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Measurement of Physical Activity in Adults with Muscular Dystrophy: A Systematic Review

Sarah F. Roberts-Lewis*, Michael R. Rose, Claire M. White, Farah Seedat

School of Population Health and Environmental Sciences, King’s College London, SE1 1UL, United Kingdom

Abstract: There is little consensus about measurement of physical activity in adults with muscular dystrophy. This systematic review summarizes evidence for measurement properties of direct and indirect measures of physical activity in adults with muscular dystrophy. A two-phase search for peer-reviewed articles identified firstly, studies which measured physical activity in this population and secondly, studies reporting the measurement properties of activity measures. Methodological quality was assessed using COSMIN guidelines and a best evidence synthesis conducted. Phase 1 included 53 studies identifying 63 measures including accelerometers, direct observation, heartrate monitors, calorimetry, positional sensors, activity diaries, single scales and questionnaires. Phase 2 included 26 studies of measurement properties for 32 measures. Methodological quality of the included studies was low, only 2 were rated good. There was insufficient evidence to robustly recommend any physical activity measures and further research is required to validate measures of physical activity for adults with muscular dystrophy. Based on the findings of this review, measures with potential for further study have been highlighted.

Keywords: measure, physical activity, muscular dystrophy, adult, validity

Received November 04, 2018; Revised December 07, 2018; Accepted December 18, 2018

Citation: Sarah F. Roberts-Lewis, Michael R. Rose, Claire M. White, Farah Seedat, Measurement of Physical Activity in Adults with Muscular Dystrophy: A Systematic Review. Journal of Physical Activity Research, 4 (1). 1-25. January 2019. doi:10.12691/jpar-4-1-1

1. Introduction

The aim of this review was to appraise measures of physical activity for the assessment of adults with muscular dystrophy. Effective physical activity measurement is important to evaluate outcomes in randomised controlled trials (RCTs), to monitor disease progression and to make recommendations for optimising physical activity [1]. For adults with muscular dystrophy, physical activity has been linked to health benefits, such as improved fitness and self-management [2,3]. However, more research reporting quantified physical activity levels is required to determine optimal activity for adults with muscular dystrophy and to evaluate potential risks, such as exercise-induced damage to dystrophic muscle [4,5].

Figure 1. FITT framework for measurement of physical activity. Diagram created by author (SRL) based on common clinical practice and physical activity measurement analysis frameworks applied in the literature [8,9]

Physical activity is defined as behaviours involving bodily movements and energy expenditure [6,7]. Measurement of physical activity can be defined using a well-recognised conceptual framework [8,9] which considers Frequency, Intensity, Timing and Type (FITT) of activity or overall measurement encompassing these parameters (see Figure 1).

The qualities of measurement tools can be defined in terms of measurement characteristics and properties, according to the COnsensus-based Standards for the selection of health Measurement INstruments (COSMIN) taxonomy [10] (see Figure 2).

Measurement characteristics (generalizability and interpretability) of physical activity measures are variable because they depend on population and setting, and because there are numerous diverse ways to measure physical activity. These include indirect self-report tools, such as diaries and questionnaires, and direct tools which record the physiological consequences of activity, including bodily movements, metabolism and cardio-respiratory responses [11,12]. The characteristic pros and cons of these measurement tools (such as ease of use, burden, range and ability to capture FITT parameters) have been discussed in healthy individuals [8,12,13,14,15] older adults [9], wheelchair users [16] and people with neuromuscular diseases [17]. However, it is not known which measures might be most suitable for the assessment of physical activity specifically in adults with muscular dystrophy which is characterised by progressive weakness, heterogeneous presentations and variable function. It is therefore important to ascertain the generalizability and interpretability of physical activity measures in adults with muscular dystrophy to aid selection of appropriate measurement tools.

Figure 2. Framework of measurement characteristics and measurement properties. Diagram created by author (SRL) based on COnsensus-based Standards for the selection of health Measurement INstruments (COSMIN) checklist [28] and manual taxonomy and definitions [10]

The measurement properties (reliability, responsiveness and validity) of physical activity measures have also been investigated in multiple studies in various populations, including other neurological, rheumatological, oncological or pulmonary conditions and healthy, elderly, disabled or cognitively impaired individuals [9,12,13,17]. However, cumulative evidence is inconclusive due to conflicting reports, varied study design, diversity of measures and lack of consensus about gold standard criterion measures. Furthermore, reliability, responsiveness and validity of physical activity measures established in other populations may not be transferable to adults with muscular dystrophy who may have very different muscle, metabolic and cardiac functioning [18,19,20,21]. Thus, the measurement properties of physical activity measures when used with adults with muscular dystrophy remain unclear. To the authors’ knowledge, this is the first review to examine population specific evidence for the reliability, responsiveness and validity of physical activity measurement in adults with muscular dystrophy.

The objectives of this review were, firstly, to identify direct and indirect physical activity measures used to assess adults with muscular dystrophy in a range of study designs and to describe their generalizability and interpretability. Secondly, to appraise the evidence of reliability, responsiveness and validity for physical activity measures in studies which included adults with muscular dystrophy. Finally, based on a narrative synthesis, to make recommendations, where possible, for the selection of suitable physical activity measurement tools for use with adults who have muscular dystrophy.

2. Methods

The protocol was registered on PROSPERO in July 2017 (Registration Number CRD42017070514) and follows the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines [22].

2.1. Search

The search was conducted in 2 phases. Phase 1 was designed to identify physical activity measures used to assess adults with muscular dystrophy and to describe their generalizability and interpretability. Phase 2 was designed to identify and appraise evidence for their reliability, responsiveness and validity.

In July 2017 (phase 1) and January 2018 (phase 2) the following databases were searched: Medline (1946-2017/8), Embase + Embase Classic (1947-2017/8), Global Health (1973-2017/8), PsycINFO (1806-2017/8), HMIC Health Management Information Consortium (1979-2017/8) and Journals @ Ovid Full Text. In phase 1, Ovid search terms were expanded from ‘muscular dystrophy’, ‘physical activity’ and ‘measure’. In phase 2, the search strategy was informed by the previous search results and additional ‘measurement property’ search terms were added. (For full search see supplementary material appendix I.)

2.1.1. Study Selection

Studies were selected by 3 reviewers using the eligibility criteria listed in Table 1. (In phase 1: SRL and CW (10% sample); in phase 2: SRL, FS and CW (10% sample)). Disagreements were resolved by consensus discussion at this stage and throughout (arbitrated by CW).

Studies of any design were included if they had measured physical activity in any adult(s) with muscular dystrophy. Only studies where the measurement of activity spanned more than 10 minutes were included as shorter bouts of activity are not considered to contribute to recommended daily activity tallies [23,24,25]. The FITT framework (see Figure 1) was applied to ensure that only those intending to quantify physical activity overall or in 3 or more FITT parameters were included. When several reports pertained to the same study, the most recent or comprehensive article in terms of physical activity measurement was selected. In phase 2, inclusion was further limited to full text articles that evaluated reliability, responsiveness and validity. A scarcity of physical activity measurement evaluation studies in adults with muscular dystrophy was anticipated. So, inclusion encompassed not only studies that overtly reported validity, reliability and responsiveness but also those that included hypothesis testing which incidentally indicated measurement properties of physical activity measures.

2.1.2. Data Extraction

The data extraction form was developed a priori, customised from previously published extraction tools [26,27] (see supplementary material appendix II). In phase 1, descriptive data were extracted by a single reviewer (SRL). In phase 2, 2 reviewers (SRL and FS) independently extracted the data.

2.1.3. Methodological Quality

In phase 1, methodological quality assessment was unnecessary because data were descriptive only. In phase 2, methodological quality was independently assessed by 2 reviewers (SRL and FS) using the COSMIN guidelines [28] to rate evidence supporting measure reliability, responsiveness or validity as excellent, good, fair or poor.

2.1.4. Synthesis

In phase 1, physical activity measures identified were described, listed and categorised. Their generalizability was quantified in terms of number of studies, number of participants, demographics (including age range, gender, diagnoses and mobility) and environment. Their interpretability was considered in terms of FITT measurement scope (i.e. capture of how often and how long different activities were carried out for and at what intensity, for example light, moderate or vigorous), timeframe, mode, metric and range of scores. In phase 2, evidence, and its methodological quality rating, for the validity, reliability and responsiveness of physical activity measures was listed for each included study. A narrative synthesis was carried out, considering the strength and consistency of evidence.

Table 1. Inclusion and exclusion criteria

Figure 3. Study selection schematics for phase 1 (A) and phase 2 (B)

3. Results

3.1. Phase 1

Study selection is summarised in Figure 3a. Agreement between reviewers (SRL and CW) was 90% and 87% for abstract and full text screening respectively, with full agreement after consensus discussion. Included articles are listed and described in Table 2; 63 physical activity measures were identified (see Table 3 and 3a supplement).

3.1.1. Generalizability

Activity measurement was generalizable across gender, mobility from independent walking to wheelchair use, age range from teenager to elderly and amongst different muscular dystrophy diagnoses. Myotonic Dystrophy and Facioscapulohumeral Dystrophy were the most commonly assessed. Indirect measures were used to assess larger numbers of participants than direct measures, particularly standardised questionnaires (n=1567). Of the direct measures, the greatest number of participants were assessed using accelerometry (n=731). Many studies used standardised questionnaires, non-standardised diaries, heartrate monitoring, direct observation and accelerometry (15 studies [29,30,31,32,33,34,35,36,37,38,39,40,41,42,43] including 3 RCTs [29,33,41], 18 studies [29,33,40,41,44,45,46,47,48,49,50,51,52,53,54,55,56,57] including 4 RCTs [33,41,44,48], 15 studies [29,33,40,44,45,48,49,50,51,52,53,54,55,58,59] including 5 RCTs [29,33,44,48,58], 13 studies [29,44,48,51,58,59,60,61,62,63,64,65,66] including 4 RCTs [29,48,58,65] and 13 studies [29,33,37,41,44,46,53,61,67,68,69,70,71] including 6 RCTs [29,33,41,44,67,68] respectively). Whereas, single and sub-scale activity measures, calorimetry and positioning systems were the least widely used in the fewest participants.

Free-living physical activity was most usually assessed, especially by questionnaires, diaries, continuous heartrate monitoring and accelerometry. However, prescribed activities were also assessed at home and in other environments, including the gym, sports pitch and laboratory, where activity was monitored by indirect calorimetry, periodic heartrate monitoring and some training logs.

The most generalizable tools within each category, used in the most studies and participants with the widest spectrum of demographics, included 2 standardised questionnaires (the International Physical Activity Questionnaire (IPAQ), the Physical Activity Scale for Individuals with Physical Disabilities (PASIPD)), activity logs, Polar heartrate monitors and triaxial, ankle accelerometers (although, the only accelerometer used to assess non-ambulant participants was wrist-worn [46]).

Table 2. Description of 53 included studies

Table 3. List of 63 measures used to assess adults with muscular dystrophy

3.1.2. Interpretability

Indirect measures collected activity spanning 3 days to a year (or lifetime), some in real-time, including activity diaries of 3 days to 6 months, and others by recall, including standardised questionnaires often over 7 days. Whereas, all direct measures recorded activity in real-time from 10 minutes to 6 months. Most recording periods lasted 1-14 days, except for direct observation, periodic heartrate monitoring and indirect calorimetry which were conducted over shorter timeframes of between 10-90 minutes. There was great variability in the metrics of activity measures, making it difficult to compare activity measurement ranges (see table 3 and 3a supplement). Standardised questionnaires and diaries had the best scope to quantify discrete FITT parameters; whereas direct measures like accelerometry and energy expenditure calculations were usually concerned with overall physical activity.

Interpretability was boosted by using multiple physical activity measures in 32 included studies [29,32,33,36,37,38,40,41,44,45,46,48,49,50,51,52,53,54,55,56,57,58,59,60,62,63,64,65,66,72,73,74], including 7 of the 9 RCTs [29,33,41,44,48,58,65]. Multiple measures increased the scope of physical activity measurement in terms of FITT in 29 studies [29,33,38,40,41,44,45,46,48,49,50,51,52,53,54,55,56,57,58,59,60,62,63,64,65,66,72,73,74] and ocomplementary indirect and direct measures were employed in 29 studies [29,33,37,40,41,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,60,62,63,64,65,66,72,73,74].

Table 4. Study characteristics of studies and evaluated measures included in phase 2

3.2. Phase 2

Study selection is summarised in Figure 3b. Agreement between the 2 reviewers (SRL and FS) was 86%, 87%, 91% and 86% for abstract, full text screening, data extraction and COSMIN ratings respectively, with full agreement after consensus discussion. Evidence for the reliability, responsiveness and validity of 32 physical activity measures is listed in Table 4 (and 4a supplement). Only 5 included studies [42,46,47,71,75] had as their primary objective the evaluation of measurement properties of a physical activity measure; the remaining 21 articles were included for incidental measurement properties from hypothesis testing relating to other objectives. No studies were rated as excellent; 2 were rated as good [36,42], 12 as fair and 11 as poor. This was largely due to low sample sizes and incidental measure evaluation.

3.2.1. Reliability and Responsiveness

There was very little evidence for reliability or responsiveness testing of any physical activity measures. Of the indirect measures, there was good quality evidence of internal consistency of the PASIPD from an evaluative study including 372 participants, an estimated 7% of whom had muscular dystrophy [42]. There was fair quality evidence of internal consistency of the Physical Self-Description Questionnaire (PSDQ-S) from an evaluative study including 50 participants, 8% of whom had muscular dystrophy [75]. There was also incidental report of moderate to high test-re-test reliability of the Canada Fitness Survey (CFS) [43,76].

Of the direct measures, there was poor quality evidence of good test-re-test reliability of the StepWatch [71] accelerometer and moderate measurement error of Ubitrak (a Wi-Fi and GPS (Global Positioning System) movement tracker) [47]. There was poor quality, incidental evidence of inter-rater reliability between indirect calorimetry gaseous analysers, K4 b2c and Oxycon Mobiled [60] and responsiveness of a pedometer compared to the Physical Activity Scale for the Elderly was tenuously indicated, as neither detected significant changes in physical activity post intervention [41].

3.2.2. Validity

There was a small amount of evidence supporting the validity of 2 indirect measures (see table 4). The strongest evidence was for the PASIPD, which had good quality evidence of significant discriminative validity between extreme groups [42] and some incidental, consistent, fair quality evidence for concurrent validity [30,32]. There was also fair quality evidence for convergent validity of the PSDQ-S activity subscale [75]. Based on incidental findings only, there was some cumulative evidence for 2 other questionnaires: The Bone-specific Physical Activity Questionnaire (BPAQ), which had consistent, fair quality evidence for discriminative validity [30,32] and convergent validity [32] and the IPAQ, which had good quality evidence for convergent validity [36] and mixed, poor quality evidence for [29] and against discriminative validity [31]. Evidence for the validity of other direct measures was even more sparse. However, incidental validity of diaries was tentatively indicated, including low quality evidence of discriminative validity for an activity diary [54,55] and convergent validity of a training log [48].

There was no good quality evidence supporting the validity of any direct measures. However, there was some collective, low-quality evidence concerning accelerometry and heartrate monitoring. There was cumulative, predominantly incidental, evidence of discriminative and convergent validity of accelerometry, which was stronger for triaxial accelerometers (Omron [29], Motionlogger [46] and Actilog [67,69]) than biaxial (StepWatch [70,71]) or uniaxial devices (Yamax digi-walker [53]) and for ankle [44,67,69,70,71] rather than trunk [29] or wrist [46] placement. There was incidental, consistent evidence for discriminative validity [40,54] and convergent validity [48] of Polar heartrate monitors and mixed evidence for [54,55] and against [53] discriminative validity of heartrate monitoring used with indirect calorimetry equivalence to estimate total energy expenditure.

4. Discussion

The main finding of this systematic review is that physical activity has been measured in numerous and various ways in a range of 53 studies assessing adults with muscular dystrophy. There is no consensus about the most generalizable or interpretable activity measurement tools for this group. Furthermore, evidence is limited about measure reliability, responsiveness and validity for the assessment of physical activity in adults with muscular dystrophy. Only 5 studies overtly evaluated the measurement properties of physical activity measures and none have provided high quality evidence of reliability, responsiveness and validity.

4.1. Direct Measures

Despite the paucity of evidence for reliability, responsiveness and validity of direct measures of physical activity in adults with muscular dystrophy, tools like accelerometry and heartrate monitoring might have potential. As demonstrated in the literature [9,14,15,16,77] and by the studies identified in this review, accelerometry and heartrate monitoring are both fairly generalizable and interpretable. Accelerometry can capture free-living activity over the medium (days/weeks) to long-term (months) and can detect frequency, absolute intensity, and timing, also yielding an overall quantification of physical activity. Although accelerometry cannot discern relative exertion or type of activity, it is adaptable, relatively inexpensive, and unobtrusive. In terms of measurement properties, tentative construct validity of accelerometry has been indicated in this review, with the best evidence in support of triaxial devices. Multi-plane movement detection, although not integral for regular walking, may be more suited to irregular torsions [78], characteristic of abnormal mobility in adults with muscular dystrophy [79]. Furthermore, for healthy people and those with chronic diseases, multi-axial devices have also demonstrated stronger criterion validity and lower measurement error than uniaxial devices [80]. Similarly, the triaxial GENEActiv has been validated over 6 minutes or less in adults with myotonic dystrophy [81] with construct validity supported incidentally in a high quality RCT [82] (too recent for inclusion in this systematic search) and the biaxial StepWatch has been extensively validated in ambulant people with Multiple Sclerosis, Parkinson’s Disease and children with Duchenne’s Muscular Dystrophy [71,83,84,85]. In contrast, criterion validity was reportedly low and measurement error unacceptably high for the uniaxial Digi-walker over 2 minutes, in ambulant adults with neuromuscular diseases, including muscular dystrophy [86]. In this review, there was more evidence for generalizability of accelerometer placement on the ankle than the trunk or wrist, although it came only from ambulant participants; whereas, wrist placement better encompassed a range of mobility including wheelchair users [46]. In the literature, wrist accelerometry has been linked to non-ambulant assessment [87] and lower measurement error at slow walking speeds [88] which may become relevant as muscular dystrophy progresses [79]. Thus, triaxial accelerometry, placed at the ankle or wrist, represents a potential tool for the assessment of physical activity in adults with muscular dystrophy, subject to establishing robust reliability, responsiveness and validity in both ambulant and non-ambulant.

Heartrate monitoring may also have potential, particularly for monitoring compliance with, and recording intensity of, prescribed exercise interventions in adults with muscular dystrophy. In this review there were tentative indications for construct validity of Polar devices. They are generalizable and can record frequency, timing and relative intensity of exertion, which is particularly useful for quantifying prescribed activity [89]. However, heartrate monitors cannot differentiate between activity and emotional heartrate responses, thus there is a requirement to collect supplementary information, such as a diary or predetermined personal activity zone heartrates [54,55]. In addition, reduced heartrate variability in muscular dystrophies [20] might impact the interpretation of heartrate comparisons, especially relative to predicted values. Higher resting and lower submaximal/maximal heartrates have been reported in Duchenne’s Muscular Dystrophy [83] and increased sympathetic drive with progressive parasympathetic dampening in Facioscapulohumeral Dystrophy [21]. Similar caution is required for energy expenditure extrapolations from heartrate or accelerometry data due to potentially altered metabolic functioning in adults with muscular dystrophy [18,19,90,91]. Thus, it is advisable to report actual recorded heartrate in beats per minute, or absolute step counts, and to treat extrapolated values with circumspection.

4.2. Indirect Measures

The same reservations about energy expenditure extrapolations must be applied to indirect measures that estimate metabolic expenditure. Additional caution is also necessary when interpreting questionnaire scores due to the potential for self-report, re-call and/or social desirability bias, which usually produce overestimations [8]. However, indirect, self-report measures of physical activity for adults with muscular dystrophy are widely generalizable, inexpensive, acceptable and easy to use [9,11,12].

Several standardized questionnaires were identified as having potential in this review. The PASIPD had the strongest evidence supporting its reliability and validity which is consistent with evidence from other populations including strong test-re-test reliability [92,93], discriminative validity [94] and low [92,93,95,96] to moderate [94] criterion validity. However, significant overestimation measurement error has been reported [95]. In terms of interpretability, PASIPD comprehensively covers FITT and is sensitive to disabled and low-level activities, although it is unsuitable for comparisons with non-disabled populations. The IPAQ, BPAQ and PSDQ-S are suitable for comparison with other populations; the BPAQ and PSDQ-S are situation specific to bone health [97] and self-perception [98] respectively. The IPAQ is the most generalizable questionnaire identified in this review and various versions are available including short, long and modified versions (more sensitive to lower activity intensities and non-ambulant mobility [99,100]). In this review, the validity of the IPAQ was inconclusive. However, measurement properties established in other populations include strong test-re-test reliability [23,101,102] moderate responsiveness [103,104], low [23,100,101,103,104] to moderate [23,105] criterion and convergent [105] validity and predominantly overestimation measurement error [104,106]. Thus, if acceptable reliability, responsiveness and validity can be established and energy expenditure scores are treated circumspectly, both the PASIPD and IPAQ have potential for the assessment of physical activity in adults with muscular dystrophy.

Activity diaries also have potential as generalizable and interpretable activity measures, especially those designed to span FITT which are often used for prescribed activity monitoring. In addition, diaries might have potential as an adjunctive activity measure. Supplementary activity logs have been shown, for example, to mitigate IPAQ overestimation [107] and to improve criterion validity and measurement error [104]. Diaries have also been advocated alongside direct activity measures [14,15] and, in this review, diaries appeared to strengthen interpretation of heartrate monitoring and indirect calorimetry equivalence [53,54,55]. Activity diaries are, therefore, not only useful for monitoring prescribed activity, they may have an application as adjuncts to enhance interpretability of free-living physical activity measurement.

4.3. Implications

Clearly, all physical activity measures have limitations, both general and specific to adults with muscular dystrophy. These must be considered in study design and some authors have compiled checklists to aid measure selection [17,108]. There is also an argument, reflected by the findings of this review, for a multi-measurement approach, where multiple, complementary activity measures are employed, to improve the interpretation of physical activity measurement [14,15,16,80] and potentially improve measurement properties [104,107]. Recall bias can be neutralised by triangulation with real-time measurement and social desirability responding can be minimised by the knowledge that responses will be verified directly [109]. Recording both relative and absolute activity, by heartrate monitoring and accelerometry or GPS, can enrich physical activity data interpretation and has also been shown to improve measurement properties [110,111,112,113]. Thus, diaries, heartrate monitoring and, possibly, GPS might be suitable adjuncts to standardised questionnaires or accelerometry. A multi-measurement approach is recommended for the assessment of physical activity in adults with muscular dystrophy.

The current lack of research evaluating measurement properties of physical activity measurement in adults with muscular dystrophy means that authors should be encouraged to report study level reliability and validity of the measures employed in trials or observational studies.

In addition, measure evaluation studies are required to determine the validity, reliability and responsiveness of physical activity measures for use with adults with muscular dystrophy. The evidence, both evaluative and incidental, compiled in this review was predominantly low quality-rated, often linked to sample sizes below the 50-100 participant threshold set by COSMIN for high quality-ratings [27]. Sample size challenges include the rarity of adults with muscular dystrophy and restricting study designs to single diagnoses and/or separating ambulant and non-ambulant [1,17]. In larger samples, it is also difficult to find an activity measure suitable to encompass activity heterogeneity within and between muscular dystrophic diagnoses [114,115] and stages of disease progression [116,117,118]. Restrictive sampling is advocated for experimental designs [1]. However, to optimise statistical power, a larger, heterogeneous sample (with whole and sub-group analyses) is recommended for future evaluative studies where measurement properties are to be elucidated.

For evaluative research, it is also difficult to identify a gold-standard criterion measure of physical activity. In the wider physical activity literature, criterion measures include calorimetry, accelerometry and direct observation [8,12,13,119]. Due to burden and cost, direct observation and indirect calorimetry are limited to smaller samples and short timeframes (<1 day). Calorimetry by double-labelled water is suitable over a timeframe of 1-2 weeks, but burdensome. Energy expenditure calculations should also be viewed with caution because calorimetry is likely to be impacted by metabolic abnormalities and progressive physiological changes in muscular dystrophy [18,19,90]. Whereas, direct observation has inherent content validity [119] and, in this review, it was interpretable and generalizable in 13 studies. Thus, it represents a suitable, initial gold-standard criterion for short-term validation. Accelerometry is generalizable in larger samples and over various timeframes. Thus, accelerometry, with prior validation against direct observation, might represent a suitable criterion against which to validate other activity measures for adults with muscular dystrophy.

4.4. Strengths and Limitations

To the authors’ knowledge, this is the first systematic review about measurement characteristics and properties of physical activity measures specifically for adults with muscular dystrophy. The review employed a broad, sensitive search strategy, 3 independent reviewers and rigorous COSMIN appraisal. However, there are some limitations. These include, firstly, exclusion of non-English language articles which means relevant articles published in other languages may have been missed. Nevertheless, a recent review of physical activity measures in adults and children with neuromuscular diseases [17] did not identify additional measurement approaches beyond those identified in this review; which suggests no pertinent measures were missed. Secondly, there is potential for bias in phase 1 as only a 10% sample was second reviewed and there was no methodological appraisal. However, the descriptive nature of phase 1 was straightforward, and the methodological quality of the studies did not impact description of the tool. Thirdly, COSMIN methodology was developed for patient-reported outcome measures, and as such, the participant number cut offs may be too stringent for direct measure evaluation where smaller participant numbers can be statistically robust [120]. Finally, risk of reporting bias was introduced by the inclusion of incidental hypothesis testing (indicative of discriminative or convergent relationships for which null findings are less frequently reported) thus the case for construct validity might have been artificially inflated.

5. Conclusions

Accelerometry, heartrate monitoring, direct observation, calorimetry, GPS, questionnaires and diaries have been used to assess physical activity in adults with muscular dystrophy. They were largely generalizable for adult age ranges, both genders and ambulant and non-ambulant people with a range of muscular dystrophy diagnoses. However, interpretability varied between measures and there was insufficient evidence to support their reliability, validity or responsiveness for use with adults who have muscular dystrophy. Measures identified as having most potential in this review included multi-axial accelerometry and the PASIPD questionnaire. Future evaluative studies of these, and/or other, physical activity measures for use with adults with muscular dystrophy are required. Future evaluative study design should consider direct observation as a fundamental criterion and maximizing sample size. Study design should include an awareness of activity measure limitations (in general and specific to muscular dystrophy) and the potential for improved interpretability by multi-measurement.

Acknowledgements

Medical Research Council PhD studentship funding. The authors have no competing interests.

References

Appendix 1. Full search

1. EXP Muscular Dystrophies

2. Muscular dystrophy

3. Facioscapulohumeral

4. Limb girdle muscular dystrophy

5. Becker’s muscular dystrophy

6. Myotonic dystrophy

7. Sarcoglycanopathy

8. Duchene muscular dystrophy

9. 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8

10. Wheelchair

11. 9 or 10

12. Physical activity

13. EXP human activities/ or “activities of daily living”/ or EXP social participation/ or EXP exercise/ or EXP circuit-based exercise/ or EXP cool-down exercise/ or EXP muscle stretching exercises/ or EXP physical conditioning, human/ or EXP plyometric exercise/ or EXP resistance training/ or EXP running/ or EXP swimming/ or EXP walking/ or EXP warm-up exercise/ or leisure activities/ or recreation/ or dancing/ or gardening/ or EXP sports/ or EXP athletic performance/ or EXP physical endurance/ or EXP physical fitness/ or baseball/ or basketball/ or EXP bicycling/ or boxing/ or football/ or golf/ or gymnastics/ or hockey/ or martial arts/ or mountaineering/ or racquet sports/ or return to sport/ or running/ or jogging/ or skating/ or snow sports/ or soccer/ or EXP sports for persons with disabilities/ or swimming/ or “track and field”/ or volleyball/ or weight lifting/ or wrestling/ or youth sports/

14. EXP Motor Activity

15. Energy expenditure

16. Exercise

17. Exercise movement techniques/ or breathing exercises/ or dance therapy/ or tai ji/ or yoga/

18. Exercise Test/ or Warm-Up Exercise/ or Cool-Down Exercise/ or Exercise Therapy/ or Plyometric Exercise/ or Circuit-Based Exercise/ or Exercise Tolerance/ or exp Exercise/ or Exercise Movement Techniques/

19. Aerobic

20. Training

21. 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20

22. Measures

23. Self report

24. Test

25. Score

26. Scale

27. Ergometer

28. Accelerometer

29. Actometer

30. Pedometer

31. Treadmill

32. Questionnaire

33. Assess

34. Index

35. Level

36. MET

37. Week

38. Frequency

39. Intensity

40. 22 or 23 or 24 or 25 or 26 or 27 or 28 or 29 or 30 or 31 or 32 or 33 or 34 or 35 or 36 or 37 or 38 or 39

41. Evaluation.mp. or EXP evaluation study/

42. EXP methodology/ or EXP validation process/ or valid$.mp.

43. Sensitivity.

44. Specificity.

45. Reliability

46. EXP reliability/ or EXP observation/ or direct observation.mp.

47. Responsiveness

48. Validity

49. EXP outcome research/ or minimal clinically important difference.mp.

50. 41 or 42 or 43 or 44 or 45 or 46 or 47 or 48 or 49

51. 11 and 21 and 40

51. 50 and 51

52. EXP Health behaviour/ or EXP exercise/ or EXP Physical Activity/ or exercise behaviour.mp.

53. Workload.mp. or EXP Workload/

54. EXP resistance training or resistance.mp.

55. Effort.mp. or EXP exercise

56. Speed.mp. or EXP velocity/

57. Heart rate.mp. or EXP heart rate/

58. Pulse rate/ or Pulse watch.mp. or heart rate/

59. Heart monitor.mp.

60. EXP accelerometer/ or Ankle step watch.mp

61. EXP ambulatory monitoring/ or EXP Actimetry/ or EXP accelerometer/ or actigraph.mp.

62. Actometer.mp.

63. Muscle metabolism/ or EXP oxygen consumption/ or metabolism/ or oxidative capacity.mp.

64. EXP energy metabolism/ or EXP energy expenditure/ or metabolic enery expenditure.mp. or walking/

65. Movement tracking.mp.

66. GPS.mp.

67. Training log.mp.

68. Daily life activity/ or activity log.mp.

69. Training Diary.mp.

70. Physical activity/ or physical performance/ or activity diary.mp. or questionnaire/

71. EXP resitance training/ or EXP exercise intensity/ or EXP exercise test/ or EXP bicycle ergometry/ or rating of perceived exertion.mp. or EXP rating scale/

72. Borg.mp.

73. EXP rating scale/ or EXP visual analog scale/ or numerical rating scale.mp.

74. Semi structured interview/ or structure interview/ or interview.mp. or telephone interview/ or unstructured interview/ or interview/

75. Frenchay Activities Index.mp.

76. Checklist Individual Strength.mp.

77. Sickness Impact Profile.mp. or Sickness Impact Profile/

78. Activity Card Sort.mp.

79. Daily observation of activity.mp.

80. Bouchard.mp.

81. PASIPD.mp. or Physical Activity Scale for Individuals with Physical Disabilites.mp.

82. IPAQ.mp. or EXP reproducibility/ or EXP physical activity/ or questionnaire/ or EXP validation study/ or EXP walking/ or self report/

83. International Physical Activity Questionnaire.mp.

84. GLTEQ.mp. or Godin Leisure Time Exercise Questionnaire.mp.

85. Oxidative capacity.mp.

86. Physical self description questionnaire.mp.

87. 52 or 53 or 54 or 55 or 56 or 57 or 58 or 59 or 60 or 61 or 62 or 63 or 64 or 65 or 66 or 67 or 68 or 69 or 70 or 71 or 72 or 73 or 74 or 75 or 76 or 77 or 78 or 79 or 80 or 81 or 82 or 83 or 84 or 85 or 86

88. 51 and 87

89. Remove duplicates from 88.

Appendix 2. Data extraction tool

Table

Table 3a. List of 63 measures used to assess adults with muscular dystrophy (27 indirect and 36 direct measures)

Table 4a. Study characteristics of studies and evaluated measures included in phase 2

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[25]  
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[42]   | Washburn RA, Zhu W, McAuley E, Frogley M, Figoni SF. The physical activity scale for individuals with physical disabilities: development and evaluation. Arch Phys Med Rehabil 2002; 83(2): 193-200.
[43]   | Longmuir PEaB-O, O. Factors influencing the physical activity levels of youths with physical and sensory disabilities. Adapted Physical Activity Quarterly 2000; 17: 40-53.
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[46]   | Kimura S, Ozasa S, Nomura K, Yoshioka K, Endo F. Estimation of muscle strength from actigraph data in Duchenne muscular dystrophy. Pediatr Int 2014; 56(5): 748-752.
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Veenhuizen Y, Cup EH, Groothuis JT, Hendriks JC, Adang EM, van Engelen BG, Geurts AC. Effectiveness and cost-effectiveness of a self-management group program to improve social participation in patients with neuromuscular disease and chronic fatigue: protocol of the Energetic study. BMC Neurol 2015; 15: 58.

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[62]  
Andersen G, Orngreen MC, Preisler N, Jeppesen TD, Krag TO, Hauerslev S, van Hall G, Vissing J. Protein-carbohydrate supplements improve muscle protein balance in muscular dystrophy patients after endurance exercise: a placebo-controlled crossover study. Am J Physiol Regul Integr Comp Physiol 2015; 308(2): R123-130.

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Van Remoortel H, Giavedoni S, Raste Y, Burtin C, Louvaris Z, Gimeno-Santos E, Langer D, Glendenning A, Hopkinson NS, Vogiatzis I, Peterson BT, Wilson F, Mann B, Rabinovich R, Puhan MA, Troosters T, consortium PR. Validity of activity monitors in health and chronic disease: a systematic review. Int J Behav Nutr Phys Act 2012; 9: 84.

[81]   | Jimenez-Moreno AC, Charman SJ, Nikolenko N, Larweh M, Turner C, Gorman G, Lochmuller H, Catt M. Analyzing walking speeds with ankle and wrist worn accelerometers in a cohort with myotonic dystrophy. Disabil Rehabil 2018: 1-7.

[82]  
Okkersen K, Jimenez-Moreno C, Wenninger S, Daidj F, Glennon J, Cumming S, Littleford R, Monckton DG, Lochmuller H, Catt M, Faber CG, Hapca A, Donnan PT, Gorman G, Bassez G, Schoser B, Knoop H, Treweek S, van Engelen BGM, consortium O. Cognitive behavioural therapy with optional graded exercise therapy in patients with severe fatigue with myotonic dystrophy type 1: a multicentre, single-blind, randomised trial. Lancet Neurol 2018; 17(8): 671-680.

[83]   | McDonald CM, Widman LM, Walsh DD, Walsh SA, Abresch RT. Use of step activity monitoring for continuous physical activity assessment in boys with Duchenne muscular dystrophy. Arch Phys Med Rehabil 2005; 86(4): 802-808.
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