Isolated serratus palsy etiology influences its long-term outcome

ARTICLE IN PRESS J Shoulder Elbow Surg (2017) ■■, ■■–■■

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ORIGINAL ARTICLE

Isolated serratus palsy etiology influences its long-term outcome Martti Vastamäki, MD, PhD*, Leena Ristolainen, PT, ScD, Heidi Vastamäki, MD, PhD, Veera Pikkarainen, MD Research Institute, Orton Foundation and Orton Orthopaedic Hospital, Helsinki, Finland Hypothesis and Background: The cause of isolated serratus palsy is multifactorial, but evaluation of the mechanism of the injury indicates that the lesion to the long thoracic nerve is mechanical in origin in most cases. What is unknown, however, is how etiology influences its long-term outcome. We believed that overuse injuries may recover sooner and better than acute traumatic, infectious, or inflammatory injuries. Methods: We determined the presumed etiology of isolated serratus palsy in 92 patients treated by brace or observation only and compared it with its long-term outcome after a mean follow-up of 18.1 years (range, 2.1-26.9) by measuring pain, range of motion, and winging of the scapula. Results: Trauma preceded 22 (24%) of the cases, exertion 37 (40%), infection 14 (15%), and surgery/ anesthesia 10 (11%). In 9 (10%) cases, no etiologic factor was evident. Serratus palsy preceded by infection recovered better than did cases with no infection, and those with palsy preceded by surgery/anesthesia had a poorer outcome than did those with no surgery (axilla, chest, or any other areas) or anesthesia. Those palsies caused by acute trauma or acute or chronic overuse/exertion had the same recovery course. Discussion and Conclusion: Etiology of isolated serratus palsy influenced long-term outcome less than we had expected. It seems, however, that palsies caused by infection recover better and those caused by surgery wherever in the body recover most poorly. Level of evidence: Level IV; Case Series; Prognosis Study © 2017 Journal of Shoulder and Elbow Surgery Board of Trustees. All rights reserved. Keywords: Serratus palsy; etiology; outcome; winged scapula; scapula alata; winging scapula

Scapular winging caused by serratus palsy is painful, disabling, and difficult to treat. The most disabling dysfunction is the lack of adequate fixation of the scapula against the rib cage during active flexion and abduction.3,8,25,26 The etiology The Ethical Committee of the University Hospital District approved the study: No. 311/13/03/02/2008. Each author certifies that his or her institution approved the human protocol for this investigation, that all investigations were conducted in conformity with ethical principles of research, and that informed consent for participation in the study came from each participant. *Reprint requests: Martti Vastamäki, MD, PhD, Tammistontie 30, Kuusisto 21620, Finland. E-mail address: [email protected] (M. Vastamäki).

of this disorder is multifactorial, often impossible to prove. Anatomic causes may play some role,9,13 but the mechanism of injury may exert even more influence. The etiology of serratus palsy is mostly related to shoulder trauma or overuse.6,7,11,12,17,23 Iatrogenic serratus palsy is associated with only partial recovery14 but sometimes with better recovery, even after a stretching injury caused by first rib resection.27 Traumatic palsies have poorer outcome,3,5 as do inflammatory causes,3 but other clinical factors do not appear to correlate with recovery of serratus function.10 We consider that better knowledge of the role of etiology may help us choose an appropriate treatment for isolated

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ARTICLE IN PRESS M. Vastamäki et al.

3.7 ± 1.3 (1-7) 3.3 ± 1.4 4.1 ± 1.3 3.2 ± 1.0 3.8 ± 1.5 3.9 ± 0.7 .263 .674 .095 .359 .754 152 ± 34 (15-200) 145 ± 37 154 ± 29 166 ± 22 143 ± 32 149 ± 55 138 ± 26 (20-180) 136 ± 19 138 ± 26 143 ± 21 134 ± 26 135 ± 48 32 ± 10 (17-64) 34 ± 12 31 ± 9 31 ± 8 37 ± 13 29 ± 8 81 (88) 20 (91) 34 (92) 14 (100) 5 (50) 8 (89) 64 (70) 18 (82) 27 (73) 5 (36) 7 (70) 7 (78) 92 22 (24) 37 (40) 14 (15) 10 (11) 9 (10) All patients Trauma Exertion Infection Surgery No etiologic factor

SD, standard deviation. P = P value between this item and all others. Boldface indicates P < .05. * Baseline at first examination by the senior author (M.V.).

Initial abduction (°), mean ± SD (range) P Initial flexion (°), mean ± SD (range) Age at onset (years), mean ± SD (range) Right side (%) Male (%) No. (%)

Characteristics of patients with isolated serratus palsy at baseline*

Scapular winging caused by serratus palsy Isolated long thoracic nerve palsy verified by electromyography Adequate recordings of history and clinical findings at the beginning of symptoms

Suggested etiologic factor

Table I Criteria for inclusion in the study on serratus palsy and etiologic factors

Table II

We retrospectively evaluated 92 patients with scapular winging diagnosed as isolated neurogenic serratus palsy. Criteria for inclusion in the study are shown in Table I. A scapular brace was the treatment for 61 patients, and 31 received no special treatment, only our prohibition of strenuous use of the arm to avoid scapular winging. The senior author (M.V.) applied the brace to those patients with scapular winging of 4 cm or more and also to those with winging >2 to 3 cm if their work demanded lifting, bearing, or shoulderlevel arm positions. The mean age of patients at onset of symptoms was 32 ± 10 years (range, 17-64 years). Mean follow-up was 18.1 years (range, 2.126.9 years). Palsy existed on the right side in 81 patients (88%) and on the dominant side in 83 patients (90%) (Table II). We obtained permission to perform this study from the Ethics Committee of the hospital district where the study was conducted. Initial evaluation by the senior author included detailed medical history and physical examination and an electromyographic examination.21 Scapular winging was recorded with a hand-held measure in centimeters as the posterior displacement of the medial border of the scapula from the posterior thorax, ie, from the level of the healthy scapula, at the level of maximal winging.21 The first consultation took place a mean 1.0 year (range, 0.17.4 years) after symptom onset. Custom-made, in part literaturebased questionnaires21 were mailed to the patients along with the invitation to participate in the study. At follow-up, all 92 patients underwent a physical examination by an independent observer (V.P.). The etiologic subgroups were recorded as traumatic (eg, hit to shoulder area or stretching to shoulder area), inflammatory (preceded by viral or bacterial infection), or idiopathic (no obvious etiology).3,21 Because we found a clear etiologic subgroup of exertion (eg, overhead work, abundant lifting or carrying, or strenuous sports), it also became a subgroup. Scapular winging and active shoulder ROM were measured. Shoulder flexion strength was measured with a Salter spring balance and grip strength with a Jamar dynamometer (Lafayette Instrument Co., Lafayette, IN, USA). We determined whether the palsy was totally, partially, or not at all healed as indicated by scapular winging, flexion strength, and ROM (totally healed = no scapular winging, normal flexion strength and ROM compared with the contralateral side; not at all healed = situation similar to or worse than situation at the first consultation; partially healed = the others). Clinical healing was considered obvious when the physician or the patient could not find any winging. The patients also completed custom-made, partly

P

Methods

.711 .961 .431 .564 .839

Initial winging (cm), mean ± SD (range)

P

serratus palsy. We therefore studied the etiology of symptoms and the long-term outcome, determining pain, range of motion and strength in flexion, and presence of long-term scapular winging in 92 patients with isolated serratus palsy.

.115 .014 .098 .327 .551

2

ARTICLE IN PRESS 3

43 (47) .895 11 (50) .185 17 (46) .048 8 (57) .962 1 (10) .694 6 (67) 66 (72) .986 16 (73) .255 24 (65) .002 13 (93) .554 7 (70) .672 6 (67) 1.1 ± 1.7 1.0 ± 1.8 1.3 ± 1.8 0.2 ± 0.8 1.4 ± 2.2 1.3 ± 1.9 .112 .466 .079 .115 .124 79 ± 26 (82) 86 ± 25 (92) 76 ± 30 (79) 67 ± 27 (81) 66 ± 25 (69) 92 ± 26 (92) .578 .552 .002 .014 .378 173 ± 25 (95) 175 ± 19 (97) 174 ± 21 (96) 183 ± 10 (99) 137 ± 42 (78) 179 ± 14 (97) 40 (43) 11 (50) 17 (46) 5 (36) 2 (20) 5 (56)

.512 .899 .499 .106 .460

2.1 2.0 2.1 1.9 2.7 1.7

.466 .794 .980 .019 .149

2.5 2.3 2.5 2.1 3.2 2.3

.448 .843 .182 .002 .694

156 ± 19 (99) 156 ± 14 (97) 155 ± 22 (96) 165 ± 7 (101) 140 ± 29 (89) 169 ± 19 (98) 92 22 37 14 10 9 All Trauma Exertion Infection Surgery No etiologic factor

Mean flexion (°) at followup ± SD (%) of contralateral shoulder Mean pain P during exertion, Likert 4-point scale* Mean pain P at rest, Likert 4-point scale*

SD, standard deviation. P = P value between this item and all others. Boldface indicates P < .050. * Likert 4-point scale: 1, not at all; 2, seldom; 3, sometimes; 4, constantly.

Strength P of flexion (N) ± SD (%) of contralateral shoulder P Mean abduction (°) at follow-up ± SD (%) of contralateral shoulder No. No pain P due to serratus palsy at follow-up, No. (%) Suggested etiologic factor

P

Correlation of suggested etiology of serratus palsy to long-term outcome Table III

At the first consultation for the 92 patients, flexion was normal (≥155°) for 31 (34%), between 125° and 155° for 36 (39%), and ≤120° for 25 (27%). Abduction was normal (≥165°) for 44 (48%), between 115° and 160° for 35 (38%), and ≤110° for 13 (14%) patients. Initially, the etiologic groups did not differ from each other significantly (Table II). Mean patient follow-up was 18.1 years (range, 2.1-26.9 years). Mean duration of disease according to statements of the 57 patients who considered themselves cured (no scapular winging or any discomfort around the shoulder area) was 15 months (range, 2-30 months), with 28 (49%) achieving healing in 1 year and 53 (93%) in 2 years. Winging measured in 90° flexion resolved in 66 patients (72%). In the other 26 patients (28%), winging averaged 3.4 cm, and in 4 of them (4%), winging remained >4 cm. ROM improved almost to the level of the contralateral shoulder (Table III). Flexion improved from 138° ± 26° to 156° ± 19°, and abduction improved from 152° ± 34° to 173° ± 25°. The strength in flexion averaged 79 ± 26 N and 97 ± 19 N in the contralateral shoulder. Of the 92 patients, 40 (43%) were pain free; pain at rest was absent from 32 (35%), occurred seldom in 24 (26%), and was temporary in 32 (35%); 2 patients had pain at rest continuously (Table III). Etiology was acute trauma in 22 patients (24%); overuse or heavy exertion in 37 (40%); infection in 14 (15%); surgery or anesthesia in 10 (11%); and of unknown cause, probably some kind of neuritis, in 9 (10%). Stretching of the shoulder area was the most common etiology in the trauma group, continuous heavy lifting or carrying in the exertion group, and surgery of the thoracic long nerve domain in the surgical procedure group (Table IV). Surgery/anesthesia and infection as an etiologic factor significantly influenced long-term outcome of isolated serratus palsy. Mean pain on the Likert scale was significantly higher in the surgery group than in the other etiologic groups (pain at rest, 2.7 vs. 2.0 [P = .019]; pain during exertion, 3.2 vs. 2.4 [P = .002]); shoulder abduction was significantly lower (137° vs. 176° [P = .014]) (Table III). On the other hand, palsies caused by infection recovered better than did all the others (shoulder flexion, 165° vs. 147° [P = .001]; abduction, 183° vs. 162° [P = .002]; and winging, 0.2 cm vs. 1.2 cm [P = .002]). Trauma, exertion, or “neuritis”

Mean P winging (cm) ± SD at follow-up

Results

.975 .670 .001 .080 .488

No P winging objectively, No. (%)

Cured P subjectively, No. (%)

literature-based questionnaires, 21 including questions about demographics, work history, onset of symptoms and preceding factors, treatment, healing, and current condition. Pain was assessed using the Likert 4-point scale (not at all, seldom, sometimes, or constantly). Descriptive data are proportions or means (range). Statistical differences in patients’ characteristics, such as ROM, scapular winging, and pain, were determined in categorical variables by Pearson χ2 test and in continuous variables by Student t-test. Statistical analysis was performed with SPSS 23.0 for Windows (SPSS Inc., Armonk, NY, USA).

.094 .747 .397 .014 .207

Serratus palsy etiology influences its outcome

ARTICLE IN PRESS 4

M. Vastamäki et al. Table IV

Suggested etiologic factors in 92 patients with serratus palsy

Trauma (all) Hit to shoulder area Stretching to shoulder area Others

22 5 12 5

Infection (all) Mild infection Severe infection demanding bed rest

14 9 5

No apparent etiologic factor

9

etiology (Parsonage-Turner), each as an etiologic factor for serratus palsy, had no influence on long-term outcome.

Discussion We did find two significant etiologic factors influencing the outcome of isolated serratus palsy. Surgery also outside the domain of the long thoracic nerve had a debilitating effect on outcome, and palsies presumably caused by infection— also by severe infections—recovered better than others. This study is, to our knowledge, the first one dealing with the association of etiology with long-term outcome of isolated serratus palsy. Its etiology is multifactorial. Often, it is impossible to decide whether some event or factor plays a decisive role as this disorder’s cause. What is also almost unknown is how different etiologic factors for the disorder influence its outcome. No study exists to tell us how etiologic factors influence the long-term outcome of this entity. We theorized that traumatic palsies or infection-caused palsies may have a worse recovery. We acknowledge limitations in our study. Concerning evaluation, we obtained no validated functional scores, either at the time most patients initially were seen or at follow-up, because no suitable valid score presently exists for serratus palsy. We therefore opted for a self-made one with pain, shoulder ROM, strength in flexion, and scapular winging, which are the most important factors in serratus palsy. Second, the etiology mostly cannot be proven. Some patients thought their problems arose from repetitive trauma, such as strenuous

Table V

Exertion (all) Overhead work Abundant lifting or carrying Strenuous sports Delivery Other strenuous exertion

37 11 14 6 1 5

Surgery (all) Axilla, chest, or throat area Other areas

10 6 4

sports, although they had practiced these sports regularly. Sometimes they also had suffered from influenza, and according to our experience after treating more than 350 serratus palsies, we believe the influenza was more accurate as a cause. In fact, etiology is often more or less debatable. We tried to be as thorough as possible to dig out all necessary data relevant to a valid etiology. Foo and Swann2 reported 20 cases with isolated paralysis of the serratus anterior muscle. Attributed etiology was an injury to the shoulder region in 15%, overuse in 30%, infection in 5%, surgical procedure/anesthesia in no patients, and unknown in 50%. They also followed up 14 patients for 1 to 10 (mean 5.8) years but found no differences in outcomes regarding etiology. Klebe et al15 described 64 patients with a supposed etiology amounting to a respective 25%, 23%, 11%, 18%, and 23%, but they did not focus on the influence of etiology. We reported in 1993 on the etiology of 197 isolated serratus palsies as being 26%, 35%, 7%, 16%, and 15%, respectively, without any outcome measures.23 Here, our etiologic distribution in 92 patients was about the same as earlier reported elsewhere (Table V). Surgery also outside the domain of the long thoracic nerve had a debilitating effect on outcome, presumably because of poor positioning during anesthesia. Postoperative isolated serratus palsy may be caused by faulty transport, handling, or positioning of the patient at the time of surgery (in lateral, decubitus, or prone position; no accurate padding; too advanced abduction of the arm). Martin 18 presented 2 postoperative serratus palsy patients with full recovery in 6 and 8 months and 1 patient who recovered incompletely in

Literature on etiologic factors of serratus palsy

Supposed etiologic factor

Vastamäki and Kauppila23

Klebe et al15

Kaptelin and Pavlova12

Friedenberg et al3

Overbeck and Chormley19

Johnson and Kendall11

Foo and Swann2

Current study

No. Overuse/exertion, % Trauma, % Surgery/anesthesia, % Infection/inflammation, % Miscellaneous, % Unknown, %

197 35 26 16 7 1 15

64 23 25 18 11 0 23

62 61 29 0 0 10 0

50 0 28 6 40 0 26

28 25 54 0 7 3 11

20 30 10 0 15 20 25

20 30 15 0 5 0 50

92 40 25 11 15 0 9

ARTICLE IN PRESS Serratus palsy etiology influences its outcome 2 years. Twenty years ago, we observed 26 patients with postoperative serratus palsy; 9 palsies followed anesthesia and 17 local invasive procedures on the anterolateral aspect of the thorax. They did not heal well; all but 1 had residual symptoms after a mean 6-year follow-up.14 In this study, of 10 postoperative cases, only 3 recovered well. Friedenberg et al interviewed their serratus palsy patients by phone a mean 4 years after symptom onset and concluded that traumatic serratus palsies were associated with a poor outcome.3 Goodman et al5 also confirmed that traumatic palsies are more severe than palsies due to other etiology in their series of 12 patients showing only partial or no recovery. Klingelhöfer et al16 stated that serratus palsy preceded by abdominal or gynecologic surgery under general anesthesia may not improve, but follow-up of their 5 patients was <1 year. In this study, 2 patients said that their position on the operating table had been uncomfortable. One appendicectomy patient declared that the position of the affected hand was poor, and a lumbar spondylodesis patient said that the position of the affected shoulder had been poor. At followup, they had no scapular winging, but their ROM was inferior to others’ ROM, with flexion of 130° and 140° and abduction of 120° and 95°, respectively. Of 4 rib resection patients, 2 recovered well and 2 still had winging of 4.5 and 5 cm and poor ROM. On the other hand, palsies presumably caused by infection—also by severe infections— recovered better than others. Eight patients had suffered influenza, 1 had severe encephalitis, and 1 had severe gastroenteritis. They all recovered well. Why palsies presumably caused by infection recovered better than the others is not clear. Perhaps infection causes swelling in the nerve that does not cause total axonotmesis. However, our hypothesis that overuse injuries may recover sooner and better than acute traumatic, infectious, or inflammatory injuries was incorrect. The incidence of serratus palsy is approximately 0.3% of all patients with shoulder disorders.19 Serratus palsy occurs on the dominant side in 86% to 95%2,3 and in this study in 88%. Whereas we do not know the explanation for this occurrence, the palsy may result from more exertion occurring for the dominant hand. The most common treatment options depend on severity: observation without any specific treatment,1-3,5,21 a scapular protective brace,15,24 neurolysis of the long thoracic nerve, or dynamic muscle transfers.2,4,20,22

Conclusions Postoperative isolated serratus palsies may recover more poorly than other palsies, but palsies caused by infection presumably show a better outcome. Serratus palsies caused by acute trauma, overuse, or strenuous exertion as well as neuritis palsies (ie, isolated Parsonage-Turner type palsies) seem to recover equally without depending on etiology of the palsy.

5

Acknowledgments We thank Carol Norris, PhD, for language revision.

Disclaimer During the study period, the authors’ institution received funding from EVO, HUS (government grant from the Helsinki University Hospital District). The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.

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ARTICLE IN PRESS 6 18. Martin JT. Postoperative isolated dysfunction of the long thoracic nerve: a rare entity of uncertain etiology. Anesth Analg 1989;69:614-9. 19. Overpeck DO, Ghormley RK. Paralysis of the serratus magnus muscle caused by lesion of the long thoracic nerve. JAMA 1940;114: 1994-6. 20. Perlmutter GS, Leffert RD. Results of transfer of the pectoralis major tendon to treat paralysis of the serratus anterior muscle. J Bone Joint Surg Am 1999;81:377-84. 21. Pikkarainen V, Kettunen J, Vastamäki M. The natural course of serratus palsy at 2 to 31 years. Clin Orthop Relat Res 2013;471:1555-63. http://dx.doi.org/10.1007/s11999-012-2723-7. 22. Steinmann SP, Wood MB. Pectoralis major transfer for serratus anterior paralysis. J Shoulder Elbow Surg 2003;12:555-60. http://dx.doi.org/ 10.1016/S1058-2746(03)00174-5

M. Vastamäki et al. 23. Vastamäki M, Kauppila L. Etiologic factors in isolated paralysis of the serratus anterior muscle: a report of 197 cases. J Shoulder Elbow Surg 1993;2:240-3. 24. Vastamäki M, Pikkarainen V, Vastamäki H, Ristolainen L. Scapular bracing is effective in some patients but symptoms persist in many despite bracing. Clin Orthop Relat Res 2015;473:2650-7. http://dx.doi.org/ 10.1007/s11999-015-4310-1 25. Warner JJ, Navarro RA. Serratus anterior dysfunction: recognition and treatment. Clin Orthop Relat Res 1998;349:139-48. 26. Wiater JM, Flatow EL. Long thoracic nerve injury. Clin Orthop Relat Res 1999;368:17-27. 27. Wood VE, Frykman GK. Winging of the scapula as a complication of first rib resection: a report of six cases. Clin Orthop Relat Res 1980;149:160-3.