; formal analysis, S.F.; writing—original draft preparation, I.B. and F.B.; writing—review and editing, C.L., N.C. and M.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethical review and approval were waived for this study because, according to Italian law, when anonymous surveys are conducted without the use of clinical data, ethics approval from the IRB/local ethics committee is not required.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

With publication, we declare to make the data that support the findings of this study available on request. This should be done through the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Miravitlles, M.; Ribera, A. Understanding the impact of symptoms on the burden of COPD. Respir. Res. 2017, 18, 67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Kosteli, M.C.; Heneghan, N.R.; Roskell, C.; Williams, S.E.; Adab, P.; Dickens, A.P.; Enocson, A.; Fitzmaurice, D.A.; Jolly, K.; Jordan, R.; et al. Barriers and enablers of physical activity engagement for patients with COPD in primary care. Int. J. Chronic Obstr. Pulm. Dis. 2017, 12, 1019–1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Donaire-Gonzalez, D.; Gimeno-Santos, E.; Balcells, E.; Rodríguez, D.A.; Farrero, E.; de Batlle, J.; Benet, M.; Ferrer, A.; Barberà, J.A.; Gea, J.; et al. Physical activity in COPD patients: Patterns and bouts. Eur. Respir. J. 2013, 42, 993–1002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Vorrink, S.N.; Kort, H.S.; Troosters, T.; Lammers, J.W. Level of daily physical activity in individuals with COPD compared with healthy controls. Respir. Res. 2011, 12, 33. [Google Scholar] [CrossRef] [Green Version]
  5. Fermont, J.M.; Fisk, M.; Bolton, C.E.; MacNee, W.; Cockcroft, J.R.; Fuld, J.; Cheriyan, J.; Mohan, D.; Mäki-Petäjä, K.M.; Al-Hadithi, A.B.; et al. Cardiovascular risk prediction using physical performance measures in COPD: Results from a multicentre observational study. BMJ Open 2020, 10, e038360. [Google Scholar] [CrossRef]
  6. Watz, H.; Pitta, F.; Rochester, C.L.; Garcia-Aymerich, J.; ZuWallack, R.; Troosters, T.; Vaes, A.W.; Puhan, M.A.; Jehn, M.; Polkey, M.I.; et al. An official European Respiratory Society statement on physical activity in COPD. Eur. Respir. J. 2014, 44, 1521–1537. [Google Scholar] [CrossRef] [Green Version]
  7. Garcia-Aymerich, J.; Lange, P.; Benet, M.; Schnohr, P.; Antó, J.M. Regular physical activity reduces hospital admission and mortality in chronic obstructive pulmonary disease: A population based cohort study. Thorax 2006, 61, 772–778. [Google Scholar] [CrossRef] [Green Version]
  8. Yohannes, A.M.; Baldwin, R.C.; Connolly, M. Mortality predictors in disabling chronic obstructive pulmonary disease in old age. Age Ageing 2002, 31, 137–140. [Google Scholar] [CrossRef] [Green Version]
  9. Ramos, M.; Lamotte, M.; Gerlier, L.; Svangren, P.; Miquel-Cases, A.; Haughney, J. Cost-effectiveness of physical activity in the management of COPD patients in the UK. Int. J. Chronic Obstr. Pulm. Dis. 2019, 14, 227–239. [Google Scholar] [CrossRef] [Green Version]
  10. Waschki, B.; Kirsten, A.; Holz, O.; Müller, K.C.; Meyer, T.; Watz, H.; Magnussen, H. Physical activity is the strongest predictor of all-cause mortality in patients with COPD: A prospective cohort study. Chest 2011, 140, 331–342. [Google Scholar] [CrossRef]
  11. Caspersen, C.J.; Powell, K.E.; Christenson, G.M. Physical activity, exercise, and physical fitness: Definitions and distinctions for health-related research. Public Health Rep. 1985, 100, 126–131. [Google Scholar] [PubMed]
  12. Bull, F.C.; Al-Ansari, S.S.; Biddle, S.; Borodulin, K.; Buman, M.P.; Cardon, G.; Carty, C.; Chaput, J.P.; Chastin, S.; Chou, R.; et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br. J. Sports Med. 2020, 54, 1451–1462. [Google Scholar] [CrossRef] [PubMed]
  13. Chou, W.T.; Tomata, Y.; Watanabe, T.; Sugawara, Y.; Kakizaki, M.; Tsuji, I. Relationships between changes in time spent walking since middle age and incident functional disability. Prev. Med. 2014, 59, 68–72. [Google Scholar] [CrossRef] [PubMed]
  14. Rogers, N.T.; Marshall, A.; Roberts, C.H.; Demakakos, P.; Steptoe, A.; Scholes, S. Physical activity and trajectories of frailty among older adults: Evidence from the English Longitudinal Study of Ageing. PLoS ONE 2017, 12, e0170878. [Google Scholar] [CrossRef] [Green Version]
  15. Teba, P.P.; Esther, M.G.; Raquel, S.G. Association between physical activity and patient-reported outcome measures in patients with lung cancer: A systematic review and meta-analysis. Qual. Life Res. 2022, 31, 1963–1976. [Google Scholar] [CrossRef]
  16. Sritharan, S.S.; Østergaard, E.B.; Callesen, J.; Elkjaer, M.; Sand, L.; Hilberg, O.; Skaarup, S.H.; Løkke, A. Barriers toward Physical Activity in COPD: A Quantitative Cross-Sectional, Questionnaire-Based Study. J. Chronic Obstr. Pulm. Dis. 2021, 18, 272–280. [Google Scholar] [CrossRef]
  17. Thorpe, O.; Kumar, S.; Johnston, K. Barriers to and enablers of physical activity in patients with COPD following a hospital admission: A qualitative study. Int. J. Chronic Obstr. Pulm. Dis. 2014, 9, 115–128. [Google Scholar] [CrossRef] [Green Version]
  18. Sievi, N.A.; Senn, O.; Brack, T.; Brutsche, M.H.; Frey, M.; Irani, S.; Leuppi, J.D.; Thurnheer, R.; Franzen, D.; Kohler, M.; et al. Impact of comorbidities on physical activity in COPD. Respirology 2015, 20, 413–418. [Google Scholar] [CrossRef]
  19. Carl, J.; Schultz, K.; Janssens, T.; von Leupoldt, A.; Pfeifer, K.; Geidl, W. The “can do, do do” concept in individuals with chronic obstructive pulmonary disease: An exploration of psychological mechanisms. Respir. Res. 2021, 22, 260. [Google Scholar] [CrossRef]
  20. Lee, S.H.; Kim, K.U.; Lee, H.; Kim, Y.S.; Lee, M.K.; Park, H.K. Factors associated with low-level physical activity in elderly patients with chronic obstructive pulmonary disease. Korean J. Intern. Med. 2018, 33, 130–137. [Google Scholar] [CrossRef]
  21. Chen, M.L.; Chen, L.S.; Chen, Y.T.; Gardenhire, D.S. The Association of Health-Related Factors with Leisure-Time Physical Activity among Adults with COPD: A Cross-Sectional Analysis. Healthcare 2022, 10, 249. [Google Scholar] [CrossRef] [PubMed]
  22. Hartman, J.E.; Ten Hacken, N.H.; Boezen, H.M.; De Greef, M.H. Self-efficacy for physical activity and insight into its benefits are modifiable factors associated with physical activity in people with COPD: A mixed-methods study. J. Physiother. 2013, 59, 117–124. [Google Scholar] [CrossRef] [Green Version]
  23. Holland, A.E.; Cox, N.S.; Houchen-Wolloff, L.; Rochester, C.L.; Garvey, C.; ZuWallack, R.; Nici, L.; Limberg, T.; Lareau, S.C.; Yawn, B.P.; et al. Defining Modern Pulmonary Rehabilitation. An Official American Thoracic Society Workshop Report. Ann. Am. Thorac. Soc. 2021, 18, e12–e29. [Google Scholar] [CrossRef]
  24. Paixão, C.; Rocha, V.; Brooks, D.; Marques, A. Unsupervised physical activity interventions for people with COPD: A systematic review and meta-analysis. Pulmonology 2022, in press. [Google Scholar] [CrossRef] [PubMed]
  25. Christian, H.E.; Westgarth, C.; Bauman, A.; Richards, E.A.; Rhodes, R.E.; Evenson, K.R.; Mayer, J.A.; Thorpe, R.J., Jr. Dog ownership and physical activity: A review of the evidence. J. Phys. Act. Health 2013, 10, 750–759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Westgarth, C.; Christley, R.M.; Jewell, C.; German, A.J.; Boddy, L.M.; Christian, H.E. Dog owners are more likely to meet physical activity guidelines than people without a dog: An investigation of the association between dog ownership and physical activity levels in a UK community. Sci. Rep. 2019, 9, 5704. [Google Scholar] [CrossRef] [Green Version]
  27. Reeves, M.J.; Rafferty, A.P.; Miller, C.E.; Lyon-Callo, S.K. The impact of dog walking on leisure-time physical activity: Results from a population-based survey of Michigan adults. J. Phys. Act. Health 2011, 8, 436–444. [Google Scholar] [CrossRef]
  28. Riske, J.; Janert, M.; Kahle-Stephan, M.; Nauck, M.A. Owning a Dog as a Determinant of Physical Activity and Metabolic Control in Patients with Type 1 and Type 2 Diabetes Mellitus. Exp. Clin. Endocrinol. Diabetes 2021, 129, 379–384. [Google Scholar] [CrossRef]
  29. Maugeri, A.; Medina-Inojosa, J.R.; Kunzova, S.; Barchitta, M.; Agodi, A.; Vinciguerra, M.; Lopez-Jimenez, F. Dog Ownership and Cardiovascular Health: Results from the Kardiovize 2030 Project. Mayo Clin. Proc. Innov. Qual. Outcomes 2019, 3, 268–275. [Google Scholar] [CrossRef]
  30. Forbes, C.C.; Blanchard, C.M.; Mummery, W.K.; Courneya, K.S. Dog ownership and physical activity among breast, prostate, and colorectal cancer survivors. Psychooncology 2017, 26, 2186–2193. [Google Scholar] [CrossRef]
  31. Kuban, M.; Królikowski, J.; Nowicki, M. Dog ownership status and self-assessed health, life-style and habitual physical activity in chronic hemodialysis patients. Hemodial Int. 2016, 20, 447–452. [Google Scholar] [CrossRef] [PubMed]
  32. Hancock, J.; Jackson, S.; Johnson, A.B. The Importance of Dog Ownership: Implications for Long-Term Weight Reduction after Gastric Banding. Am. J. Lifestyle Med. 2016, 11, 86–89. [Google Scholar] [CrossRef] [PubMed]
  33. Jones, P.W.; Harding, G.; Berry, P.; Wiklund, I.; Chen, W.H.; Kline Leidy, N. Development and first validation of the COPD Assessment Test. Eur. Respir. J. 2009, 34, 648–654. [Google Scholar] [CrossRef] [Green Version]
  34. Singh, D.; Agusti, A.; Anzueto, A.; Barnes, P.J.; Bourbeau, J.; Celli, B.R.; Criner, G.J.; Frith, P.; Halpin, D.M.G.; Han, M.; et al. Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Lung Disease: The GOLD science committee report 2019. Eur. Respir. J. 2019, 53, 1900164. [Google Scholar] [CrossRef] [PubMed]
  35. Devlin, N.J.; Brooks, R. EQ-5D and the EuroQol group: Past, present and future. Appl. Health Econ. Health Policy 2017, 15, 127–137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Wacker, M.E.; Jörres, R.A.; Karch, A.; Koch, A.; Heinrich, J.; Karrasch, S.; Schulz, H.; Peters, A.; Gläser, S.; Ewert, R.; et al. Relative impact of COPD and comorbidities on generic health-related quality of life: A pooled analysis of the COSYCONET patient cohort and control subjects from the KORA and SHIP studies. Respir. Res. 2016, 17, 81. [Google Scholar] [CrossRef] [Green Version]
  37. Yellen, S.B.; Cella, D.F.; Webster, K.; Blendowski, C.; Kaplan, E. Measuring fatigue and other anemia-related symptoms with the Functional Assessment of Cancer Therapy (FACT) measurement system. J. Pain Symptom. Manag. 1997, 13, 63–74. [Google Scholar] [CrossRef]
  38. Stridsman, C.; Skär, L.; Hedman, L.; Rönmark, E.; Lindberg, A. Fatigue affects health status and predicts mortality among subjects with COPD: Report from the population based OLIN COPD study. J. Chronic Obstr. Pulm. Dis. 2015, 12, 199–206. [Google Scholar] [CrossRef]
  39. Stridsman, C.; Svensson, M.; Johansson Strandkvist, V.; Hedman, L.; Backman, H.; Lindberg, A. The COPD Assessment Test (CAT) can screen for fatigue among patients with COPD. Ther. Adv. Respir. Dis. 2018, 12, 1753466618787380. [Google Scholar] [CrossRef] [Green Version]
  40. Baghai-Ravary, R.; Quint, J.K.; Goldring, J.J.; Hurst, J.R.; Donaldson, G.C.; Wedzicha, J.-A. Determinants and impact of fatigue in patients with chronic obstructive pulmonary disease. Respir. Med. 2009, 103, 216–223. [Google Scholar] [CrossRef]
  41. Cella, D. Manual of the Functional Assessment of Chronic Illness Therapy (FACIT) Measurement System; Center on Outcomes, Research and Education (Core), Evanston Northwestern Healthcare and Northwestern University: Evanston, IL, USA, 1997. [Google Scholar]
  42. Lipovetsky, S.; Nowakowska, E. Modeling with Structurally Missing Data by OLS and Shapley Value Regressions. Int. J. Oper. Quant. Manag. 2013, 19, 169–178. [Google Scholar]
  43. Soares, J.; Epping, J.N.; Owens, C.J.; Brown, D.R.; Lankford, T.J.; Simoes, E.J.; Caspersen, C.J. Odds of Getting Adequate Physical Activity by Dog Walking. J. Phys. Act. Health 2015, 12, S102–S109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Arbillaga-Etxarri, A.; Gimeno-Santos, E.; Barberan-Garcia, A.; Balcells, E.; Benet, M.; Borrell, E.; Celorrio, N.; Delgado, A.; Jané, C.; Marin, A.; et al. Long-term efficacy and effectiveness of a behavioural and community-based exercise intervention (Urban Training) to increase physical activity in patients with COPD: A randomised controlled trial. Eur. Respir. J. 2018, 52, 1800063. [Google Scholar] [CrossRef] [PubMed]
  45. Powell, L.; Edwards, K.M.; Bauman, A.; McGreevy, P.; Podberscek, A.; Neilly, B.; Sherrington, C.; Stamatakis, E. Does dog acquisition improve physical activity, sedentary behaviour and biological markers of cardiometabolic health? Results from a three-arm controlled study. BMJ Open Sport Exerc. Med. 2020, 6, e000703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Brown, D.R.; Carroll, D.D.; Workman, L.M.; Carlson, S.A.; Brown, D.W. Physical activity and health-related quality of life: US adults with and without limitations. Qual. Life Res. 2014, 23, 2673–2680. [Google Scholar] [CrossRef] [Green Version]
  47. Ozdemir, K.; Keser, I.; Sen, I.; Ozgur Tan, M. Investigating the relationships between quality of life, fatigue and leisure time physical activity in prostate cancer patients. J. Back Musculoskelet. Rehabil. 2019, 32, 497–503. [Google Scholar] [CrossRef]
  48. Cui, Y.; Russel, M.; Davern, M.; Christian, H. Longitudinal evidence of the impact of dog ownership and dog walking on mental health. J. Public Health 2021, 43, e145–e152. [Google Scholar] [CrossRef]
  49. Waschki, B.; Spruit, M.A.; Watz, H.; Albert, P.S.; Shrikrishna, D.; Groenen, M.; Smith, C.; Man, W.D.; Tal-Singer, R.; Edwards, L.D.; et al. Physical activity monitoring in COPD: Compliance and associations with clinical characteristics in a multicenter study. Respir. Med. 2012, 106, 522–530. [Google Scholar] [CrossRef] [Green Version]
  50. Garcia-Rio, F.; Rojo, B.; Casitas, R.; Lores, V.; Madero, R.; Romero, D.; Galera, R.; Villasante, C. Prognostic value of the objective measurement of daily physical activity in patients with COPD. Chest 2012, 142, 338–346. [Google Scholar] [CrossRef]
  51. Pitta, F.; Troosters, T.; Probst, V.S.; Spruit, M.A.; Decramer, M.; Gosselink, R. Physical activity and hospitalization for exacerbation of COPD. Chest 2006, 129, 536–544. [Google Scholar] [CrossRef] [Green Version]
  52. Barberà, J.A.; Roca, J.; Ferrer, A.; Félez, M.A.; Díaz, O.; Roger, N.; Rodriguez-Roisin, R. Mechanisms of worsening gas exchange during acute exacerbations of chronic obstructive pulmonary disease. Eur. Respir. J. 1997, 10, 1285–1291. [Google Scholar] [CrossRef] [PubMed]
  53. Maltais, F.; LeBlanc, P.; Simard, C.; Jobin, J.; Bérubé, C.; Bruneau, J.; Carrier, L.; Belleau, R. Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 1996, 154, 442–447. [Google Scholar] [CrossRef] [PubMed]
  54. Das, U.N. Anti-inflammatory nature of exercise. Nutrition 2004, 20, 323–326. [Google Scholar] [CrossRef]
  55. Wright, R.A. Refining the prediction of effort: Brehm’s distinction between potential motivation and motivation intensity. Soc. Personal. Psychol. Compass 2008, 2, 682–701. [Google Scholar] [CrossRef]
  56. Westgarth, C.; Christley, R.M.; Christian, H.E. How might we increase physical activity through dog walking?: A comprehensive review of dog walking correlates. Int. J. Behav. Nutr. Phys. Act. 2014, 11, 83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Lim, C.; Rhodes, R.E. Sizing up physical activity: The relationships between dog characteristics, dog owners’ motivations, and dog walking. Psychol. Sport Exerc. 2016, 24, 65–71. [Google Scholar] [CrossRef]
  58. Fletcher, M.J.; Upton, J.; Taylor-Fishwick, J.; Buist, S.A.; Jenkins, C.; Hutton, J.; Barnes, N.; Van Der Molen, T.; Walsh, J.W.; Jones, P.; et al. COPD uncovered: An international survey on the impact of chronic obstructive pulmonary disease [COPD] on a working age population. BMC Public Health 2011, 11, 612. [Google Scholar] [CrossRef] [Green Version]
  59. Kwon, H.Y.; Kim, E. Factors contributing to quality of life in COPD patients in South Korea. Int. J. Chronic Obstr. Pulm. Dis. 2016, 13, 103–109. [Google Scholar] [CrossRef] [Green Version]
  60. Esquinas, C.; Ramon, M.A.; Nuñez, A.; Molina, J.; Quintano, J.A.; Roman-Rodríguez, M.; Naberan, K.; Llor, C.; Roncero, C.; Miravitlles, M.; et al. Correlation between disease severity factors and EQ-5D utilities in chronic obstructive pulmonary disease. Qual. Life Res. 2020, 29, 607–617. [Google Scholar] [CrossRef]
Figure 1. The distribution of FACIT score by dog-walking duration. Boxplots represent the median (central line), 25th–75th percentiles (box), and min-max non-outlier values (whiskers).
Figure 1. The distribution of FACIT score by dog-walking duration. Boxplots represent the median (central line), 25th–75th percentiles (box), and min-max non-outlier values (whiskers).
Healthcare 10 02317 g001
Table 1. Participant characteristics by dog-ownership.
Table 1. Participant characteristics by dog-ownership.
Overall
n = 200
Dog Owners
n = 99
Non-Dog Owners
n = 101
p-Value 1
Age (years)64.35 (9.56)62.9 (9.4)65.7 (9.6)0.038
Gender 1.000
  Male102 (51) 50 (51) 52 (51)
  Female98 (49) 49 (49) 49 (49)
Education ≥8 years132 (66) 69 (70) 63 (62) 0.345
Retired89 (44) 42 (42) 47 (47) 0.658
Living alone31 (16) 13 (13) 18 (18) 0.471
Physical activity frequency 0.071
  Never/hardly ever63 (32) 27 (27) 36 (36)
  <1 times/week29 (14) 11 (11) 18 (18)
  1–2 times/week36 (18) 16 (16) 20 (20)
  3–4 times/week26 (13) 18 (18) 8 (8)
  Almost every day46 (23) 27 (27) 19 (19)
Dog-ownership duration -
  Non-dog owner101 (50) 0 (0) 101 (100)
  0–2 years14 (7) 14 (14) 0 (0)
  3–5 years34 (17) 34 (34) 0 (0)
  >5 years51 (26) 51 (52) 0 (0)
Dog-walking duration -
  Non-dog owner101 (50) 0 (0) 101 (100)
  <15 min40 (20) 40 (40) 0 (0)
  15–30 min47 (24) 47 (47) 0 (0)
  >30 min12 (6) 12 (13) 0 (0)
Data are presented as n (%) or mean (SD). 1 One-way ANOVA for quantitative variables, chi-square test for categorical variables. Significant p-values (<0.05) are in bold.
Table 2. The distribution of questionnaire scores (mean, SD) and exacerbations (n, %) by physical activity, dog-ownership duration, and dog-walking duration.
Table 2. The distribution of questionnaire scores (mean, SD) and exacerbations (n, %) by physical activity, dog-ownership duration, and dog-walking duration.
Physical ActivityNever/Hardly Ever
(1)
<1 Times/Week
(2)
1–2 Times/Week
(3)
3–4 Times/Week
(4)
Almost Every Day
(5)
p-Value 1Group
Separation 2
  CAT29.32 (5.35)23.17 (7.27)24.42 (5.13)24.15 (5.24)23.93 (5.80)<0.001{2543}{1}
  EQ5D0.69 (0.20)0.83 (0.13)0.81 (0.11)0.84 (0.08)0.85 (0.07)<0.001{1}{3245}
  VAS53.97 (14.19)64.45 (13.68)61.42 (13.45)62.69 (10.29)64.98 (10.50)<0.001{1}{3425}
  FACIT23.27 (8.75)32.72 (10.99)31.89 (7.89)32.54 (9.53)31.96 (8.62)<0.001{1}{3542}
  >1 exacerb.35 (56) 13 (45) 8 (22) 5 (19) 12 (26) <0.001{4352}{21}
Dog-ownershipNon-dog owner
(1)
0–2 years
(2)
3–5 years
(3)
>5 years
(4)
-p-value 1Group
separation 2
  CAT25.16 (6.31)24.86 (8.24)25.32 (5.35)27.00 (5.87)-0.340-
  EQ5D0.79 (0.15)0.83 (0.16)0.78 (0.17)0.79 (0.15)-0.735-
  VAS60.45 (14.99)66.57 (10.19)60.47 (9.43)58.94 (13.02)-0.316-
  FACIT29.03 (9.14)32.57 (14.17)29.38 (9.87)29.25 (10.06)-0.663-
  >1 exacerb.41 (41) 3 (21) 10 (29) 19 (37) -0.415-
Dog-walkingNon-dog owner
(1)
<15 min
(2)
15–30 min
(3)
>30 min
(4)
-p-value 1Group
separation 2
  CAT25.16 (6.31)27.52 (6.55)25.49 (5.40)23.92 (6.47)-0.154-
  EQ5D0.79 (0.15)0.74 (0.20)0.82 (0.11)0.88 (0.06)-0.015{213}{34}
  VAS60.45 (14.99)58.42 (12.71)60.77 (10.47)66.75 (11.34)-0.313-
  FACIT29.03 (9.14)26.77 (11.05)30.55 (9.82)36.67 (8.81)-0.017{213}{34}
  >1 exacerb.41 (41) 15 (38) 14 (30) 3 (25) -0.504-
1 One-way ANOVA for quantitative variables, chi-square test for categorical variables. Significant p-values (<0.05) are in bold. 2 Group separation: group numbers are reported in increasing order of mean/percentage for each variable. After applying the Holm’s method for multiple comparisons, significant separation occurs between groups included within different pairs of brackets. For instance, {213}{34} indicates similarity between pairs 2–1, 2–3, 1–3 and 3–4, and a statistically significant difference between pairs 2–4 and 1–4. CAT: COPD Assessement Test; FACIT-Fatigue: Functional Assessment of Chronic Illness Therapy Fatigue Scale; VAS: visual analogue scale.
Table 3. Questionnaire scores: crude and adjusted β coefficients (mean differences) and 95% confidence intervals from linear regression models.
Table 3. Questionnaire scores: crude and adjusted β coefficients (mean differences) and 95% confidence intervals from linear regression models.
Unadjusted ModelsCATEQ5DVASFACIT
βp-Valueβp-Valueβp-Valueβp-Value
Intercept23.92 (20.41, 27.43)<0.0010.88 (0.85, 0.91) §<0.00166.75 (59.12, 74.38)<0.00136.67 (31.15, 42.18)<0.001
Dog-walking >30 min (ref.)--------
  Non-dog owner 1.24 (−2.47, 4.96)0.510−0.09 (−0.14, −0.05) §0.043−6.30 (−14.38, 1.77)0.125−7.64 (−13.47, −1.80)0.011
  Dog-walking <15 min3.61 (−0.39, 7.61)0.077−0.14 (−0.22, −0.08) §0.004−8.33 (−17.03, 0.38)0.061−9.89 (−16.18, −3.60)0.002
  Dog-walking 15–30 min1.57 (−2.36, 5.51)0.431−0.07 (−0.11, 0.02) §0.177−5.98 (−14.54, 2.57)0.169−6.11 (−12.29, 0.07)0.053
Adjusted ModelsCATEQ5DVASFACIT
βp-Valueβp-Valueβp-Valueβp-Value
Intercept29.51 (22.16, 36.87)<0.0010.77 (0.59, 0.97) §<0.00166.14 (50.44, 81.83)<0.00114.28 (3.13, 25.43)0.012
Dog-walking >30 min (ref.)--------
  Non-dog owner −0.42 (−3.91, 3.07)0.813−0.05 (−0.10, 0.01) §0.262−2.23 (−9.68, 5.21)0.555−6.00 (−11.29, −0.71)0.026
  Dog-walking <15 min1.60 (−2.16, 5.37)0.402−0.09 (−0.16, −0.03) §0.043−3.98 (−12.01, 4.06)0.330−7.61 (−13.32, −1.90)0.009
  Dog-walking 15–30 min0.77 (−2.86, 4.41)0.675−0.04 (−0.09, 0.01) §0.348−3.28 (−11.04, 4.49)0.406−4.97 (−10.49, 0.54)0.077
Age (unit increase)−0.03 (−0.15, 0.08)0.5840.0007 (−0.002, 0.003) §0.584−0.02 (−0.27, 0.23)0.8680.31 (0.13, 0.49)0.001
Female gender0.88 (−0.75, 2.51)0.287−0.03 (−0.07, 0.01) §0.098−6.63 (−10.1, −3.15)<0.001−2.10 (−4.56, 0.37)0.095
Education <8 years0.14 (−1.74, 2.02)0.883−0.02 (−0.07, 0.02) §0.334−1.75 (−5.77, 2.26)0.390−1.2 (−4.06, 1.65)0.406
Retired 1.08 (−1.09, 3.24)0.327−0.06 (−0.10, −0.01) §0.021−5.75 (−10.37, −1.13)0.015−4.64 (−7.92, −1.36)0.006
Living alone 2.23 (0.03, 4.43)0.047−0.05 (−0.12, 0.02) §0.064−1.27 (−5.98, 3.43)0.594−3.85 (−7.19, −0.51)0.024
Physical activity−4.92 (−6.72, −3.12)<0.0010.12 (0.07, 0.17) §<0.0017.31 (3.46, 11.16)<0.0017.20 (4.47, 9.94)<0.001
Significant p-values (<0.05) are in bold. § Bootstrap confidence intervals (1000 replications).
Table 4. Exacerbations: crude and adjusted odds ratios and 95% confidence intervals from logistic regression models.
Table 4. Exacerbations: crude and adjusted odds ratios and 95% confidence intervals from logistic regression models.
Unadjusted Models>1 Exacerbations
Odds Ratiop-Value
Dog-walking >30 min (ref.)--
  Non-dog owner2.05 (0.57, 9.66)0.303
  Dog-walking <15 min1.80 (0.45, 9.07)0.428
  Dog-walking 15–30 min1.27 (0.32, 6.38)0.744
Adjusted Models>1 Exacerbations
Odds Ratiop-Value
Dog-walking >30 min (reference)--
  Non-dog owner1.31 (0.32, 6.81)0.725
  Dog-walking <15 min1.02 (0.22, 5.71)0.985
  Dog-walking 15–30 min0.85 (0.19, 4.63)0.839
Age (unit increase)0.96 (0.92, 1.01)0.123
Female gender1.42 (0.75, 2.68)0.279
Education <8 years0.70 (0.32, 1.47)0.347
Retired2.63 (1.10, 6.56)0.033
Living alone0.76 (0.31, 1.78)0.541
Regular physical activity §0.30 (0.15, 0.57)<0.001
Significant p-values (<0.05) are in bold. § At least once a week.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Baiardini, I.; Fasola, S.; Lorenzi, C.; Colombo, N.; Bruno, M.; La Grutta, S.; Scognamillo, C.; Braido, F. Might Dog Walking Reduce the Impact of COPD on Patients’ Life? Healthcare 2022, 10, 2317. https://doi.org/10.3390/healthcare10112317

AMA Style

Baiardini I, Fasola S, Lorenzi C, Colombo N, Bruno M, La Grutta S, Scognamillo C, Braido F. Might Dog Walking Reduce the Impact of COPD on Patients’ Life? Healthcare. 2022; 10(11):2317. https://doi.org/10.3390/healthcare10112317

Chicago/Turabian Style

Baiardini, Ilaria, Salvatore Fasola, Chiara Lorenzi, Nicole Colombo, Matteo Bruno, Stefania La Grutta, Carla Scognamillo, and Fulvio Braido. 2022. "Might Dog Walking Reduce the Impact of COPD on Patients’ Life?" Healthcare 10, no. 11: 2317. https://doi.org/10.3390/healthcare10112317

APA Style

Baiardini, I., Fasola, S., Lorenzi, C., Colombo, N., Bruno, M., La Grutta, S., Scognamillo, C., & Braido, F. (2022). Might Dog Walking Reduce the Impact of COPD on Patients’ Life? Healthcare, 10(11), 2317. https://doi.org/10.3390/healthcare10112317

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop