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Applied Physiology, Nutrition, and Metabolism

The Effects of Pilates on Health-related Outcomes in


Individuals with Increased Risk of Fracture: A Systematic
Review

Journal: Applied Physiology, Nutrition, and Metabolism

Manuscript ID apnm-2021-0462.R1

Manuscript Type: Systematic Review

Date Submitted by the


07-Oct-2021
Author:

Complete List of Authors: McLaughlin, Emily; University of Waterloo, Department of Kinesiology


Bartley, Joan; Osteoporosis Canada, Canadian Osteoporosis Patient
Network
Ashe, Maureen; University of British Columbia,
Dr

Butt, Debra; University of Toronto, Department of Family and


Community Medicine
Chilibeck, Philip; University of Saskatchewan,
Wark, John; The University of Melbourne Department of Medicine Royal
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Melbourne Hospital, Bone and Mineral Medicine


Thabane, Lehana; McMaster University, Department of Heath Research
Methods, Evidence and Impact
Stapleton, Jackie; University of Waterloo, University of Waterloo Library
Giangregorio, Lora; University of Waterloo, ; Schlegel Research Institute
for Aging,

Pilates, exercise, osteoporosis < bone health, Low bone mass, exercise
Keyword: prescription < exercise, exercise therapy < exercise, fracture, fracture
prevention

Is the invited manuscript for


consideration in a Special Not applicable (regular submission)
Issue? :

© The Author(s) or their Institution(s)


Page 1 of 34 Applied Physiology, Nutrition, and Metabolism

1 The Effects of Pilates on Health-related Outcomes in Individuals with Increased Risk of

2 Fracture: A Systematic Review

4 Emily Claire McLaughlin1, Joan Bartley2, Maureen C. Ashe3, Debra A. Butt4, Philip D.

5 Chilibeck5, John D. Wark6, Lehana Thabane7, Jackie Stapleton8, Lora M. Giangregorio1,9*

7 1Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada, N2L 3G1

8 2Canadian Osteoporosis Patient Network, Osteoporosis Canada

9 3Department of Family Practice, University of British Columbia, Vancouver, BC, Canada V5Z

10 1M0, Canada

11 4Department of Family and Community Medicine, University of Toronto, Toronto, ON, Canada
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12 M5G 1V7
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13 5College of Kinesiology, University of Saskatchewan, Saskatoon, SK, Canada, S7N 5A2

14 6University of Melbourne Department of Medicine, Bone and Mineral Medicine, Royal

15 Melbourne Hospital, Parkville, Victoria, Australia, 3050

16 7Department of Health Research Methods, Evidence and Impact, McMaster University,

17 Hamilton ON, Canada

18 8University of Waterloo Library, University of Waterloo, Waterloo, ON, Canada, N2L 3G1

19 9Schlegel-University of Waterloo Research Institute for Aging, University of Waterloo, ON, N2J

20 0E2, Canada

21 Email addresses: ECM (ecmclaughlin@uwaterloo.ca), JB (bartleyj65@gmail.com), MA


22 (maureen.ashe@ubc.ca), DB (debra.butt@utoronto.ca), PC (phil.chilibeck@usask.ca), JW
23 (jdennisw1@gmail.com), LT (thabanl@mcmaster.ca), JS (jstapleton@uwaterloo.ca), LG
24 (lora.giangregorio@uwaterloo.ca) *Corresponding Author: Lora M. Giangregorio, Department
25 of Kinesiology, University of Waterloo, 200 University Ave W, Waterloo, ON, N2L 3G1.
26 Phone: +1 519-888-4567 ext. 36357

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27 Abstract:

28 This systematic review examined the effect of Pilates on health-related outcomes in

29 individuals with increased fracture risk to inform the 2021 Clinical Practice Guidelines for

30 Management of Osteoporosis and Fracture Prevention in Canada. Seven electronic databases were

31 searched to December 2020. Studies of Pilates in men and postmenopausal women aged ≥ 50

32 years with low BMD, history of fragility fracture, or moderate-high risk of fragility fracture were

33 included. Two reviewers independently screened studies and performed risk of bias assessment.

34 Of 7286 records and 504 full-text articles, five studies were included, encompassing data from 143

35 participants (99% female). Data were insufficient for meta-analyses. There is low-certainty

36 evidence that Pilates improved physical functioning and health-related quality of life. The effect

37 of Pilates on falls and BMD is uncertain. No evidence was available for the effect of Pilates on
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38 mortality, fractures, or adverse events. Overall, Pilates may improve physical functioning and
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39 quality of life. Evidence of benefits relative to harms of Pilates in people with increased fracture

40 risk, particularly males, is limited. PROSPERO registration: CRD42019122685.

41

42 Novelty Bullets:

43  Pilates may improve physical functioning and quality of life in women with osteoporosis.

44  Evidence of the effect of Pilates on BMD, falls, fractures, or adverse events is limited.

45

46 Keywords: Pilates, Exercise, Osteoporosis, Fracture Prevention

47

48

49

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50 INTRODUCTION

51 Osteoporosis is a common skeletal disorder characterized by compromised bone strength,

52 predisposing a person to an increased risk of fracture(NIH Consensus Development Panel on

53 Osteoporosis Prevention, Diagnosis, and Therapy, and Therapy, NIH Consensus Development

54 Panel on Osteoporosis Prevention and Therapy, 2001). Osteoporotic fragility fractures can cause

55 pain, functional impairment and loss of independence, resulting in activity limitations and reduced

56 quality of life, and can lead to hospitalization and early mortality(Ioannidis et al., 2009; Gajic-

57 Veljanoski et al., 2018). Fragility fractures place an economic burden of $4.6 billion yearly on the

58 Canadian healthcare system(Hopkins et al., 2016).

59 Exercise is an integral component in the prevention and management of osteoporosis. In

60 older adults, there is strong evidence that exercise prevents falls and reduces the risk of
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61 fracture(Sherrington et al., 2019). However, the risks and benefits of exercise for fracture
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62 prevention may vary by individual and by type of exercise. Exercise that involves flexion or

63 rotation of the spine, quick transitions between movements, use of loads when proper spinal

64 alignment is not maintained, or activities that challenge balance without support may require

65 modification or careful progression for individuals at a high risk of fracture(Giangregorio et al.,

66 2015).

67 Exercise programs for individuals with osteoporosis should target the prevention of falls,

68 safe movement with a focus on body mechanics, and maintenance of muscular strength in an effort

69 to slow the rate of bone loss(Giangregorio et al., 2015). Pilates, originally developed by Joseph

70 Pilates in the 1930s (Pilates and Miller, 1945), employs principles of core stability, postural

71 alignment, balance, and muscular strength and endurance. Movements are completed with

72 precision and fluidity, through controlled sequences paired with full, rhythmic breathing(di

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73 Lorenzo, 2011). Pilates emphasizes quality of movement, developing foundational patterning that

74 can be progressed to more difficult exercises. Progressions involve decreasing the base of support

75 and altering the centre of gravity to challenge balance, or reducing the amount of assistance

76 provided to increase muscular challenge, working towards functional movement against gravity

77 that is relevant to everyday life(Anderson et al., 2005). Pilates exercise often includes resistance

78 training against spring-loaded apparatuses or elastic resistance bands in addition to floor-based

79 mat work(di Lorenzo, 2011). Though the principles of Pilates align with the therapeutic goals of

80 exercise for preventing fracture, a synthesis of available evidence on Pilates in people with low

81 bone mass is needed to determine if it is appropriate to recommend in guidelines. The aim of this

82 systematic review is to determine the effects of Pilates exercise (versus no intervention, placebo

83 or attention control) on falls, fractures, and other health-related outcomes in men and
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84 postmenopausal women aged 50 years or older at increased risk of fracture. This systematic review
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85 is part of a series of systematic reviews that will inform the 2021 Clinical Practice Guidelines for

86 Management of Osteoporosis and Fracture Prevention in Canada. Each review focused on a

87 specific type of exercise. Pilates emerged as an area of interest during consultation with

88 patients(Morin et al., 2020), therefore a separate review was performed.

89

90 METHODS

91 This systematic review follows the Preferred Reporting Items for Systematic Review and

92 Meta-Analysis (PRISMA) guidelines(Moher et al., 2009). The protocol was informed by the

93 Cochrane Handbook for Systematic Reviews of Interventions(Higgins and Green, 2011), and

94 designed by a working group of researchers, physiotherapists, physicians, a patient advocate, and

95 graduate students. The protocol was registered via the International Prospective Register of

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96 Systematic Reviews (PROSPERO) at https://www.crd.york.ac.uk/prospero/ (Registration

97 number: CRD42019122685; submitted March 6, 2019).

98

99 Data Sources and Searches

100 A librarian with experience conducting systematic reviews (JS) developed a common

101 literature search and used a deduplication process to identify studies for six different types of

102 exercise interventions to be considered in the guidelines. The search was conducted in MEDLINE

103 (Ovid), EMBASE (Ovid), Cochrane CENTRAL (clinical trials), Cochrane database of systematic

104 reviews (meta-analyses), CINAHL (allied health journal content), Epistemonikos, and Web of

105 Science in August 2018 and updated in December 2020. Search terms consisted of a combination

106 of subject headings (i.e. MeSH) and author keywords related to interventions used in the
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107 prevention and treatment of osteoporosis in older adults. The full search strategy can be found in
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108 Supplement S1. No restrictions were placed on gender, ethnicity, exercise setting, country of

109 origin, or language, however only human studies written in English, Portuguese, Spanish, Italian,

110 or Farsi were included due to language limitations of the working group. Randomized controlled

111 trials (RCTs) and quasi-randomized controlled trials comparing Pilates to placebo, attention

112 control, or non-physical activity interventions, as well as cohort studies, case-control studies,

113 cross-sectional studies and case reports were considered for inclusion in the systematic review to

114 ensure that all available studies of Pilates interventions were captured. We included non-

115 randomized trials because we hypothesized that there would be a limited number of RCTs, and we

116 wanted to capture all available evidence for each outcome. Editorials and opinion pieces were

117 excluded. References were stored and managed using EndNote

118 (https://www.myendnoteweb.com/, Clarivate Analytics, Philadelphia, PA, USA). Titles and

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119 abstracts were imported into Covidence (Veritas Health Innovation, Melbourne, Australia) for

120 screening and data extraction.

121

122 Study selection

123 Two authors (EM and JB) independently assessed study eligibility at each phase: level 1

124 screening (title and abstract review), level 2 screening (full-text review) and level 3 data extraction.

125 Conflicts were resolved by discussion between reviewers or by a third author (LG) when

126 agreement was not reached.

127

128 Data items

129 Population
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130 We included studies of men or postmenopausal women with a mean age of 50 years or
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131 older with either a) low bone mineral density (BMD) at the femoral neck or lumbar spine (T-score

132 ≤ -1.00), measured with dual-energy X-ray absorptiometry (DXA); b) history of ≥1 fragility

133 fracture (i.e., fracture of the spine, hip, wrist, humerus); or c) moderate or high-risk of fragility

134 fracture based on the CAROC(Siminoski et al., 2007), FRAX(Kanis et al., 2009), or

135 GARVAN(Nguyen et al., 2008) calculators. Studies of individuals with secondary osteoporosis,

136 glucocorticoid-induced osteoporosis, or pathological fractures were excluded. Studies of older

137 adults were only included if a subgroup analysis was conducted in individuals with low bone mass,

138 or ≥80% of participants had low bone mass. If it was unclear whether studies met inclusion

139 criteria, authors were contacted.

140

141

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142 Intervention

143 We included studies that defined their intervention as Pilates. Interventions could be home-

144 or centre-based, individual or group-based, and either supervised or unsupervised. Studies

145 combining Pilates with pharmacological or other co-interventions (excluding whole-body

146 vibration) were included unless unevenly administered to the intervention and control groups. We

147 attempted to differentiate between studies of interventions that aligned with accepted definitions

148 of classical or hybrid Pilates, or were Pilates-inspired, but could not find established guidelines on

149 how to categorize a Pilates intervention.

150

151 Comparator

152 Studies were included if at least one comparator group received either no intervention,
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153 placebo, a non-exercise or non-physical therapy intervention (e.g., educational intervention), or an


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154 attention control not expected to affect outcomes of interest.

155

156 Outcomes:

157 A list of outcomes deemed critical or important to individuals living with osteoporosis and

158 to exercise professionals was established (Rodrigues, 2019; Morin et al., 2020) The outcomes of

159 interest were: 1) mortality due to any cause, including natural death, disease, or circumstance

160 resulting in fatal injury or death; 2) fracture-related mortality, defined as deaths attributed to a

161 fragility fracture; 3) fragility fractures, either self-reported or X-ray verified fracture of the spine,

162 wrist, humerus or pelvis that occurred from a low-trauma event; 4) hip fractures, either self-

163 reported or X-ray verified fracture of the femoral neck or trochanter; 5) number of fallers, falls,

164 and fall-related injuries; 6) physical functioning and disability, using any validated tool measuring

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165 activities of daily living or performance-based measures of physical functioning (e.g., gait speed,

166 Timed Up-and-Go, Sit-to-Stand test). Measures of strength of individual muscles or muscle

167 groups (e.g., quadriceps strength) were not included; 7) health-related quality of life, using any

168 validated generic or osteoporosis-specific quality of life questionnaire; and 8) serious adverse

169 events, defined as any untoward medical occurrence that at any dose resulted in death, life-

170 threatening injury, inpatient hospitalisation, prolongation of existing hospitalisation, or persistent

171 or significant disability or incapacity, and non-serious adverse events, defined as any reaction

172 related to the intervention such as musculoskeletal injuries (e.g., sprains, strains, joint pain, overuse

173 injuries). Pain and BMD were not voted as critical outcomes for the guidelines but were included

174 in this systematic review. We reported BMD measures determined by DXA at any bone site. BMD

175 was used as an indirect measure of fracture risk when data on fractures was unavailable or of very
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176 low certainty. Pain outcomes reported using any validated questionnaire (e.g., Visual Analogue
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177 Scale) or pain subscale from a generic functional status questionnaire (e.g., SF-36, Nottingham

178 Health Profile) were included.

179

180 Time

181 We included studies with interventions lasting a minimum of four weeks.

182

183 Data Extraction and Quality Assessment:

184 Two independent reviewers (EM and JB) extracted the following information from eligible

185 studies: year of publication, study setting, participant characteristics, details of the intervention

186 and control groups including exercise frequency, intensity and duration, the number of recruited

187 participants at baseline, adherence rates in intervention group(s), drop-out rates, outcomes of

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188 interest, and adverse events. If data were missing, authors were contacted. Data were only reported

189 from subscales when the study did not report total scores. For example, we preferentially reported

190 total quality of life scores compared with scales that individually reported physical or mental health

191 aspects of quality of life. If a study reported multiple study arms, we only extracted data from

192 groups of interest.

193 The same independent reviewers (EM and JB) assessed risk of bias using the Cochrane

194 Risk of Bias Assessment Tool (Sterne et al., 2019). When assessing risk of bias due to “other

195 sources of bias” we considered factors such as between group differences in participant

196 characteristics or health status at baseline, differences in the length of follow-up period,

197 measurement error, and consistency in exercise instruction (e.g., did they provide a familiarization

198 period to ensure all participants were prepared to begin exercise). Conflicts were resolved by
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199 discussion between reviewers, or by a third author (LG) when agreement was not reached. A
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200 rating of low, unclear, or high risk of bias was assigned. Certainty of evidence was determined for

201 each outcome using the Grading of Recommendations, Assessment, Development and Evaluations

202 (GRADE) framework(Zhang et al., 2019).

203

204 Data Synthesis and Analysis:

205 Statistical analysis was performed using Review Manager 5.3 (RevMan 5) (Cochrane

206 Community, London, UK; https://community.cochrane.org/help/tools-and-software/revman-5).

207 Mean difference (MD) with 95% confidence intervals (CI) was calculated for continuous

208 outcomes. Risk ratio (RR) or rate ratio (RaR) with 95% CI was calculated for dichotomous

209 outcomes. Our original protocol dictated that study outcomes would be pooled, and standardized

210 mean difference (SMD) would be calculated when pooling total scores across studies. Due to the

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211 small number of included trials and heterogeneity in duration of follow-up, comparators, and

212 measurement tools used to assess outcomes, we present a narrative synthesis of findings instead.

213

214 RESULTS

215 Description of studies

216 The initial search strategy identified 7286 references. After removing duplicates and

217 reviewing titles and abstracts, 504 full-text articles were assessed for eligibility (Figure 1). Five

218 studies were included, encompassing data from 143 unique participants in two countries (Table

219 1)(Kopitzke, 2007; Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Cabot

220 and Shrier, 2017; Oksuz and Unal, 2017). Three studies were randomized controlled trials

221 (n=141)(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and Unal,
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222 2017) and two were case reports of individuals (n=2)(Kopitzke, 2007; Cabot and Shrier, 2017).
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223 Reasons for exclusion are listed in Figure 1. References for excluded studies can be found in

224 Supplement S2.

225

226 Participant characteristics

227 All 141 participants in the RCTs were postmenopausal women diagnosed with

228 osteoporosis (T-score ≤ -2.5 SD)(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can,

229 2015; Oksuz and Unal, 2017). Two studies required this diagnosis be confirmed by

230 DXA(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015). The average age of

231 participants ranged from 57 to 64 years(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden

232 and Can, 2015; Oksuz and Unal, 2017). Participants with a history of fracture were excluded

233 from all RCTs, as were those with mobility or communication limitations(Angin, Erden and Can,

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234 2015; Oksuz and Unal, 2017), or diseases or systemic conditions that may preclude them from

235 exercise(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and Unal,

236 2017). Küçükçakir (2013) excluded individuals with secondary osteoporosis or those taking

237 medications that may lead to it. Both Küçükçakir (2013) and Oksuz (2017) also excluded

238 individuals unwilling to participate in an exercise program. Angin (2015) excluded individuals

239 who had regularly exercised in the preceding 6 months. For the two case reports, one subject

240 was male, aged 52 years (Cabot and Shrier, 2017), and the other subject was female, aged 67

241 years(Kopitzke, 2007). Both had a T-score ≤ -2.5 SD, with no reported fractures. Demographic

242 information including place of residence, race, occupation, religion, education, socio-economic

243 status and social capital (a concept referring to social networks, civic participation and

244 interpersonal trust)(O’Neill et al., 2014), was not reported in any of the included studies.
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245
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246 Setting and supervision:

247 Studies were conducted in two countries: Turkey (3 RCTs)(Küçükçakir, Altan and

248 Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and Unal, 2017) and the United States (2

249 case-reports)(Kopitzke, 2007; Cabot and Shrier, 2017). Pilates interventions were instructed and

250 supervised by a physiotherapist, either one-to-one(Kopitzke, 2007; Cabot and Shrier, 2017) or in

251 a small group(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and

252 Unal, 2017). It was not reported whether physiotherapists had additional qualification or training

253 for Pilates instruction or osteoporosis. Four interventions took place at a physical therapy and

254 rehabilitation centre(Kopitzke, 2007; Angin, Erden and Can, 2015; Cabot and Shrier, 2017;

255 Oksuz and Unal, 2017); one did not report the setting (Küçükçakir, Altan and Korkmaz, 2013).

256

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257

258 Frequency, intensity and duration of the exercise intervention:

259 The experimental interventions consisted of a one-hour exercise session performed two to

260 three times weekly. Sessions included mat-based and standing exercises, resistance bands and

261 balls, and a warm-up and cool-down period(Küçükçakir, Altan and Korkmaz, 2013; Angin,

262 Erden and Can, 2015; Oksuz and Unal, 2017). Progressions were used to advance intervention

263 difficulty over time. A single training session familiarized participants with basic Pilates

264 principles prior to beginning the intervention in two studies(Angin, Erden and Can, 2015; Oksuz

265 and Unal, 2017). Interventions described in the case studies were not consistent with the

266 randomized trials. Cabot (2017) used the Pilates Reformer and Wunda chair, but did not provide

267 details of the exercises performed(Cabot and Shrier, 2017). We included the case study by
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268 Kopitzke (2007) because the author defined the intervention as Pilates, however there was no
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269 description of a Pilates program beyond single-leg heel raises (Kopitzke, 2007). Further details

270 of intervention are provided in Table 1 and Supplement S3.

271

272 Comparator:

273 Angin (2015) compared Pilates to no intervention. Oksuz (2017) instructed participants to

274 continue a normal daily routine, refraining from exercise. Küçükçakir (2013) used an attention

275 control, where participants in the control group were instructed to complete 3 sets of 20

276 repetitions of seated thoracic extensions at home, and received monthly telephone follow-up.

277

278 Adherence and dropouts:

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279 Adherence to Pilates exercise sessions was not reported(Kopitzke, 2007; Küçükçakir,

280 Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Cabot and Shrier, 2017; Oksuz and

281 Unal, 2017). Angin (2015) reported that 100% of participants in the intervention group

282 completed the study, while 3 of 22 participants (13.64%) in the control group did not.

283 Küçükçakir (2013) reported 14.3% attrition (5 of 35 participants) in intervention and control

284 groups, respectively. Oksuz (2017) reported no attrition.

285

286 Outcomes

287 There were no studies that examined the effect of Pilates on mortality, hip fractures,

288 fragility fractures or adverse events.

289
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290 Bone Mineral Density as an Indirect Measure of Fracture Risk


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291 There is very low certainty evidence from one RCT and two case studies that Pilates may

292 improve BMD (Table 2). Angin (2015) reported an improvement in lumbar spine BMD

293 following a 6-month Pilates intervention compared with no intervention (MD 0.06, 95% CI 0.01

294 to 0.11; n=44). Kopitzke (2007) noted an improvement in T-score at the lumbar spine and the

295 femoral neck in one case after 12 months of Pilates; no BMD values were reported. Cabot

296 (2017) reported an improvement in BMD from 0.815 to 0.893 g/cm2 after 48 weeks of Pilates in

297 one case, but the site of measurement and method of ascertainment of BMD was not disclosed.

298

299 Falls and Fall-related Injuries

300 There is inadequate evidence to make inferences about Pilates and falls. Küçükçakir

301 (2013) reported that two participants experienced one fall each in the Pilates group while one

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302 participant experienced one fall and two participants experienced two falls each in the home

303 exercise group. Between group differences were not evaluated due to the low number of falls.

304 Evidence is of very low certainty (Table 2).

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306 Physical Functioning and Disability

307 There is low certainty evidence from three RCTs and one case study that Pilates may

308 improve physical functioning (Table 2)(Kopitzke, 2007; Küçükçakir, Altan and Korkmaz, 2013;

309 Angin, Erden and Can, 2015; Oksuz and Unal, 2017) .

310

311 Six-Minute Walk Test

312 Two RCTs, including a total of 101 participants, examined the effect of Pilates on the
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313 Six-Minute Walk Test (6MWT)(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can,
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314 2015). Angin (2015) reported a non-significant improvement in distance travelled during the

315 6MWT following a 6-month Pilates intervention compared with no intervention (MD=53.40

316 metres, 95% CI -3.81 to 110.61; n=41). Küçükçakir (2013) reported a significant improvement

317 in distance travelled during the 6MWT following a year-long Pilates intervention compared with

318 an attention control (MD=91.80 metres, 95% CI 54.12 to 129.48; n=60).

319

320 Seated to Standing Tests

321 Küçükçakir (2013) reported significant improvements in 1-minute sit-to-stand test score

322 after one year of Pilates compared to control (MD 9.50 repetitions, 95% CI 7.32 to 11.68; n=60),

323 while Oksuz (2017) reported improvements in 30-second chair stand test score following the 6-

324 week Pilates intervention compared to control (MD 2.90 repetitions, 95% CI 2.05 to 3.75; n=40).

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325 Oksuz (2017) also noted significant improvements in Timed-Up-and-Go score (MD -1.44

326 seconds, 95% CI -2.04 to -0.84; n=40) following Pilates intervention compared to control.

327

328 Balance tests

329 Oksuz (2017) reported significant improvements in the Berg Balance Test following 6-

330 weeks of Pilates compared with no intervention (MD 1.70, 95% CI 1.14 to 2.26; n=40). An

331 improvement in single leg standing time following one year of Pilates was noted in one case

332 study(Kopitzke, 2007).

333

334 Health-related quality of life

335 There is low certainty evidence from three RCTs that Pilates improved health-related
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336 quality of life(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and
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337 Unal, 2017). Küçükçakir (2013) and Oksuz (2017) reported QUALEFFO-41 total score

338 demonstrating relative improvements (lower score is better) in quality of life in the Pilates group

339 compared to control (MD -20.20, 95% CI -23.71 to -16.69) and (MD -7.59, 95% CI -9.35 to -

340 5.83), respectively. For presentation using GRADE methodology, these values were pooled

341 (Table 2). Angin et. al (2015) reported QUALEFFO-41 subscales only, also demonstrating

342 relative improvements in each quality of life domain in the Pilates group compared with

343 control(Angin, Erden and Can, 2015). Additionally, Küçükçakir (2013) reported all subscales of

344 the RAND 36-item Short Form Survey (SF-36), demonstrating relative improvements in the

345 Pilates intervention group compared with the control group (Küçükçakir, Altan and Korkmaz,

346 2013). Oksuz (2017) reported the Hospital Anxiety and Depression scale (HADS), the Health

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347 Assessment Questionnaire (HAQ), and the Satisfaction with Life Scale (SLS), demonstrating

348 relative improvements in the Pilates group compared with the control (Oksuz and Unal, 2017).

349

350 Adverse Events

351 No studies examined the effect of Pilates on serious or minor adverse events. One study

352 reported that no participants withdrew due to complications from the exercise program, and no

353 adverse events were reported in the remaining study population (Küçükçakir, Altan and

354 Korkmaz, 2013), however they did not describe any methods for ascertaining possible adverse

355 events.

356

357 Pain
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358 All three RCTs evaluated pain using a visual analogue scale(Küçükçakir, Altan and
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359 Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and Unal, 2017), and reported that

360 participation in Pilates significantly reduced pain compared with control (very low certainty

361 evidence).

362

363 Visual Analogue Scale for pain at rest

364 Angin (2015) reported a significant reduction in pain at rest following the Pilates

365 intervention compared with no intervention (MD= -2.98, 95% CI -4.12 to -1.84; n=41). Oksuz

366 (2017) also demonstrated a significant reduction in pain at rest (MD= -2.57, 95% CI -3.61 to -

367 1.53; n=40) as well as a significant reduction in morning pain in the Pilates group compared with

368 no intervention (MD -2.10, 95% CI -2.84 to -1.36; n=40). Küçükçakir (2013) reported a

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369 significant reduction in pain at rest, following the Pilates intervention compared with the

370 attention control (MD= -2.70, 95% CI -3.20 to -2.20; n=60).

371

372 Visual Analogue Scale for pain with movement or during intervention

373 Angin (2015) and Oksuz (2017) both reported a significant reduction in pain with

374 movement in the Pilates group compared with no intervention (MD= -4.94, 95% CI -5.83 to -

375 4.05; n=41)(Angin, Erden and Can, 2015) and (MD= -1.70 95% CI -2.43 to -0.97; n=40)

376 respectively(Oksuz and Unal, 2017).

377

378 Other pain measurements

379 Oksuz (2017) reported pain using the short form McGill questionnaire and subscales, the
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380 Pain Disability Index (PDI) and the Oswestry Low Back Pain Disability Scale (ODI). In all pain
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381 measures completed by Oksuz (2017), Pilates exercise significantly reduced reports of pain

382 compared with no intervention (Oksuz and Unal, 2017).

383

384 Risk of Bias Assessment

385 The three included RCTs were determined to have a high risk of bias using the Cochrane

386 Risk of Bias Assessment tool (Figure 2). Case reports were automatically considered high risk of

387 bias and were not assessed. Randomization techniques were not described by two of three

388 RCTs, and all studies employed inadequate allocation concealment. Due to the nature of the

389 exercise intervention, blinding of participants and personnel administering the intervention was

390 not possible(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and

391 Unal, 2017). Angin (2017) reported that outcome assessment was performed by the same

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392 physiotherapist who administered treatment (high risk). Blinding of outcome assessors was not

393 described in the study by Oksuz (2017) (unclear risk). Intention-to-treat analysis was not

394 conducted in any of the studies(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can,

395 2015; Oksuz and Unal, 2017) despite missing data due to participants dropping out prior to the

396 end of the study period. Küçükçakir (2013) reported equal rates of attrition in both study arms,

397 and stated reasons for drop-outs. Angin (2015) provided no explanation of dropouts. While the

398 published article by Oksuz (2017) reported that all 40 participants completed the study, the

399 registered protocol, identified following a search of clinicaltrials.gov (Identifier: NCT02716855),

400 reported that 47 participants were randomized, and 7 participants did not complete the study.

401 Details of group allocation and reason for drop-out were not disclosed(Oksuz and Unal, 2017).

402 Clinical trial registrations were not reported in any of the published papers, and were not
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403 available for two of the studies. Outcomes listed in the available protocol were consistant with
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404 the published paper(Oksuz and Unal, 2017).

405

406 Discussion

407 Our review identified low-certainty evidence that Pilates improved health-related quality

408 of life and physical functioning, and reduced pain in postmenopausal women with osteoporosis.

409 Very-low certainty evidence suggested that Pilates improved BMD. There was no available

410 evidence for several outcomes including mortality, hip fractures and fragility fractures, and serious

411 and non-serious adverse events. Results were consistent between included studies, however the

412 limited number of studies, very small sample size, and heterogeneity in duration of follow-up,

413 comparators, and measurement tools used for each outcome prevented meaningful pooling of

414 results. There were limited data on the safety of Pilates for individuals at risk of osteoporotic

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415 fracture. Therefore, it is difficult to make inferences about the benefits relative to harms when

416 considering Pilates practice in individuals at risk of fracture. When creating guidelines or

417 developing therapeutic programs for individuals with osteoporosis, researchers, clinicians, and

418 fitness professionals should balance the available evidence related to benefits and harms of Pilates,

419 the values and preferences of the patient, the qualifications of the Pilates instructor, and whether

420 stronger evidence may exist for other types of exercise (Kistler-Fischbacher et al., 2021). (Table

421 3).

422 Evidence on the effects of Pilates on health outcomes in individuals with low bone mass

423 may be augmented by indirect evidence from other populations. Systematic reviews and meta-

424 analyses of Pilates interventions in adults 60 years of age and older that were not selected for low

425 bone mass have previously reported improvements in physical functioning using performance-
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426 based measures including variations of the sit-to-stand test, the Timed-Up-and-Go test and the
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427 Berg Balance Scale(Barker, Bird and Talevski, 2015; Bueno De Souza et al., 2018; Moreno-

428 Segura et al., 2018). Pilates also improved measures of static and dynamic balance, flexibility,

429 and functional cardiovascular endurance (e.g. 6MWT) in adults 60 years of age and older(Barker,

430 Bird and Talevski, 2015; de Oliveira Francisco, de Almeida Fagundes and Gorges, 2015; Bueno

431 De Souza et al., 2018). Existing systematic reviews of Pilates in older adults without low bone

432 mass also range in quality of reporting and included evidence, and include very few primary studies

433 with small sample sizes(Barker, Bird and Talevski, 2015; de Oliveira Francisco, de Almeida

434 Fagundes and Gorges, 2015; Bueno De Souza et al., 2018; Moreno-Segura et al., 2018). Higher

435 quality research into the effects of Pilates on physical functioning is needed, particularly among

436 individuals with osteoporosis.

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437 While the determined benefits of Pilates may be promising, the risks associated with

438 participation in Pilates remain unknown. In studies of Pilates in people at risk of fracture, fragility

439 fractures have not been measured. Adverse events were not systematically monitored or reported

440 in any study(Küçükçakir, Altan and Korkmaz, 2013; Angin, Erden and Can, 2015; Oksuz and

441 Unal, 2017). Falls were reported in one study(Küçükçakir, Altan and Korkmaz, 2013), however

442 falls were not defined as an outcome a priori, validated methods of falls ascertainment were not

443 used, and sample sizes were small. Some understanding of the risks associated with Pilates may

444 be drawn from populations not selected for low bone mass, however similar limitations persist. In

445 a previous systematic review of Pilates interventions in healthy community-dwelling adults 60

446 years of age and older(Moreno-Segura et al., 2018), two included RCTs reported that a 12-week

447 Pilates program reduced the rate of falls compared with no intervention (Rate Ratio [RaR] 0.28,
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448 95% CI 0.15 to 0.55; 1 RCT, n=60)(Irez et al., 2011) or twenty minutes of daily home exercise
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449 (RaR 1.17, 95% CI 0.43 to 3.19; 1 RCT, n=44)(Barker et al., 2016). One adverse event (hip pain)

450 was reported in the Pilates group (n=44)(Barker et al., 2016). Future research should examine the

451 effects of Pilates on falls, fractures and adverse events.

452 BMD was used as a surrogate measure of bone strength as data were unavailable for the

453 effect of Pilates on hip fractures or fragility fractures. Studies examining the effect of Pilates on

454 BMD have limitations related to sample size, short study duration (6 months) and risk of bias that

455 limited our ability to make inferences about efficacy. While moderate-high intensity resistance

456 and impact exercise may maintain or improve BMD in people with low bone mass(Watson et al.,

457 2018) improvements have not been consistently demonstrated across exercise types and were not

458 observed in a Pilates-inspired intervention which emphasized low-intensity resistance and impact

459 exercise(Kistler-Fischbacher et al., 2021). Further confirmational studies to determine if the

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460 resistance training component of Pilates is sufficient to stimulate maintenance of BMD at fracture-

461 prone sites would be valuable (Howe et al., 2011).

462 There remains an overall need to improve reporting of clinical trials of non-

463 pharmacological interventions(Boutron et al., 2017), particularly the factors that influence efficacy

464 of the intervention. Adherence to the Pilates intervention was not adequately reported in any of the

465 studies, making it challenging to assess the acceptability or feasibility of the program to

466 participants. All studies in this review described clinical Pilates interventions that were conducted

467 under the supervision of a physiotherapist. It is unclear how these results would generalize to a

468 community-based setting where classes may not have a therapeutic focus or be taught by a health

469 care professional. Future studies of Pilates should state the qualifications or Pilates training

470 credentials of the instructor, and individuals with osteoporosis who wish to participate in Pilates
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471 should consider formal instruction by qualified instructors with expertise in osteoporosis. When
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472 considering spaces in which individuals may practice Pilates, the group component of the Pilates

473 classes in the randomized studies offered more social interaction than the control group, which

474 may have influenced health outcomes. Pilates is not a trademarked term and therefore Pilates

475 exercise programs are not standardized. Variability in the duration, intensity or types of exercises

476 included in Pilates interventions can contribute to heterogeneity, therefore specifics relating to

477 dosage, supervision, and delivery method should be clearly reported in future trials.

478

479 Limitations

480 There are limitations in both the quantity and quality of studies examining Pilates in men

481 and post-menopausal women at risk of fracture. Evidence was unavailable for several critical

482 outcomes. Few eligible studies, high risk of bias, and small sample sizes limited the certainty of

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483 evidence presented. The inclusion of case studies and non-randomized studies limits the quality

484 of available evidence. Results of our systematic review may not be generalizable to all people

485 with osteoporosis as the studies included in our review excluded people with a history of fracture,

486 co-morbid health conditions, or risk of secondary osteoporosis. Other than one included case study

487 (Cabot and Shrier, 2017), there are no studies of Pilates in males with low bone mass.

488 The lack of a formal definition for Pilates is a limitation of this study. Pilates is not a

489 trademarked exercise, and there is no single accreditation which standardizes Pilates exercises.

490 Therefore, to reflect the current state of evidence as well as the broad range of Pilates exercise

491 programs that may be available to the public, we included all studies that referred to themselves

492 as Pilates and screened other exercise studies for interventions that may have been more similar to

493 Pilates. As such, we may have represented studies that deviate from original Pilates methodology
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494 and may be better described as Pilates-inspired or Pilates-hybrid interventions.


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495

496 Conclusion

497 Physiotherapist-supervised Pilates interventions may improve quality of life and physical

498 functioning and may reduce reported pain in postmenopausal women with low bone mass.

499 Evidence to support the benefits of Pilates in individuals with low bone mass is limited and of very

500 low quality, particularly for men. There is no information on the effects of Pilates on fracture risk,

501 falls or potential harms. We cannot make recommendations about participation in Pilates in

502 settings outside of supervised classes in physical therapy clinics, or among individuals at high risk

503 of fracture. Adequately powered studies examining the effects of Pilates on outcomes important

504 to patients with low bone mass are needed.

505

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506 Conflict of Interest Statement

507 Funding: This research was supported by Osteoporosis Canada. Dr. Lora Giangregorio holds a

508 Schlegel-UW Research Institute for Aging Research Chair in Mobility and Aging. Dr. John D.

509 Wark has received grants-in-aid from Amgen & Actavis Australia/Allergan for a project separate

510 from work on this systematic review. The remaining authors have no competing interests to

511 disclose.

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Figure 1: PRISMA Flow Chart of the Study Selection Process

Records identified through database search Duplicates removed


(n = 7286) (n = 3043)

Records screened Records excluded


(n = 4243) (n = 3739)

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Full-text articles excluded, with
Full-text articles assessed for eligibility reasons
(n = 504) (n = 499)
n=160 Wrong patient population
n=148 Wrong intervention
n=106 Wrong study design
n=35 Wrong outcome
n=22 Wrong comparator
Full studies included n=11 Unable to retrieve full text
(n=5) n=9 Language other than English,
Portuguese, Spanish or Italian
n=8 Duplicate

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Table 1: Characteristics of Included Studies

Study Participants Main Inclusion/Exclusion Criteria Outcomes Details of Intervention and Control
Angin, 2015 N=41 Inclusion:  Physical functioning: 6MWT I: Clinical Pilates: 5 Pilates elements using mat
(RCT) Mean age Menopausal women aged >40 years with (metres) work, resistance bands and balls. One 1:1 session,
Turkey (years): osteoporosis, on Fosamax  Pain: VAS (rest and with plus group exercise supervised by physiotherapist.
I: 58.23 Exclusion: movement) 1 hour session, 3 times /week for 24 weeks.
C: 55.95 History of fracture, endoprosthesis or joint  BMD g/cm2 (lumbar spine) C: No intervention
fixation; chronic health condition; visual, hearing  QoL: QUALEFO-41 (subscales
or communication problems; exercising regularly only)
for 6 months
Küçükçakir, N=60 Inclusion:  Physical functioning: 6MWT I: Clinical Pilates: postural education on neutral
2013 Mean age Post-menopausal women aged 45-60 years with (metres), 1-minute sit to stand position, sitting, antalgic and stretching exercises,
(RCT) (years): osteoporosis  QoL: QUALEFFO-41 (total score proprioceptive and respiratory training. Exercise
Turkey I: 56.6, Exclusion: and subscales), SF-36 (subscales) bands and balls (26-inch diameter) were used.
C: 56.3 History of fracture, secondary osteoporosis or  Pain: VAS 1 hour session, 2 times/week for 1 year.
medications that may lead to it; systemic disease C: Thoracic extensions (3 sets of 20 repetitions) in

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limiting ability to exercise; not willing to exercise seated position at home, monthly phone call
Oksuz, 2017 N=40 Inclusion:  Physical functioning: TUG, BBT, I: Clinical Pilates: Participants attended special
(RCT) Mean age Women aged 50-75 years with osteoporosis, session to learn 5 main areas of Pilates, then

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30-second CST
Turkey (years): Physical activity > 3 times/week  QoL: QUALEFFO-41 (total score qualified for group exercise supervised by
I: 63.6 Exclusion: and subscales), HADS, HAQ, SLS1 physiotherapist. Progression from closed to open-
C: 61 History of fracture, joint replacement or fixation;  Tampa Kinesiophobia Scale chain kinetic exercises, increased endurance and
secondary disease causing decreased functional  Pain: VAS (rest, performance, movement capacity in final 3 weeks.
status; mental, visual, hearing or communication movement), SF-McGill, PDI, ODI 1 hour session, 3 times/week for 6 weeks.
problems. C: Continue normal daily routine.

Cabot, 2017 N=1; Age= N/A  BMD g/cm2 (location unknown) I: Exercises using the Pilates Reformer and Wunda
(Case Report) 52 years,  T-score chair with 1:1 supervision. Exercises included
USA male footwork, jumping on jump board, supine arm
circles, hundred preps with neutral pelvis, kneeling
abdominals, kneeling arm series, legs in straps
series, and standing leg (VMO) press.
3 times/week for 48 weeks
Kopitzke, N=1; N/A  Physical functioning: SLS2 I: Pilates with 1:1 supervision under the care of a
2007 Age=67  T-score (lumbar spine and femoral physiotherapist. Exercises involved single heel
(Case Report) years; neck) raises. 3 times/week for 1 year
USA female.
Abbreviations: I: Intervention; C: Control; 6MWT, Six-minute Walk Test; VAS, Visual Analogue Scale; QoL, Quality of Life; QUALEFFO-41, Quality of Life questionnaire in patients with vertebral fractures; BMD, bone
mineral density; TUG, Timed Up-and-Go; BBT, Berg Balance Test; 30-s CST, 30-second Chair Stand Test; BST, Back Scratch Test; HADS, Hospital Anxiety and Disability Scale; HAQ, Health Assessment Questionnaire;
SLS1, Satisfaction with Life Survey; SF-McGill, Short-Form McGill Pain Questionnaire; PDI, Pain Disability Index; ODI, Oswestry Low Back Pain Disability Scale; SLS2, Single-leg stance;

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Figure 2: Risk of Bias summary: review author’s judgements about each risk of bias item for each included study

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Page 33 of 34 Applied Physiology, Nutrition, and Metabolism

Table 2: Summary of Findings Table using GRADE Methodology

Outcome Anticipated Absolute Effects* (95% CI) Relative Number of Certainty


Risk with no Intervention Risk with Pilates Effect participants of
(95% CI) (studies) Evidence

Health Related Quality of Life The mean Health Related MD 13.8 units lower (26.16 - 100 (2 RCTs) Lowa,b,c,d
Assessed with: QUALEFFO-41; Scale from 0- Quality of Life score was 33.6 lower to 1.44 lower)
100 units
Follow-up range: 6 weeks to 12 months

Physical Functioning The mean Physical MD 1.44 seconds lower - 40 (1 RCT) Lowa,b,d
Assessed with: Timed Up-and-Go (TUG) Functioning score ranged (2.04 lower to 0.84 lower)
Follow up: 6 weeks from 7 to 12 seconds
Physical Functioning The mean Physical MD 1.23 seconds lower - 144 (4 RCTs) Lowd,e,h

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(Systematic Review) Functioning score (2.3 lower to 0.15 lower)
Assessed with: Timed Up-and-Go (TUG) (Systematic Review) ranged
Follow up: 4 weeks to 12 weeks from 7-12 seconds

Falls
Assessed with: Self-reported number of people
who fall
Follow up: 12 months
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2 people who fell in the Pilates group (n=30) versus 3
people who fell in the control group (n=30)
- 60 (1 RCT) Very Lowa,d

Lumbar spine BMD (surrogate for fragility The mean Lumbar Spine MD 0.06 g/cm2 higher (0.01 - 41 (1 RCT) Very
fracture) BMD (surrogate for fragility higher to 0.11 higher) Lowa,b,d,f,g
Follow up: 6 months fracture) was 0.653 g/cm2

Abbreviations: CI: Confidence interval; MD: Mean difference. Note: Hip Fractures (or Hip/Femoral Neck BMD), Adverse Events, and Mortality were not reported.

*The risk in the intervention group (and its 95% confidence interval) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI).

GRADE Working Group grades of evidence:


High certainty: We are very confident that the true effect lies close to that of the estimate of effect
Moderate certainty: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different
Low certainty: Our confidence is the effect estimate is limited: The true effect may be substantially different from the estimate of the effect
Very low certainty: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect

Explanations:
a. “Intention-to-treat” analysis was not used which could result in overestimation or underestimation of effect.
b. Allocation of groups is not adequately concealed
c. There is substantial heterogeneity which likely can be explained by differences in length of intervention
d. Small sample size
e. Heterogeneity is substantial to considerable: I2=76%
f. Outcome assessors not adequately blinded to experimental groups
g. BMD is a surrogate measure of fragility fracture
h. Indirect evidence from population not selected for low bone mass
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Table 3: Research-to-practice Summary and Tips for Pilates Instruction and Practice

Evidence summary: Pilates in Individuals at Risk of Fracture:


 Pilates may improve physical functioning, quality of life, and reduce pain.
 There are very few studies of Pilates conducted in people with osteoporosis, and there is very little
information about its effect on bone mineral density, falls, fractures or adverse events.

Recommendations for Pilates Instruction and Practice:


 Emphasize control of movement over intensity.
 Coach safe transitions between movements.
 Pilates movements that include rapid, repetitive, weighted, sustained or end-range flexion or twisting of
the spine may be risky and should be modified or avoided in individuals with osteoporosis (e.g.,
abdominal prep, roll-up/down and roll-over, jack-knife, criss cross, spinal twist).

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 Example movements in a Pilates class modified for osteoporosis may include Pilates breath, head nod,
imprint and release, shoulder/scapula isolation, shoulder bridge, breast stroke prep, side leg series,

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plank, or shell stretch modified with hip hinge.
 Individuals may choose to wear socks with rubber grips (e.g., yoga socks) for better traction.
 Fitness professionals are encouraged to seek additional training on exercise for individuals with
osteoporosis and apply the principles to Pilates instruction.
 When possible, clients should look for Pilates instructors who know how to modify practice for
individuals with osteoporosis, and they should inform the instructor that they have osteoporosis.

Note: Tips for Pilates practice were developed in consultation with a patient advocate from the Canadian Osteoporosis
patient network who has experience with Merrithew Stott PilatesⓇ, and align with previous expert recommendations
(Giangregorio et al., 2015)

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