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Eur J Cardiothorac Surg 2002;21:298-301
© 2002 Elsevier Science NL

Preliminary findings in the neurophysiological assessment of intercostal nerve injury during thoracotomy

^a Department of Cardiothoracic Surgery, Nottingham City Hospital, Nottingham NG5 1PB, UK
^b Department of Clinical Neurophysiology, Queen's Medical Centre, Nottingham NG7 2UH, UK

Received 22 November 2000; received in revised form 25 October 2001; accepted 20 November 2001.

* Corresponding author. Tel.: +44-115-9691169; fax: +44-115-8402605
e-mail: jduffy{at}ncht.org.uk

	Abstract

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
Objective: Previous work has suggested that intercostal nerve injury is a major factor in the aetiology of chronic postthoracotomy pain. The aim of this study was to establish if there was identifiable intercostal nerve injury during thoracotomy. Methods: Intercostal nerves were stimulated and motor evoked potentials were recorded from intercostal muscles in 13 patients undergoing thoracotomy. Measurements were taken before and after entering the pleural space, after removal of the rib retractor and after intercostal space closure. Results: Intercostal nerves functioned normally before and after entering the pleural space. After the rib retractor was removed, there was a total conduction block in the nerve immediately above the incision in every patient. In the nerves above this, six had a total block, one a partial block and three had normal conduction. There was a total conduction block in the nerve immediately below the incision in all but one patient. Of the nerves below this, four had a total block, two a partial block and three had normal conduction. In the cases of total conduction block, there was either a discrete block at the level of the distal end of the rib retractor or impairment throughout the whole nerve. Intercostal space closure did not injure any previously uninjured nerve. In a solitary patient where rib retraction was not employed, there was no impairment of the intercostal nerves throughout the operation. Conclusions: This study demonstrates for the first time that intercostal nerve injury occurs routinely due to rib retraction during thoracotomy. We believe that it may be an important step toward understanding the cause of postthoracotomy neuralgia.

Key Words: Thoracotomy • Intercostal nerve injury

	1. Introduction

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
Previous work has postulated that intercostal nerve damage sustained at thoracotomy may be responsible for chronic postthoracotomy pain [1,2]. This work has been undertaken in the postoperative period, however, and the exact mechanism of nerve injury has not been established. Potentially the nerve above or below the incision could be injured, either during incision, rib spreading or closure.

There have been many reports concerning the treatment of chronic postthoracotomy pain but very few concerning its aetiology [3]. Establishing the presence and cause of intercostal nerve injury would be an important step in the understanding of chronic postthoracotomy pain and potentially would allow modification of surgical technique to avoid injury. In order to identify nerve injury during thoracotomy, intercostal nerve motor evoked potentials (MEPs) were performed intraoperatively.

	2. Methods

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
2.1. Patients
The protocol was approved by the hospital ethics committee. Written informed consent was obtained from each patient. Thirteen consecutive patients were recruited with benign or malignant pulmonary or oesophageal disease. Patients were excluded if they had an existing neurological disorder or a previous thoracotomy. There were six men and seven women with a mean age of 69.6 years.

2.2. Intercostal nerve conduction measurements
Anaesthesia was induced with propofol (1–2 mg/kg) and maintained with nitrous oxide and isofluorane at concentrations equivalent to 1.1–1.3 MAC (Minimum Alveolar Concentration). Vecuronium (neuromuscular blockade) 0.1 mg/kg was used to facilitate endotracheal intubation. For the period of the study, Vecuronium was given as a continuous infusion and the dosage was adjusted to maintain two twitches of adductor pollicis muscle upon train-of-four (TOF) stimulation of the ulnar nerve. This strategy allowed adequate neuromuscular blockade for surgery whilst maintaining a consistent activity at the neuromuscular junction for recording intercostal nerve MEPs. The patients were placed in the lateral position for thoracotomy. For postoperative pain relief, an epidural or paravertebral catheter [4] was placed in each patient, but local anaesthetic was not used until after the final set of measurements.

Skin, fat, latissimus dorsi and serratus anterior were divided in a posterolateral muscle-cutting incision [5]. Bipolar recording needle electrodes were placed in the anterior end of the intercostal muscles of the two intercostal spaces either side of the planned intercostal incision (Nerves B,C). Additional recording electrodes were placed in the intercostal space above Nerve B in ten cases (Nerve A), and in the intercostal space below Nerve C in nine cases (Nerve D). A ground electrode was placed in serratus anterior. A hand-held monopolar stimulating probe was employed. A stimulating reference needle electrode was placed in the erector spinae muscle. The distance from the recording electrodes to a point (the stimulating point) 1 cm lateral to erector spinae was measured (Fig. 1 ).

View larger version (41K): [in this window] [in a new window]   Fig. 1. Diagram illustrating the positions of the neurophysiology equipment on the chest wall (left thoracotomy).

The fifth, sixth or seventh intercostal space was entered, either by employing diathermy to the superior rib border to strip the intercostal muscles off the rib (three patients), or by subperiosteal rib resection (ten patients) [5]. MEPs were recorded (Recording 2).

The ribs were retracted using a ratcheted rib spreader with either two blades fixed at right angles to the axis of retraction (Guidacelli) or with two blades which could rotate so that their axis was parallel to the rib (Sellars). The ribs were spread to a variable degree as determined necessary by the surgeon for the individual operation. The range of rib spread was 7–16 cm (mean 10.6 cm). In the 13th case, in a lady with lung cancer, rib retraction was not employed as the presence of inoperable pleural metastases was noted after entering the pleural cavity. In the remaining cases, the intrathoracic operation was performed and at the end of the operation the rib retractor was removed. MEPs were recorded using the initial stimulus current (Recording 3). Intercostal drains were placed. The intercostal space was closed, either by pericostal sutures or by direct approximation of the intercostal muscles. MEPs were recorded if present in Recording 3 (Recording 4). Serratus anterior, latissimus dorsi, fat and skin were closed in layers.

If a total conduction block was noted at the stimulating point, then the nerve was stimulated at 1 cm from the stimulating point and ‘inched’ anteriorly along the nerve until conduction occurred or the recording electrodes were reached. For the purposes of this pilot study, a partial conduction block was determined as a nerve which recorded an MEP when stimulated at the stimulating point, but whose latency (time from stimulus to response) had increased by a factor of two or more.

	3. Results

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
3.1. Cases 1–12 (Rib retractor employed)
3.1.1. Recording 1 (Before intercostal incision)
All the stimulated nerves in all 12 patients recorded MEPs. The mean latency rate (velocity) was 35.34 m/s (SD=6.89 m/s).

3.1.2. Recording 2 (After intercostal incision)
Three patients were paralysed at this stage. In the remaining nine patients, all the stimulated nerves recorded MEPs with latencies similar to Recording 1.

3.1.3. Recording 3 (After removal of rib retractor) (Fig. 2 )
Intercostal nerve impairment was noted in every case. However, the number of nerves involved varied, as did the type of injury (i.e. total or partial) and the site of injury. This is described for each nerve in turn as follows.

View larger version (19K): [in this window] [in a new window]   Fig. 2. Extent of intercostal nerve injury after removal of rib retractor.

3.1.3.2. Nerve above incision (B)
In every case, the nerve above the incision did not conduct at all at the stimulating point. When inched proximally from the recording electrodes, a discrete conduction block at the distal level of the rib retractor was present in nine cases. In three cases, there was a conduction block along the whole length of the intercostal nerve.

3.1.3.3. Nerve below incision (C)
In every case but one, the nerve below the incision did not conduct at all. In eight cases, the conduction block was at the distal level of the rib retractor. In three cases, there was a conduction block along the whole length of the nerve. In the case where the nerve did conduct, the latency increased but did not double.

3.1.3.4. Lowest intercostal nerve (D)
Of nine cases, the lowest intercostal nerve had a total nerve block in four, three being at the distal retractor level and one along the whole nerve length. There were two partial nerve blocks, and the nerve conducted normally in three cases.

In the nerves which had a total conduction block at the distal level of the rib retractor, the latency rate (velocity) of the conducting distal nerve had decreased to 9.03 m/s (SD=4.88 m/s).

3.1.4. Recording 4 (After intercostal space closure)
This fourth recording was performed only in three cases as either the intercostal nerves were previously injured or the patient was paralysed. There was no further nerve impairment noted from Recording 3 in any case. In one case, however, one highest intercostal nerve with a conduction block along its whole length had recovered its function by this recording.

3.2. Case 13 (Rib spreading not employed)
In the last case, all four nerves recorded normal MEPs. Recording 2 was not possible due to complete paralysis. Recording 3 (before intercostal closure) showed normal conduction, as did Recording 4 (after intercostal closure).

	4. Discussion

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
The sensation of pain in response to a normally non-painful stimulus, especially when accompanied by numbness, is virtually pathognomonic for nerve injury [3]. This is a frequent feature of chronic postthoracotomy pain and implicates intercostal nerve injury as a major factor in the aetiology. Muscle sparing thoracotomy [6], in which latissimus dorsi and serratus anterior are retracted, not divided, has not reduced the incidence of chronic pain when compared to standard posterolateral muscle-cutting thoracotomy [7,8]. This suggests that division of the muscle-layer of the chest wall is unlikely to contribute to chronic pain. Rib retraction and closure is the same in both of these techniques and could potentially damage the intercostal nerves or other structures at this level [9]. Other potential contributory factors include healing rib fracture, ‘frozen’ shoulder, local infection/pleurisy or costochondritis/costochondral dislocation [10].

Assessment of intercostal nerve injury postoperatively is difficult and does not give specific information with regards to the relationship of the damaged nerves to the incision. Most thoracotomies are performed through the fourth, fifth or sixth intercostal space making the T4–6 nerves the most likely to be injured. However, the only muscles that T6 and above reliably innervate are the intercostal muscles themselves [11,12], which are deeply situated and difficult to record from. Percutaneous needle electrodes placed in the intercostal spaces have been used to detect intercostal muscle function and thoracic radiculopathies, but difficulties with accuracy and an 8.8% pneumothorax rate have effectively prohibited further use of the technique [13–15]. Skin electrodes placed over rectus abdominis have been used to measure MEPs from T7–11 using both electrical and magnetic stimulation [16,17,18], which may be useful in studying intercostal nerve function following a thoracotomy through the seventh space or below.

By studying superficial abdominal reflexes after scar stimulation, Benedetti et al. [1] noted that patients with absent reflexes after thoracotomy for lung resection (fifth, sixth intercostal space) had higher pain scores at three months postoperatively. In another study, in addition to using superficial abdominal reflexes, the same group measured somatosensory evoked potentials and drew similar conclusions [2]. Although Benedetti et al may well have been monitoring T7,8 supplying the abdominal wall, and not T5,6 which were closest to the incision, this does correlate with our findings as we found that the nerve two spaces below the incision was often injured.

Pain is a sensory modality. Richardson et al. [19] have used somatosensory evoked potentials to assess the efficacy of intercostal nerve blocks in chronic pain conditions including chronic postthoracotomy pain. However, this technique would have been difficult to perform intraoperatively and would not have given information regarding the site of the conduction block. As the intercostal nerves are mixed nerves, it is reasonable to assume that a motor conduction block will equate with a sensory conduction block.

We believe that this study demonstrates for the first time that intercostal nerves are injured during thoracotomy and that this occurs routinely to multiple nerves during rib spreading. No nerve was injured whilst entering the pleural space. After rib spreading, however, the nerves immediately above and below were invariably injured. The injury caused by the retractor is striking as a conduction block was often seen at the distal end of the rib retractor. It is possible that the rib retractor causes two injuries: direct ischaemic injury caused by pressure from the retractor and a stretch injury (viz traction injuries of the brachial plexus). This may explain why in some cases the nerve had a discrete conduction block and why in others the whole nerve was injured.

Although only assessed in a few cases, closure did not appear to increase nerve injury but this needs to be explored further. In one patient who did not undergo rib retraction, the intercostal nerves remained intact throughout incision, operation and closure.

If compression and ischaemia is applied to a nerve, a neuropraxia will develop at a rate dependent upon the severity of the insult. This explains why some of the highest and lowest nerves developed a partial block as the insult would not have been so severe. Neuropraxia will resolve if the compression is removed within a short period of time and the nerve is allowed to recover. However, if the compression persists then the neuropraxia becomes permanent as the nerve dies and loses its function. Partial nerve injury is as significant as complete section with regards to altered nerve function, opiate unresponsiveness and acute and chronic pain [20]. As 50% of patients develop chronic postthoracotomy pain and all the patients who had rib retraction had nerve injury, one hypothesis is that it is the nerves that do not fully recover their function generate chronic postthoracotomy pain.

We accept that chronic postthoracotomy pain is a complex multifactorial condition. However, we believe that these early findings are highly significant and are an important first step in trying to understand chronic postthoracotomy pain and the refinement of surgical technique to prevent it.

	Acknowledgments

 
The authors gratefully acknowledge the contribution of Mr F.D. Salama, Mr F.D. Beggs, Miss VM McNamara and the thoracic anaesthetic, surgical and theatre teams in accommodating the research; Mr Chris Hovey from The Magstim Company for tailoring the neurophysiological equipment to intercostal nerve studies and for the loan of the equipment in the initial phases of the research; Mr Lyndon Cochrane, Department of Medical Illustration, Queen's Medical Centre, Nottingham for the illustration; The Royal College of Surgeons of England for the pump-priming grant to support the full project.

	Footnotes

 
Presented at the 8th European Conference on General Thoracic Surgery of the European Society of Thoracic Surgeons, London, UK, November 1–4, 2000.

	References

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 

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