Early Electrophysiological Study of CC7 Transfer to Median Nerve and Deep Branch of Ulnar Nerve by Medial Antebrachial Cutaneous Nerve

Abstract

Background:

Due to the possibility of intrinsic muscle recovery, we modified the traditional contralateral cervical seventh (CC7) nerve transfer to repair both the median nerve and deep branch of the ulnar nerve (DBUN) for patients with total brachial plexus avulsion (TBPA).

Methods:

A retrospective comparative study of different CC7 transfers for patients with TBPA was carried out. The modified group (20 patients) had CC7 transfer to the median nerve and DBUN by ulnar nerve with vascular pedicle and medial antebrachial cutaneous nerve. The control group (20 patients) had traditional CC7 transfer to median nerve by ulnar nerve with vascular pedicle.

Results:

Motor unit potentials (MUPs) could be recorded in the abductor digiti minimi (ADM) and dorsal interosseous muscle in 5 and 2 patients, respectively, in the modified group, whereas nobody had MUP in the ADM or dorsal interosseous muscle in the control group. There was significant difference between the 2 groups in the recovery of MUPs in ADM. As for median nerve recovery, there were no statistical differences in the positive rates of MUPs in abductor pollicis brevis. No significant differences of compound motor action potential existed in flexor digitorum profundus of index finger or flexor carpi radialis between the 2 groups.

Conclusions:

From the perspective of electrophysiology, it was possible to regenerate intrinsic muscles using CC7 transfer to the median nerve and DBUN by pedicled ulnar nerve and medial antebrachial cutaneous nerve in patients with TBPA while not affecting the recovery of the median nerve.

Takeaways

Question: How can we maximize the recovery of intrinsic muscles for patients with total brachial plexus avulsion (TBPA)?

Findings: Some patients with TBPA had motor unit potential or compound motor action potential appearing in intrinsic muscles after contralateral cervical seventh nerve transfer to median nerve and deep branch of ulnar nerve.

Meaning: From the perspective of electrophysiology, it is possible to regenerate intrinsic muscles using contralateral cervical seventh nerve transfer to the median nerve and deep branch of the ulnar nerve in patients with TBPA.

INTRODUCTION

Posttraumatic brachial plexus injuries are devastating, as the brain and spinal cord are disconnected from the upper limb.¹ Management of brachial plexus injuries has changed radically in the past couple of decades, but treatment of patients with total brachial plexus palsy is still a major reconstructive challenge.² The main treatment options include phrenic nerve transfer,³ accessary nerve transfer,⁴ intercostal nerve transfer,⁵ and contralateral cervical seventh (CC7) nerve transfer.⁶ The functional improvements are mainly embodied in shoulder abduction and elbow flexion.⁷ However, the recoveries of intrinsic muscles are not satisfying,^8,9 particularly because motor end plates irreversibly degenerate before the regenerated ulnar nerve axons are able to reinnervate the intrinsic muscles of the hand.¹⁰ Wang et al¹¹ reported reinnervation of thenar muscle after repair of total brachial plexus avulsion (TBPA) with CC7 root transfer in 5 cases. This indicated that CC7 nerve transfer could make the abductor pollicis brevis (APB) muscles regenerate, which provided a possibility for the reconstruction of hand function after TBPA. Because the number of myelinated nerve fibers of the CC7 root is much more than that of any recipient nerve, some scholars tried to repair 2 recipient nerves simultaneously by CC7 transfer.^12–14 They found that both recipient nerves achieved recovery. Owing to the possibility of intrinsic muscle recovery, we modified the traditional CC7 nerve transfer to repair both the median nerve and deep branch of the ulnar nerve (DBUN) (Fig. 1). In the present study, we investigated the early electrophysiological recovery of the modified CC7 transfer in patients with TBPA.

Fig. 1.

The diagrammatic sketch of modified CC7 nerve transfer. A, CC7 transfer to ulnar nerve to median nerve and MACN. B, MACN transfer to DBUN.

METHODS

A retrospective review of patients treated with different CC7 nerve transfers after posttraumatic TBPA was carried out. The clinical study was reviewed and approved by the institutional review board of our hospital. The inclusion criteria were as follows: patients with total root avulsion and those who had undergone 4 nerve transfers, including phrenic nerve transfer to anterolateral bundles of the anterior division of the upper trunk, accessory nerve transfer to suprascapular nerve, intercostal nerve transfer to thoracodorsal nerve and triceps branch, and conventional or modified CC7 nerve transfer. The CC7 root was used to repair the median nerve separately or both the median nerve and DBUN. The exclusion criteria included patients with diabetes, Volkmann contracture, fracture on the affected limb, and brain trauma.

According to inclusion and exclusion criteria, 40 patients were enrolled: 20 patients in the modified group and 20 in the control group. All the patients were treated with 2-stage CC7 nerve transfers between 2018 and 2021.

Surgical Techniques

The First Stage of CC7 Transfer

Timing

It was performed 1 month after brachial plexus exploration, and phrenic and accessory nerve transfers in both groups.

Surgical Design

Control group

The ulnar nerve was cut at the transverse line of the wrist, including the DBUN, superficial branch (SB), and dorsal sensory branch (DSB). The vascularized ulnar nerve graft based on the superior ulnar collateral artery was harvested from the affected arm. The distal end of the ulnar nerve was delivered to the contralateral supraclavicular fossa through a subcutaneous tunnel and sutured to the whole CC7 nerve root under 2.5× magnification, using 8-0 microsuture, whereas the proximal part of ulnar nerve was intact to preserve blood supply of the ulnar nerve graft.

Modified group

The DBUN was separated from the SB and DSB from the wrist to forearm. When the DBUN was separated from the ulnar nerve, microseparation was carried out to minimize the disruption of blood supply in the DBUN, SB, and DSB to the greatest extent. The DBUN was freed as far as possible toward the proximal end of the forearm until it could not be separated from the main trunk of ulnar nerve microscopically. The medial antebrachial cutaneous nerve (MACN) was exposed and divided as distally as possible (Fig. 2A). The SB and DSB were cut at the transverse line of the wrist. The DBUN was cut proximally at the point where the branch emerged from the main trunk. Then the MACN was cut at its insertion point. The MACN was sutured to the DBUN under 2.5× magnification, using 8-0 microsuture (Fig. 2B). The vascularized ulnar nerve graft based on the superior ulnar collateral artery was harvested from the affected arm. Then the distal ends of the SB and DSB were delivered to the contralateral supraclavicular fossa through a subcutaneous tunnel and sutured to the whole CC7 root under 2.5× magnification, using 8-0 microsuture (Fig. 2C), whereas the proximal part of ulnar nerve was intact to preserve blood supply of the ulnar nerve graft.

Fig. 2.

Suturing the DBUN to the MACN and the CC7 to the SB and DSB. A, The DBUN (★) was separated from the SB () and DSB (♦) of the ulnar nerve from the wrist to forearm. The MACN (▲) was exposed. B, The distal ends of the SB () and DSB (♦) were cut off. The distal end of the MACN (▲) would be sutured to the proximal end of the DBUN (★). C, The distal ends of the SB () and DSB (♦) of the ulnar nerve were sutured to the whole CC7 root (●).

Every patient in each group was immobilized by a head and arm brace to keep the head from turning to the affected side for 1 month.

The Second Stage of CC7 Transfer

Timing

It was performed 6 months after the first stage of CC7 transfer in both groups.

Surgical Design

Control group

The ulnar and median nerves were exposed and cut off on the inner side of the upper arm near the axilla. The proximal end of the ulnar nerve, which connected to the CC7, was sutured to the distal end of the median nerve without tension under 2.5× magnification, using 8-0 microsuture.

Modified group

The MACN and ulnar and median nerves were identified and cut off near the retracing point of the ulnar nerve (Fig. 3A). The proximal end of the ulnar nerve, which connected to the CC7, was sutured to the distal ends of the MACN and median nerve without tension, under 2.5× magnification, using 8-0 microsuture (Fig. 3B).

Fig. 3.

Suturing the ulnar nerve to the MN and MACN. A, The UN (★), MACN (▲), and MN () were exposed near the axilla on the inner side of the upper arm. B, The proximal end of the UN (★) was sutured to the distal ends of the MACN (▲) and MN (). MN, median nerve; UN, ulnar nerve.

A sling was used to keep elbow flexion at 90 degrees for 1 month.

Postoperative Rehabilitation

Patients were advised to take neurotrophic drugs, which included vitamin B1, vitamin B6, and mecobalamin, after surgery. All drugs were taken orally 3 times a day, 1 tablet each time.

Physical exercise and electrostimulation therapy were started 4 weeks after the second stage of CC7 transfer. Patients in both the modified and control groups were instructed to do physical exercise and electrostimulation therapy.

Exercise Method

Wrist and finger flexion were tried in the affected limb while adducting the contralateral shoulder 1000 times a day.

Electrostimulation Therapy

Electrodes were put on the inner side of the affected upper arm near the axilla and thenar and hypothenar muscles for electrostimulation. Low-frequency stimulation of each target muscle area was performed twice a day, 20 minutes each time.

Evaluation

Electromyogram (EMG) examination was used to evaluate nerve regeneration. EMG showed the condition of nerve regeneration, which included compound motor action potential (CMAP), motor unit potential (MUP), and no MUP. An MUP shown by EMG was regarded as a muscle regeneration signal, and a CMAP was regarded as an effective recovery of motor function. No MUPs were shown in the intrinsic muscles, flexor digitorum profundus of the index finger (FDPI), or flexor carpi radialis (FCR) in the affected limb of the 2 groups before surgery.

Statistical Analysis

Comparisons between the modified and control groups were performed using the Fisher exact test. The P values were 2-tailed, and a P value of less than 0.05 was considered significant. All analyses were performed using the Statistical Package for the Social Sciences version 19.0 software.

RESULTS

In the modified group, 15 patients were men and 5 patients were women, with a mean age of 28.3 ± 10.1 years (range, 18–43 y) at the time of injury. Of these, 6 patients had an injury on the left side and 14 had an injury on the right side. The time from injury to surgery was 2–7 months (average 3.05 ± 1.73 mo). The mean follow-up period was 2.5 years (range, 2–2.9 y). In the control group, 17 patients were men and 3 patients were women, with a mean age of 30.2 ± 9.3 years (range, 19–50 y) at the time of injury. Of these, 8 patients had an injury on the left side and 12 had an injury on the right side. The time from injury to surgery was from 1 to 6 months (average 2.85 ± 1.53 mo). The mean follow-up period was 2.5 years (range, 2–3 y). There was no statistically significant difference in the general data between the 2 groups of patients (P > 0.05).

In the modified group, motorcycle accidents accounted for TBPA in 16 patients. Two patients had injuries following a fall from height. One patient had a machine traction injury. One patient experienced a shoulder injury due to a falling weight. In the control group, motorcycle accidents accounted for TBPA in 14 patients. Other road accidents included a pedestrian accident. Three patients had machine traction injuries in the upper limbs. One patient experienced a shoulder injury due to a falling weight, and 1 patient had injury following a fall from height.

When patients were followed up for at least 2 years after the second stage of CC7 transfer, EMG was performed.

As for the abductor digiti minimi (ADM), 5 patients in the modified group recorded MUP and 1 of them recorded CMAP after stimulating the DBUN at the wrist. No patient gained MUP in ADM in the control group. MUP was recorded in the dorsal interosseous muscle (DIM) in 2 patients in the modified group, and 1 of them had CMAP recorded in all DIMs. No MUP was recorded in the DIM in the control group.

For the APB, in the modified group, 5 patients had MUP recorded and 2 of them had CMAP recorded after stimulating the median nerve. In the control group, 4 patients had MUP recorded and 1 of them had CMAP recorded in the APB.

Table 1 shows that there was a statistically significant difference in the recovery of MUP in the ADM (P < 0.05), whereas there was no statistically significant difference in the recovery of MUP in the DIM or APB (P > 0.05).

Table 1.

Comparison of MUP/CMAP in Different Muscles Between 2 Groups

Muscle	APB		ADM		DIM		FDPI		FCR
Group	No MUP	MUP	No MUP	MUP	No MUP	MUP	CMAP	MUP	CMAP	MUP
Modified group	15	5	15	5	18	2	10	4	11	5
Conventional group	16	4	20	0	20	0	9	5	11	6
P	0.705		0.047		0.487		1.000	1.000	1.000	1.000

As for the FDPI, EMG showed CMAP appearing in 10 (50%) patients and MUP appearing in 4 patients in the modified group. Nine (45%) patients had CMAP and 5 patients had MUP in the control group. For the FCR, in the modified group, 11 (55%) patients had CMAP and 5 patients had MUP. In the control group, 11 (65%) patients had CMAP and 6 patients had MUP in the FCR. There were no statistical differences of CMAP in the FDPI or FCR between the 2 groups (P > 0.05).

The Video shows MUPs appearing in the ADM and the fourth DIM after modified CC7 nerve transfer. (See Video [online], in which MUPs appearing in the hypothenar muscle and the fourth DIM after the modified CC7 nerve transfer are shown.)

Video 1. Motor unit potentials (MUPs) appeared in hypothenar muscle and the fourth dorsal interosseous muscle (DIM) after modified CC7 nerve transfer.

Download video file ^{(57MB, mp4)}

All the muscle strengths were M0 in the affected limb preoperatively in the 2 groups. After surgery, as for the ADM, 1 patient had M3 recovery, 2 patients had M2 recovery, and 2 patients had M1 recovery in the modified group, whereas no patients had recovery in the control group. The APB recovered to M3 in 2 patients, M2 in 1 patient, and M1 in 1 patient in the modified group, which was the same as that in the control group. Ten patients’ FDPI and FCR strengths recovered to M3 or higher in the modified group, whereas 9 patients got M3 or higher in FDPI and FCR in the control group (Table 2).

Table 2.

Comparison of Muscle Strength in Different Muscles Between 2 Groups

	ADM		APB		FDPI		FCR
	Modified Group	Conventional Group	Modified Group	Conventional Group	Modified Group	Conventional Group	Modified Group	Conventional Group
M4	0	0	0	0	3	4	4	4
M3	1	0	2	2	7	5	6	5
M2	2	0	1	1	2	3	3	3
M1	2	0	1	1	2	2	2	2
M0	15	20	16	16	6	6	5	6

Compared with the British Medical Research Council grading system evaluation, electrophysiological results can reflect muscle regeneration earlier, more accurately and objectively, especially for intrinsic muscles.

Complication

A total of 40 patients experienced paresthesia on the thumb, index, and middle pulp of the donor hand within 3 months after the first stage of CC7 transfer, and the sensory deficit completely recovered spontaneously in all patients when they followed up.

DISCUSSION

Regarding TBPA, it was initially believed that there was no possibility of recovery in the intrinsic muscles of the hand until the report by Wang et al¹¹: of 32 patients with TBPA who had CC7 transfer to the median nerve, 5 showed reinnervation of thenar muscle. APB strength of grade M2 was found in 4 patients. The incomplete interference pattern in the APB was detected by EMG in 2 patients, and the minority MUP was detected in another 2 patients. The strength of the APB was M1 in 1 patient with EMG showing MUP. Subsequently, Yang et al¹⁵ reported that 53 of 95 patients with TBPA exhibited MUP recovery of the APB after CC7 nerve transfer. Otherwise, the conventional CC7 transfer uses the whole ulnar nerve in the affected limb to connect the CC7 with target nerves, which makes it impossible to reserve the affected ulnar nerve and loses the possibility of recovery in the intrinsic muscles innervated by the DBUN.

Most of the intrinsic muscles are innervated by the DBUN. If we reserve the DBUN and use the DSB, SB, and another nerve to connect the CC7 with the DBUN as a bridge, there is a possibility of intrinsic muscle recovery. Which nerve could be selected to connect the proximal end of the ulnar nerve and DBUN? The MACN is a good choice based on its location and length. Therefore, we designed a modified CC7 nerve transfer: CC7 → DSB + SB → median nerve + MACN → DBUN.

In the study, the modified CC7 transfer was compared with conventional CC7 transfer. The MUP of the ADM and DIM innervated by the DBUN appeared in 5 and 2 patients, respectively, in the modified group. However, there was no MUP present in the ADM or DIM in any patient in the control group, because the DUBN, SB, and DSB were used as bridging nerves. One patient had M3 recovery, 2 patients had M2 recovery, and 2 patients had M1 recovery in the ADM in the modified group, whereas no patients had muscle strength recovery in the ADM in the control group. This indicated that the modified CC7 transfer could regenerate the intrinsic muscles innervated by the DBUN. The APB, FDPI, and FCR were innervated by the median nerve. Both of the CC7 transfers were used to repair the median nerve. There were no statistical differences of MUP in the APB and CMAP in the FDPI or FCR between the 2 groups. The 2 groups also had similar recovery rates of muscle strength in the APB, FDPI, and FCR, which suggested that compared with CC7 transfer to the median nerve, CC7 transfer to both the median nerve and DBUN did not affect the recovery of the median nerve.

Compared with the conventional procedure, this modified procedure increased the exposure, separation, and anastomosis of the DBUN and MACN. The DBUN could generally be noninvasively separated to about 8 cm above the wrist. Although the distal end of the MACN in the forearm was not constant, it was generally located in the upper one-third of the forearm. Therefore, the DBUN required further invasive microseparation toward the proximal end for suturing with the MACN. Because the MACN at the proximal end of the upper arm was close to the inverted ulnar nerve, it was easy to suture the inverted ulnar nerve to the median nerve and MACN simultaneously. Hong et al¹⁶ carried out an anatomy study. In 10 cadavers, the distances between the starting point of the DBUN and the midpoint of the line between the medial and lateral epicondyles of the humerus were close to the distances between the branching point of the MACN and the midpoint of the line between the medial and lateral epicondyles of the humerus. Therefore, the distal end of the MACN and the proximal end of the DBUN were close to each other. The ratios of the MACN to the DBUN in axon numbers were 0.61:1 on the left side and 0.65:1 on the right side. The ratios of ulnar nerve to the sum of the median nerve and MACN in axon numbers were 0.94:1 on the left side and 0.93:1 on right side. According to the principle that the axon number in the donor nerve should equal to at least 30% of that in the recipient nerve,^17–19 it was feasible to suture the MACN with the DBUN, and the ulnar nerve with the median nerve and MACN.

There are few clinical reports on the recovery of intrinsic muscles of the patients with TBPA after surgery. The CC7 nerve root is the main donor nerve for intrinsic muscle recovery. In addition to the reports on APB recoveries after CC7 nerve transfer by Wang et al¹¹ and Yang et al,¹⁵ Wang et al²⁰ proposed a procedure of direct CC7 nerve transfer to the lower trunk in the affected limb through the prespinal route without a graft. Among 20 patients, the ADM recovered muscle strength of M3 in 1 patient and M2 in 1 patient. However, this surgical procedure was more complicated and riskier for making the prespinal route and dissecting the lower trunk to the peripheral nerves compared with our modified CC7 nerve transfer. In addition, 11 patients had humeral shortening osteotomy for reducing nerve suture tension in their study. The modified CC7 nerve transfer to both the median nerve and DBUN has not been reported earlier and is innovative.

This study had some limitations. We did not collect the actual information of patients’ postoperative rehabilitation, which might induce some potential bias. Although we provided patients with relatively unified and detailed rehabilitation protocols, each patient’s compliance was different. Not every patient strictly followed the rehabilitation protocols after surgery, which was a potentially confounding factor for the results. This study belonged to a single-center clinical study, so the results had certain regional limitations. The mean follow-up period was 2.5 years in each group, which was relatively short for the intrinsic muscle recovery, and so this study was an early electrophysiological study. Longer follow-up studies are needed to confirm the long-term benefits of the modified procedure on functional outcomes. In a future study, we will conduct a long-term follow-up.

CONCLUSIONS

From the perspective of electrophysiology, this study indicated that it was possible to regenerate intrinsic muscles using CC7 transfer to the median nerve and DBUN by pedicled ulnar nerve and MACN in patients with TBPA while not affecting the recovery of the median nerve.

DISCLOSURES

The authors have no financial interest to declare in relation to the content of this article. This study was supported by the National Natural Science Foundation of China (81972122), Shanghai Municipal Key Clinical Specialty (shslczdzk05601), Shanghai Key Laboratory of Peripheral Nerve and Microsurgery (20DZ2270200), and Shenzhen Sanming Project (SZSM202111015).