Alternative scapular stabilization exercises to target strength, endurance and function of shoulders in tetraplegia: A prospective non-controlled intervention study

Abstract

Objective

Scapular stabilization exercises (SSE) are well-established for the able-bodies. The aim of the current study is to access the potential benefits of SSE on isometric internal and external rotator strength, endurance and function of the shoulder in persons with tetraplegia, throughout a 12-week exercise program consisting of five resisted movements with elastic bands.

Design

Prospective non-controlled intervention study.

Setting/Participants/Interventions

A convenience sample of 17 subjects (age, 40.0±10.0 years old) with SCI was recruited from the University Hospital at the State University of Campinas (UNICAMP) from March 2015 to February 2016. They performed 5-resisted-SSE for 12 weeks, using Thera-band® elastic bands. Four evaluations were required: Baseline1, Baseline2, 6W and 12W.

Outcome measures

The dependent variables were isometric internal and external rotation strength, flexion and abduction endurance and the Disabilities of the Arm, Shoulder and Hand (DASH) score.

Results

Isometric external rotation strength and flexion endurance increased after SSE and were classified as "clinically relevant" using minimal importance difference (MID). Abduction endurance increased but it was classified as "not clinically relevant". DASH score reported no significant differences but it was classified as "potentially clinically relevant". Correlations were observed among time since injury and endurance improvements.

Conclusion

This study demonstrated that specific training of the scapula muscles shows a benefit for shoulder strength, endurance and function of the shoulder in subjects with tetraplegia and should be part of the rehabilitation program. Besides, the SSE can be performed by subjects with tetraplegia themselves on a regular basis.

Introduction

Wheelchair dependent persons with spinal cord injury (SCI) rely entirely on their upper limbs for locomotion and weight-bearing activities, such as wheelchair propulsion, transfers and push-up pressure relief, increasing the risk of overload injuries of the shoulders.¹ Several studies in the literature report that the most common shoulder problems affecting persons with SCI are supraspinatus tendinosis, bursitis, and acromioclavicular joint degeneration.^1–3 In earlier studies persons at older age, with longer time since injury, higher body mass index (BMI) and muscle weakness showed to have an even greater risk for developing shoulder overloaded injuries.⁴

With reference to muscle weakness, it is suggested by several studies that scapula stabilization muscles play an important role in the development of shoulder problems in persons with SCI. Due to loss of muscle strength of the shoulder and scapular muscles in persons with tetraplegia, stabilization of the shoulder is insufficient. A systematic review of Mateo et al.⁵ on muscle weakness, including 15 studies and 3 case series studies (164 SCI, 131 Able-bodies controls) examined spatial and temporal kinematic measures, and electromyographic recordings, when available, in a population with tetraplegia. One of the main kinematic features observed in tetraplegia was motor slowing attested by increased movement time. Another finding was the reduction of maximal superior reaching during overhead movements. According to the authors, one of the reasons for the observed results could be caused by strength deficit in proximal synergic muscles promoting scapulothoracic and glenohumeral joint stability. Such studies may suggest the importance of improving shoulder strength and biomechanics in tetraplegia.⁵

One approach to shoulder strengthening is the practice of Scapular Stabilization Exercises (SSE) which are frequently recommended as a part of shoulder rehabilitation programs and they are possible to be performed at home by the persons.⁶ SSE enhance stability and strength of the shoulder girdle muscles, leading to proper scapular positioning and decrease shoulder pain.⁷

The effectiveness of these exercises is well established for the able-bodied population. Buttagat et al.⁷ the effects of SSE on pain intensity, pressure pain threshold, muscle tension and anxiety in 36 persons with scapulocostal syndrome. Results indicated that the SSE group showed a significant improvement in all parameters after the intervention period and at 2 weeks after the intervention period.⁷ In addition, Kuhn⁸ concluded in a systematic review that the synthesis of the investigated studies clearly showed that strengthening exercises for rotator cuff impingement should focus on the rotator cuff and scapular stabilizing muscles.⁸

Studies on SSE programs for persons with SCI only focused on pain and function. Van Straaten et al.⁹ studied the effects of a 12-week home exercising program including SSE in wheelchair users. Isometric glenohumeral rotator strength was a secondary outcome of the study on which no improvements were observed. Nawocsenski et al.¹⁰ studied a sample of 41 persons with SCI that performed 8-week-home exercising program, focused on strengthening and stretching exercises addressed to the anterior serratus muscle, the middle and lower trapezius, and the glenohumeral external rotator muscles. The authors only observed improvements on the shoulder function and reduction of shoulder pain as compared to the control group.¹⁰

Although other studies showed the effects of SSE on pain and function, there is very limited evidence that SSE programs improve shoulder strength and endurance in persons with tetraplegia. The hypothesis is that SSE may increase strength, endurance and function of the shoulder in this population. Therefore, the aim of the current study is to evaluate the potential benefits of SSE on isometric internal and external rotator strength, endurance and function of the shoulder in persons with tetraplegia throughout a 12-week exercising program consisting of five resisted exercises with elastic bands.

Methods

Study design

This is a prospective non-controlled intervention study in a convenience sample of persons with SCI. The design and the steps of the study are detailed in the Measurements section and illustrated in a flowchart (Fig. 1).

Figure 1.

The flowchart of study design.

Participants

A convenience sample of 17 persons (age: 40.0±10.0 years old) with SCI was recruited from the University Hospital at the State University of Campinas (UNICAMP) from March 2015 to February 2016. All of them actively participated in the neuromuscular electrical stimulation program for lower limbs at University Hospital. The sample size calculation was previously calculated by using the G*Power 3.2.1 (Test Family - F tests) software based on the following assumptions: Type error I (α) of 5%, moderate effect size (f=0.3), repeated measures correlations (r) of 0.5 and nonsphericity correction (ϵ) as 1. It ensured a power of 80% of the study.^11,12

All the persons reported pain in their shoulders which did not prevent them from performing their daily activities. Prior to the study all persons gave their written informed consent, approved by the local Institution Review Board. This paper followed the STROBE guideline requirements (Table 1).¹³

Table 1. STROBE Statement.

	Item No	Recommendation
Title and abstract	1	(a) Indicate the study's design with a commonly used term in the title or the abstract - OK
		(b) Provide in the abstract an informative and balanced summary of what was done and what was found - OK
Introduction
Background/rationale	2	Explain the scientific background and rationale for the investigation being reported - OK
Objectives	3	State specific objectives, including any prespecified hypotheses - OK
Methods
Study design	4	Present key elements of study design early in the paper - OK
Setting	5	Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data collection - OK
Participants	6	(a) Give the eligibility criteria, and the sources and methods of case ascertainment and control selection. Give the rationale for the choice of cases and controls - OK
		(b) For matched studies, give matching criteria and the number of controls per case – THE PRESENT STUDY DOES NOT HAVE CONTROLS
Variables	7	Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if applicable - OK
Data sources/ measurement	8*	For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe comparability of assessment methods if there is more than one group - OK
Bias	9	Describe any efforts to address potential sources of bias - OK
Study size	10	Explain how the study size was arrived at - OK
Quantitative variables	11	Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and why - OK
Statistical methods	12	(a) Describe all statistical methods, including those used to control for confounding - OK
		(b) Describe any methods used to examine subgroups and interactions
		(c) Explain how missing data were addressed - OK
		(d) If applicable, explain how matching of cases and controls was addressed
		(e) Describe any sensitivity analyses
Results
Participants	13*	(a) Report numbers of individuals at each stage of study—eg numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analysed - OK
		(b) Give reasons for non-participation at each stage – OK
		(c) Consider use of a flow diagram - OK
Descriptive data	14*	(a) Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential confounders - OK
		(b) Indicate number of participants with missing data for each variable of interest - OK
Outcome data	15*	Report numbers in each exposure category, or summary measures of exposure - OK
Main results	16	(a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% confidence interval). Make clear which confounders were adjusted for and why they were included - OK
		(b) Report category boundaries when continuous variables were categorized
		(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period
Other analyses	17	Report other analyses done—eg analyses of subgroups and interactions, and sensitivity analyses
Discussion
Key results	18	Summarise key results with reference to study objectives - OK
Limitations	19	Discuss limitations of the study, taking into account sources of potential bias or imprecision. Discuss both direction and magnitude of any potential bias - OK
Interpretation	20	Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from similar studies, and other relevant evidence - OK
Generalisability	21	Discuss the generalisability (external validity) of the study results - OK
Other information
Funding	22	Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on which the present article is based

The inclusion criteria were (i) participation in the neuromuscular electrical stimulation program for lower limbs at University Hospital, (ii) male persons with tetraplegia between C4 and C7, (iii) C4 and C5 myotomes preserved, (iv) physically non-active, i.e., not practicing sports activities (v) aged 18–60 and (vi) able to perform the test positions required for the study. Persons with (i) autonomic dysreflexia during the test, (ii) active urinary tract infection, (iii) strong neuropathic pain that would be an obstacle to the implementation of the proposed protocol or (iv) upper limb fractures were excluded. Persons admitted to the research were required to stop upper-limb exercising and physical rehabilitation in order to avoid possible confounders.

All of 17 persons were evaluated at the time points Baseline1 and Baseline2, described below. After Baseline2 two persons dropped out of the study, and after 10 weeks two persons were excluded from the study. Therefore, 13 persons completed the 12-week exercise program.

Outcome measures

Three dependent variables were evaluated: (i) isometric internal and external rotation strength of the shoulder, (ii) endurance of flexion and abduction of the shoulder, and (iii) self-reported function of the shoulder. Hand dominance was taken into account for data analysis.

Shoulder strength

Maximal isometric internal and external rotation strength of the shoulder was assessed with an isometric dynamometer (Lafayette Manual Muscle Testing System®). The intrarater reliability and intraclass correlation coefficients of the hand-held dynamometer were mentioned in several studies in different populations including persons with tetraplegia.⁶ The persons were transferred to a hospital stretcher in a lying position with shoulder abduction and elbow flexion to 90 degrees, and wrist to neutral position. The device was placed 2 cm proximal to the styloid process of the ulna, on the dorsal or ventral forearm; the persons were instructed in the movements required for the test.¹⁴ They were required to produce maximal isometric contractions for six seconds while a physical therapist immobilized their tested arm and lower limbs (Fig. 2). This procedure was repeated three times with rest periods of two minutes in between.

Figure 2.

The patient's position for the strength test.

Shoulder endurance

A shoulder endurance test was developed to check whether the persons could maintain their upper limb in flexion and abduction position. Persons were seated on a wheelchair, and a ruler with a right angle was used as the 90-degree reference for shoulder in both positions (Fig. 3). A chronometer (seconds) was started when persons first positioned their shoulders as instructed by principal investigator, and it was stopped when the persons were unable to keep the proposed position even with verbal command.

Figure 3.

The ruler for the endurance test.

Shoulder function

The Disabilities of the Arm, Shoulder and Hand (DASH) Outcome Measure is a 30-item, self-report questionnaire designed to measure physical function and symptoms in patients with any or several musculoskeletal disorders of the upper limb. The questionnaire was designed to help describe the disability experienced by people with upper-limb disorders and also to monitor changes in symptoms and function over time. It is a reliable and validated score in the able-bodied population, and it is more specific from an orthopedic perspective.¹⁵ Additionally, it was previously used by Van Straaten et al.⁹ in persons with SCI and by Bartels et al.¹⁶ in persons with incomplete cervical cord syndrome. The DASH scores ranged from 0 to 100 with low scores indicating better upper limb conditions.

Measurements

Four measurements were performed to collect data on the dependent variables as explained in the “Outcome Measures Section”:

Baseline1: initial data collection.

Baseline2: collection of data 4 weeks after Baseline1 prior to the start of the SSE protocol.

6W: collection of data 6 weeks after Baseline2, during which time period the subjects participated in the SSE protocol.

12W: collection of data 12 weeks after Baseline2 during which time period the subjects continued the SSE protocol.

Procedure

A randomized list of hand dominance and sequence of movements was generated by computer to perform the isometric strength test and endurance test to avoid bias.

The study procedure was as follows: at the beginning of the study each person was individually informed of and instructed in the study protocol. During the instructions, the therapist ensured each person would be able to practice the exercises as required without guidance. The program consisted of five exercises: (i) bilateral external rotation with scapula adduction (“W”exercise); (ii) External Rotation exercise with the shoulder at zero degree of abduction; (iii) bilateral arm extension with scapula adduction (Low-Row exercise); (iv) scapula protraction (Push-up exercise), and (v) Horizontal Abduction with the palms up (Fig. 4). All of them were performed in a seated position with elastic bands. The persons performed 3 sets of 15 repetitions, with a 30-second rest between sets.

Figure 4.

5-adapted SSE: i- “W”exercise; ii- External Rotation exercise with the shoulder at zero degree of abduction; iii- Low-Row exercise; iv- Push-up exercise and v- Horizontal Abduction with the palms up.

The persons were provided with (i) a printed illustrated guide and (ii) a mobile phone video on how to perform exercises by themselves, (iii) a calendar to ensure they would practice the exercises every Monday, Tuesday, Thursday and Friday, summing up 4 times a week, (iv) a red medium-resistance Theraband® for the first 6 weeks of the program, and (v) a blue extra-heavy-resistance Theraband® for the last 6 weeks of the program.

Different Theraband® Elastic Resistance Bands were tested to modulate the intensity of the exercises based on the principle of progressive overload in order to achieve continuous adaptation throughout the physical training.^17,18 The red and blue elastic bands were tested in a pilot study and selected in order to ensure the persons would perform 15 repetitions in a quasi-maximal effort. Additionally, each elastic band was adapted for each person, according to the length of their upper limbs. That ensured the individuality principle of training and relative lever arm for each person. Besides, a ring was tied to each tip of the elastic bands to ensure adequate exercising because the hand-grip function of the persons was limited.

During the research, the persons were allowed to contact the principal investigator for questions regarding data collection and exercises.

Statistical analysis

The reliability of data of the current study was measured by using Intraclass Correlation Coefficient (ICC), 95% Confidence Interval (CI 95%) and Typical Error of Measurement (TEM), based on test-retest of five subjects in a pilot study (Table 2).

Table 2. Intraclass correlation coeficient (ICC) and typical error measurement (TEM) of measured variables.

Variable	ICC (CI 95%)	TEM
Hand Dominance: DS
DASH score (points)	1.00 (1.00–1.00)	0.11
Flexion endurance (s)	1.00 (1.97–1.00)	0.22
Abduction endurance (s)	0.99 (0.93–1.00)	0.28
IR strength (kgf)	1.00 (0.98–1.00)	0.21
ER strength (kgf)	0.99 (0.90–1.00)	0.31
Hand Dominance: NDS
Flexion endurance (s)	0.96 (0.68–1.00)	0.45
Abduction endurance (s)	0.99 (0.90–1.00)	0.31
IR strength (kgf)	1.00 (1.00–1.00)	0.12
ER strength (kgf)	1.00 (0.96–1.00)	0.23

CI, confidence interval; DS, dominant side; NDS, non-dominance side; IR, internal rotation; ER, external rotation.

After checking normality (Shapiro-Wilk Test) and sphericity (Mauchly Test) of the data, the paired t-test was used to compare dependent variables between Baseline1 and Baseline2 (n = 17). The aim was to measure potential changes over time.

Considering an attrition rate of two persons after Baseline2 (11.7%) and two persons after a 6W period (13.3%), an intention-to-treat analysis was performed. A total sample size of 15 persons was considered in the final analysis (Baseline2×6W×12W). Missing data were treated as missing-completely-at-random (MCAR), using an average of 20 imputations generated by linear regression for each missing data in all 3 variables: strength, endurance and function of the shoulder. After that, the training improvements were analyzed, by comparing the 3 variables among Baseline2, 6W and 12W by a casewise one-way repeated measures analysis of variance (ANOVA) followed by Sidak post hoc tests whenever required.

The clinical effects of the intervention were analyzed by calculating the effect size (ES), Cohen's d, and classified as follows: < 0.31, small effect; 0.31–0.7, medium effect; > 0.7, large effect. Significant changes (P < 0.05) were considered important when the effects observed throughout the intervention period were higher than those observed between Baseline1 and Baseline2.

In addition, the minimal importance difference (MID) criterion was adopted to check whether the improvement observed was clinically relevant. MID consists of the smallest difference in score in the domain of interest that persons perceive as important, either beneficial or harmful, and which would lead the clinician to consider a change in the treatment management. One method of determining MID is multiplying the ES of the difference obtained between time points or groups considered as important (0.2 or 0.5 ES, according to Cohen), by the pooled standard deviation (pooled SD) between the same time points or groups (MID = 0.2×pooled SD or MID = 0.5×pooled SD).¹⁹ As recommended by Armijo-Olivo et al.¹⁹, who studied muscle strength and endurance in cervical spine, ES, MID and mean difference (MD) were used to make a final decision on clinical relevance. A result was “clinically relevant” if ES ≥ 0.40 and MIDs were less than the MD obtained between Baseline2 and 12W. A result was “potentially clinically relevant” if the ES was medium and only one of the MIDs was less than the MD obtained between Baseline2 and 12W. A result was “not clinically relevant” if ES < 0.40 and the MIDs were greater than the MD obtained between Baseline2 and 12W.¹⁹ Pearson's correlation was used to check associations of time since injury (TSI) with changes in endurance and strength records. If significant correlations were observed (P < 0.05) a linear regression was performed to obtain the explained variance. The significance level was set at P < 0.05. The SPSS 18.0 statistical software was used for statistical analysis (SPSS Inc., Chicago, IL, USA).²⁰

Results

Initially, the study sample consisted of 17 persons. According to the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI), the severity (i.e. completeness) of injury was classified by using ASIA Impairment Scale (AIS)²¹. The persons participating in this study were classified as AIS A (78.3%) and AIS B (21.4%). The mean TSI was 9.0±6 years (Table 3). Two persons dropped out of the study before the beginning of the intervention due to personal problems, and another 2 persons were excluded a few weeks later after the second phase of the intervention due to urinary infection. Fifteen persons were included in the analysis.

Table 3. Sample characteristics (n = 17).

Subject	Age (years)	Lesion level	AIS	TSI (years)
1	49	C6	A	16
2	31	C5	A	9
3	40	C6	A	20
4	44	C6	B	2
5	46	C5	B	12
6	43	C4	A	19
7	42	C4	A	4
8	44	C5	A	13
9	26	C6	B	5.5
10	28	C6	A	1.4
11	44	C5	A	15
12	56	C4	A	4
13	30	C6	B	3
14	51	C5	A	1.5
15	51	C5	A	15
16	24	C5	B	4
17	37	C6	A	4

The graphs of improvement of strength and endurance showed that the results of Baseline2 are higher than the results of Baseline1 but they were not significant. In the comparison between Baseline1 and Baseline2 the ES was small, which explains lower effects of variable changes within the period without intervention (Fig. 5 and Fig. 6).

Figure 5.

Means and standard deviations in time points of strength. d, Cohen's d; *P<0.05; DS, dominant side; NDS, non-dominant side.

Figure 6.

Means and standard deviations in time points of endurance. d, Cohen's d; *P<0.05; DS, dominant side; NDS, non-dominant side.

The MID was calculated to check whether a non-significant result could present clinical relevance. The MDs and 95% confidence intervals between Baseline2 and 12W in the variables of interest as well as values for clinical relevance were calculated (Table 4). Pearson's correlation was performed to analyze associations among TSI and improvements findings (Table 5).

Table 4. Clinical relevance assessment strength and endurance shoulder, and the DASH score: Baseline2 vs 12W.

Variable	MD	IC 95% FOR MD		Pooled SD	MID * 0.2	MID * 0.5	Effect Size	Clinical Relevance
		LL	UL
DASH score	-9.12	-24.59	6.36	20.09	4,018	10,045	-0.44	PCR
IR Strength DS	1.05	-3.57	5.66	6.17	1,234	3,085	0.17	NCR
IR Strength NDS	0.91	-3.55	5.37	5.96	1,192	2.98	0.15	NCR
ER Strength DS	2.47	-1.04	5.98	4.7	0.94	2.35	0.53	CR
ER Strength NDS	3.37	-0.99	7.73	5.83	1,166	2,915	0.58	CR
Endurance Flexion DS	102.32	-22.67	227.3	167.1	33.42	83.55	0.61	CR
Endurance Flexion NDS	58.89	-66.63	184.4	148.6	29.72	74.3	0.35	NCR
Endurance Abduction DS	62.83	-25.16	150.82	117.64	23,528	58.82	0.53	NCR
Endurance Abduction NDS	50.07	-47.44	147.59	130.37	26,074	65,185	0.38	NCR

MD, mean differences; IC 95% = Limits with 95% of reliability; LL, lower limit; UL, upper limit; SD, standard deviation;

MID, minimal importance difference; NCR, not clinically relevant; PCR, potentially clinically relevant; CR, clinically relevant; DS, dominant side; NDS, non-dominant side.

Table 5. Coefficient's correlation and linear regression for significant associations between observed improvements in muscle endurance and TSI.

Associated Variable	r	r2	Intercept	B	IC 95% for B		P Valor
					LL	UL
TSI
Flexion Endurance - NDS	-0.59	0.35	157.4	-9.7	-17.7	-1.7	0.021
(6W vs. Baseline)
Abduction Endurance - NDS	-0.58	0.34	162.4	-9.1	-16.8	-1.4	0.024
(6W vs. Baseline)

IC 95% = Limits with 95% of reliability; LL, lower limit; UL, upper limit; TSI, time since injury; DS, dominant side; NDS, non-dominant side.

Strength

Hand dominance was described as dominant side (DS) and non-dominant side (NDS). External rotation strength of both sides increased when comparing Baseline2 with 6W (DS, P = 0.015; NDS, P = 0.040) and 12W (DS, P = 0.004; NDS, P = 0.013). The ES between Baseline1 and Baseline2 (D, d = 0.22; NDS, d = 0.18), Baseline2 and 6W, Baseline2 and 12W evidenced improvements in external rotation strength (Fig. 4). Internal rotational strength of the DS and the NDS did not increase significantly when comparing Baseline2 with 6W (DS, P = 0.978; NDS, P = 0.992) and 12W (DS, P = 0.474; NDS, P = 0.699) (Fig. 5). External rotation strength of both sides was classified as “clinically relevant”. Changes in internal rotation strength were considered “not clinically relevant” (Table 4).

Endurance

Flexion endurance of the DS significantly improved after intervention in 6W (P = 0.035) and 12W (P = 0.003). The ES between Baseline2 and 6W (d=0.50), and Baseline2 and 12W (d=0.55) was also greater than the ES between Baseline1 and Baseline2 (d=0.37). Regarding abduction endurance, significant increase was observed for the DS and the NDS. For the DS, both 6W (P = 0.003) and 12W (P = 0.026) differed from Baseline2 while for the NDS findings only showed differences between 6W and Baseline2 (P = 0.012) (Fig. 6). These three values were greater than the ES. Flexion endurance of the DS was classified as “clinically relevant” and abduction endurance of both sides, and flexion endurance of the NDS were considered “not clinically relevant” (Table 4).

DASH score

The DASH scores obtained throughout the study showed no significant difference (Fig. 7). The MID was calculated to check whether a non-significant result could present clinical relevance. The MID between Baseline2 and 12W classified changes in the DASH score as “potentially clinically relevant” (Table 4).

Figure 7.

Means and standard deviations in time points of the DASH score.

Association with improvements and lesion characteristics

No significant correlations were observed among TSI, lesion characteristics and changes in isometric external and internal strength (P > 0.05). However, a negative correlation was found between TSI and improvements in flexion endurance of the DS (r = -0.59) and abduction endurance of the NDS (r = -0.58) after a 6-week intervention, which explains the variance of these parameters to be 34% and 35%, respectively (Table 5).

Discussion

Main findings: the exercise program focused on scapula stabilizers as proposed herein improved muscle strength, endurance and function of the shoulders in male persons with tetraplegia.

Shoulder strength

An important result in this study was that SSE significantly increased isometric external rotational strength of the shoulders. Internal rotation strength did not change significantly. This might be due to the fact that the SSE program focused on external rotational movements and it is not beneficial to gaining internal rotation strength.

To ensure gain of strength the exercise program of the present study was based on higher resistance and fewer repetitions. On the other hand, Van Straaten et al.⁹ opted for more repetitions and less resistance in their 12-week home exercise program. They investigated shoulder pain and function by focusing on scapula stabilizers and rotator cuff muscles in wheelchair users. They observed increase in isometric measurements of the serratus anterior and scapular retractors after the exercise intervention. However, they found no improvements on external and internal rotators strength, which was their secondary outcome. Their loading scheme resulted in the decrease of shoulder pain without hypertrophy gain.⁹

Shoulder endurance

The SSE promoted improvement of endurance in shoulder flexion and abduction. The DS gain was greater than the NDS gain. The hand dominance could be the reason for this finding. A suggestion for future protocols is to increase the series, repetitions and load of the NDS to achieve the same results as DS. The increase of endurance might be due to the fact that SSE improved stability to the shoulder girdle of persons with tetraplegia as it does to the able-bodied.²² Unfortunately, there is no evidence in the literature to compare these findings.

DASH score

Whereas no significant differences were found in the DASH score, the MID classified these changes as “potentially clinically relevant”. The same results were shown by Van Straaten et al.⁹ with similar exercises executed in a different way as mentioned in the “Shoulder Strength” section. Both studies suggest potential benefits in function of the shoulder after the 12-week SSE program. Although not measured in the current study, a relevant point is that the persons reported improvements in daily tasks, including driving without shoulder pain, and eating and transferring by themselves. Nawoczenski et al.¹⁰ studied an 8-week-home exercising program for spinal cord injury persons, focused on strengthening and stretching exercises. Although the protocol of exercises was similar to the present study, the outcomes were completely different. Persons may not have increased muscle hypertrophy and strength due to the 8-week duration of their study, the resistance applied and the fact that only one exercise focused on external rotation strength. On the other hand, the results demonstrated that SSE improved shoulder function and reduced shoulder pain compared with the control group. Besides, the sample of 41 persons was not homogeneous, and included only 3 persons with tetraplegia.¹⁰

The present study also investigated the associations between improvements and lesion characteristics. The correlation suggested the earlier persons start performing the proposed protocol, the better their muscle endurance will be.

An important benefit to be considered is that SSE were performed by the persons themselves at home with just one elastic band. SSE do not replace physical therapy care. It may be an alternative option to maintain regular activities of upper extremities for a population who may have limited access to assistance, mobility and resources.

Limitations

The recruitment of a large and homogenous sample as well as the inclusion of a control group was a difficulty faced by the authors. Another limitation of this study was that the evaluations were performed only in male persons due to the fact that there were few female persons with tetraplegia at the local hospital.

Future studies

Further studies, with different methodologies and designs, including males and females with tetraplegia and shoulder pain should be carried out for comparison with the results obtained herein. It may ensure and increase the external validity of the SSE program across the population with tetraplegia in various settings and times.

Conclusion

The current study shows that in male persons with tetraplegia a 12-week SSE program improved isometric external rotation strength, flexion and abduction endurance of the shoulder of the dominant side. Based on these results it may be advised to train scapula stabilization muscles in all persons with tetraplegia to prevent shoulder overload injuries.

Acknowledgement

FAPESP – São Paulo Research Foundation and CNPq- National Council for Science and Technology.

Disclaimer statements

Contributors None.

Funding None.

Conflicts of interest None.

Ethics approval None.

ORCID

Carolina Linshttp://orcid.org/0000-0002-7595-3303

Giovanna I.S. Medinahttp://orcid.org/0000-0002-2266-9640