- Email: [email protected]
Complications of Intercostal Nerve Transfer for Brachial Plexus Reconstruction
SCIENTIFIC ARTICLE
Complications of Intercostal Nerve Transfer for Brachial Plexus Reconstruction Rudy Kovachevich, MD, Michelle F. Kircher, BSN, Christina M. Wood, MS, Robert J. Spinner, MD, Allen T. Bishop, MD, Alexander Y. Shin, MD Purpose Although numerous publications discuss outcomes of intercostal nerve transfer for brachial plexus injury, few publications have addressed factors associated with intercostal nerve viability or the impact perioperative nerve transfer complications have on postoperative nerve function. The purposes of this study were to report the results of perioperative intercostal nerve transfer complications and to determine whether chest wall trauma is associated with damaged or nonviable intercostal nerves. Methods All patients who underwent intercostal nerve transfer as part of a brachial plexus reconstruction procedure as a result of injury were identified. A total of 459 nerves in 153 patients were transferred between 1989 and 2007. Most nerves were transferred for use in biceps innervation, free-functioning gracilis muscle innervation, or a combination of the two. Patient demographics, trauma mechanism, associated injuries, intraoperative nerve viability, and perioperative complications were reviewed. Results Complications occurred in 23 of 153 patients. The most common complication was pleural tear during nerve elevation, occurring in 14 of 153 patients. Superficial wound infection occurred in 3 patients, whereas symptomatic pleural effusion, acute respiratory distress syndrome, and seroma formation each occurred in 2 patients. The rate of complications increased with the number of intercostal nerves transferred. Nerves were harvested from previously fractured rib levels in 50 patients. Rib fractures were not associated with an increased risk of overall complications but were associated with an increased risk of lack of nerve viability. In patients with rib fractures, intraoperative nerve stimulation revealed 148 of 161 nerves to be functional; these were subsequently transferred. In patients with preoperative ipsilateral phrenic nerve palsy, the risk of increased complications was marginally significant. Conclusions Brachial plexus reconstruction using intercostal nerves can be challenging, especially if there is antecedent chest wall trauma. Complications were associated with increasing numbers of intercostal nerves transferred. Ipsilateral rib fracture was adversely associated with intercostal nerve viability; it was not significantly associated with complication risk and should not be considered a contraindication to transfer. Preoperative phrenic nerve palsy was marginally associated with the likelihood of complications but not postoperative respiratory dysfunction when associated with intercostal nerve transfer. (J Hand Surg 2010;35A:1995–2000. Copyright © 2010 by the American Society for Surgery of the Hand. All rights reserved.) Type of study/level of evidence Therapeutic IV. Key words Brachial plexus, intercostal nerve, nerve transfer, neurotization, complications.
From the Mayo Clinic College of Medicine; the Department of Orthopaedic Surgery, Division of Hand Surgery; the Department of Statistics; and the Department of Neurological and Orthopaedic Surgery, Mayo Clinic, Rochester, MN. Received for publication December 14, 2009; accepted in revised form September 13, 2010.
Corresponding author: Alexander Y. Shin, MD, Mayo Clinic E14A, 200 First Street SW, Rochester, MN 55905; e-mail: [email protected]. 0363-5023/10/35A12-0013$36.00/0 doi:10.1016/j.jhsa.2010.09.013
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
© ASSH 䉬 Published by Elsevier, Inc. All rights reserved. 䉬 1995
1996
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
injuries are devastating events frequently resulting in severe functional impairment. The multiple nerve root avulsions common in such cases limit reconstructive options. Refinement of direct nerve transfers and development of advanced microsurgical techniques have improved outcomes in recent years. Intercostal nerve (ICN) transfers have become a mainstay treatment for reconstructing the brachial plexus since Seddon’s initial description in 19631 and the subsequent work of others.2–12 Their extraplexal origin and proximity to the infraclavicular plexus makes them an excellent source of viable motor and sensory nerves.13 The minimal motor and sensory functional loss resulting from their use provides additional incentive to consider their use. A tremendous volume of publications regarding the outcomes of these procedure can be found in the current literature.3,5,6,8,11,12,14 Information is scarce regarding the effect of chest wall trauma on ICN availability and occurrence of perioperative ICN harvest complications. Some authors have suggested that the presence of rib fractures is a contraindication to intercostal nerve use of that rib.15,16 The purposes of this study were to report our experience with perioperative ICN harvest complications and to determine whether chest wall trauma is associated with damaged or nonviable intercostal nerves.
T
RAUMATIC BRACHIAL PLEXUS
MATERIALS AND METHODS We conducted a retrospective review to identify all patients who underwent ICN transfer as part of a brachial plexus reconstruction for injury between 1989 and 2007. We excluded obstetrical brachial plexus palsy patients from the study. After obtaining approval from our institutional review board, we identified 153 consecutive patients. Information regarding patient demographics, mechanism of injury, associated injuries, intercostal nerve transfer procedure performed, intercostal nerve viability, and complications was evaluated. The technique of ICN transfer used at our institution is similar to that described previously in the literature.16 Between 1989 and 2007, 153 patients underwent ICN transfer; 136 patients were male and 17 were female. The mean age at the time of surgery was 27 ⫾ 11 years (range, 6 – 65 y). The mechanism of injury involved motorcycle accidents in 51 patients, motor vehicle accidents in 43 patients, snowmobile/all-terrain vehicle accidents in 41 patients, and miscellaneous mechanisms in 18 patients. The right side was involved in 87 cases. The majority of patients had extensive nerve avulsion injuries, with 91 having 3 to 5 avulsions, 44 having 2 avulsions, and 18 with no or one avulsion.
TABLE 1. Associated Organ System Dysfunction in Brachial Plexus Injury Patients Organ System
No. (%)
Appendicular bone/soft tissue injury
124 (81)
Craniofacial trauma
55 (36)
Ipsilateral rib fractures
50 (33)
Lung parenchymal injury
33 (21)
Appendicular vascular injury
22 (14)
Intra-abdominal injury
17 (11)
Phrenic nerve palsy
16 (10)
Injuries involving multiple organ systems were extremely common in our patient cohort. The most common injuries associated with the traumatic brachial plexus lesions were appendicular fractures, seen in 124 patients. Fifty patients had ipsilateral rib fractures. A total of 33 patients had a previous lung injury (hemothorax, hemopneumothorax, pneumothorax, etc.). Table 1 lists the remaining associated organ system injuries. The median duration of time from injury to surgical intervention was 6 months (range, 3–120 mo). The most common application in our cohort of patients was biceps reanimation, which was performed in 67 patients. This transfer was only performed for injuries that occurred less than 12 months before surgery. We used intercostal motor nerves for combined biceps and freefunctioning gracilis muscle transfer in 37 patients and gracilis innervation alone in 31 patients. The remaining 18 patients underwent various combinations of biceps and/or gracilis neurotization procedures along with transfer to other sources as indicated by dysfunction. The ICNs transferred included the second through seventh intercostals, with most being from the third through sixth intercostals. A total of 459 motor nerves were harvested in this cohort. In most surgical procedures, 2 to 4 ICNs were transferred for motor reconstruction (94% of the cohort). In addition, we used the sensory portions of the transferred ICNs in an attempt to restore protective sensation to the injured extremity 134 patients (88%). Complications were documented through review of the extensive patient medical record. All iatrogenic pleural tears were noted in the surgical reports and confirmed with review of postoperative chest radiographs showing small pneumothoraces and chest tube placement. Postoperative respiratory dysfunction was noted in clinical and intensive care unit documentation. Acute respiratory distress syndrome was documented clinically with the development of progressive tachy-
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COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
TABLE 2. Complications of ICN Transfer for Traumatic Brachial Plexus Reconstruction Complication
No. (%)
Overall
23 (15)
Iatrogenic pleural tear
14 (9)
Superficial wound infection
3 (2)
Symptomatic pleural effusion
2 (1)
Acute respiratory distress syndrome
2 (1)
Subcutaneous wound seroma
2 (1)
pnea, decreased oxygenation, and increased oxygen dependence. It was confirmed by arterial blood gas and chest x-ray showing the development of bilateral alveolar infiltrates. Symptomatic pleural effusions were also suspected clinically and confirmed by chest radiographs. Patients and nerves are described using mean ⫾ standard deviation, median (range), or count (percentage) as appropriate. We used Fisher’s exact test to assess associations between complications (any or specifically respiratory) and phrenic nerve palsy or rib fracture. When appropriate owing to few complications, 95% exact binomial confidence intervals were also calculated. We used univariate logistic regression to assess the association between having complications and the number of nerves transferred. All statistical tests were 2-sided, and p values less than .05 were considered statistically significant. We used SAS version 9.1 (SAS Institute, Inc., Cary, NC) for all analyses. RESULTS Perioperative complications occurred in 23 of 153 patients (Table 2). The most common complication was an iatrogenic pleural tear during nerve elevation, which occurred in 14 of 153 patients. Treatment in all patients consisted of a small chest tube placed in the operating room. Chest tube duration ranged from 2 to 7 days (average, 3 d). All of our chest tubes were managed by our thoracic surgery colleagues. In 2 patients, symptomatic postoperative pleural effusions required prolonged intensive care unit stays with therapeutic pleurocentesis. Two patients developed acute respiratory distress syndrome requiring prolonged intubation (1–3 d). All 4 patients responded to aggressive pulmonary management and supportive care with no long-term sequelae. Other more minor complications including superficial wound infections and subcutaneous wound seroma formation were infrequent, occurring in 3 and 2 patients, respectively. Complication fre-
1997
quency increased as the number of ICNs harvested increased, with higher percentages found in those with 4 or greater at the time of surgery (Fig. 1). Having an additional nerve transferred was associated with 2.49 times the odds of having a complication (p ⬍ .001). In patients with previously fractured ipsilateral ribs, 161 nerves were transferred in 50 patients. Among rib fracture patients, 45 of 50 did not have complications, whereas among non–rib fracture patients, 85 of 103 did not have complications. This association was not statistically significant (p ⫽ .33). There was, however, a significant association between the presence of rib fractures and nerve viability (p ⬍ .001). In those 103 patients without rib fractures, all patients were found to have usable nerves at time of transfer (95% confidence interval, 0%–3.5%). In comparison, in those 50 patients with associated rib fractures, 6 patients had unusable nerves owing to rib fracture (95% confidence interval, 4.5%–24.3%). For all ICN transfers, 446 of 459 were viable intraoperatively by direct nerve stimulation and underwent successful transfer. All 13 nonviable nerves were in patients with rib fractures; therefore, 92% of ICNs transferred in rib fracture patients were viable intraoperatively. In the 16 patients with ipsilateral phrenic nerve palsy, 50 intercostal nerves were transferred. Among patients with phrenic nerve injuries, 5 of 16 had complications, whereas among nonphrenic injury patients 18 of 137 had complications. This association was marginally statistically significant (p ⫽ .07). Looking more closely at respiratory outcomes, 1 of the 16 phrenic nerve injury patients developed postoperative pleural effusion. In contrast, the overall rate of respiratory dysfunction in those with intact phrenic nerve function was 3 of 138, in the form of adult respiratory distress syndrome (2) and symptomatic pleural effusions requiring pleurocentesis (1). The association of phrenic nerve injury and respiratory complications was not statistically significant (p ⫽ .36). DISCUSSION Brachial plexus reconstruction with ICNs following injury can be challenging, especially if there is antecedent trauma to the chest wall. Despite numerous publications on the outcome of ICN transfers, little attention has been given to the perioperative complications of intercostal transfer or to identification of factors affecting ICN viability. We observed an overall 15% complication rate in the acute perioperative period. Wahegaonkar et al.16 noted that complications in brachial plexus surgical procedures are rare with proper surgical
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1998
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
FIGURE 1: Occurrence of complications with respect to the number of ICNs harvested.
technique and meticulous dissection. The most common complication in their study was seroma formation (not quantified). They also noted 2 patients who experienced iatrogenic pneumothorax and were treated with defect closure, chest tube placement, and positive pressure ventilation. Our study population represented a cohort of patients for whom nerve transfer procedures are generally performed. Most of our patients underwent intercostal nerve transfer owing to multiple nerve root avulsion injuries confirmed by computed tomography myelography, electrodiagnostic studies, and clinical examination.17–19 These patients all had absence of clinical or electrical recovery or injuries that made spontaneous recovery impossible. Most patients also had nerve transfers performed to restore elbow flexion. This was performed mostly by either transfer to the musculocutaneous nerve,2,3,6,8,11,12,20 –26 innervation of a gracilis free-functioning muscle transfer,10,27–33 or a combination of the two. The mechanisms of injury in most of our patients were similar to those normally found in patients with this type of injury, in that they were mainly high-energy in nature,34,35 most commonly motorcycle accidents. The magnitude of force imparted to the body at the time of these events tended to cause damage to multiple organ systems. We found that as-
sociated organ system injuries were extremely common in our patient population and we were able to quantify these frequencies. Previous studies have claimed ipsilateral rib fracture and ipsilateral phrenic nerve palsy as contraindications to ICN transfers.15,16 Concern with ICN transfer in these patients has been with damage of the nerves owing to the chest wall trauma and fracture. One third of our patient population had associated rib fractures. Despite the associated chest wall trauma, nerve transfer using ICN was successful in 92% of these patients, as documented intraoperatively via nerve stimulation testing. Preoperative phrenic nerve palsy has also been recommended as a contraindication to ICN transfer owing to the presumed increase in respiratory dysfunction after surgery. We found an almost 3-fold increase in the rate of respiratory compromise in patients with preoperative phrenic nerve palsy compared with those without; however, this finding was not statistically significant. The small amount of patients with this complication makes statistical analysis difficult and a future study with increased power would be needed to attempt to detect a significant difference. This is relevant in the preoperative consent process for our patients, but the benefit of ICN transfer on postoperative function has brought us to conclude that it remains a reasonable
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COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
option in our reconstructive armamentarium. These findings would challenge the current dogma that ICN transfer is not an option in these 2 patient groups. Most of the current literature on postoperative respiratory complications after ICN transfer shows minimal clinical effect of respiratory function. Krakauer and Wood8 in 1994 found that 4 of 12 patients had mild decline in objective pulmonary function testing without subjective deficiency. Numerous other studies have found no clinical decrease in respiratory function.22,36 Chalidapong et al.4 noted that objective pulmonary function study results were only notably reduced for 2 weeks and all normalized within 3 months. Close evaluation of the cases with postoperative respiratory dysfunction as well as iatrogenic pleural tear revealed that 74% of these complications occurred when 4 or more ICNs were used for transfer. Increased complications coincided with increasing complexity of reconstructions that were being undertaken using increasing numbers of ICNs. The limitations of this study include the fact that we retrospectively gathered data on complications. This may have underestimated the overall number of complications as a result of failure to document at the time the complication occurred or because of missed perioperative complications. The aggressive nature of our treatment of pleural tears with chest tube placement could also be argued as unnecessary. The prophylactic use of chest tubes after iatrogenic pleural tearing and subsequent repair remains controversial, with most recent thoracic surgery literature supporting primary closure without the need for chest tube placement.37,38 The invasiveness of the treatment strategy for dealing with intraoperative iatrogenic pleural injury has been an ongoing discussion at our institution, involving not only the brachial plexus service but also our thoracic surgery and anesthesia colleagues. Our decision to insert a small chest tube into the pleural defect at the time of surgery involved concern over the lack of intraoperative feedback over whether a pneumothorax had occurred owing to the protective positive pressure ventilation and the concern that if a pneumothorax or a large amount of fluid accumulation was present, subsequent return to surgery for chest tube placement or bedside placement would place our ICN transfers at tremendous risk for injury. In addition, owing to the complex nature of the procedures being performed, our patients required lengthy hospitalizations. Most patients with pleural tears (12 of 14) also underwent free-functioning gracilis muscle transfer at the time of ICN transfer and required 4 to 6 days of hospitalization because of close vascular
1999
monitoring of the muscle, similar to that of patients without chest tubes. Based on these results, a surgeon performing brachial plexus reconstructive surgery should be able to more accurately discuss with patients the potential complications and likely viability of ICNs for planned transfer. We have found this information to be useful in our practice when counseling patients and performing informed consent discussions before complex reconstructive procedures. REFERENCES 1. Seddon HJ. Nerve grafting. J Bone Joint Surg 1963;45B:447– 461. 2. El-Gammal TA, Fathi NA. Outcomes of surgical treatment of brachial plexus injuries using nerve grafting and nerve transfers. J Reconstr Microsurg 2002;18:7–15. 3. Merrell GA, Barric KA, Katz DL, Wolfe SW. Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature. J Hand Surg 2001;26A:303–314. 4. Chalidapong P, Sananpanich K, Kraisarin J, Bumroongkit C. Pulmonary and biceps function after intercostal and phrenic nerve transfer for brachial plexus injuries. J Hand Surg 2004;29B:8 –11. 5. Samardzic M, Rasulich L, Grujicic D, Milicic B. Results of nerve transfers to the musculocutaneous and axillary nerves. Neurosurgery 2000;46:93–103. 6. Malessy MJ, Thomeer RT. Evaluation of intercostal to musculocutaneous nerve transfer in reconstructive brachial plexus surgery. J Neurosurg 1998;88:266 –271. 7. Doi K, Shigetomi M, Kaneko K, Soo-Heong T, Hiura Y, Hattori Y, et al. Significance of elbow extension in reconstruction of prehension with reinnervated free-muscle transfer following complete brachial plexus avulsion. Plast Reconstr Surg 1997;100:364 –374. 8. Krakauer JD, Wood MB. Intercostal nerve transfer for brachial plexopathy. J Hand Surg 1994;19A:829 – 835. 9. Narakas AO, Hentz VR. Neurotization in brachial plexus injuries. Indication and results. Clin Orthop Relat Res 1988;237:43–56. 10. Doi K, Sakai K, Kuwata N, Ihara K, Kawai S. Reconstruction of finger and elbow function after complete avulsion of the brachial plexus. J Hand Surg 1991;16A:796 – 803. 11. Chuang DC, Yeh MC, Wei FC. Intercostal nerve transfer of the musculocutaneous nerve in avulsed brachial plexus injuries: evaluation of 66 patients. J Hand Surg 1992;17A:822– 828. 12. Nagano A, Ochiai N, Okinaga S. Restoration of elbow flexion in root lesions of brachial plexus injuries. J Hand Surg 1992;17A:815– 821. 13. Wood MB, Murray PM. Heterotopic nerve transfers: recent trends with expanding indication. J Hand Surg 2007;32A:397– 408. 14. Samardzic M, Grujicic D, Antunovic V. Nerve transfer in brachial plexus traction injuries. J Neurosurg 1992;76:191–197. 15. Ruch DS, Friedman A, Nunley JA. The restoration of elbow flexion with intercostal nerve transfers. Clin Orthop Relat Res 1995;314: 95–103. 16. Wahegaonkar AL, Doi K, Hattori Y, Addosooki AI. Technique of intercostal nerve harvest and transfer for various neurotization procedures in brachial plexus injuries. Tech Hand Up Extrem Surg 2007;11:184 –194. 17. Walker AT, Chaloupka JC, deLotbiniere AC, Wolfe SW, Goldman R, Kier EL. Detection of nerve rootlet avulsion on CT myelography in patients with birth palsy and brachial plexus injury after trauma. AJR Am J Roentgenol 1996;167:1283–1287. 18. Nagano A, Ochiai N, Sugioka H, Hara T, Tsuyama N. Usefulness of myelography in brachial plexus injuries. J Hand Surg 1989;14B:59 – 64. 19. Carvalho GA, Nikkhah G, Matties C, Penkart G, Samii M. Diagnosis of root avulsions in traumatic brachial plexus injuries: value of
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2000
20.
21.
22.
23. 24. 25. 26.
27.
28.
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
computerized tomography myelography and magnetic resonance imaging. J Neurosurg 1997;86:69 –76. Minami M, Ishii S. Satisfactory elbow flexion in complete (preganglionic) brachial plexus injuries: produced by suture of third and fourth intercostal nerves to musculocutaneous nerve. J Hand Surg 1987;12A:1114 –1118. Akasaka Y, Hara T, Takahashi M. Restoration of elbow flexion and wrist extension in brachial plexus paralyses by means of free muscle transplantation innervated by intercostal nerve. Ann Chir Main Memb Super 1990;9:341–350. Waikakul S, Wongtragul S, Vanadurongwan V. Restoration of elbow flexion in brachial plexus avulsion injury: comparing spinal accessory nerve transfer with intercostal nerve transfer. J Hand Surg 1999;24A:571–577. Nagano A. Intercostal nerve transfer for elbow flexion. Tech Hand Up Extrem Surg 2001;5:136 –140. Nagano A. Treatment of brachial plexus injury. J Orthop Sci 1998; 3:71– 80. Chuang DC. Neurotization procedures for brachial plexus injuries. Hand Clin 1995;11:633– 645. Chuang DC, Epstein MO, Yeh MC, Wei FC. Functional restoration of elbow flexion in brachial plexus injuries: results in 167 patients (excluding obstetric brachial plexus injury). J Hand Surg 1993;18A: 285–291. Doi K, Sakai K, Kuwata N, Ihara K, Kawai S. Double free-muscle transfer to restore prehension following complete brachial plexus avulsion. J Hand Surg 1995;20A:408 – 414. Doi K, Kuwata N, Muramatsu K, Hattori Y, Kawai S. Double muscle
29.
30. 31. 32.
33.
34. 35. 36.
37. 38.
transfer for upper extremity reconstruction following complete avulsion of the brachial plexus. Hand Clin 1999;15:757–767. Doi K, Hattori Y, Kuwata N, Soo-heong T, Kawakami F, Otuka K, et al. Free muscle transfer can restore hand function after injuries of the lower brachial plexus. J Bone Joint Surg 1998;80B:117–120. Chuang D. Functioning free muscle transplantation for brachial plexus injury. Clin Orthop Relat Res 1995;314:104 –111. Berger A, Flory PJ, Schaller E. Muscle transfers in brachial plexus lesions. J Reconstr Microsurg 1990;6:113–116. Barrie KA, Steinmann SP, Shin AY, Spinner RJ, Bishop AT. Gracilis free muscle transfer for restoration of function after complete brachial plexus avulsion. Neurosurg Focus 2004;16:1– 8. Doi K, Muramatsu K, Hattori Y, Otsuka K, Tan SH, Nanda V. Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexus. Indications and long-term results. J Bone Joint Surg 2000;82A:652– 666. Midha R. Epidemiology of brachial plexus injuries in a multitrauma population. Neurosurgery 1997;40:1182–1189. Narakas AO. The treatment of brachial plexus injuries. Int Orthop 1985;9:29 –36. Giddins GE, Kakkar N, Altree J, Birch R. The effect of unilateral intercostal nerve transfer upon lung function. J Hand Surg 1995; 20B:675– 676. Gordon CE, Feller-Kopman D, Balk EM, Smetana GW. Pneumothorax following thoracentesis. Arch Intern Med 2010;170:332–339. Luckraz H, Rammohan KS, Phillips M, Abel R, Karthikeyan S, Kulatilake NE, et al. Is an intercostal chest drain necessary after video-assisted thoracoscopic (VATS) lung biopsy? Ann Thorac Surg 2007;84:237–239.
JHS 䉬 Vol A, December
Complications of Intercostal Nerve Transfer for Brachial Plexus Reconstruction Rudy Kovachevich, MD, Michelle F. Kircher, BSN, Christina M. Wood, MS, Robert J. Spinner, MD, Allen T. Bishop, MD, Alexander Y. Shin, MD Purpose Although numerous publications discuss outcomes of intercostal nerve transfer for brachial plexus injury, few publications have addressed factors associated with intercostal nerve viability or the impact perioperative nerve transfer complications have on postoperative nerve function. The purposes of this study were to report the results of perioperative intercostal nerve transfer complications and to determine whether chest wall trauma is associated with damaged or nonviable intercostal nerves. Methods All patients who underwent intercostal nerve transfer as part of a brachial plexus reconstruction procedure as a result of injury were identified. A total of 459 nerves in 153 patients were transferred between 1989 and 2007. Most nerves were transferred for use in biceps innervation, free-functioning gracilis muscle innervation, or a combination of the two. Patient demographics, trauma mechanism, associated injuries, intraoperative nerve viability, and perioperative complications were reviewed. Results Complications occurred in 23 of 153 patients. The most common complication was pleural tear during nerve elevation, occurring in 14 of 153 patients. Superficial wound infection occurred in 3 patients, whereas symptomatic pleural effusion, acute respiratory distress syndrome, and seroma formation each occurred in 2 patients. The rate of complications increased with the number of intercostal nerves transferred. Nerves were harvested from previously fractured rib levels in 50 patients. Rib fractures were not associated with an increased risk of overall complications but were associated with an increased risk of lack of nerve viability. In patients with rib fractures, intraoperative nerve stimulation revealed 148 of 161 nerves to be functional; these were subsequently transferred. In patients with preoperative ipsilateral phrenic nerve palsy, the risk of increased complications was marginally significant. Conclusions Brachial plexus reconstruction using intercostal nerves can be challenging, especially if there is antecedent chest wall trauma. Complications were associated with increasing numbers of intercostal nerves transferred. Ipsilateral rib fracture was adversely associated with intercostal nerve viability; it was not significantly associated with complication risk and should not be considered a contraindication to transfer. Preoperative phrenic nerve palsy was marginally associated with the likelihood of complications but not postoperative respiratory dysfunction when associated with intercostal nerve transfer. (J Hand Surg 2010;35A:1995–2000. Copyright © 2010 by the American Society for Surgery of the Hand. All rights reserved.) Type of study/level of evidence Therapeutic IV. Key words Brachial plexus, intercostal nerve, nerve transfer, neurotization, complications.
From the Mayo Clinic College of Medicine; the Department of Orthopaedic Surgery, Division of Hand Surgery; the Department of Statistics; and the Department of Neurological and Orthopaedic Surgery, Mayo Clinic, Rochester, MN. Received for publication December 14, 2009; accepted in revised form September 13, 2010.
Corresponding author: Alexander Y. Shin, MD, Mayo Clinic E14A, 200 First Street SW, Rochester, MN 55905; e-mail: [email protected]. 0363-5023/10/35A12-0013$36.00/0 doi:10.1016/j.jhsa.2010.09.013
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
© ASSH 䉬 Published by Elsevier, Inc. All rights reserved. 䉬 1995
1996
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
injuries are devastating events frequently resulting in severe functional impairment. The multiple nerve root avulsions common in such cases limit reconstructive options. Refinement of direct nerve transfers and development of advanced microsurgical techniques have improved outcomes in recent years. Intercostal nerve (ICN) transfers have become a mainstay treatment for reconstructing the brachial plexus since Seddon’s initial description in 19631 and the subsequent work of others.2–12 Their extraplexal origin and proximity to the infraclavicular plexus makes them an excellent source of viable motor and sensory nerves.13 The minimal motor and sensory functional loss resulting from their use provides additional incentive to consider their use. A tremendous volume of publications regarding the outcomes of these procedure can be found in the current literature.3,5,6,8,11,12,14 Information is scarce regarding the effect of chest wall trauma on ICN availability and occurrence of perioperative ICN harvest complications. Some authors have suggested that the presence of rib fractures is a contraindication to intercostal nerve use of that rib.15,16 The purposes of this study were to report our experience with perioperative ICN harvest complications and to determine whether chest wall trauma is associated with damaged or nonviable intercostal nerves.
T
RAUMATIC BRACHIAL PLEXUS
MATERIALS AND METHODS We conducted a retrospective review to identify all patients who underwent ICN transfer as part of a brachial plexus reconstruction for injury between 1989 and 2007. We excluded obstetrical brachial plexus palsy patients from the study. After obtaining approval from our institutional review board, we identified 153 consecutive patients. Information regarding patient demographics, mechanism of injury, associated injuries, intercostal nerve transfer procedure performed, intercostal nerve viability, and complications was evaluated. The technique of ICN transfer used at our institution is similar to that described previously in the literature.16 Between 1989 and 2007, 153 patients underwent ICN transfer; 136 patients were male and 17 were female. The mean age at the time of surgery was 27 ⫾ 11 years (range, 6 – 65 y). The mechanism of injury involved motorcycle accidents in 51 patients, motor vehicle accidents in 43 patients, snowmobile/all-terrain vehicle accidents in 41 patients, and miscellaneous mechanisms in 18 patients. The right side was involved in 87 cases. The majority of patients had extensive nerve avulsion injuries, with 91 having 3 to 5 avulsions, 44 having 2 avulsions, and 18 with no or one avulsion.
TABLE 1. Associated Organ System Dysfunction in Brachial Plexus Injury Patients Organ System
No. (%)
Appendicular bone/soft tissue injury
124 (81)
Craniofacial trauma
55 (36)
Ipsilateral rib fractures
50 (33)
Lung parenchymal injury
33 (21)
Appendicular vascular injury
22 (14)
Intra-abdominal injury
17 (11)
Phrenic nerve palsy
16 (10)
Injuries involving multiple organ systems were extremely common in our patient cohort. The most common injuries associated with the traumatic brachial plexus lesions were appendicular fractures, seen in 124 patients. Fifty patients had ipsilateral rib fractures. A total of 33 patients had a previous lung injury (hemothorax, hemopneumothorax, pneumothorax, etc.). Table 1 lists the remaining associated organ system injuries. The median duration of time from injury to surgical intervention was 6 months (range, 3–120 mo). The most common application in our cohort of patients was biceps reanimation, which was performed in 67 patients. This transfer was only performed for injuries that occurred less than 12 months before surgery. We used intercostal motor nerves for combined biceps and freefunctioning gracilis muscle transfer in 37 patients and gracilis innervation alone in 31 patients. The remaining 18 patients underwent various combinations of biceps and/or gracilis neurotization procedures along with transfer to other sources as indicated by dysfunction. The ICNs transferred included the second through seventh intercostals, with most being from the third through sixth intercostals. A total of 459 motor nerves were harvested in this cohort. In most surgical procedures, 2 to 4 ICNs were transferred for motor reconstruction (94% of the cohort). In addition, we used the sensory portions of the transferred ICNs in an attempt to restore protective sensation to the injured extremity 134 patients (88%). Complications were documented through review of the extensive patient medical record. All iatrogenic pleural tears were noted in the surgical reports and confirmed with review of postoperative chest radiographs showing small pneumothoraces and chest tube placement. Postoperative respiratory dysfunction was noted in clinical and intensive care unit documentation. Acute respiratory distress syndrome was documented clinically with the development of progressive tachy-
JHS 䉬 Vol A, December
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
TABLE 2. Complications of ICN Transfer for Traumatic Brachial Plexus Reconstruction Complication
No. (%)
Overall
23 (15)
Iatrogenic pleural tear
14 (9)
Superficial wound infection
3 (2)
Symptomatic pleural effusion
2 (1)
Acute respiratory distress syndrome
2 (1)
Subcutaneous wound seroma
2 (1)
pnea, decreased oxygenation, and increased oxygen dependence. It was confirmed by arterial blood gas and chest x-ray showing the development of bilateral alveolar infiltrates. Symptomatic pleural effusions were also suspected clinically and confirmed by chest radiographs. Patients and nerves are described using mean ⫾ standard deviation, median (range), or count (percentage) as appropriate. We used Fisher’s exact test to assess associations between complications (any or specifically respiratory) and phrenic nerve palsy or rib fracture. When appropriate owing to few complications, 95% exact binomial confidence intervals were also calculated. We used univariate logistic regression to assess the association between having complications and the number of nerves transferred. All statistical tests were 2-sided, and p values less than .05 were considered statistically significant. We used SAS version 9.1 (SAS Institute, Inc., Cary, NC) for all analyses. RESULTS Perioperative complications occurred in 23 of 153 patients (Table 2). The most common complication was an iatrogenic pleural tear during nerve elevation, which occurred in 14 of 153 patients. Treatment in all patients consisted of a small chest tube placed in the operating room. Chest tube duration ranged from 2 to 7 days (average, 3 d). All of our chest tubes were managed by our thoracic surgery colleagues. In 2 patients, symptomatic postoperative pleural effusions required prolonged intensive care unit stays with therapeutic pleurocentesis. Two patients developed acute respiratory distress syndrome requiring prolonged intubation (1–3 d). All 4 patients responded to aggressive pulmonary management and supportive care with no long-term sequelae. Other more minor complications including superficial wound infections and subcutaneous wound seroma formation were infrequent, occurring in 3 and 2 patients, respectively. Complication fre-
1997
quency increased as the number of ICNs harvested increased, with higher percentages found in those with 4 or greater at the time of surgery (Fig. 1). Having an additional nerve transferred was associated with 2.49 times the odds of having a complication (p ⬍ .001). In patients with previously fractured ipsilateral ribs, 161 nerves were transferred in 50 patients. Among rib fracture patients, 45 of 50 did not have complications, whereas among non–rib fracture patients, 85 of 103 did not have complications. This association was not statistically significant (p ⫽ .33). There was, however, a significant association between the presence of rib fractures and nerve viability (p ⬍ .001). In those 103 patients without rib fractures, all patients were found to have usable nerves at time of transfer (95% confidence interval, 0%–3.5%). In comparison, in those 50 patients with associated rib fractures, 6 patients had unusable nerves owing to rib fracture (95% confidence interval, 4.5%–24.3%). For all ICN transfers, 446 of 459 were viable intraoperatively by direct nerve stimulation and underwent successful transfer. All 13 nonviable nerves were in patients with rib fractures; therefore, 92% of ICNs transferred in rib fracture patients were viable intraoperatively. In the 16 patients with ipsilateral phrenic nerve palsy, 50 intercostal nerves were transferred. Among patients with phrenic nerve injuries, 5 of 16 had complications, whereas among nonphrenic injury patients 18 of 137 had complications. This association was marginally statistically significant (p ⫽ .07). Looking more closely at respiratory outcomes, 1 of the 16 phrenic nerve injury patients developed postoperative pleural effusion. In contrast, the overall rate of respiratory dysfunction in those with intact phrenic nerve function was 3 of 138, in the form of adult respiratory distress syndrome (2) and symptomatic pleural effusions requiring pleurocentesis (1). The association of phrenic nerve injury and respiratory complications was not statistically significant (p ⫽ .36). DISCUSSION Brachial plexus reconstruction with ICNs following injury can be challenging, especially if there is antecedent trauma to the chest wall. Despite numerous publications on the outcome of ICN transfers, little attention has been given to the perioperative complications of intercostal transfer or to identification of factors affecting ICN viability. We observed an overall 15% complication rate in the acute perioperative period. Wahegaonkar et al.16 noted that complications in brachial plexus surgical procedures are rare with proper surgical
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FIGURE 1: Occurrence of complications with respect to the number of ICNs harvested.
technique and meticulous dissection. The most common complication in their study was seroma formation (not quantified). They also noted 2 patients who experienced iatrogenic pneumothorax and were treated with defect closure, chest tube placement, and positive pressure ventilation. Our study population represented a cohort of patients for whom nerve transfer procedures are generally performed. Most of our patients underwent intercostal nerve transfer owing to multiple nerve root avulsion injuries confirmed by computed tomography myelography, electrodiagnostic studies, and clinical examination.17–19 These patients all had absence of clinical or electrical recovery or injuries that made spontaneous recovery impossible. Most patients also had nerve transfers performed to restore elbow flexion. This was performed mostly by either transfer to the musculocutaneous nerve,2,3,6,8,11,12,20 –26 innervation of a gracilis free-functioning muscle transfer,10,27–33 or a combination of the two. The mechanisms of injury in most of our patients were similar to those normally found in patients with this type of injury, in that they were mainly high-energy in nature,34,35 most commonly motorcycle accidents. The magnitude of force imparted to the body at the time of these events tended to cause damage to multiple organ systems. We found that as-
sociated organ system injuries were extremely common in our patient population and we were able to quantify these frequencies. Previous studies have claimed ipsilateral rib fracture and ipsilateral phrenic nerve palsy as contraindications to ICN transfers.15,16 Concern with ICN transfer in these patients has been with damage of the nerves owing to the chest wall trauma and fracture. One third of our patient population had associated rib fractures. Despite the associated chest wall trauma, nerve transfer using ICN was successful in 92% of these patients, as documented intraoperatively via nerve stimulation testing. Preoperative phrenic nerve palsy has also been recommended as a contraindication to ICN transfer owing to the presumed increase in respiratory dysfunction after surgery. We found an almost 3-fold increase in the rate of respiratory compromise in patients with preoperative phrenic nerve palsy compared with those without; however, this finding was not statistically significant. The small amount of patients with this complication makes statistical analysis difficult and a future study with increased power would be needed to attempt to detect a significant difference. This is relevant in the preoperative consent process for our patients, but the benefit of ICN transfer on postoperative function has brought us to conclude that it remains a reasonable
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option in our reconstructive armamentarium. These findings would challenge the current dogma that ICN transfer is not an option in these 2 patient groups. Most of the current literature on postoperative respiratory complications after ICN transfer shows minimal clinical effect of respiratory function. Krakauer and Wood8 in 1994 found that 4 of 12 patients had mild decline in objective pulmonary function testing without subjective deficiency. Numerous other studies have found no clinical decrease in respiratory function.22,36 Chalidapong et al.4 noted that objective pulmonary function study results were only notably reduced for 2 weeks and all normalized within 3 months. Close evaluation of the cases with postoperative respiratory dysfunction as well as iatrogenic pleural tear revealed that 74% of these complications occurred when 4 or more ICNs were used for transfer. Increased complications coincided with increasing complexity of reconstructions that were being undertaken using increasing numbers of ICNs. The limitations of this study include the fact that we retrospectively gathered data on complications. This may have underestimated the overall number of complications as a result of failure to document at the time the complication occurred or because of missed perioperative complications. The aggressive nature of our treatment of pleural tears with chest tube placement could also be argued as unnecessary. The prophylactic use of chest tubes after iatrogenic pleural tearing and subsequent repair remains controversial, with most recent thoracic surgery literature supporting primary closure without the need for chest tube placement.37,38 The invasiveness of the treatment strategy for dealing with intraoperative iatrogenic pleural injury has been an ongoing discussion at our institution, involving not only the brachial plexus service but also our thoracic surgery and anesthesia colleagues. Our decision to insert a small chest tube into the pleural defect at the time of surgery involved concern over the lack of intraoperative feedback over whether a pneumothorax had occurred owing to the protective positive pressure ventilation and the concern that if a pneumothorax or a large amount of fluid accumulation was present, subsequent return to surgery for chest tube placement or bedside placement would place our ICN transfers at tremendous risk for injury. In addition, owing to the complex nature of the procedures being performed, our patients required lengthy hospitalizations. Most patients with pleural tears (12 of 14) also underwent free-functioning gracilis muscle transfer at the time of ICN transfer and required 4 to 6 days of hospitalization because of close vascular
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monitoring of the muscle, similar to that of patients without chest tubes. Based on these results, a surgeon performing brachial plexus reconstructive surgery should be able to more accurately discuss with patients the potential complications and likely viability of ICNs for planned transfer. We have found this information to be useful in our practice when counseling patients and performing informed consent discussions before complex reconstructive procedures. REFERENCES 1. Seddon HJ. Nerve grafting. J Bone Joint Surg 1963;45B:447– 461. 2. El-Gammal TA, Fathi NA. Outcomes of surgical treatment of brachial plexus injuries using nerve grafting and nerve transfers. J Reconstr Microsurg 2002;18:7–15. 3. Merrell GA, Barric KA, Katz DL, Wolfe SW. Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature. J Hand Surg 2001;26A:303–314. 4. Chalidapong P, Sananpanich K, Kraisarin J, Bumroongkit C. Pulmonary and biceps function after intercostal and phrenic nerve transfer for brachial plexus injuries. J Hand Surg 2004;29B:8 –11. 5. Samardzic M, Rasulich L, Grujicic D, Milicic B. Results of nerve transfers to the musculocutaneous and axillary nerves. Neurosurgery 2000;46:93–103. 6. Malessy MJ, Thomeer RT. Evaluation of intercostal to musculocutaneous nerve transfer in reconstructive brachial plexus surgery. J Neurosurg 1998;88:266 –271. 7. Doi K, Shigetomi M, Kaneko K, Soo-Heong T, Hiura Y, Hattori Y, et al. Significance of elbow extension in reconstruction of prehension with reinnervated free-muscle transfer following complete brachial plexus avulsion. Plast Reconstr Surg 1997;100:364 –374. 8. Krakauer JD, Wood MB. Intercostal nerve transfer for brachial plexopathy. J Hand Surg 1994;19A:829 – 835. 9. Narakas AO, Hentz VR. Neurotization in brachial plexus injuries. Indication and results. Clin Orthop Relat Res 1988;237:43–56. 10. Doi K, Sakai K, Kuwata N, Ihara K, Kawai S. Reconstruction of finger and elbow function after complete avulsion of the brachial plexus. J Hand Surg 1991;16A:796 – 803. 11. Chuang DC, Yeh MC, Wei FC. Intercostal nerve transfer of the musculocutaneous nerve in avulsed brachial plexus injuries: evaluation of 66 patients. J Hand Surg 1992;17A:822– 828. 12. Nagano A, Ochiai N, Okinaga S. Restoration of elbow flexion in root lesions of brachial plexus injuries. J Hand Surg 1992;17A:815– 821. 13. Wood MB, Murray PM. Heterotopic nerve transfers: recent trends with expanding indication. J Hand Surg 2007;32A:397– 408. 14. Samardzic M, Grujicic D, Antunovic V. Nerve transfer in brachial plexus traction injuries. J Neurosurg 1992;76:191–197. 15. Ruch DS, Friedman A, Nunley JA. The restoration of elbow flexion with intercostal nerve transfers. Clin Orthop Relat Res 1995;314: 95–103. 16. Wahegaonkar AL, Doi K, Hattori Y, Addosooki AI. Technique of intercostal nerve harvest and transfer for various neurotization procedures in brachial plexus injuries. Tech Hand Up Extrem Surg 2007;11:184 –194. 17. Walker AT, Chaloupka JC, deLotbiniere AC, Wolfe SW, Goldman R, Kier EL. Detection of nerve rootlet avulsion on CT myelography in patients with birth palsy and brachial plexus injury after trauma. AJR Am J Roentgenol 1996;167:1283–1287. 18. Nagano A, Ochiai N, Sugioka H, Hara T, Tsuyama N. Usefulness of myelography in brachial plexus injuries. J Hand Surg 1989;14B:59 – 64. 19. Carvalho GA, Nikkhah G, Matties C, Penkart G, Samii M. Diagnosis of root avulsions in traumatic brachial plexus injuries: value of
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2000
20.
21.
22.
23. 24. 25. 26.
27.
28.
COMPLICATIONS OF INTERCOSTAL NERVE HARVEST
computerized tomography myelography and magnetic resonance imaging. J Neurosurg 1997;86:69 –76. Minami M, Ishii S. Satisfactory elbow flexion in complete (preganglionic) brachial plexus injuries: produced by suture of third and fourth intercostal nerves to musculocutaneous nerve. J Hand Surg 1987;12A:1114 –1118. Akasaka Y, Hara T, Takahashi M. Restoration of elbow flexion and wrist extension in brachial plexus paralyses by means of free muscle transplantation innervated by intercostal nerve. Ann Chir Main Memb Super 1990;9:341–350. Waikakul S, Wongtragul S, Vanadurongwan V. Restoration of elbow flexion in brachial plexus avulsion injury: comparing spinal accessory nerve transfer with intercostal nerve transfer. J Hand Surg 1999;24A:571–577. Nagano A. Intercostal nerve transfer for elbow flexion. Tech Hand Up Extrem Surg 2001;5:136 –140. Nagano A. Treatment of brachial plexus injury. J Orthop Sci 1998; 3:71– 80. Chuang DC. Neurotization procedures for brachial plexus injuries. Hand Clin 1995;11:633– 645. Chuang DC, Epstein MO, Yeh MC, Wei FC. Functional restoration of elbow flexion in brachial plexus injuries: results in 167 patients (excluding obstetric brachial plexus injury). J Hand Surg 1993;18A: 285–291. Doi K, Sakai K, Kuwata N, Ihara K, Kawai S. Double free-muscle transfer to restore prehension following complete brachial plexus avulsion. J Hand Surg 1995;20A:408 – 414. Doi K, Kuwata N, Muramatsu K, Hattori Y, Kawai S. Double muscle
29.
30. 31. 32.
33.
34. 35. 36.
37. 38.
transfer for upper extremity reconstruction following complete avulsion of the brachial plexus. Hand Clin 1999;15:757–767. Doi K, Hattori Y, Kuwata N, Soo-heong T, Kawakami F, Otuka K, et al. Free muscle transfer can restore hand function after injuries of the lower brachial plexus. J Bone Joint Surg 1998;80B:117–120. Chuang D. Functioning free muscle transplantation for brachial plexus injury. Clin Orthop Relat Res 1995;314:104 –111. Berger A, Flory PJ, Schaller E. Muscle transfers in brachial plexus lesions. J Reconstr Microsurg 1990;6:113–116. Barrie KA, Steinmann SP, Shin AY, Spinner RJ, Bishop AT. Gracilis free muscle transfer for restoration of function after complete brachial plexus avulsion. Neurosurg Focus 2004;16:1– 8. Doi K, Muramatsu K, Hattori Y, Otsuka K, Tan SH, Nanda V. Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexus. Indications and long-term results. J Bone Joint Surg 2000;82A:652– 666. Midha R. Epidemiology of brachial plexus injuries in a multitrauma population. Neurosurgery 1997;40:1182–1189. Narakas AO. The treatment of brachial plexus injuries. Int Orthop 1985;9:29 –36. Giddins GE, Kakkar N, Altree J, Birch R. The effect of unilateral intercostal nerve transfer upon lung function. J Hand Surg 1995; 20B:675– 676. Gordon CE, Feller-Kopman D, Balk EM, Smetana GW. Pneumothorax following thoracentesis. Arch Intern Med 2010;170:332–339. Luckraz H, Rammohan KS, Phillips M, Abel R, Karthikeyan S, Kulatilake NE, et al. Is an intercostal chest drain necessary after video-assisted thoracoscopic (VATS) lung biopsy? Ann Thorac Surg 2007;84:237–239.
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