Musculoskelet Surg DOI 10.1007/s12306-015-0363-2
ORIGINAL ARTICLE
Risk factors for shoulder pain in patients with spinal cord injury: a multicenter study G. Ferrero1 • E. Mijno1 • M. V. Actis2 • A. Zampa3 • N. Ratto1 • A. Arpaia1 A. Masse`4
•
Received: 2 January 2015 / Accepted: 16 February 2015 Ó Istituto Ortopedico Rizzoli 2015
Abstract Introduction Shoulder pain in spinal cord injury (SCI) is common due to the repetition of the wheelchair propulsion and the increased intra-articular pressure during transfers. Known risk factors for the onset of shoulder pain are age and level of SCI. Aims of this study were to assess how body mass index affects the onset of shoulder pain and to evaluate the relationship between the age at the moment of SCI and the number of years between SCI and the onset of shoulder pain. Methods A retrospective study was performed including subjects with SCI between C5 and S3. Excluding criteria were spina bifida and subjects not using manual wheelchair or presenting with shoulder pain before SCI. Patients in the two spinal cord units were reviewed with a self-made questionnaire, and patients were also enrolled during sport events. Age at the moment of SCI, current age and number of years between SCI and the onset of shoulder pain were recorded. Results Ninety-six patients were enrolled: 77 men and 19 women; 46.4 % reported shoulder pain. Overweight patients who do more than 12 transfers per day showed an
& G. Ferrero [email protected] 1
Department of Orthopaedics and Traumatology Surgery, San Luigi Hospital, University of Torino, Turin, Italy
2
Department of Orthopaedics, Traumatology and Rehabilitation, AO Citta` della Salute e della Scienza, CTO Hospital, Turin, Italy
3
Spinal Unit, Department of Rehabilitation Medicine, Physical Medicine and Rehabilitation Institute, Udine, Italy
4
Department of Orthopaedics and Traumatology, C.T.O.Maria Adelaide Hospital, University of Torino, Turin, Italy
increased incidence of shoulder pain (p = 0.0434). A linear regression showed a significant relationship between the age of the subject at the moment of SCI and the number of years between the SCI and the onset of pain. Conclusion Our study confirms that age and level of SCI are risk factors for shoulder pain, but we demonstrated also that overweight patients who do more than 12 transfers per day have higher chances of having shoulder pain. Keywords Shoulder pain Spinal cord injury Wheelchair Overweight Overuse Multicenter study
Introduction Shoulder pain in patients with spinal cord injury (SCI) has been reported up to 78 % [1–6]. The main causes of shoulder pain are overload due to the repetition of the wheelchair propulsion and the increase in intra-articular pressure [7, 8]. Literature showed that wheelchair users have a strength imbalance between abductor and adductor muscles. This condition may cause the migration of the humeral head upward resulting in impingement syndrome due to the reduction in the subacromial space and possibly result in an impairment of the rotator cuff. The imbalance between intra- and extra-rotator muscles may also result in a loss of horizontal centering and may create an impairment of the anterior capsular ligament [9]. Shoulder pain in the patient with SCI reduces subject’s independence and the quality of life. To prevent this disability, several authors focused their studies in the identification of most important risk factors. To date, the most important risk factors are the age, more than 20 years after SCI and level of SCI [10, 11]. Until now, there is not a consensus in considering sport activities as risk factors.
123
Musculoskelet Surg
Aims of these studies were to analyze the impact of body mass index (BMI) and number of transfers on the shoulder pain onset and to evaluate the relationship between the age at the moment of SCI and the number of years between SCI and the onset of shoulder pain.
Data were analyzed using the Statistical Package for the Social Sciences. p value was set at 0.05. The Chi-square test was used to correlate age, the level of SCI, practice of sports (agonist or not), BMI, number of transfers per day and shoulder pain prevalence. A linear regression was used to correlate the patient age at SCI and the number of years between SCI and the onset of shoulder pain.
Materials and methods A retrospective study was performed enrolling patients with SCI between C5 and S3. The study patients with spina bifida or shoulder pain before SCI or not using manual wheelchair were excluded. Subjects were recruited from two spinal cord units (Torino and Udine) or during sport competition events. Age at the moment of SCI, current age and number of years between SCI and the onset of shoulder pain were recorded. Enrolled patients underwent a self-made questionnaire (Table 1). The period of data collection began in November 2013 and ended in June 2014. The age of 50 years was used as cutoff to analyze how age influenced the onset of shoulder pain. To assess the relationship of the pain and level of SCI, we divided the sample into two groups: those with high SCI from T2 to T7 and subjects with SCI from T8 to T12. Subjects were considered athletes if they met at least two of the following three criteria: training time a week longer than 3 h; involved in at least three competitions per year; and using a wheelchair modified for sports [3]. We divided our sample into two groups: overweight patients (BMI C 25) and normal subjects (BMI \ 25). A cutoff of 12 transfers/day was used to evaluate the relationship between BMI and shoulder pain prevalence. This cutoff was chosen because it is the mean number of transfers that a person with an active lifestyle makes on average per day. Pain was evaluated with a scale from 0 to 10.
Results One hundred and seven patients were enrolled in our study, 11 were excluded because they did not meet the inclusion criteria, 77 patients were male, and 19 were female. The mean age of the subjects was 47.4 years: 49.6 years for male and 38.4 for female. Mean time of wheelchair use was 17.73 years; 46.4 % patients reported shoulder pain, of whom 62.2 % report a difficulty during common daily activities. There was a significant correlation between patient’s age and the onset of shoulder pain (Table 2). Of the subjects, 38 and 35 had high and low levels of lesions, respectively. A significant relationship between level of SCI and shoulder pain was found (Table 3). Subjects with high level of SCI showed a higher rate of shoulder pain. There was no statistically significant relationship between shoulder pain and the practice of sport (all p values [ 0.05) (Table 4). No correlation was found between BMI and shoulder pain if BMI was considered alone (Table 5). Significant differences were found between shoulder pain prevalence and BMI if weight was evaluated together with number of transfers per day, p = 0.0434 (Table 6). Linear regression showed a relationship between the patient age at SCI and the number of years between the SCI and the onset of pain. Older patients needed less time to have shoulder pain than younger patients (Fig. 1).
Table 1 Self-made questionnaire Age
Type of sport
Gender
Since how many years do you practice sports?
Weight
How many hours a week do you do sport activities?
Height
Do you use a wheelchair which had been modified for sports?
Level of SCI
Did you experience shoulder pain before the spinal cord injury?
Time from trauma to shoulder pain onset
Did you experience shoulder pain after the first few months/years after the spinal cord injury?
Wheelchair weight (ex. \di 8 kg; 8–10 kg; [di 10 kg)
How soon arose the pain?
Mean numbers of transfers per day
Value of pain from 1 to 10
Do you play sport?
Does pain affect your daily living?
123
Musculoskelet Surg Table 2 Cross-table between patients’ age and shoulder pain C50 years
\50 years
Shoulder pain
30
17
No shoulder pain
21
28 p = 0.0395
Number of years between the SCI and the onset of shoulder pain
Table 3 Cross-table between shoulder pain onset and level of SCI High SCI
Low SCI
Shoulder pain
22
11
No shoulder pain
16
23 p = 0.0299
Table 4 Cross-table between shoulder pain and practice of sport
Athletes
Shoulder pain
No shoulder pain
18
14
Non-athletes
5
9
Athletes
18
14
No sport
22
29
5
9
22
29
Non-athletes No sport
0.3368 0.3482 0.7629
BMI C 25
BMI \ 25
Shoulder pain
21
24
No shoulder pain
18
33 p = 0.25
Table 6 Relationship between number of transfers and shoulder pain in overweight and normal subject C12
\12
10
10
3
15
BMI C 25 No shoulder pain
p = 0.0434 BMI \ 25 Shoulder pain No shoulder pain
9 10
Fig. 1 Linear regression showed a relationship between age at SCI and number of years between SCI and the onset of shoulder pain
p value
Table 5 Cross-table between overweight and shoulder pain
Shoulder pain
Age at SCI
19 25 p = 0.094
Discussion According to our results, number of transfers in overweight patients is a risk factor to develop shoulder pain after SCI. Younger patients at the moment of SCI required more time
to develop shoulder pain than older patients at the moment of SCI. Furthermore, our study confirms literature data and states once again that age and level of neurologic injury are risk factors for shoulder pain development in SCI patients. Our study presents several limits: The most important ones are the retrospective nature, patients’ enrollment (a structured selection would avoid the risk of bias) and the absence of a priori analysis of the study power. Another limitation is the short period of time during which the data were collected. Literature showed that shoulder pain manifestation is highly correlated with age. In our study, the mean age of patients with SCI and shoulder pain is 48.8, lower than that the age published by Akbar et al. [12], and it should be considered that the mean age of shoulder pain onset in nonSCI patients is much higher: 67.8 [13]. In our study, we found a correlation between age and shoulder pain prevalence using cutoff 50 years. This result confirms that patient’s age is an important risk factor for shoulder pain onset. Results of correlation between level of SCI and shoulder pain are similar to published data [10, 11, 14–16]. Furthermore, in our study, high thoracic SCI (T2–T7) patients have more chances of presenting shoulder pain. This finding may be explained by the adaptations of trunk control during wheelchair propulsions causing muscle strength imbalances between the shoulder adductors and abductors [16]. An overweight subject has to move a heavier body than a normal weight subject. In our study, we found no correlation between shoulder pain and BMI if BMI was evaluated alone, but BMI becomes a significant risk factor if the subject does more than 12 transfers per day. This result may be explained in an increased intra-articular pressure during transfers. This pressure exceeded the
123
Musculoskelet Surg
arterial pressure by 2.5 times [7]. Therefore, it is possible that in overweight subjects, the pressure increases even further. In our study, the mean age between SCI and shoulder pain onset was 10.9, similar to literature data [3]. We have analyzed whether the time of pain shoulder onset changes depending on the patient’s age at the SCI moment. According to our results, the younger is the patients at the moment of SCI, the shorter is the time between SCI and the shoulder pain onset. This result may be explained by the adaptation of tendons and muscles: in young patients, this process may be more efficient than in older patients. Another possible explanation is that older patients may present a subclinical lesion of shoulder tendons at the moment of SCI. Several published studies examined sport activities and shoulder pain prevalence. To date, there is no agreement on this topic [3, 17]. Our data showed no significant relationship between sports practice and shoulder pain. About 63 % of patients who reported shoulder pain were not athletes, but this finding should be carefully interpreted according to the limits of this study. Future studies should focus on the reduction in those biases and analyze a larger number of patients.
Conclusion Overweight patients who do more than twelve transfers per day have an increased risk of occurrence of shoulder pain. Conflict of interest of interest.
The authors declare that they have no conflict
Human and animal rights This article does not contain any studies with human or animal subjects performed by any of the authors.
References 1. Alm M, Saraste H, Norrbrink C (2008) Shoulder pain in persons with thoracic spinal cord injury: prevalence and characteristics. J Rehabil Med 40(4):277–283
123
2. Finley MA, Rasch EK, Keyser RE, Rodgers MM (2004) The biomechanics of wheelchair propulsion in individuals with and without upper-limb impairment. J Rehabil Res Dev 41(3B): 385–395 3. Fullerton HD, Borckardt JJ, Alfano AP (2003) Shoulder pain: a comparison of wheelchair athletes and nonathletic wheelchair users. Med Sci Sports Exerc 35(12):1958–1961 4. Hastings J, Goldstein B (2004) Paraplegia and the shoulder. Phys Med Rehabil Clin N Am 15(3):699–718 5. Pentland WE, Twomey LT (1994) Upper limb function in persons with long term paraplegia and implications for independence: part I. Paraplegia 32(4):211–218 6. Subbarao JV, Klopfstein J, Turpin R (1995) Prevalence and impact of wrist and shoulder pain in patients with spinal cord injury. J Spinal Cord Med 18(1):9–13 7. Bayley JC, Cochran TP, Sledge CB (1987) The weight-bearing shoulder. The impingement syndrome in paraplegics. J Bone Joint Surg Am 69(5):676–678 8. Gagnon D (2008) Comparison of peak shoulder and elbow mechanical loads during weight-relief lifts and sitting pivot transfers among manual wheelchair users with spinal cord injury. J Rehabil Res Dev 45(6):863–874 9. Porcellini G (2011) La patologia di spalla e gomito negli sport olimpici e paralimpici (TIMEO Ed.). ISBN 9788897162155 10. Curtis KA, Drysdale GA, Lanza RD, Kolber M, Vitolo RS, West R (1999) Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil 80(4):453–457 11. Gil-Agudo A, Del Ama-Espinosa A, Perez-Rizo E, PerezNombela S, Pablo Rodriguez-Rodriguez L (2010) Upper limb joint kinetics during manual wheelchair propulsion in patients with different levels of spinal cord injury. J Biomech 43(13):2508–2515 12. Akbar M, Brunner M, Balean G, Grieser T, Bruckner T, Loew M, Raiss P (2012) Etiology of rotator cuff tears in paraplegic patients: a case–control study. J Shoulder Elbow Surg 21(1):23–28 13. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA (2006) The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 88(8):1699–1704 14. Lal S (1998) Premature degenerative shoulder changes in spinal cord injury patients. Spinal Cord 36(3):186–189 15. Medina GI, Nascimento FB, Rimkus CM, Zoppi Filho A, Cliquet A Jr (2011) Clinical and radiographic evaluation of the shoulder of spinal cord injured patients undergoing rehabilitation program. Spinal Cord 49(10):1055–1061 16. Sinnott KA, Milburn P, McNaughton H (2000) Factors associated with thoracic spinal cord injury, lesion level and rotator cuff disorders. Spinal Cord 38(12):748–753 17. Finley MA, Rodgers MM (2004) Prevalence and identification of shoulder pathology in athletic and nonathletic wheelchair users with shoulder pain: a pilot study. J Rehabil Res Dev 41(3B):395–402
ORIGINAL ARTICLE
Risk factors for shoulder pain in patients with spinal cord injury: a multicenter study G. Ferrero1 • E. Mijno1 • M. V. Actis2 • A. Zampa3 • N. Ratto1 • A. Arpaia1 A. Masse`4
•
Received: 2 January 2015 / Accepted: 16 February 2015 Ó Istituto Ortopedico Rizzoli 2015
Abstract Introduction Shoulder pain in spinal cord injury (SCI) is common due to the repetition of the wheelchair propulsion and the increased intra-articular pressure during transfers. Known risk factors for the onset of shoulder pain are age and level of SCI. Aims of this study were to assess how body mass index affects the onset of shoulder pain and to evaluate the relationship between the age at the moment of SCI and the number of years between SCI and the onset of shoulder pain. Methods A retrospective study was performed including subjects with SCI between C5 and S3. Excluding criteria were spina bifida and subjects not using manual wheelchair or presenting with shoulder pain before SCI. Patients in the two spinal cord units were reviewed with a self-made questionnaire, and patients were also enrolled during sport events. Age at the moment of SCI, current age and number of years between SCI and the onset of shoulder pain were recorded. Results Ninety-six patients were enrolled: 77 men and 19 women; 46.4 % reported shoulder pain. Overweight patients who do more than 12 transfers per day showed an
& G. Ferrero [email protected] 1
Department of Orthopaedics and Traumatology Surgery, San Luigi Hospital, University of Torino, Turin, Italy
2
Department of Orthopaedics, Traumatology and Rehabilitation, AO Citta` della Salute e della Scienza, CTO Hospital, Turin, Italy
3
Spinal Unit, Department of Rehabilitation Medicine, Physical Medicine and Rehabilitation Institute, Udine, Italy
4
Department of Orthopaedics and Traumatology, C.T.O.Maria Adelaide Hospital, University of Torino, Turin, Italy
increased incidence of shoulder pain (p = 0.0434). A linear regression showed a significant relationship between the age of the subject at the moment of SCI and the number of years between the SCI and the onset of pain. Conclusion Our study confirms that age and level of SCI are risk factors for shoulder pain, but we demonstrated also that overweight patients who do more than 12 transfers per day have higher chances of having shoulder pain. Keywords Shoulder pain Spinal cord injury Wheelchair Overweight Overuse Multicenter study
Introduction Shoulder pain in patients with spinal cord injury (SCI) has been reported up to 78 % [1–6]. The main causes of shoulder pain are overload due to the repetition of the wheelchair propulsion and the increase in intra-articular pressure [7, 8]. Literature showed that wheelchair users have a strength imbalance between abductor and adductor muscles. This condition may cause the migration of the humeral head upward resulting in impingement syndrome due to the reduction in the subacromial space and possibly result in an impairment of the rotator cuff. The imbalance between intra- and extra-rotator muscles may also result in a loss of horizontal centering and may create an impairment of the anterior capsular ligament [9]. Shoulder pain in the patient with SCI reduces subject’s independence and the quality of life. To prevent this disability, several authors focused their studies in the identification of most important risk factors. To date, the most important risk factors are the age, more than 20 years after SCI and level of SCI [10, 11]. Until now, there is not a consensus in considering sport activities as risk factors.
123
Musculoskelet Surg
Aims of these studies were to analyze the impact of body mass index (BMI) and number of transfers on the shoulder pain onset and to evaluate the relationship between the age at the moment of SCI and the number of years between SCI and the onset of shoulder pain.
Data were analyzed using the Statistical Package for the Social Sciences. p value was set at 0.05. The Chi-square test was used to correlate age, the level of SCI, practice of sports (agonist or not), BMI, number of transfers per day and shoulder pain prevalence. A linear regression was used to correlate the patient age at SCI and the number of years between SCI and the onset of shoulder pain.
Materials and methods A retrospective study was performed enrolling patients with SCI between C5 and S3. The study patients with spina bifida or shoulder pain before SCI or not using manual wheelchair were excluded. Subjects were recruited from two spinal cord units (Torino and Udine) or during sport competition events. Age at the moment of SCI, current age and number of years between SCI and the onset of shoulder pain were recorded. Enrolled patients underwent a self-made questionnaire (Table 1). The period of data collection began in November 2013 and ended in June 2014. The age of 50 years was used as cutoff to analyze how age influenced the onset of shoulder pain. To assess the relationship of the pain and level of SCI, we divided the sample into two groups: those with high SCI from T2 to T7 and subjects with SCI from T8 to T12. Subjects were considered athletes if they met at least two of the following three criteria: training time a week longer than 3 h; involved in at least three competitions per year; and using a wheelchair modified for sports [3]. We divided our sample into two groups: overweight patients (BMI C 25) and normal subjects (BMI \ 25). A cutoff of 12 transfers/day was used to evaluate the relationship between BMI and shoulder pain prevalence. This cutoff was chosen because it is the mean number of transfers that a person with an active lifestyle makes on average per day. Pain was evaluated with a scale from 0 to 10.
Results One hundred and seven patients were enrolled in our study, 11 were excluded because they did not meet the inclusion criteria, 77 patients were male, and 19 were female. The mean age of the subjects was 47.4 years: 49.6 years for male and 38.4 for female. Mean time of wheelchair use was 17.73 years; 46.4 % patients reported shoulder pain, of whom 62.2 % report a difficulty during common daily activities. There was a significant correlation between patient’s age and the onset of shoulder pain (Table 2). Of the subjects, 38 and 35 had high and low levels of lesions, respectively. A significant relationship between level of SCI and shoulder pain was found (Table 3). Subjects with high level of SCI showed a higher rate of shoulder pain. There was no statistically significant relationship between shoulder pain and the practice of sport (all p values [ 0.05) (Table 4). No correlation was found between BMI and shoulder pain if BMI was considered alone (Table 5). Significant differences were found between shoulder pain prevalence and BMI if weight was evaluated together with number of transfers per day, p = 0.0434 (Table 6). Linear regression showed a relationship between the patient age at SCI and the number of years between the SCI and the onset of pain. Older patients needed less time to have shoulder pain than younger patients (Fig. 1).
Table 1 Self-made questionnaire Age
Type of sport
Gender
Since how many years do you practice sports?
Weight
How many hours a week do you do sport activities?
Height
Do you use a wheelchair which had been modified for sports?
Level of SCI
Did you experience shoulder pain before the spinal cord injury?
Time from trauma to shoulder pain onset
Did you experience shoulder pain after the first few months/years after the spinal cord injury?
Wheelchair weight (ex. \di 8 kg; 8–10 kg; [di 10 kg)
How soon arose the pain?
Mean numbers of transfers per day
Value of pain from 1 to 10
Do you play sport?
Does pain affect your daily living?
123
Musculoskelet Surg Table 2 Cross-table between patients’ age and shoulder pain C50 years
\50 years
Shoulder pain
30
17
No shoulder pain
21
28 p = 0.0395
Number of years between the SCI and the onset of shoulder pain
Table 3 Cross-table between shoulder pain onset and level of SCI High SCI
Low SCI
Shoulder pain
22
11
No shoulder pain
16
23 p = 0.0299
Table 4 Cross-table between shoulder pain and practice of sport
Athletes
Shoulder pain
No shoulder pain
18
14
Non-athletes
5
9
Athletes
18
14
No sport
22
29
5
9
22
29
Non-athletes No sport
0.3368 0.3482 0.7629
BMI C 25
BMI \ 25
Shoulder pain
21
24
No shoulder pain
18
33 p = 0.25
Table 6 Relationship between number of transfers and shoulder pain in overweight and normal subject C12
\12
10
10
3
15
BMI C 25 No shoulder pain
p = 0.0434 BMI \ 25 Shoulder pain No shoulder pain
9 10
Fig. 1 Linear regression showed a relationship between age at SCI and number of years between SCI and the onset of shoulder pain
p value
Table 5 Cross-table between overweight and shoulder pain
Shoulder pain
Age at SCI
19 25 p = 0.094
Discussion According to our results, number of transfers in overweight patients is a risk factor to develop shoulder pain after SCI. Younger patients at the moment of SCI required more time
to develop shoulder pain than older patients at the moment of SCI. Furthermore, our study confirms literature data and states once again that age and level of neurologic injury are risk factors for shoulder pain development in SCI patients. Our study presents several limits: The most important ones are the retrospective nature, patients’ enrollment (a structured selection would avoid the risk of bias) and the absence of a priori analysis of the study power. Another limitation is the short period of time during which the data were collected. Literature showed that shoulder pain manifestation is highly correlated with age. In our study, the mean age of patients with SCI and shoulder pain is 48.8, lower than that the age published by Akbar et al. [12], and it should be considered that the mean age of shoulder pain onset in nonSCI patients is much higher: 67.8 [13]. In our study, we found a correlation between age and shoulder pain prevalence using cutoff 50 years. This result confirms that patient’s age is an important risk factor for shoulder pain onset. Results of correlation between level of SCI and shoulder pain are similar to published data [10, 11, 14–16]. Furthermore, in our study, high thoracic SCI (T2–T7) patients have more chances of presenting shoulder pain. This finding may be explained by the adaptations of trunk control during wheelchair propulsions causing muscle strength imbalances between the shoulder adductors and abductors [16]. An overweight subject has to move a heavier body than a normal weight subject. In our study, we found no correlation between shoulder pain and BMI if BMI was evaluated alone, but BMI becomes a significant risk factor if the subject does more than 12 transfers per day. This result may be explained in an increased intra-articular pressure during transfers. This pressure exceeded the
123
Musculoskelet Surg
arterial pressure by 2.5 times [7]. Therefore, it is possible that in overweight subjects, the pressure increases even further. In our study, the mean age between SCI and shoulder pain onset was 10.9, similar to literature data [3]. We have analyzed whether the time of pain shoulder onset changes depending on the patient’s age at the SCI moment. According to our results, the younger is the patients at the moment of SCI, the shorter is the time between SCI and the shoulder pain onset. This result may be explained by the adaptation of tendons and muscles: in young patients, this process may be more efficient than in older patients. Another possible explanation is that older patients may present a subclinical lesion of shoulder tendons at the moment of SCI. Several published studies examined sport activities and shoulder pain prevalence. To date, there is no agreement on this topic [3, 17]. Our data showed no significant relationship between sports practice and shoulder pain. About 63 % of patients who reported shoulder pain were not athletes, but this finding should be carefully interpreted according to the limits of this study. Future studies should focus on the reduction in those biases and analyze a larger number of patients.
Conclusion Overweight patients who do more than twelve transfers per day have an increased risk of occurrence of shoulder pain. Conflict of interest of interest.
The authors declare that they have no conflict
Human and animal rights This article does not contain any studies with human or animal subjects performed by any of the authors.
References 1. Alm M, Saraste H, Norrbrink C (2008) Shoulder pain in persons with thoracic spinal cord injury: prevalence and characteristics. J Rehabil Med 40(4):277–283
123
2. Finley MA, Rasch EK, Keyser RE, Rodgers MM (2004) The biomechanics of wheelchair propulsion in individuals with and without upper-limb impairment. J Rehabil Res Dev 41(3B): 385–395 3. Fullerton HD, Borckardt JJ, Alfano AP (2003) Shoulder pain: a comparison of wheelchair athletes and nonathletic wheelchair users. Med Sci Sports Exerc 35(12):1958–1961 4. Hastings J, Goldstein B (2004) Paraplegia and the shoulder. Phys Med Rehabil Clin N Am 15(3):699–718 5. Pentland WE, Twomey LT (1994) Upper limb function in persons with long term paraplegia and implications for independence: part I. Paraplegia 32(4):211–218 6. Subbarao JV, Klopfstein J, Turpin R (1995) Prevalence and impact of wrist and shoulder pain in patients with spinal cord injury. J Spinal Cord Med 18(1):9–13 7. Bayley JC, Cochran TP, Sledge CB (1987) The weight-bearing shoulder. The impingement syndrome in paraplegics. J Bone Joint Surg Am 69(5):676–678 8. Gagnon D (2008) Comparison of peak shoulder and elbow mechanical loads during weight-relief lifts and sitting pivot transfers among manual wheelchair users with spinal cord injury. J Rehabil Res Dev 45(6):863–874 9. Porcellini G (2011) La patologia di spalla e gomito negli sport olimpici e paralimpici (TIMEO Ed.). ISBN 9788897162155 10. Curtis KA, Drysdale GA, Lanza RD, Kolber M, Vitolo RS, West R (1999) Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil 80(4):453–457 11. Gil-Agudo A, Del Ama-Espinosa A, Perez-Rizo E, PerezNombela S, Pablo Rodriguez-Rodriguez L (2010) Upper limb joint kinetics during manual wheelchair propulsion in patients with different levels of spinal cord injury. J Biomech 43(13):2508–2515 12. Akbar M, Brunner M, Balean G, Grieser T, Bruckner T, Loew M, Raiss P (2012) Etiology of rotator cuff tears in paraplegic patients: a case–control study. J Shoulder Elbow Surg 21(1):23–28 13. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA (2006) The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 88(8):1699–1704 14. Lal S (1998) Premature degenerative shoulder changes in spinal cord injury patients. Spinal Cord 36(3):186–189 15. Medina GI, Nascimento FB, Rimkus CM, Zoppi Filho A, Cliquet A Jr (2011) Clinical and radiographic evaluation of the shoulder of spinal cord injured patients undergoing rehabilitation program. Spinal Cord 49(10):1055–1061 16. Sinnott KA, Milburn P, McNaughton H (2000) Factors associated with thoracic spinal cord injury, lesion level and rotator cuff disorders. Spinal Cord 38(12):748–753 17. Finley MA, Rodgers MM (2004) Prevalence and identification of shoulder pathology in athletic and nonathletic wheelchair users with shoulder pain: a pilot study. J Rehabil Res Dev 41(3B):395–402
