Accepted Manuscript Letter to the Editor Unusual ultrasonographic findings after nerve trauma explained by MartinGruber anastomosis Z. Arányi, J. Böhm PII: DOI: Reference:
S1388-2457(14)00292-2 http://dx.doi.org/10.1016/j.clinph.2014.05.017 CLINPH 2007114
To appear in:
Clinical Neurophysiology
Accepted Date:
17 May 2014
Please cite this article as: Arányi, Z., Böhm, J., Unusual ultrasonographic findings after nerve trauma explained by Martin-Gruber anastomosis, Clinical Neurophysiology (2014), doi: http://dx.doi.org/10.1016/j.clinph.2014.05.017
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Unusual ultrasonographic findings after nerve trauma explained by Martin-Gruber anastomosis Arányi Z1, Böhm J2 1
MTA-SE NAP B Peripheral Nervous System Research Group, Dept. of Neurology,
Semmelweis University, Budapest, Hungary 2
Dept. of Neurology, Freiberg County Hospital, Freiberg, Germany
Corresponding author: Zsuzsanna Arányi, MD, Ph.D. Department of Neurology, Semmelweis University Balassa u. 6., Budapest, Hungary-1083 Tel: +36-20-825-0357 Fax: +36-1-210-1368 E-mail: [email protected]
1
High resolution ultrasonography (HRUS) is a valuable tool in the assessment of nerve trauma, adding complementary information to electrophysiological findings (Kopf et al., 2011; Padua et al., 2013). For example, it can differentiate between complete axonotmesis and neurotmesis in the acute setting or it can detect neuroma formation following a nerve suture, indicating suture failure at an earlier time point compared to the usually long time interval needed to judge signs of reinnervation. Furthermore, HRUS is also able to detect ʻneuromas-in-continuity’ within intact nerves. Neuroma formation indicates an unsuccessful attempt of the nerve to re-establish nerve continuity (Sunderland, 1990). After disruption of the whole nerve or some of its fascicles, sprouting of axons and Schwann cells occurs at the proximal site of injury. This turns into an overgrowth of nerve tissue intermingled with fibrous tissue, called neuroma, in the event regenerating axons do not have a pathway (i.e. discontinuous fascicular or nerve sheath in Sunderland Grade 4 and 5 injury) to reach their distal target. Stump or terminal neuroma forms on the proximal nerve stump after complete transection of the nerve (Sunderland Grade 5 injury), whereas ‘neuromas-in-continuity’ develop within nerves with intact epineurium when only some of the nerve fascicles suffer disruption (Sunderland Grade 4 injury), for example in traction (stretch) injuries. We present a case where ‘neuromas-in-continuity’ are observed in the ulnar nerve, despite the complete transection of the nerve at a more proximal level. This was a surprising finding, as neuromas can only develop from axons connected to the body of the neuron. The 41-year-old male patient suffered an occupational injury of the right arm by a rotating wire that caused both severe laceration of soft tissues above the elbow and considerable traction of the arm. No direct injury or compression occurred at the level of the forearm. Complete transection of the ulnar nerve was noted above the elbow, for which primary nerve suture was done and the other injuries were also attended to. Five months after the suture, clinical and electrophysiological assessment showed complete denervation of muscles supplied
2
by the ulnar nerve, which was the expected finding at this time point. The radial nerve showed signs of marked distal axonal loss, but continuity was preserved, and the median nerve showed a mild degree of axonal loss. Ultrasonography (Philips HD15 device, 5-12 MHz linear array transducer) of upper limb nerves was then performed. On the posterior interosseus nerve, the motor branch of the radial nerve, a hypoechoic focal fusiform enlargement with deranged fascicular structure was seen just proximal to its entry into the supinator muscle (Fig. 1C). On the median nerve, a similar lesion was seen at the proximal forearm, under the pronator muscle (Fig. 1B). Concerning the ulnar nerve, two types of lesions were noted: 1. A large stump neuroma (cross-sectional area [CSA]: 100 mm2 ) was seen at the proximal side of the suture just above the medial epicondyle (Fig. 1D). Although the thin distal stump was seen apposed to the neuroma, neuroma formation indicated an unsuccessful suture. 2. Scanning further distally on the forearm, two sites of marked focal enlargement and abnormal structure were noted, one 10 cm proximal to the wrist extending 8 cm in length (CSA: 33.4 mm2) (Fig. 1A), the other on the proximal forearm, extending 2 cm in length (CSA: 27.1 mm2 ). On cross-sectional scan, the individual enlarged fascicles of mixed echogenicity are recognisable, and their appearance are strikingly similar to that of the stump neuroma above the elbow (Fig. 1D). The epineurium was continuous. Other segments of the nerve up to the elbow exhibited normal fascicular nerve structure, including the segment in between the two forearm lesions. The focal lesions seen on the ulnar nerve on the forearm are believed to be ‘neuromasin-continuity’ resulting from the stretch injury associated with the severe traction of the arm at the time of accident (Sunderland Grade 4 injury). This is supported by the following arguments: (a) no direct trauma or compression affected the forearm; (b) focal abnormalities due to stretch injury were demonstrated on the radial and median nerves as well both by electrophysiology and ultrasound; these lesions may reflect focal scarring (Sunderland Grade 3 injury) or ‘neuromas-in-continuity’ (Sunderland Grade 4 injury); (c) the forearm lesions of the ulnar nerve were strikingly similar in appearance to the stump neuroma of the ulnar nerve above the elbow
3
(Fig. 1D). The presence of traction neuromas distal to the complete transection of the ulnar nerve came as a surprise, as theoretically no axons would be left for neuroma formation. Regenerating axons are also not to be expected yet on the distal forearm at this time point, but apart from this, the presence of the large proximal stump neuroma most certainly precludes any regenerating axons reaching the forearm. Therefore, the only possible explanation for this finding is the presence of a Martin-Gruber anastomosis (MGA), which is a cross-over of median-to-ulnar motor nerve fibres on the forearm, present in 15-30% of individuals either unilaterally or bilaterally (Lee et al., 2005; Cho et al., 2013). In other words, some ulnar nerve fibres descend with the median nerve and reach the ulnar nerve only at the level of the forearm, which fibres are spared in case of a proximal ulnar nerve injury. In our patient, MGA would explain the presence of axons on the forearm unaffected by the proximal transection, which however in their turn suffered a stretch injury. It appears that in this patient the complete ulnar nerve lesion is the combined effect of two different lesions: nerve transection above the elbow and stretch injury of remaining anastomotic fibres on the forearm. Given the complete denervation of all the ulnar nerve innervated small hand muscles, electrophysiological proof of MGA could not be obtained on the affected side. Although type 1 MGA (involving the abductor digiti minimi muscle) was demonstrated on the normal left side, this is not a proof of MGA on the contralateral side. The ultrasonographic identification of anastomotic fibres is also not feasible due to their small size. Thus, the presence of MGA was inferred alone from these unusual ultrasonographic findings following nerve trauma. The patient was followed up one year after the initial assessment. Two months before this second assessment, the ulnar nerve suture above the elbow was re-operated with graft implantation. Electrophysiologic assessment showed improvement in radial and median nerve function, the ulnar nerve still showed complete axonotmesis. Ultrasonographic findings of all three nerves on the forearm were identical to the initial assessment, and unfortunately stump neuroma formation was seen again at the proximal suture of the nerve graft.
4
HRUS of peripheral nerves may provide valuable complementary information in nerve traumas, such as the detection of neuroma formation. As observed in our case, it may also reveal unusual findings such as “double injury” of a nerve and may indirectly suggest the presence of an innervation anomaly.
Conflict of interest None declared.
Acknowledgments Zsuzsanna Arányi was supported by the National Brain Research Program (NAP B) of the Hungarian government.
5
References Cho NS, Kim DH, Kim MY, Park BK. Electrophysiological and ultrasonographic findings in ulnar neuropathy with Martin-Gruber anastomosis. Muscle Nerve 2013; 47:604–607. Kopf H, Loizides A, Mostbeck GH, Gruber H. Diagnostic sonography of peripheral nerves: indications, examination techniques and pathological findings. Ultraschall Med 2011; 32:242263. Lee KS, Oh CS, Chung IH, Sunwoo I. An anatomic study of the Martin-Gruber anastomosis: electrodiagnostic implications. Muscle Nerve 2005; 31:95-97. Padua L, Di Pasquale A, Liotta G, Granata G, Pazzaglia C, Erra C et al. Ultrasound as a useful tool in the diagnosis and management of traumatic nerve lesions. Clin Neurophysiol 2013; 124:1237-1243. Sunderland S. The anatomy and physiology of nerve injury. Muscle Nerve 1990; 13:771-784.
6
Figure Legend
Figure 1 A. Longitudinal ultrasound scan of the ulnar nerve on the distal forearm. B. Longitudinal ultrasound scan of the median nerve in the pronator area. C. Longitudinal ultrasound scan of the posterior interosseus nerve just proximal to its entry into the supinator muscle. D. Left image: Cross-sectional scan of the ulnar nerve on the distal forearm. Right image: Cross-sectional scan of the stump (suture) neuroma of the ulnar nerve above the elbow On the longitudinal scans, note the hypoechoic fusiform enlargements on the nerves as a result of stretch injury. On cross-sectional scan of this lesion of the ulnar nerve, the abnormal, swollen, individual fascicles are recognisable and have a remarkably similar appearance to the proximal stump neuroma, suggestive of ‘neuroma-in-continuity’ due to traction.
7
Fig. 1.
8
S1388-2457(14)00292-2 http://dx.doi.org/10.1016/j.clinph.2014.05.017 CLINPH 2007114
To appear in:
Clinical Neurophysiology
Accepted Date:
17 May 2014
Please cite this article as: Arányi, Z., Böhm, J., Unusual ultrasonographic findings after nerve trauma explained by Martin-Gruber anastomosis, Clinical Neurophysiology (2014), doi: http://dx.doi.org/10.1016/j.clinph.2014.05.017
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Unusual ultrasonographic findings after nerve trauma explained by Martin-Gruber anastomosis Arányi Z1, Böhm J2 1
MTA-SE NAP B Peripheral Nervous System Research Group, Dept. of Neurology,
Semmelweis University, Budapest, Hungary 2
Dept. of Neurology, Freiberg County Hospital, Freiberg, Germany
Corresponding author: Zsuzsanna Arányi, MD, Ph.D. Department of Neurology, Semmelweis University Balassa u. 6., Budapest, Hungary-1083 Tel: +36-20-825-0357 Fax: +36-1-210-1368 E-mail: [email protected]
1
High resolution ultrasonography (HRUS) is a valuable tool in the assessment of nerve trauma, adding complementary information to electrophysiological findings (Kopf et al., 2011; Padua et al., 2013). For example, it can differentiate between complete axonotmesis and neurotmesis in the acute setting or it can detect neuroma formation following a nerve suture, indicating suture failure at an earlier time point compared to the usually long time interval needed to judge signs of reinnervation. Furthermore, HRUS is also able to detect ʻneuromas-in-continuity’ within intact nerves. Neuroma formation indicates an unsuccessful attempt of the nerve to re-establish nerve continuity (Sunderland, 1990). After disruption of the whole nerve or some of its fascicles, sprouting of axons and Schwann cells occurs at the proximal site of injury. This turns into an overgrowth of nerve tissue intermingled with fibrous tissue, called neuroma, in the event regenerating axons do not have a pathway (i.e. discontinuous fascicular or nerve sheath in Sunderland Grade 4 and 5 injury) to reach their distal target. Stump or terminal neuroma forms on the proximal nerve stump after complete transection of the nerve (Sunderland Grade 5 injury), whereas ‘neuromas-in-continuity’ develop within nerves with intact epineurium when only some of the nerve fascicles suffer disruption (Sunderland Grade 4 injury), for example in traction (stretch) injuries. We present a case where ‘neuromas-in-continuity’ are observed in the ulnar nerve, despite the complete transection of the nerve at a more proximal level. This was a surprising finding, as neuromas can only develop from axons connected to the body of the neuron. The 41-year-old male patient suffered an occupational injury of the right arm by a rotating wire that caused both severe laceration of soft tissues above the elbow and considerable traction of the arm. No direct injury or compression occurred at the level of the forearm. Complete transection of the ulnar nerve was noted above the elbow, for which primary nerve suture was done and the other injuries were also attended to. Five months after the suture, clinical and electrophysiological assessment showed complete denervation of muscles supplied
2
by the ulnar nerve, which was the expected finding at this time point. The radial nerve showed signs of marked distal axonal loss, but continuity was preserved, and the median nerve showed a mild degree of axonal loss. Ultrasonography (Philips HD15 device, 5-12 MHz linear array transducer) of upper limb nerves was then performed. On the posterior interosseus nerve, the motor branch of the radial nerve, a hypoechoic focal fusiform enlargement with deranged fascicular structure was seen just proximal to its entry into the supinator muscle (Fig. 1C). On the median nerve, a similar lesion was seen at the proximal forearm, under the pronator muscle (Fig. 1B). Concerning the ulnar nerve, two types of lesions were noted: 1. A large stump neuroma (cross-sectional area [CSA]: 100 mm2 ) was seen at the proximal side of the suture just above the medial epicondyle (Fig. 1D). Although the thin distal stump was seen apposed to the neuroma, neuroma formation indicated an unsuccessful suture. 2. Scanning further distally on the forearm, two sites of marked focal enlargement and abnormal structure were noted, one 10 cm proximal to the wrist extending 8 cm in length (CSA: 33.4 mm2) (Fig. 1A), the other on the proximal forearm, extending 2 cm in length (CSA: 27.1 mm2 ). On cross-sectional scan, the individual enlarged fascicles of mixed echogenicity are recognisable, and their appearance are strikingly similar to that of the stump neuroma above the elbow (Fig. 1D). The epineurium was continuous. Other segments of the nerve up to the elbow exhibited normal fascicular nerve structure, including the segment in between the two forearm lesions. The focal lesions seen on the ulnar nerve on the forearm are believed to be ‘neuromasin-continuity’ resulting from the stretch injury associated with the severe traction of the arm at the time of accident (Sunderland Grade 4 injury). This is supported by the following arguments: (a) no direct trauma or compression affected the forearm; (b) focal abnormalities due to stretch injury were demonstrated on the radial and median nerves as well both by electrophysiology and ultrasound; these lesions may reflect focal scarring (Sunderland Grade 3 injury) or ‘neuromas-in-continuity’ (Sunderland Grade 4 injury); (c) the forearm lesions of the ulnar nerve were strikingly similar in appearance to the stump neuroma of the ulnar nerve above the elbow
3
(Fig. 1D). The presence of traction neuromas distal to the complete transection of the ulnar nerve came as a surprise, as theoretically no axons would be left for neuroma formation. Regenerating axons are also not to be expected yet on the distal forearm at this time point, but apart from this, the presence of the large proximal stump neuroma most certainly precludes any regenerating axons reaching the forearm. Therefore, the only possible explanation for this finding is the presence of a Martin-Gruber anastomosis (MGA), which is a cross-over of median-to-ulnar motor nerve fibres on the forearm, present in 15-30% of individuals either unilaterally or bilaterally (Lee et al., 2005; Cho et al., 2013). In other words, some ulnar nerve fibres descend with the median nerve and reach the ulnar nerve only at the level of the forearm, which fibres are spared in case of a proximal ulnar nerve injury. In our patient, MGA would explain the presence of axons on the forearm unaffected by the proximal transection, which however in their turn suffered a stretch injury. It appears that in this patient the complete ulnar nerve lesion is the combined effect of two different lesions: nerve transection above the elbow and stretch injury of remaining anastomotic fibres on the forearm. Given the complete denervation of all the ulnar nerve innervated small hand muscles, electrophysiological proof of MGA could not be obtained on the affected side. Although type 1 MGA (involving the abductor digiti minimi muscle) was demonstrated on the normal left side, this is not a proof of MGA on the contralateral side. The ultrasonographic identification of anastomotic fibres is also not feasible due to their small size. Thus, the presence of MGA was inferred alone from these unusual ultrasonographic findings following nerve trauma. The patient was followed up one year after the initial assessment. Two months before this second assessment, the ulnar nerve suture above the elbow was re-operated with graft implantation. Electrophysiologic assessment showed improvement in radial and median nerve function, the ulnar nerve still showed complete axonotmesis. Ultrasonographic findings of all three nerves on the forearm were identical to the initial assessment, and unfortunately stump neuroma formation was seen again at the proximal suture of the nerve graft.
4
HRUS of peripheral nerves may provide valuable complementary information in nerve traumas, such as the detection of neuroma formation. As observed in our case, it may also reveal unusual findings such as “double injury” of a nerve and may indirectly suggest the presence of an innervation anomaly.
Conflict of interest None declared.
Acknowledgments Zsuzsanna Arányi was supported by the National Brain Research Program (NAP B) of the Hungarian government.
5
References Cho NS, Kim DH, Kim MY, Park BK. Electrophysiological and ultrasonographic findings in ulnar neuropathy with Martin-Gruber anastomosis. Muscle Nerve 2013; 47:604–607. Kopf H, Loizides A, Mostbeck GH, Gruber H. Diagnostic sonography of peripheral nerves: indications, examination techniques and pathological findings. Ultraschall Med 2011; 32:242263. Lee KS, Oh CS, Chung IH, Sunwoo I. An anatomic study of the Martin-Gruber anastomosis: electrodiagnostic implications. Muscle Nerve 2005; 31:95-97. Padua L, Di Pasquale A, Liotta G, Granata G, Pazzaglia C, Erra C et al. Ultrasound as a useful tool in the diagnosis and management of traumatic nerve lesions. Clin Neurophysiol 2013; 124:1237-1243. Sunderland S. The anatomy and physiology of nerve injury. Muscle Nerve 1990; 13:771-784.
6
Figure Legend
Figure 1 A. Longitudinal ultrasound scan of the ulnar nerve on the distal forearm. B. Longitudinal ultrasound scan of the median nerve in the pronator area. C. Longitudinal ultrasound scan of the posterior interosseus nerve just proximal to its entry into the supinator muscle. D. Left image: Cross-sectional scan of the ulnar nerve on the distal forearm. Right image: Cross-sectional scan of the stump (suture) neuroma of the ulnar nerve above the elbow On the longitudinal scans, note the hypoechoic fusiform enlargements on the nerves as a result of stretch injury. On cross-sectional scan of this lesion of the ulnar nerve, the abnormal, swollen, individual fascicles are recognisable and have a remarkably similar appearance to the proximal stump neuroma, suggestive of ‘neuroma-in-continuity’ due to traction.
7
Fig. 1.
8
