[TECHNIQUE]

Techniques in Hand and Upper Extremity Surgery

Issue: Volume 11(3), September 2007, pp 184-194
Copyright: 2007 Lippincott Williams & Wilkins, Inc.
Publication Type: [TECHNIQUE]
DOI: 10.1097/bth.0b013e31804d44d2
ISSN: 1089-3393
Accession: 00130911-200709000-00003
Keywords: brachial plexus injury, intercostal nerve transfer, technique
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Technique of Intercostal Nerve Harvest and Transfer for Various Neurotization Procedures in Brachial Plexus Injuries
Wahegaonkar, Abhijeet L. MD; Doi, Kazuteru MD, PhD; Hattori, Yasunori MD, PhD; Addosooki, Ahmad I. MD
Author Information
Department of Orthopedic Surgery Ogori Daiichi General Hospital Yamaguchi, Japan
Address correspondence and reprint requests to Abhijeet L. Wahegaonkar, MD, Department of Orthopedic Surgery, Ogori Daiichi General Hospital, 862-3 Shimogo,
Ogori, Yamaguchi City, Yamaguchi, 754-0002 Japan. E-mail: abhiwahe@yahoo.com.
No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.
ABSTRACT

Brachial plexus palsy caused by traction injury, especially spinal nerve-root avulsion, represents a severe
handicap for the patient. Despite recent progress in diagnosis and microsurgical repair, the prognosis in such
cases remains unfavorable. Neurotization is the only possibility for repair in cases of spinal nerve-root avulsion.
Intercostal neurotization is a well-established technique in the treatment of some severe brachial plexus lesions
in adults. In this article, we describe our experience and technique of intercostal nerve harvest for transfer in
various neurotization strategies in posttraumatic brachial plexus reconstruction. Intercostal nerve harvest is a
technique requiring meticulous technique and careful dissection along with proper hemostasis. It is also very
important to preserve the serratus anterior muscle insertion and keep soft tissue stripping to a minimal. We do
not osteotomize the ribs and believe that this adds to the morbidity and length of the procedure. Neurotization
using intercostal nerves is a very viable procedure in avulsion injuries of the brachial plexus; however, there is
some concern that in the presence of ipsilateral phrenic nerve palsy, it may lead to a significant compromise of
respiratory function. In our experience, this is negligible with good long-term results.


HISTORICAL BACKGROUND

The development of microsurgery and the improved technique of nerve transfers and grafting have brought
new hope in cases of brachial plexus injury. In neurotization or nerve transfer, a healthy but less valuable nerve
or its proximal stump is transferred to reinnervate a more important sensory or motor territory that has lost its
innervation through irreparable damage to its nerve. In brachial plexus injuries, extraplexal nerves, such as the
spinal accessory nerve, rami of the cervical plexus, or intercostal nerves, are transferred onto trunks or cords, or
individual nerves or else segments of the brachial plexus that maintain continuity with the spinal cord may be
coapted to trunks or cords the surgeon wishes to innervate. This method is particularly indicated in root avulsion
injuries that occur frequently after traction trauma to the brachial plexus. Since Seddon's 1 first attempt and
description of intercostal nerve transfer to the musculocutaneous nerve in 1963, there have been numerous
reports in the literature 2-18 about intercostal nerve transfer for reconstruction of functional loss in patients
who had brachial plexus injury. In Seddon's report,1,19 intercostal nerve transfer had been done using
interposition nerve grafts. However, poor results were reported when an interposition nerve graft was
used,8,20,21 and hence, nerve transfer was attempted without interposition nerve grafts. This was first reported
by Hara and Tsuyama,2 with more reports claiming good results based on this principle.9,11-13,15,16,22-28
Although, experimental studies have shown superior results with vascularized intercostal nerve transfer,21,29
clinical studies have failed to replicate the experimental results.30 Besides its use as donor nerves in brachial
plexus avulsion injuries, intercostal nerves have been used for neurotization in a few other situations.31-33
Whatever the purpose, the technique of intercostal nerve harvest fundamentally remains the same. In this article,
we describe our technique of intercostal nerve harvest based on an experience of more than 200 cases of
brachial plexus reconstruction. We have used intercostal nerve transfer for neurotization of functioning muscle
transfer, neurotization of the musculocutaneous nerve, the branch of the radial nerve to the triceps, and
transfer of the sensory rami of the intercostal nerves to the medial head of the median nerve for sensory
reconstruction.

INDICATIONS AND CONTRAINDICATIONS

Neurotization is indicated in cases of brachial plexus traction injuries with complete avulsion of the spinal
nerve roots or irreparable proximal lesions of spinal nerves. A proper evaluation of brachial plexus lesions is a
prerequisite to any reconstructive procedure. Intercostal nerves most frequently have been used to neurotize
the musculocutaneous nerve 2,8,9,12,15,22-24,27,34 for reconstruction of elbow flexion. It can also be used to
neurotize the branch of the radial nerve to the triceps for reconstruction of elbow extension 14,28,35 or to
neurotize a free-functioning muscle transfer.6,35-41 Hand sensibility can be restored by suturing the sensory rami
of the intercostal nerves to the medial head of the median nerve or the ulnar nerve component of the medial
cord.40,42 Other reported uses of intercostal nerve neurotization have been to reanimate the diaphragm in
patients confined to long-term positive-pressure ventilation because of high cervical spine injury,33 for
reconstruction in a case of Poland's syndrome,31 and for dynamic reconstruction of the abdominal wall using a
reinnervated free rectus femoris muscle transfer.32 Although advanced age is not a contraindication, better
results have been obtained in younger patients,27,43 those with a shorter time interval between injury and
surgery,8,43 and the use of direct transfer without the use of interposition nerve grafts.8,15,26 There has been
some concern about reduced pulmonary function after intercostal nerve transfer, but clinical studies have
proved otherwise.17,44,45

Cases with ipsilateral phrenic nerve palsy and rib fractures are contraindications to the procedure. Poor
local skin conditions and thoracic vertebral fractures are relative contraindications.

Intercostal nerve transfer is a technically demanding procedure and should be undertaken by surgeons
experienced in this technique. A cooperative patient who understands and can follow the protracted course of
physiotherapy is another prerequisite for this operation.46,47

SURGICAL ANATOMY OF THE SECOND TO SIXTH VENTRAL THORACIC RAMI

The second to sixth thoracic ventral rami proceed in their intercostal spaces below the intercostal vessels
(Fig. 1). Posteriorly, they are between the pleura and posterior intercostal membranes but, in most of their
course, run between the internal intercostals and the subcostalis and intercostalis intimi. Near the sternum, they
cross anterior to the internal thoracic vessels and the transversus thoracis and pierce the internal intercostals,
external intercostal membrane, and pectoralis major, ending as the anterior cutaneous nerves of the thorax,
which supply the skin on the front of the thorax (Fig. 2). The second anterior cutaneous nerve may be
connected to the medial supraclavicular nerves, and twigs from the sixth supply the abdominal skin in the upper
part of the infrasternal angle.48

FIGURE 1. Schematic of neurovascular relations in a typical intercostal space. Intercostal vein (gray arrow),
intercostal artery (black arrow), and intercostal nerve (black arrowhead).

FIGURE 2. Schematic of the course and distribution of the intercostal nerve.
BRANCHES

Numerous muscular rami supply the intercostals, serratus posterior superior, and transversus thoracis.
Anteriorly, some cross the costal cartilages from one intercostal space to another. From each intercostal nerve, a
collateral and a lateral cutaneous branch leave before the main nerve reaches the costal angle. The collateral
branch follows the inferior border of its space in the same intermuscular plane as the main nerve, which it may
rejoin before distribution as an additional anterior cutaneous nerve. The lateral cutaneous branch accompanies
the main nerve a little way and then pierces the intercostal muscles obliquely; except for the first and second,
each divides into anterior and posterior rami which pierce the serratus anterior. Anterior branches run forward
over the border of the pectoralis major to supply the overlying skin, the fifth and sixth also supplying twigs to a
variable number of upper digitations of the obliquus abdominis externus. Posterior branches run back to supply
the skin over the scapula and latissimus dorsi. The second lateral cutaneous branch is the intercostobrachial
nerve. It crosses the axilla to the medial side of the arm, joins with a branch of the medial cutaneous nerve of
the arm, pierces the deep fascia, and supplies the skin of the upper half of the posterior and medial aspects of
the arm, connecting with the posterior cutaneous branch of the radial nerve. A second intercostobrachial nerve
often branches off from the anterior part of the third lateral cutaneous nerve supplying the axilla and the medial
side of the arm.

NEUROVASCULAR ARRANGEMENT WITHIN THE INTERCOSTAL SPACE

Each intercostal artery crosses its intercostal space obliquely toward the angle of the rib above and
continues forward in its costal groove. At first between the pleura and internal (posterior) intercostal membrane
as far as the costal angle, it passes between the intercostalis internus and intercostalis intimus muscles,
anastomosing with an anterior intercostal branch from an internal thoracic or musculophrenic artery. It has a vein
above and a nerve below (Fig. 1), except in the upper spaces where the nerve is at first above the artery. Each
posterior intercostal artery has dorsal, collateral, muscular, and cutaneous branches.49

TECHNIQUE

Anesthesia, Patient Positioning, and Planning

With the patient under general anesthesia in the supine position, the arm is placed on a hand table with the
shoulder in approximately 50 to 60 degrees of abduction (Fig. 3). The body is tilted 20 degrees to the unaffected
side, by interposing a pillow under the chest wall of the affected side. The shoulder is not abducted as much in
case a free muscle transfer has been done earlier to prevent tension on the transferred muscle. Alternatively,
the upper extremity can be supported with rolled towels on the operating table with a small arm rest. This allows
more room for the operating team by eliminating the need for a side table.

FIGURE 3. Patient positioning after anesthesia.
Technique of Intercostal Nerve Harvest

The incision extends along the lower edge of the pectoralis major muscle from the anterior axillary fold
toward sternum. It is slightly gently curved medially toward the xiphoid process (Fig. 4). In women, the incision is
carried along the inframammary fold for better cosmesis. The exposure of the third to the sixth intercostal
spaces is done in the same way as described here. The skin and the subcutaneous tissue are incised using a
scalpel and electrocautery, respectively, and flaps are developed on either side of the incision. The
intercostobrachial nerves are identified and tagged for later transfer to the medial head of the median nerve. The
fascia over the lower border of the pectoralis major muscle is then incised, and the muscle is carefully dissected
and retracted. This brings into view the pectoralis minor muscle which lies immediately below the major. The
origin of the pectoralis minor muscle serves as an important and useful landmark for the identification of the
third, fourth, and fifth ribs (Figs. 5 A, B). The ribs are identified, and the soft tissue and periosteum are incised
with a Bovie over the anterior surface of the rib in the midline from the midaxillary line to the costochondral
junction (Fig. 6). Each rib is then carefully freed of the periosteum with a periosteum elevator. The periosteum is
lifted off over the anterior surface first in the direction of the fibers and then over the posterior aspect with a
curved periosteum elevator and a rib raspatory (Figs. 7 A-D). Each rib is thus completely dissected and denuded of

its periosteal cover. Except in cases where there are antecedent rib fractures, the dissection with a curved
sharp periosteum elevator is relatively easy and straightforward, and injury to the pleura is exceptional. In the
rare case of the pleura being cut or damaged during dissection, there is usually sufficient soft tissue on the
posterior aspect of the rib for an immediate tensionless closure of the pleural breach with a fine monofilament
suture. Usually, no drainage is necessary if the patient is maintained on positive-pressure ventilation. The
approach and exposure of the intercostal nerve require precision and careful dissection. The denuded rib is
elevated with a Farabeuf retractor or 2 hooks by the assistant. Another assistant then grips and retracts the free
edge of the periosteum with a pair of Kocher forceps toward him. A longitudinal incision is then made over the
deep surface of the periosteum, medial to the midclavicular line, with a no. 15 scalpel (Figs. 8A, B). At this level,
the intercostal muscles are thin, and the nerve is easier to identify. As soon as the nerve is visualized, coursing
underneath the transparent endothoracic fascia, it is carefully dissected using fine Stevens scissors and isolated
with a silicone loop. At no point during the dissection the nerve is directly gripped with the forceps. It is simply
raised gently by the silicone loop. Upon isolation, the intercostal nerve is stimulated with a nerve stimulator to
confirm its motor branch (Fig. 9). Each small collateral branch of the nerve is carefully dissected with the scissors.
Most importantly, electrocoagulation is not used for hemostasis until the entire length of the nerve is dissected
and the distal end is sectioned; the nerve is reversed toward the axillary area. In the event of any bleeding or
hemorrhage during the dissection, the corner of the gauze pad is simply packed on the hemorrhagic zone, and
the dissection is continued. This simple precaution helps avoid any inadvertent injury to the delicate intercostal
nerve. Depending on the length of the intercostal nerve required to reach the recipient nerve, the dissection
may be extended medially up to the costochondral junction. Laterally, the dissection is carried to the deep
surface of the insertion of the serratus anterior digitations. We prefer and advocate preserving the serratus
insertion when it is not completely paralytic or has been reinnervated during surgery (Fig. 10). Intercostal nerve
transfer reach toward the recipient nerve is facilitated by passing the nerves through a tunnel created in the
muscle. The intercostal nerves are then assembled together on a plastic background material and carefully
resized and recut under an operating microscope. Interfascicular suture is carried out using 10-0 or 11-0
monofilament nylon sutures (Fig. 11). We usually put in 4 to 5 sutures, and we do not use fibrin glue. In our
experience, 2 intercostal nerves put together match the diameter of the branch of the radial nerve to the long
head of the triceps, and 3 intercostal nerves form a good match with the branch of the musculocutaneous nerve
to the biceps. The suture is made with slight abduction of the shoulder, so that during the postoperative
immobilization, the risk of tension on the nerves is reduced considerably. A meticulous hemostasis is done. The
muscles and fascia over the ribs are sutured together with nonabsorbable sutures to prevent any dead space and
later seroma formation. The incision is closed in layers over a Penrose drain away from the neurorrhaphy site in
the dependent region to prevent any postoperative hematoma formation (Fig. 12). It is very important to prevent
any rubbing of the skin during cleaning of the blood stains postoperatively because the neurorrhaphy is very
susceptible to shear forces. Therefore, the skin is gently mopped and dabbed with saline-soaked sponges. Strict
immobilization is done for 3 weeks using a soft pillow support splint (Fig. 13). Passive abduction of the shoulder is
prohibited for another 2 months.

FIGURE 4. Preparation of the surgical field and the planned skin incision. Note the arm supported with rolled
towels.
Sci-Hub

FIGURE 5. A, Schematic of the origin of the pectoralis minor muscle from the third, fourth, and fifth ribs. B, The
pectoralis major (small arrow) has been retracted for the identification of the pectoralis minor (small arrow). Note
the tagged intercostobrachial nerve (arrowhead).

FIGURE 6. Inscision of the fascia and periosteum over the anterior surface of the third through fifth ribs (arrows).

FIGURE 7. Stripping off the rib periosteum from (A) the anterior surface and (B and C) the posterior surface using
a curved periosteum elevator and a rib raspatory, respectively. D, Schematic of the periosteal dissection.

FIGURE 8. A, Intraoperative view showing the simultaneous retraction and elevation of the rib (small arrow) to
improve visualization of the undersurface and the stripped periosteum in its entirety (arrowhead). The second
assistant retracts the periosteum held firmly with a pair of Kocher forceps (large arrows). The surgeon then
makes an incision on the periosteum to identify and isolate the intercostal nerve. B, Schematic of this step in the
surgery.

FIGURE 9. The intercostal nerve is identified, tagged, and dissected free (arrow). It is stimulated with a nerve
stimulator to confirm the motor branch (black arrowhead).

FIGURE 10. Schematic of the intercostal nerves tunneled through the serratus anterior muscle slips while still
preserving its insertion.

FIGURE 11. The motor branches of the intercostal nerve have been sutured to the musculocutaneous nerve
(arrowhead), whereas the sensory rami and the intercostobrachial nerves have been transferred to the medial
head of the median nerve for sensory reconstruction (small arrow).

FIGURE 12. Skin closure and placement of Penrose drains (arrowheads).

FIGURE 13. Immediate postoperative immobilization with "controlled" abduction of the ipsilateral shoulder with a
cushion pillow splint.
COMPLICATIONS

With proper surgical technique and meticulous dissection, complications are a rare occurrence. In our
experience, the most common complication has been the formation of a seroma or the collection of an effusion.
This can be prevented by careful closure of the incision in layers and the strategic placement of Penrose drains
in the dependent part of the incision. It is especially important to carefully suture the intercostal muscles which
have been elevated off the ribs to prevent the formation of any dead space. Another complication that might
occur is iatrogenic pneumothorax while dissecting out the intercostal nerve. We have had 2 cases of
pneumothorax formation, which were immediately managed by chest tubes and positive end-expiratory pressure
ventilation with no postoperative sequelae. When detected, the rent in the pleura should be immediately closed
with fine monofilament nylon or Prolene using an atraumatic round-bodied needle.

POSTOPERATIVE PROTOCOL

The arm on the operated side is immobilized in controlled slight abduction so as not to place excessive
tension on the neurorrhaphy site with a commercially available soft pillow splint. A chest radiograph is taken
before the patient is transferred to the recovery unit to rule out any pneumothorax. The arm is maintained in
this position of immobilization for a period of 3 weeks. Supervised gentle, passive, range-of-motion exercises are
commenced thereafter, but any abduction of the shoulder is prevented for a further 2 months. Postoperative
rehabilitation program varies according to the purpose for which the intercostal nerve transfer was performed.
But, essentially, the patient is trained to achieve contraction of the reinnervated muscle by deep breathing
exercises and is then progressively trained to achieve independent contraction of the reinnervated muscle.50,51
The recovery after intercostal nerve transfer is monitored clinically by eliciting the Tinel sign and by
electromyography. We have observed that audiovisual biofeedback exercise using electromyography is very
effective for a patient to know which effort is best to achieve efficient muscle contraction and to learn how to
continue the contraction.46,47,52 The details of the rehabilitation program are beyond the scope of this article
and shall be described elsewhere in the near future.

OUTCOMES

Chuang et al 8 have reported a success rate of up to 81% in 66 patients with brachial plexus injuries treated
by means of intercostal nerve transfer to the musculocutaneous nerve, with or without nerve grafts to obtain
elbow flexion. Krakauer and Wood 11 reported that useful elbow function was obtained in of 9 of 13 patients with
traumatic brachial plexopathy who underwent intercostal nerve transfer to the biceps motor branch (9 patients)
or combined gracilis muscle and intercostal nerve transfer (4 patients). They concluded that intercostal nerve
transfer and combined gracilis muscle and intercostal nerve transfer are viable, although technically demanding,
alternatives for restoring active elbow motion in patients with irreparable brachial plexus lesions when
conventional tendon transfers are not feasible. Malessy and Thomeer 15 performed direct coaptation of the
intercostal nerve to the musculocutaneous nerve in 25 patients and obtained useful elbow flexion in 64% of the
patients. Other studies in the literature have reported successful results varying from 50% to 87%.12,16,53,54
Merrell et al 26 performed a meta-analysis of the English literature, designed to quantitatively assess the efficacy
of individual nerve transfers for restoration of elbow and shoulder function. One thousand eighty-eight nerve
transfers from 27 studies met their inclusion criteria of the analysis. Seventy-two percent of direct intercostal to
musculocutaneous transfers (without interposition nerve grafts) achieved biceps strength equal to M3 or more
versus 47% using interposition grafts. They concluded that interposition nerve grafts should be avoided when
possible when performing nerve transfers. Better results for restoration of elbow flexion were obtained with
intercostal to musculocutaneous transfers than with spinal accessory nerve transfers. This finding is also
supported by an experimental study by Hattori et al.55 The results of intercostal nerve transfer in our institution
parallel those reported in the literature. However, in a more recent study, Matejcik 56 reported very poor
results of intercostal nerve transfer for elbow flexion in 7 patients with not a single patient recovering any useful
function of the elbow. He concluded that the time gap between the injury and the operation, the level and the
extent of the nerve injury, and the type of the reconstructive procedure are the main prognostic factors for the
functional recovery of the paralyzed muscles, resulting from brachial plexus traction injury.

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Keywords: brachial plexus injury; intercostal nerve transfer; technique


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