Muscle strength cutoff-points for men with SCI Muscle strength cutoff-points for functional independence and wheelchair ability in men with spinal cord injury

Muscle strength cutoff-points for men with SCI Muscle strength cutoff-points for functional independence and wheelchair ability in men with spinal cord injury

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Journal Pre-proof Muscle strength cutoff-points for men with SCI Muscle strength cutoff-points for functional independence and wheelchair ability in men with spinal cord injury Frederico Ribeiro Neto, PhD, Rodrigo Rodrigues Gomes Costa, MSc, Ricardo Antônio Tanhoffer, PhD, Josevan Cerqueira Leal, PhD, Martim Bottaro, PhD, Rodrigo Luiz Carregaro, PhD PII:

S0003-9993(20)30085-X

DOI:

https://doi.org/10.1016/j.apmr.2020.01.010

Reference:

YAPMR 57769

To appear in:

ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION

Received Date: 15 March 2019 Revised Date:

18 November 2019

Accepted Date: 8 January 2020

Please cite this article as: Neto FR, Gomes Costa RR, Tanhoffer RA, Leal JC, Bottaro M, Carregaro RL, Muscle strength cutoff-points for men with SCI Muscle strength cutoff-points for functional independence and wheelchair ability in men with spinal cord injury ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2020), doi: https://doi.org/10.1016/j.apmr.2020.01.010. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Inc. on behalf of the American Congress of Rehabilitation Medicine

Muscle strength cutoff-points for men with SCI

Muscle strength cutoff-points for functional independence and wheelchair ability in men with spinal cord injury

Authors: Frederico Ribeiro Neto, PhD1,2,* Rodrigo Rodrigues Gomes Costa, MSc2 Ricardo Antônio Tanhoffer, PhD3 Josevan Cerqueira Leal, PhD1,4 Martim Bottaro, PhD1 Rodrigo Luiz Carregaro, PhD1,4

1. College of Physical Education, Universidade de Brasilia (UnB), Brasilia, Brazil. 2. SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil. 3. Physiology Department, Metabolism Laboratory, Universidade Federal do Paraná (UFPR), Setor de Ciências Biológicas, Curitiba, Brazil. 4. School of Physical Therapy, Universidade de Brasilia (UnB), Brasilia, Brazil.

We certify that no party having a direct interest in the results of the research supporting this article has or will confer a benefit on us or on any organization with which we are associated.

*Corresponding author: Frederico Ribeiro Neto Department: Spinal Cord Injury Program Institution: SARAH Rehabilitation Hospital Network/SARAH Brasilia Country: Brazil Tel: 55 61 3319-1831 Mob: 55 61 99184-1550 Fax: 55 61 3319-1538 Email: [email protected]

1

MUSCLE STRENGTH CUTOFF-POINTS FOR FUNCTIONAL INDEPENDENCE AND

2

WHEELCHAIR ABILITY IN MEN WITH SPINAL CORD INJURY

3 4

ABSTRACT

5

Objective: Determine trunk and shoulder muscle strength cutoff-points for functional independence

6

and wheelchair skills, and verify the predictive capacity of relative and absolute peak torque in men

7

with spinal cord injury (SCI).

8

Design: Cross-sectional study.

9

Setting: Rehabilitation Hospital Setting.

10

Participants: Fifty-four men with SCI were recruited and stratified into high and low paraplegia

11

groups.

12

Interventions: All subjects performed maximum strength tests for shoulder abduction/adduction

13

(isokinetic) and trunk flexion/extension (isometric) to determine relative and absolute peak torque

14

cutoff-points for the Spinal Cord Independence Measure (SCIM-III) and Adapted Manual

15

Wheelchair Circuit (AMWC).

16

Main outcomes: The primary outcomes were SCIM-III, AMWC-Brazil test, and strength variables

17

(peak torques). Demographic characteristics obtained from participants’ electronic medical records

18

were the secondary outcomes used as predictor variables of functional independence.

19

Results: The best predictive model for SCIM-III (R=0.78, P≤0.05) used the sum of trunk flexion

20

and extension relative peak torque values to determine the cutoff-points (1.42 N.m/kg for a score of

21

70). Relative shoulder abduction peak torque was used in the predictive models for AMWC

22

outcomes: performance score (R=0.77, P≤0.05 and cutoff-points of 0.97 N.m/kg for 300.0 meters)

23

and 3-minute overground wheeling (R=0.72, P≤0.05 and cutoff-points of 0.96 N.m/kg for 18.5

24

seconds).

25

Conclusions: Relative peak torque showed better predictive capacity compared to absolute peak

26

torque. Cutoff-points were established for relative muscle strength and could help health

1

27

professionals set appropriate goals for individuals with SCI to achieve high functional independence

28

and wheelchair ability.

29 30

Keywords: muscle strength dynamometer; rehabilitation; resistance training; test taking skills;

31

reference values.

32 33

Abbreviations: AMWC: Adapted Manual Wheelchair Circuit; BMI: body mass index; HP: high

34

paraplegia group; LP: low paraplegia group; MVIC: maximum voluntary isometric contraction;

35

OMNI-RES: perceived exertion scale for resistance exercises; SCI: spinal cord injury; SCIM-III:

36

Spinal Cord Independence Measure; TSI: time since injury; 1RM: one maximum repetition test.

37

2

38

INTRODUCTION

39 40 41

Functional independence is one of the main goals of individuals with spinal cord injury

42

(SCI).1 Improvements in walking speed, transfers, and upper limb strength are relevant outcomes

43

targeted by a wide range of interventions.1-3 Wheelchair ability is a major determinant of functional

44

independence,1 since it governs the autonomy of this population.4 Additionally, it has long been

45

recognized that age,5, 6 age at the SCI event,6 level and severity of injury,1, 7 time since injury,5, 7

46

initial SCI level6, 7 and length of hospital stay1, 7 are good predictors of functional independence.

47

However, these variables are not influenced by exercise, whereas muscle strength and power,1, 8

48

aerobic fitness,1 musculoskeletal pain,1 physical activity level,5 body composition,8 and spasticity1

49

are directly affected by interventions such as strength training.

50 51

Muscle strength is deemed essential for individuals with SCI9, and reduced strength has

52

been associated with a decline in physical function.10 Nevertheless, the relationship between

53

strength and independence remains a challenging topic, since predicting functional independence

54

based on strength measurements has yet to be clearly defined.11, 12 However, to the best of our

55

knowledge, only one study has used the one repetition maximum (1RM) bench press performance

56

to establish reference values for strength in individuals with SCI.8 Although cutoff-points to achieve

57

a higher level of independence (absolute and relative strength of 51.0 kg and 0.77 kg.kg-1,

58

respectively) have been reported,8 the 1RM bench press is not a gold standard for strength

59

assessment,13, 14 assesses only fully preserved muscles and it could not differentiate high and low

60

paraplegia.8 Although, evidence suggests a positive relationship between strength and functional

61

independence based on fully preserved muscles of individuals with paraplegia,5, 8 optimal functional

62

independence may also be affected by partially compromised muscles (e.g., trunk muscles),15 which

63

are not traditionally assessed in individuals with SCI16 and unfeasible to evaluate in 1RM bench

64

press test. 3

65 66

The adoption of absolute or relative strength can influence functional independence

67

assessment, and absolute values are considered a good predictor for different functional

68

independence instruments.8 Likewise, relative strength is the best mobility predictor. However,

69

using absolute values as a reference can be misleading.17 Relative strength is increasingly

70

recognized as a good health predictor in other populations and has proved useful in strength

71

research. While reduced strength may limit transfer agility and wheelchair propulsion regardless of

72

body mass,11 strong obese individuals may exhibit further complications. Although cross-sectional

73

muscle area (muscle thickness) is a major determinant of strength, strong overweight individuals do

74

not necessarily perform better in endurance activities.18 Similarly, increased body mass associated

75

with decreased strength may result in poor functional independence.8

76 77

Thus, the present study aimed to: (1) determine optimal trunk and shoulder strength cutoff-

78

points for greater functional independence and wheelchair skills in men with SCI; (2) establish

79

predictive equations for functional independence in men with SCI, based on relative and absolute

80

strength and wheelchair skills; and (3) compare strength between high and low paraplegia

81

(exhibiting fully and partially preserved muscles).

82 83

METHODS

84 85 86

Participants

87 88

Fifty-four men with SCI were consecutively recruited from the rehabilitation program of a

89

Network Centre of Rehabilitation Hospitals until the calculated sample size for each group was

90

achieved. Data were collected from September 2016 to February 2017. The study was approved by 4

91

the institutional Ethics Committee (protocol n. 2.447.149), and all participants were outpatients and

92

provided written informed consent.

93 94

Inclusion criteria were: 1) male, 2) diagnosed with traumatic SCI paraplegia, 3) at least six

95

months of time since injury, 4) complete motor lesion (ASIA Impairment Scale A or B)19 and 5)

96

manual wheelchair user. Participants were excluded if they had a history of metabolic disorders,

97

cardiovascular, cardiac, or orthopedic surgery that would hamper performance in functional tests or

98

an adequate exercise technique and were a user of walking equipment (e.g., braces or crutches) for

99

daily life activities.

100 101 102

Subjects were sequentially assigned to a high (HP, T1 to T6) or low paraplegia group (LP, T7 to L3) until reaching the estimated sample size.

103 104

Procedures

105 106

On day one, the participants were advised of the procedures, received instructions, and

107

underwent clinical, functional independence, and wheelchair ability assessments. Wheelchair mass,

108

frames, and ownership were recorded for intergroup comparison since these variables can affect

109

wheelchair skills.20 Strength assessments were conducted after a 24 to 72-hour interval.

110 111

Clinical Assessment

112 113

Body mass was assessed, and height was calculated based on Rufino et al.,21 who

114

determined the height multiplying the half arm span by two and dividing the result by 1.06. Two

115

physiotherapists evaluated the muscle tone of hips and knees (flexion and extension) with the

5

116

Modified Ashworth Scale,22 The total score for the left and right limbs was used in analyses, and

117

item 1+ was set to 1.5.

118 119

Functional Independence and Wheelchair Ability (SCIM-III and AMWC-Brazil)

120 121

Functional independence was assessed using the Spinal Cord Independence Measure

122

version III (SCIM-III)23, 24. The SCIM-III scale items are graded by difficulty level according to the

123

individual’s skill level.24 The total score ranges from 0 to 100, with high scores indicating greater

124

skill and independence. The three subscales assess self-care (20 points, 4 items), respiratory and

125

sphincter management (40 points, 4 items), and mobility (40 points, 9 items).23

126 127

Wheelchair ability was determined using the Adapted Manual Wheelchair Circuit (AMWC-

128

Brazil).25 Participants were allowed to adjust the hand rims and gloves to match their normal

129

propulsion conditions. Subjects used their own manual wheelchairs or those provided by the

130

rehabilitation center. Fourteen standard AMWC items were performed with fixed order and two

131

minutes’ rest between them. Before the execution of each item, the assessor explained how it should

132

be performed and the required time to complete the task. The item performed within the estimated

133

time was marked as ‘1’ point. Half point was available to the doorstep, platform, and transfer

134

items.25 The outcomes provided by the AMWC-Brazil were: (1) ability score (sum of the scores for

135

all fourteen items); (2) performance score (total time, in seconds, of the three items that should be

136

performed in the shortest possible time: Figure-of-eight, 15-m sprint and 4-m artificial grass); (3) 3-

137

minute overground wheeling (meters): the highest distance covered in 3 minutes during wheelchair

138

propulsion; (4) total time of thirteen items (in seconds, excluding item 14, the 3-minute overground

139

wheeling).25

140

6

141

Strength Assessment

142 143

Three maximum strength tests were carried out in a fixed order on an isokinetic

144

dynamometer (Biodex System 4), with 5-minute rest between them, as follows: (1) Concentric

145

shoulder abduction and adduction at 60°/s; (2) Maximum voluntary isometric contraction (MVIC)

146

of trunk flexion and; (3) MVIC of trunk extension. The same assessor conducted all the tests and

147

gave standardized verbal encouragement.

148 149

Concentric shoulder abduction and adduction: participants were allowed to hold the handle

150

with their non-involved limb to increase trunk stabilization (Figure 1A and 1B). Familiarization

151

consisted of two sets of 10 submaximal concentric and reciprocal repetitions, at 60°/s, with a 1-

152

minute rest between sets and level 2 on the perceived exertion scale for resistance exercises

153

(OMNI-RES).26 This was followed by shoulder abduction and adduction assessments (5 maximal

154

concentric and reciprocal contractions, at 60°/s).

155 156

FIGURE 1

157 158

MVIC of trunk flexion and extension: in a pilot study, 80º trunk flexion was the position of

159

balance for individuals with SCI in the sitting position, without assistance. Due to reduced trunk

160

muscle strength in subjects with a high-level injury, tests were performed at 55º and 105º in the

161

sagittal plane for hip flexion and extension, respectively. The participants were unbalanced in the

162

direction of the movement being tested and stabilized by straps and belts to allow low torque values

163

to be detected (Figure 1C and 1D).

164 165 166

Strength assessment consisted of 2 familiarization sets and two 6-second MVIC sets separated by 1-minute intervals. The familiarization sets were submaximal (level 2 on the OMNI7

167

RES).26 For the two MVIC sets, participants were instructed to execute a continuous maximum

168

contraction and avoid bouncing movements. The highest peak torque between the two MVIC sets

169

was used for analysis. Participants performed the trunk flexion test with their arms relaxed and for

170

trunk extension were instructed to rest their hands on the belts (Figure 1C and 1D).

171 172

The highest absolute and relative peak torque in each movement, as well as the sum of peak

173

torque values for shoulder abduction and adduction and trunk flexion and extension were used in

174

analyses. For inter-group comparison, peak torque was normalized by body mass and expressed in

175

newton-meters per kilogram (N.m/kg).

176 177

Outcomes

178 179

The primary outcomes were SCIM-III scale (total score), AMWC-Brazil (ability score,

180

performance score, total time of thirteen items and 3-minute overground wheeling), and strength

181

variables (absolute and relative peak torque for shoulder abduction and adduction and trunk flexion

182

and extension, sum of shoulder abduction and adduction peak torque [relative and absolute] and

183

trunk flexion and extension peak torque values [relative and absolute]).

184 185

Demographic characteristics (birth date, time since injury, etiology, and neurological level

186

of injury), obtained from participants’ electronic medical records, were the secondary outcomes

187

used as predictor variables of functional independence.

188 189

Statistical analysis

190 191

The sample size was calculated based on fixed linear multiple regression model,

192

considering an effect size of 0.30, α of 5%, power (1 - β) of 90%, and three predictors out of a total

193

of 19 possible variables (absolute and relative peak torque for shoulder abduction and adduction and 8

194

trunk flexion and extension; sum of shoulder abduction and adduction peak torques; sum of trunk

195

flexion and extension peak torques; age; age at injury; time since injury; injury level; body mass;

196

body mass index; and spasticity), resulting in a sample of 54 individuals with SCI.

197 198

The Kolmogorov-Smirnov normality test was used to assess the data distribution.

199

Descriptive data were presented as mean and standard deviation or median and interquartile (25th

200

and 75th percentiles) for the outcomes defined as parametric or nonparametric, respectively. An

201

independent t-test was used to compare group means when normality assumptions were met and the

202

Mann-Whitney U test for independent samples to compare non-parametric variables.

203 204

Stepwise starting from linear to cubic fitting regression was used to generate equations for

205

predicting SCIM-III total score and AMWC-Brazil outcomes (ability score, performance score, 3-

206

minute overground wheeling, and total time of thirteen items). To avoid collinearity, Spearman’s

207

test was applied to correlate all the predictor variables. The correlation matrix was analyzed, and

208

variables that exhibited a high or very high correlation were considered collinear.1 Correlation

209

coefficient values were classified as very weak (below 0.20); weak (0.20 to 0.39); moderate (0.40 to

210

0.69); high (0.70 to 0.90) and very high (> 0.90).27 All strength variables were inserted in the

211

regression analysis separately to improve collinearity control. Injury level was considered a dummy

212

variable, indicating which group was used for specific observations.

213 214

Based on percentiles (10, 25, 50, 75, and 90), the cutoff-points for absolute and relative

215

peak torque for the independence scales (SCIM-III and AMWC-Brazil) were established using a

216

ROC (receiver operating characteristic) curve. The highest statistically significant percentile for an

217

area under the curve was considered for analysis. Based on the SCIM-III and AMWC-Brazil cutoff-

218

points, subjects were classified as having high or low functional independence.

219 9

220

The outlier labeling rule was used to detect outliers, and discrepancies.28 Outlier values

221

were calculated by the difference between the 25th and 75th percentiles multiplied by a factor (2.2).

222

The result is then subtracted from the 25th percentile and added to the 75th percentile.

223 224

The IBM SPSS Statistics package (version 22.0; SPSS Inc, Armonk, NY), Matlab

225

(R2014.A) and G*Power statistical power analysis software (version 3.1.9.2; Universität Kiel,

226

Germany) were used. Statistical significance was set at 5% (P≤0.05; two-tailed).

227 228

RESULTS

229 230 231

Participant characteristics

232 233 234

There were no dropouts in this study, and no significant differences were found in wheelchair mass or distribution between SCI groups (Table 1).

235 236

TABLE 1

237 238

Strength comparisons

239 240

Relative peak torque for shoulder adduction and abduction and the sum of these values

241

were significantly higher in the LP compared to HP. Relative peak torque for trunk flexion and

242

extension MVIC was higher in the LP than HP (P≤0.05) (Table 2).

243 244

TABLE 2

245 10

246

Functional independence and wheelchair skills comparisons

247 248

All the SCIM-III results were significantly higher for the LP when compared to the HP.

249

With respect to the AMWC-Brazil outcomes, only the inter-group ability score did not differ

250

between groups (P>0.05) (Table 3).

251 252

TABLE 3

253 254

Functional independence prediction

255 256

The cubic equation models produced the highest significant correlations (R2) for the

257

outcomes (supplementary data No. 1-A, No. 1-B and No. 1-C). All the regression equations were

258

significant, except for the AMWC-Brazil ability score. The total time of thirteen items equations

259

exhibited the lowest correlation and was classified as moderate (R=0.69). Both HP and LP obtained

260

the maximum result (14.0) for ability score and this outcome was removed from equation model

261

and cutoff points analysis. The correlation matrix of 19 predictor variables has been shown in

262

supplemental data No. 2.

263 264

The sum of relative peak torque values for trunk flexion and extension showed the greatest

265

predictive capacity for the SCIM-III scale (R=0.78, P≤0.05; β=0.34, P≤0.01) (Table 4), while the

266

sum of shoulder abduction and adduction relative peak torques had the highest predictive capacity

267

for the AMWC-Brazil total time of thirteen items (β=-0.57 and P=0.02) (Table 4). Relative peak

268

torque of shoulder abduction was used in the equation models for the 3-minute overground

269

wheeling and performance scores (β=0.18, β=-0.27, respectively, P≤0.05).

270 271

TABLE 4 11

272 273

Regression models associated with functional independence and wheelchair skills were

274

better for relative than absolute peak torque. Injury level, time since injury, and age were also

275

significant predictors included in regression models (Table 4 and supplementary data No. 3).

276 277

Strength cutoff-points for functional independence and wheelchair skills

278 279

The sum of relative peak torque values for trunk flexion and extension showed a cutoff

280

point of 1.42 N.m/kg to achieve a score of 70 in the SCIM-III (Table 5), while the cutoff point for

281

the sum of shoulder abduction and adduction relative peak torques was 2.35 N.m/kg, associated

282

with a total time of thirteen items of 111.90 sec (Table 5). The cutoff-points for relative peak torque

283

of shoulder abduction to obtain a 3-minute overground wheeling time of 300 m and performance

284

score of 18.5 sec were 0.96 and 0.97 N.m/kg, respectively (Table 5 and supplementary data No. 4).

285 286

TABLE 5

287 288

DISCUSSION

289 290 291

Relative and absolute peak torque from partially preserved muscles were better able to

292

discriminate between SCI levels, considering that absolute peak torque of shoulder adduction did

293

not show a significant difference between HP and LP. However, relative peak torque was a better

294

predictor of functional independence when compared to absolute strength. Although time since

295

injury, age and injury level exhibited were more important than muscle strength in the predictive

296

equations (considering the SCIM-III and three out of four AMWC-Brazil outcomes), the

297

implications of strength are significant because it is influenced by exercise interventions.

298 12

299

Our findings indicated significant differences in trunk strength (flexion and extension)

300

between the HP and LP. Trunk flexion/extension MVIC on an isokinetic dynamometer has not been

301

previously adopted in the context of SCI and was, therefore, a suitable assessment. The abdominal

302

muscles are innervated by the intercostal nerves (T7 to T11) and the erector spinae by spinal nerves,

303

with both muscle groups determinant to trunk balance. The paraplegia groups were stratified

304

considering these characteristics and significant intergroup differences in peak trunk

305

flexion/extension torque were expected. Identifying differences in trunk flexion/extension strength

306

between SCI levels is important in functional independence assessments because impaired trunk

307

balance can compromise performance in activities of daily living.29 Moreover, the trunk

308

flexion/extension peak torques of the present study were obtained at 55º and 105º in the sagittal

309

plane for hip flexion and extension, respectively. This positioning was based on a pilot study to

310

ensure that all participants could perform the test, independently of their injury level.26

311

Nevertheless, it is necessary to consider that the trunk flexion/extension isometric peak torque could

312

be achieved in other angles of trunk flexion/extension.

313 314

The regression equation model containing the sum of relative peak torque values for trunk

315

flexion and extension explained 61% of functional independence (SCIM-III). In this respect, our

316

findings corroborate those of previous studies,30, 31 in which the trunk muscles were considered vital

317

to postural balance.29 We demonstrated that a cutoff point of 1.42 N.m/kg was required for

318

isometric trunk flexion and extension to achieve 70 points on the SCIM-III scale. Prior

319

investigations have reported SCIM-III values ranging from 29 to 51 in individuals with acute SCI

320

and shorter rehabilitation times.23, 32 These studies used heterogeneous samples and broader

321

inclusion criteria, which could affect interpretations of an optimal SCIM-III score associated with

322

higher degrees of independence.32 Aidinoff et al.37 recorded SCIM-III scores between 64 and 78 for

323

individuals with thoracic and lumbar SCI at hospital discharge, with a mean stay of 5 months.33 A

324

Brazilian study reported SCIM-III scores of 68 and 65 for individuals with HP and LP, 13

325

respectively.8 As such, a score of 70 on the SCIM-III can be considered a suitable and plausible

326

goal for functional independence in individuals with thoracic and lumbar SCI.

327 328

In the present study, both trunk flexion/extension and shoulder abduction/adduction

329

provided suitable cutoff-points for outcomes related to better functional independence and

330

wheelchair skills. The strength variables with the highest predictive capacity for wheelchair skills

331

were the sum of relative peak torque values for shoulder abduction and adduction and shoulder

332

abduction relative peak torque. Wheelchair ability was assessed based on four AMWC-Brazil

333

outcomes, and only the ability score showed no significant difference between the HP and LP. This

334

outcome had a ceiling effect in studies by Kilkens et al.,4, 34 Cowan et al.35 and Ribeiro Neto et al.,25

335

albeit without paraplegic subgroup stratification. However, significant differences were observed

336

between the paraplegia groups for 3-minute overground wheeling, performance score and total time

337

of thirteen items, and the models explained 52%, 59%, and 48% of wheelchair skills, respectively.

338 339

The shoulder muscle’s strength training is traditionally excluded or present a reduced

340

workload of abduction exercises, mostly because of a high prevalence of shoulder injury in the daily

341

life of individuals with SCI.36, 37. The overall idea is to minimize the occurrence of injuries in this

342

joint during rehabilitation.36, 37 Previous studies proposed interventions based on strength training

343

mainly focused on the anterior and posterior muscles of the trunk.36, 37 However, both shoulder

344

abduction and adduction are rather important for wheelchair propulsion and activities of daily

345

living.5, 30, 38 Our findings corroborate this statement since the shoulder abduction was correlated to

346

a better performance in three of the AMWC-Brazil outcomes. Therefore, there is a paradox between

347

the risk of injury by overuse and the importance of shoulder abduction for daily life activities. It is

348

suggested that not only the prime shoulder adduction muscles should be emphasized during a

349

rehabilitation and strength training program, but also exercises focusing on synergistic and

350

stabilizing muscles. 14

351 352

In addition to relative and absolute peak torque, the covariates injury level, time since

353

injury and age were also predictors in the regression models. Only age and time since injury were

354

significantly correlated with the independence outcomes and simultaneously entered in the

355

regression equation. However, the correlation value was low (0.28), minimizing the risk of

356

collinearity (supplemental data No. 2) and presented the collinearity statistics tolerance ranging

357

from 0.95 to 0.99 for regression equation using absolute strength. In contrast to other studies that

358

found reduced β values for age and time since injury,7, 8 these predictors had the greatest influence

359

on SCIM-III and AMWC-Brazil performance scores, respectively. The equation models explained

360

48% to 61% of functional independence and the wheelchair skills assessed. Thus, our findings

361

suggest that further studies are needed to elucidate whether other predictors (such as body

362

composition, length of hospital stay and sex) affect the functional independence and wheelchair

363

ability of individuals with SCI. Moreover, further studies focusing on the feasibility of clinical tests

364

(e.g., handgrip dynamometry or 1RM tests) on the assessment of the strength of partially

365

compromised muscles are warranted and might help to establish the strength cutoff points in clinical

366

practice.

367 368

Study Limitations

369 370

Wheelchair data were recorded and similar group distribution confirmed, but many of the

371

wheelchairs were old and had minor bearings defects. Although this variable improves the external

372

validity of our study, the low socioeconomic status of the participants precluded routine or

373

necessary repairs, which might have affected performance in the AMWC-Brazil. Another limitation

374

was a possible ceiling effect in the SCIM-III, reported in previous studies.8 Trunk or shoulder

375

strength measures may be misleading, since a large section of the SCIM-III is related to respiration,

376

the bowel and bladder, which may have influenced our findings and the cutoff point determination. 15

377

In addition, it is worth noting that the weight differences of the item scores might have affected the

378

equation model. Finally, because the shoulder is a three-dimensional joint, the role of synergists and

379

assessments within a broader combination of gestures, such as specific tasks and activities of daily

380

living, may also be associated with predicting functional independence.

381 382

CONCLUSION

383 384 385

In the present study, relative peak shoulder abduction torque, the sum of relative peak

386

torques for trunk flexion/extension and shoulder abduction/adduction showed the highest predictive

387

capacity for functional independence and wheelchair ability. The cutoff-points established could be

388

adopted as a parameter for optimal functional independence and wheelchair skills.

389 390

CONFLICT OF INTEREST

391 392

The authors declare no conflict of interest.

393

16

394

REFERENCES

395

1.

396

independence and health-related functional status following spinal cord injury: a prospective study

397

of the association with physical capacity. J Rehabil Med 2008;40(10):812-8.

398

2.

399

muscles during wheelchair propulsion by paraplegic persons. Arch Phys Med Rehabil

400

1996;77(2):187-93.

401

3.

402

2016;62(1):4-11.

403

4.

404

Circuit: Construct validity and responsiveness of a test to assess manual wheelchair mobility in

405

persons with spinal cord injury. Arch Phys Med Rehabil 2004;85(3):424-31.

406

5.

407

implications for independence: Part I. Paraplegia 1994;32(4):211-8.

408

6.

409

years after spinal cord injury. Arch Phys Med Rehabil 1997;78(6):644-50.

410

7.

411

injury after inpatient rehabilitation: in Saudi Arabia. NeuroRehabilitation 2014;35(2):341-7.

412

8.

413

al. Influence of Relative Strength on Functional Independence of Patients With Spinal Cord Injury.

414

Arch Phys Med Rehabil 2017;98(6):1104-12.

415

9.

416

Rehabilitation in Spinal Cord Injury. Top Spinal Cord Inj Rehabil 2007;13(1):98-122.

417

10.

418

2012;67(1):28-40.

Haisma JA, Post MW, van der Woude LH, Stam HJ, Bergen MP, Sluis TA et al. Functional

Mulroy SJ, Gronley JK, Newsam CJ, Perry J. Electromyographic activity of shoulder

Harvey LA. Physiotherapy rehabilitation for people with spinal cord injuries. J Phys

Kilkens OJ, Dallmeijer AJ, De Witte LP, Van Der Woude LH, Post MW. The Wheelchair

Pentland WE, Twomey LT. Upper limb function in persons with long term paraplegia and

Saboe LA, Darrah JM, Pain KS, Guthrie J. Early predictors of functional independence 2

Abdul-Sattar AB. Predictors of functional outcome in patients with traumatic spinal cord

Ribeiro Neto F, Guanais P, Lopes GH, Dornelas E, de Campos Barbetta D, Coutinho AC et

Warburton DE, Eng JJ, Krassioukov A, Sproule S. Cardiovascular Health and Exercise

Manini TM, Clark BC. Dynapenia and aging: an update. J Gerontol A Biol Sci Med Sci

17

419

11.

Dost G, Dulgeroglu D, Yildirim A, Ozgirgin N. The effects of upper extremity progressive

420

resistance and endurance exercises in patients with spinal cord injury. J Back Musculoskelet

421

Rehabil 2014;27(4):419-26.

422

12.

423

in upper extremities in wheelchair athletes. J Strength Cond Res 2010;24(1):8-16.

424

13.

425

maximum equations accuracy in paralympic rowers with motor disabilities. J Strength Cond Res

426

2009;23(3):1045-50.

427

14.

428

one repetition maximum load by total and lean body mass in trained and untrained men. Med Sport

429

2012;16(3):111-7.

430

15.

431

Postural Stability and Trunk and Upper Extremity Strength on Performance during Manual

432

Wheelchair Propulsion Tests in Individuals with Spinal Cord Injury: An Exploratory Study. Rehabil

433

Res Pract 2016;2016:6842324.

434

16.

435

Sport Rehabil 2017;26(4):287-93.

436

17.

437

relative values? Rev Assoc Med Bras 2013;59(4):308-9.

438

18.

439

size with bench press and bench throw performances. J Strength Cond Res 2014;28(6):1778-82.

440

19.

441

International standards for neurological classification of spinal cord injury (revised 2011). J Spinal

442

Cord Med 2011;34(6):535-46.

443

20.

444

in rehabilitation, sports, daily life and health. Med Eng Phys 2006;28(9):905-15.

Turbanski S, Schmidtbleicher D. Effects of heavy resistance training on strength and power

Schwingel PA, Porto YC, Dias MC, Moreira MM, Zoppi CC. Predicting one repetition

Cadore E, Pinto RS, Brentano MA, Silva RF, da Silva EM, Spinelli R et al. Prediction of

Gagnon DH, Roy A, Gabison S, Duclos C, Verrier MC, Nadeau S. Effects of Seated

Saltan A, Ankarali H. The Role of Trunk Stabilization in Functional Classification Levels. J

Prestes J, Tibana RA. Muscular static strength test performance and health: absolute or

Akagi R, Tohdoh Y, Hirayama K, Kobayashi Y. Relationship of pectoralis major muscle

Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A et al.

van der Woude LH, de Groot S, Janssen TW. Manual wheelchairs: Research and innovation

18

445

21.

Rufino R, Costa CH, Antão VC, Pinheiro GA, Jansen JM. Relação envergadura/altura: um

446

valor para estudos espirométricos em brasileiros. Pulmão/RJ 1996;7:40-4.

447

22.

448

spasticity. Phys Ther 1987;67(2):206-7.

449

23.

450

Development and validation of a self-report version of the Spinal Cord Independence Measure

451

(SCIM III). Spinal Cord 2013;51(1):40-7.

452

24.

453

Catz-Itzkovich Spinal Cord Independence Measure assessment by interview and comparison with

454

observation. Am J Phys Med Rehab 2003;82(4):267-72.

455

25.

456

validation of a Brazilian version of the adapted manual wheelchair circuit (AMWC-Brazil). Phys

457

Theor Practice 2018;16:1-13.

458

26.

459

familiarization on maximum strength testing in male individuals with spinal cord injury. Isok Exerc

460

Sci 2018;26(2):125-32.

461

27.

Bohannon R. Spearman correlations of .60 are not poor. Am J Occ Ther 1992;46(5):472.

462

28.

Kannan KS, Manoj K, Arumugam S. Labeling Methods for Identifying Outliers. Int J Stat

463

Sys 2015;10(2):231-8.

464

29.

465

subjects with spinal cord injury. Arch Phys Med Rehabil 1994;75(7):761-5.

466

30.

467

paraplegia who use wheelchairs. Arch Phys Med Rehabil 2002;83(4):441-6.

468

31.

469

strength in individuals with spinal cord injury who use manual wheelchairs. J Spinal Cord Med

470

2005;28(1):26-32.

Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle

Fekete C, Eriks-Hoogland I, Baumberger M, Catz A, Itzkovich M, Luthi H et al.

Itzkovich M, Tamir A, Philo O, Steinberg F, Ronen J, Spasser R et al. Reliability of the

Ribeiro Neto F, Gomes Costa RR, Garcia Lopes AC, Carregaro RL. Cross-cultural

Ribeiro Neto F, Costa RRG, Cardoso JR, Brown L, Bottaro M, Carregaro RL. Influence of

Powers CM, Newsam CJ, Gronley JK, Fontaine CA, Perry J. Isometric shoulder torque in

Kotajarvi BR, Basford JR, An KN. Upper-extremity torque production in men with

Souza AL, Boninger ML, Fitzgerald SG, Shimada SD, Cooper RA, Ambrosio F. Upper limb

19

471

32.

Catz A, Itzkovich M, Agranov E, Ring H, Tamir A. SCIM -Spinal Cord Independence

472

Measure: a new disability scale for patients with spinal cord lesions. Spinal Cord 1997;35(12):850-

473

6.

474

33.

475

cord independence measure, third version, scores for various neurological levels after complete

476

spinal cord lesions. Spinal Cord 2011;49(8):893-6.

477

34.

478

Wheelchair Circuit: Reliability of a test to assess mobility in persons with spinal cord injuries. Arch

479

Phys Med Rehabil 2002;83(12):1783-8.

480

35.

481

Test-retest reliability and discriminative validity in persons with spinal cord injury. Arch Phys Med

482

Rehabil 2011;92(8):1270-80.

483

36.

484

during manual wheelchair propulsion in response to weakness in individual muscle groups: A

485

simulation study. Clin Biomech 2016;33:34-41.

486

37.

487

injury: a clinical practice guideline for health-care professionals. J Spinal Cord Med

488

2005;28(5):434.

489

38.

490

athletes. The role of muscle imbalance. Am J Sports Med 1993;21(2):238-42.

Aidinoff E, Front L, Itzkovich M, Bluvshtein V, Gelernter I, Hart J et al. Expected spinal

Kilkens OJ, Post MW, van der Woude LH, Dallmeijer AJ, van den Heuvel WJ. The

Cowan RE, Nash MS, de Groot S, van der Woude LH. Adapted Manual Wheelchair Circuit:

Slowik JS, McNitt-Gray JL, Requejo PS, Mulroy SJ, Neptune RR. Compensatory strategies

Paralyzed Veterans of America P. Preservation of upper limb function following spinal cord

Burnham RS, May L, Nelson E, Steadward R, Reid DC. Shoulder pain in wheelchair

20

TABLES AND FIGURES LEGENDS

Tables Table 1: Participant demographic data, considering the injury level groups. Variables are presented as median (25th and 75th percentiles). Body mass index (BMI) is expressed as mean (standard deviation). Etiology is expressed in absolute values (frequency in each group) and wheelchair characteristics as frequency (%) and mean (standard deviation).

* Significant difference in relation to the HP (P≤0.05); † Significant difference in relation to the LP (P≤0.05); ‡ Significant difference compared to rigid frame (P≤0.05). HP: high paraplegia; LP: low paraplegia. na: not applicable.

Table 2: Descriptive data for absolute (abs, N.m) and relative muscle strength (rel, N.m/kg) in the high (HP) and low paraplegia (LP) groups. Relative peak torque values for shoulder adduction and abduction as well as the sum of these values for shoulder exercises are expressed as mean (standard deviation). The other variables are expressed as median (25th and 75th percentiles).

* Significant difference compared to the HP (P≤0.05). ABD: abduction; ADD: adduction; EXT: extension; FLX: flexion; PT: peak torque; PTabs: absolute peak torque; PTrel: relative peak torque; SAAsum: shoulder abduction and adduction peak torque; TFEsum: sum of trunk flexion and extension peak torques.

21

Table 3: Descriptive data of functional independence and wheelchair ability outcomes (SCIM-III and AMWC-Brazil) in the high paraplegia (HP) and low paraplegia (LP) groups. The performance score and 3-minute overground wheeling test are expressed as mean (standard deviation) and the other variables as median (25th and 75th percentiles).

* Significant difference compared to the HP (P≤0.05). 3MinTest: 3-minute overground wheeling test; AMWC-Brazil: Adapted Manual Wheelchair Circuit - Brazilian version PS: performance score; Resp.: respiration; SCIM-III: Spinal Cord Independence Measure version III; SM: sphincter management; TT: total time of thirteen items.

Table 4: Stepwise regression (R and R2 values) for the independence scale (SCIM-III) and wheelchair skills (AMWC-Brazil), beta weights (β) and probability values (P) of the predictor variables.

* Statistical significance (P≤0.05). 3MinTest: 3-minute overground wheeling test; ABD: abduction; PS: performance score; PTabs: absolute peak torque; PTrel: relative peak torque; SAAsum: sum of shoulder abduction and adduction peak torques; TFEsum: sum of trunk flexion and extension peak torques; TSI: time since injury; TT: total time of thirteen items.

22

Table 5: Results of the ROC curve for strength variables with the best predictive values for the independence scale (SCIM-III) and wheelchair skills (AMWC-Brazil) at the highest percentile and with statistical significance for the area under curve.

Area under the curve (AUC) was statistically different from the ROC curve reference line for all strength variables (P≤0.05). 3MinTet: 3-minute overground wheeling test; ABD: abduction; CP: cutoff point for strength variables (N.m/kg); PTrel: relative peak torque; SAAsum: sum of shoulder abduction and adduction peak torques; SENS: sensitivity; SPEC: specificity; TFEsum: sum of trunk flexion and extension peak torques; TR: test result.

Figure Figure 1: Illustration of the position adopted for shoulder abduction and adduction (A and B) and trunk flexion (C) and extension (D) in maximum strength testing on an isokinetic dynamometer. A: initial shoulder abduction position in the isokinetic test, at an angle of 15º; B: initial shoulder adduction position in the isokinetic test, at an angle of 90º; C: trunk flexion position in the isometric test, at a hip angle of 55º and, D: initial trunk extension position in the isometric test, at a hip angle of 105º.

23

Table 1: Participant demographic data, considering the injury level groups. Variables are presented as median th

(25

th

and 75

percentiles). Body mass index (BMI) is expressed as mean (standard deviation). Etiology is

expressed in absolute values (frequency in each group) and wheelchair characteristics as frequency (%) and mean (standard deviation). n Age (years) 26.9 Time since injury (months) 37.4 Age at injury (years) 23.7 Body mass (kg) 68.2 Height (cm) 170.2 2 BMI (kg/m ) 23.8 Ashworth spasticity scale 3.0 Etiology (n) Auto accident 3 Diving 1 Falls 2 Gunshot wound 18 Hit by falling object 1 Knife wound 0 Motorcycle accident 2 Wheelchair frame (kg) Rigid 48.1% Folding 22.2% Double Folding 29.6% Wheelchair owner (kg) Participant 42.6% Hospital 7.4% * Significant difference in relation to the

HP 27 (22.9 - 36.8) (16.8 - 53.2) (18.8 - 34.9) (56.6 - 76.2) (167.9 - 174.5) (4.9) (2.0 - 4.0) (5.6%) (1.9%) (3.7%) (33.3%) (1.9%) (0.0%) (3.7%) 13.9 (2.4) 16.2 (2.4) 17.9‡ (1.5)

29.3 50.1 22.4 67.8 170.2 22.9 0.0* 4 0 2 19 0 1 1 59.3% 40.7% 0.0%

LP 27 (22.4 - 37.9) (21.5 - 104.8) (19.0 - 32.5) (56.5 - 77.7) (167.0 - 176.4) (4.4) (0.0 - 3.0) (7.4%) (0.0%) (3.7%) (35.2%) (0.0%) (1.9%) (1.9%) 13.8 (2.0) 16.1‡ (1.8) -

28.8 39.8 23.1 68.0 170.2 23.3 2.0 7 1 4 37 1 1 3 53.7% 31.5% 14.8%

TOTAL 54 (22.9 - 37.1) (19.4 - 82.2) (19.0 - 33.0) (56.6 – 77.2) (167.0 – 174.5) (4.7) (0.0 - 4.0) (12.9%) (1.9%) (7.4%) (68.4%) (1.9%) (1.9%) (5.6%) 13.8 (2.2) 16.1‡ (2.0) 17.9‡ (1.5)

15.5 (0.9) 37.0% 14.5 (2.5) 79.6% 15.1 (2.7) 15.7 (2.4) 13.0% 15.5 (0.9) 20.4% 15.6 (1.5) HP (P≤0.05); † Significant difference in relation to the LP (P≤0.05); ‡

Significant difference compared to rigid frame (P≤0.05). HP: high paraplegia; LP: low paraplegia. na: not applicable.

Table 2: Descriptive data for absolute (abs, N.m) and relative muscle strength (rel, N.m/kg) in the high (HP) and low paraplegia (LP) groups. Relative peak torque values for shoulder adduction and abduction as well as the sum of these values for shoulder exercises are expressed as mean (standard deviation). The other variables are th

th

expressed as median (25 and 75 percentiles).

n

HP

LP

27

27

Shoulder ABD PTabs

58.20

ABD PTrel

0.86

(0.15)

1.05*

(0.16)

ADD PTabs

82.91

(16.13)

98.83

(22.61)

ADD PTrel

1.28

(0.26)

1.48*

(0.27)

SAAsum absolute

144.31

SAAsum relative

2.14

(0.38)

ABD/ADD PT index

0.65

(0.60 – 0.74)

(49.20 – 61.70)

(25.62)

71.30*

169.73* 2.53* 0.72

(60.00 – 80.20)

(37.72) (0.41) (0.68 – 0.77)

Trunk FLX PTabs

37.10

FLX PTrel

0.53

EXT PTabs

42.10

EXT PTrel

0.65

TFEsum absolute

76.00

TFEsum relative

1.18

(25.80 – 47.90) (0.38 – 0.67) (32.30 – 47.20) (0.53 – 0.76) (62.60 – 94.50) (1.05 – 1.30)

FLX/EXT PT index 0.87 (0.70 – 1.18) * Significant difference compared to the HP (P≤0.05).

64.30* 0.93* 56.30* 0.83* 119.00*

(52.30 – 82.00) (0.78 – 1.17) (39.60 – 67.00) (0.59 – 1.00) (91.70 – 146.30)

1.71*

(1.53 – 2.10)

1.28*

(0.91 – 1.73)

ABD: abduction; ADD: adduction; EXT: extension; FLX: flexion; PT: peak torque; PTabs: absolute peak torque; PTrel: relative peak torque; SAAsum: shoulder abduction and adduction peak torque; TFEsum: sum of trunk flexion and extension peak torques.

Table 3: Descriptive data of functional independence and wheelchair ability outcomes (SCIM-III and AMWCBrazil) in the high paraplegia (HP) and low paraplegia (LP) groups. The performance score and 3-minute overground wheeling test are expressed as mean (standard deviation) and the other variables as median th

th

(25 and 75 percentiles). HP n 27 SCIM-III Self-Care 18 (17 – 18) 18* Resp. & SM 33 (33 – 33) 33* Mobility 17 (16 – 18) 19* Total 67 (66 – 68) 70* AMWC-Brazil Ability Score 14.0 (14.0 – 14.0) 14.0 PS (sec) 21.65 (2.86) 19.06* TT (sec) 130.73 (107.63 – 167.7) 92.44* 3MinTest (m) 253.6 (32.6) 291.6* * Significant difference compared to the HP (P≤0.05).

LP 27 (18 – 18) (33 – 34) (17 – 19) (68 – 71) (14.0 – 14.0) (2.17) (77.91 – 116.54) (35.3)

TOTAL 54 18 33 17 68 14.0 20.35 111.90 272.6

(18 – 18) (33 – 33) (16 – 19) (66 – 70) (14.0 – 14.0) (2.84) (90.18 – 138.39) (38.8)

3MinTest: 3-minute overground wheeling test; AMWC-Brazil: Adapted Manual Wheelchair Circuit - Brazilian version PS: performance score; Resp.: respiration; SCIM-III: Spinal Cord Independence Measure version III; SM: sphincter management; TT: total time of thirteen items.

2

Table 4: Stepwise regression (R and R values) for the independence scale (SCIM-III) and wheelchair skills (AMWC-Brazil), beta weights (β) and probability values (P) of the predictor variables. SCIM-III R 2 R

0.78* 0.61

TFEsum relative

AMWC-Brazil TT 0.69* 0.48

PS 0.77* 0.59

3MinTest 0.72* 0.52

β

p

β

p

β

p

β

p

0.34

<0.01

-

-

-

-

-

-

(TFEsum relative)

2

0.07

0.50

-

-

-

-

-

-

(TFEsum relative) Injury Level 2 (Injury Level) 3 (Injury Level) TSI 2 (TSI) 3 (TSI)

3

0.01 0.40 0.05 -0.10 0.59 -0.03 -0.06

0.71 <0.01 0.71 0.44 <0.01 0.88 0.40

-0.28 0.14 -0.02

<0.01 0.48 0.72

-0.40 -0.18 0.07 -0.11 0.20 -0.06

0.19 0.21 0.65 0.62 0.40 0.43

0.50 -0.12 -0.08 0.19 -0.14 -0.61

0.08 0.36 0.56 0.29 0.52 0.42

SAAsum relative

-

-

-

-

-0.57

0.02

-

-

(SAAsum relative)

2

-

-

-

-

0.17

0.07

-

-

(SAAsum relative)

3

-

-

-

-

0.07

0.36

-

-

-

-

-0.27

<0.01

-

-

0.18

0.04

-

-

0.03

0.75

-

-

-0.01

0.92

-

-0.11 0.42 0.14 -0.12

0.09 <0.01 0.40 0.20

-

-

0.09 -

0.18 -

ABD PTrel (ABD PTrel)

2 3

(ABD PTrel) Age 2 Age 3 Age * Statistical significance (P≤0.05).

3MinTest: 3-minute overground wheeling test; ABD: abduction; PS: performance score; PTabs: absolute peak torque; PTrel: relative peak torque; SAAsum: sum of shoulder abduction and adduction peak torques; TFEsum: sum of trunk flexion and extension peak torques; TSI: time since injury; TT: total time of thirteen items.

Table 5: Results of the ROC curve for strength variables with the best predictive values for the independence scale (SCIM-III) and wheelchair skills (AMWC-Brazil) at the highest percentile and with statistical significance for the area under curve. TR

AUC

95%CI

SENS

SPEC

CP

70

0.77

0.63 – 0.91

0.64

0.80

1.42

111.90

0.76

0.62 – 0.90

0.73

0.79

2.35

18.5

0.80

0.66 – 0.94

0.85

0.68

0.97

TFEsum relative (N.m/kg) SCIM-III SAAsum relative (N.m/kg) Total Time of Thirteen Items (sec) Shoulder ABD PTrel (N.m/kg) Performance Score (sec)

3-MinTest (m) 300.0 0.74 0.58 – 0.89 0.65 0.86 0.96 Area under the curve (AUC) was statistically different from the ROC curve reference line for all strength variables (P≤0.05). 3MinTet: 3-minute overground wheeling test; ABD: abduction; CP: cutoff point for strength variables (N.m/kg); PTrel: relative peak torque; SAAsum: sum of shoulder abduction and adduction peak torques; SENS: sensitivity; SPEC: specificity; TFEsum: sum of trunk flexion and extension peak torques; TR: test result.