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Ann Thorac Surg 2003;76:459-463
© 2003 The Society of Thoracic Surgeons


Original article: cardiovascular

Phrenic nerve injury associated with high free right internal mammary artery harvesting

Yongzhi Deng, MDa, Karen Byth, PhDb, Hugh S. Paterson, FRACSa,c*

a Department of Cardiothoracic Surgery, Westmead Hospital, Westmead, New South Wales, Australia
b Millenium Institute, Westmead, New South Wales, Australia
c Department of Surgery, University of Sydney, Sydney, New South Wales, Australia

Accepted for publication March 4, 2003.

* Address reprint requests to Dr Paterson, Department of Cardiothoracic Surgery, Westmead Hospital, PO Box 533, Wentworthville, NSW, 2145, Australia
e-mail: patersonh{at}aol.com


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: The right phrenic nerve is at risk of injury during high mobilization of the right internal mammary artery (RIMA). The incidence and implications of this injury have not been previously defined.

METHODS: Prospectively collected data on all patients who underwent RIMA harvesting between January 1995 and February 2002 were analyzed. Thirty-one patients with right phrenic nerve injury were identified and the medical charts reviewed. Phrenic nerve injury was diagnosed when a postoperative chest roentgenogram showed the right hemidiaphragm to be two or more intercostal spaces higher than the left, or transection of the nerve was seen intraoperatively. Investigations included fluoroscopy and spirometry in upright and supine positions. Diaphragm plication was offered for symptom control. Subsequent follow-up was undertaken to determine the incidence of spontaneous recovery of diaphragm function and the benefits of diaphragm plication.

RESULTS: Seven hundred and eighty-three patients underwent high mobilization of the RIMA with proximal detachment for use as a free graft. Thirty-one patients with right hemidiaphragm dysfunction were identified in the postoperative period providing an injury incidence of 4% (confidence interval, 2.6% to 5.3%). Of these, 12 patients underwent diaphragm plication (4 early and 8 late), 14 patients achieved spontaneous recovery, and 5 patients were lost to follow-up. The supine to upright forced vital capacity ratios at the time of phrenic nerve dysfunction, after diaphragm plication, and after spontaneous recovery were 0.79, 0.90, and 0.96 respectively.

CONCLUSIONS: The incidence of phrenic nerve injury associated with high RIMA harvesting was 4% but spontaneous recovery may be anticipated in two thirds (14 of 22) of patients in whom the injury is identified postoperatively. High RIMA harvesting should be used with caution in patients with preoperative pulmonary dysfunction in whom phrenic nerve injury would be poorly tolerated.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Left phrenic nerve injury in association with coronary artery surgery has been extensively reported with particular predisposing risks identified. These risks included the use of the left internal mammary artery (LIMA) [1, 2], devascularization of the periphrenic nerve blood vessels [3], surgical manipulation [2, 4], cold injury [57], poor preoperative myocardial performance [1], chronic obstructive pulmonary disease (COPD) [8], diabetes [9, 10], and increased age [11]. Right phrenic nerve injury appears substantially less common but the nerve is at risk during right internal mammary artery (RIMA) harvesting. The clinical benefits of the use of both internal mammary arteries have been recorded [12, 13] but the incidence of right phrenic nerve injury associated with the use of the RIMA has not been determined.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Prospectively collected data on all patients undergoing coronary artery surgery using the RIMA by a single surgeon from January 1995 to February 2002 were analyzed. The records of patients with right phrenic nerve injury were reviewed. Right phrenic nerve injury was considered present when the dome of the right hemidiaphragm was two or more intercostal spaces higher than the left as seen on a plain chest roentgenogram or when right phrenic nerve transection was noted intraoperatively.

Surgical procedure after sternotomy
The RIMA was exposed with a sternal retractor and the parietal pleura brushed off the endothoracic fascia. A single long diathermy incision was made in the endothoracic fascia parallel to and immediately adjacent the RIMA vascular bundle. The endothoracic fascia was reflected and the RIMA mobilized from the chest wall with the use of diathermy. In this way mobilization from the distal RIMA bifurcation to the level of insertion of the mammary vein into the subclavian vein was performed. The vein was then divided near its insertion. Cephalic mobilization was performed by blunt dissection immediately adjacent the RIMA extending up under the subclavian vein. With gentle lateral and caudal retraction on the RIMA maximal comfortable mobilization was performed. The proximal stump was then secured with two titanium clips and the RIMA divided immediately distal to the clips. The RIMA was then divided distally and prepared for use as a free graft [14, 15].

All patients underwent coronary artery bypass surgery on cardiopulmonary bypass with core cooling to 30°C to 32°C. No topical solutions were used within the pericardium. Chest plain x-ray films were routinely made on days 0, 1, 2, and 5 postoperatively. A further chest roentgenogram was performed at the time of surgical review 5 weeks postoperatively.

Management of phrenic nerve injury
Plication of the right hemidiaphragm was performed as part of the operative procedure if transection of the right phrenic nerve was identified intraoperatively. When the phrenic nerve injury was identified postoperatively it was considered appropriate to await spontaneous recovery. During this time fluoroscopic examination of the diaphragm and spirometry in upright and supine positions was performed in an attempt to determine right diaphragmatic paresis or paralysis. The forced expiratory volume at one second (FEV1) and forced vital capacity (FVC) were expressed as percentages of the predicted normal values where the normal values were calculated by the following formulas, where height was expressed in centimeters and age in years:


If there was nonparadoxical movement of the right hemidiaphragm on fluoroscopy and the supine to upright FVC and FEV1 ratios were more than 80%, a diagnosis of right phrenic neuropraxia with hemidiaphragm paresis was made. A further recommendation to await spontaneous recovery was made but operative right hemidiaphragmatic plication was offered to those who were substantially limited by symptoms of dyspnea. For those deemed to have right diaphragmatic paralysis a recommendation to wait 3 months postoperatively for signs of recovery was made. If there were no signs of recovery diaphragmatic plication was recommended. Intermittent follow-up was continued until either spontaneous recovery was identified or diaphragmatic plication was undertaken. Patients undergoing plication underwent late postoperative spirometry.

Right hemidiaphragm plication technique
The technique has previously been described in detail [16]. With double-lumen endotracheal intubation, patients were placed in a left lateral decubitus position. A small lateral thoracotomy was made at the level of the xyphisternum just sufficient for insertion and manipulation of a long needle holder. A thoracoscope was inserted through the auscultatory triangle and plication performed under a combination of direct and thoracoscopic vision of the diaphragm using a continuous 1-0 nylon suture. Plication was considered adequate when tension on the suture caused it to cut through the diaphragm rather than further plicate it. A single chest drain was inserted and removed the next day.

Data collection and follow-up
For each patient preoperative data including spirometric and radiographic results were recorded. Operative related, postoperative, and postplication data including morbidity, mortality, and length of intensive care and hospital stay were recorded. At the last follow-up visit the patient’s symptom class was also recorded.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Seven hundred and eighty-three patients underwent high RIMA harvesting and of these 31 patients (4%) were noted to have a right phrenic nerve injury (Table 1). Of the patients with phrenic nerve injury, 5 were lost to follow-up (n = 4) or had died (n = 1). These patients were excluded from the study, leaving 26 in the study group. Of these, 12 patients underwent right hemidiaphragm plication and 14 achieved spontaneous recovery. In the plication group there were 3 patients in whom phrenic nerve transection was noted intraoperatively and diaphragm plication was performed in association with coronary bypass surgery. In 1 patient the elevated hemidiaphragm was noted early postoperatively and a decision made to perform plication through the sternotomy on day 3 due to extremely poor left ventricular function. For the other 8 patients in the plication group the plication was performed through minithoracotomy with thoracoscopic assistance. In the recovery group 6 patients were offered plication but they declined.


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Table 1. Patient Demographics

 
There was no operative mortality associated with diaphragm plication. In 1 patient a subphrenic hepatic hematoma developed and resolved spontaneously.

The length of RIMA was measured after harvesting but the length was not recorded for this series. Using the same technique in a subsequent group of 64 patients the mean RIMA length was 18.6 ± 1.6 cm (15 to 22.5 cm). There was a weak but statistically significant correlation between RIMA length and the patients’ height (Pearson’s coefficient r = 0.29, p = 0.03). The mean time between coronary artery bypass graft surgery and thoracoscopic-assisted right diaphragmatic plication was 6 (3 to 9) months, the mean operative time of plication was 57 ± 19.8 (40 to 90) minutes, and the mean hospital stay was 3.6 ± 1.1 (2 to 5) days.

The mean day of right phrenic nerve injury diagnosis (excluding early plication patients) was 24.1 ± 17.5 (3 to 54) days. The diagnosis of phrenic nerve injury was usually delayed. The most common misdiagnoses were pleural effusion, subpulmonary effusion, lung collapse/consolidation/fibrosis, linear atelectasis, pneumonia, and pulmonary embolism.

The results of preoperative, postoperative, and postplication/recovery respiratory function tests are shown in Table 2. There were no significant differences between the two groups with the exception of the postoperative FVC spirometry in the upright position. However there was a trend toward the plication group having worse spirometry throughout. Only 5 patients in the recovery group underwent supine and erect spirometry in the postoperative period before radiologically evident resolution of the elevated hemidiaphragm.


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Table 2. Respiratory Functiona

 
The mean duration of follow-up was 44.5 ± 22.8 (12 to 91) months. All the patients in the plication group reported a decline in their quality of life after coronary artery bypass graft surgery but with improvement postplication. The patients in the nonplication group experienced a relatively slower recovery of their respiratory function.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Right phrenic nerve injury is most likely due to direct physical injury because of the anatomic distribution of the nerve and its relation to the IMA. The right phrenic nerve crosses the IMA from lateral to medial within the thorax. It is usually posterior to the IMA but may cross it anteriorly. Traction on the nerve, vascular compromise, the adjacent use of diathermy, or a combination may injure the nerve. Diathermy was not used in the vicinity of the nerve but the blunt dissection may have produced traction injuries. No attempt was made to identify the nerve at the time of IMA harvesting as the plane of dissection was immediately adjacent the artery. The anatomic difference between left and right phrenic nerves is such that the nerve is in closer proximity to the IMA within the thorax on the right side (Figures 1 and 2) [17].



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Fig 1. View of the apex of the right hemithorax showing proximity of the phrenic nerve and internal mammary artery (IMA).

 


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Fig 2. View of the apex of the left hemithorax showing separation of the phrenic nerve and internal mammary artery (IMA).

 
O’Brien and colleagues [3] showed in a swine model that high LIMA mobilization decreased the left phrenic nerve perfusion by 71% with resultant impaired nerve function but that there were only minimal changes associated with high RIMA mobilization. By harvesting the maximum comfortable length of the RIMA for use as a free graft the majority of patients can receive full myocardial revascularization with both IMAs without the need for a third conduit. Avoiding high proximal dissection of the RIMA decreases the risk to the phrenic nerve but commits all patients with triple-vessel disease to a three-conduit revascularization. Although the proximal portion of the RIMA is the most suitable portion for use as a coronary bypass conduit, high harvesting of the RIMA should be avoided if the full length is not required.

Theoretical basis for diaphragmatic plication for phrenic nerve injury
Peripheral nerve growth rates have been shown to differ in the proximal and distal segments of peripheral nerves ranging from 1 to 8 mm per day [18]. Assuming that the injury occurs at the level of the first rib during high mobilization of the RIMA, the length of phrenic nerve to its diaphragmatic crux is estimated at 270 mm (as the average length of RIMA was 185 mm and from the pericardiophrenic junction to the mid hemidiaphragm was about 90 mm), the recovery time will be 38 to 270 days. These figures are consistent with the reported recovery rate of diaphragmatic dysfunction after phrenic nerve injury ranging from 1 to 18 months [7, 19].

Whereas left phrenic nerve palsy usually results in minimal morbidity, right phrenic nerve palsy is more likely to be symptomatic with respiratory dysfunction. The supine to erect FVC ratio is approximately 0.8 with a right phrenic nerve injury and 0.9 with a left phrenic nerve injury. The right diaphragm plication improves the ratio to just less than 0.9 leaving a residual respiratory morbidity similar to that of left phrenic nerve injury. Plication of the paralyzed hemidiaphragm alleviates the symptoms of dyspnea and provides subjective and objective improvement in respiratory function [16, 20, 21]. It is of note that the patients who underwent diaphragm plication appeared to have worse preoperative spirometry results than those who achieved spontaneous recovery, although this did not reach statistical significance in the small groups. It is likely that the combination of preoperative impairment of lung function and right phrenic nerve injury rendered these patients more symptomatic so that they were more likely to elect diaphragm plication rather than await possible spontaneous recovery. Phrenic nerve recovery may have occurred in some patients subsequent to diaphragm plication but that would be difficult to demonstrate.

There was a higher incidence of phrenic nerve injury among female patients and among patients with preexistent lung disease (Table 1). This finding may reflect an effort to harvest greater length in shorter patients (female), and for the phrenic nerve injury to be recognized more easily in the presence of lung disease.

The technique of minithoracotomy with thoracoscopic assistance for diaphragmatic plication combines the advantages of both the open procedure and thoracoscopy. Operative repair can be accomplished largely under direct vision through the minithoracotomy with the attendant benefits of maximal preservation of intercostal muscles for respiration in the absence of diaphragmatic function, reduced analgesic requirements, procedural efficiency and accuracy, and lastly cosmesis. Purely thoracoscopic techniques for diaphragmatic plication have been reported but they can be technically difficult [21]. With a minithoracotomy and thoracoscopic lighting, most of the diaphragm can be viewed directly with ease and videoscopic vision is employed only occasionally when the view of the posterior diaphragm is obscured.

In conclusion the patients with diaphragmatic dysfunction after open-heart surgery benefited from diaphragmatic plication but it was at the expense of possible complete recovery. High harvesting of the RIMA should be avoided in patients with preoperative impaired lung function when alternative methods of revascularization may provide similar benefits.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Abd A.G., Braun N.M.T., Baskin M.I., O’Sullivan M., Alkaitis D.A. Diaphragmatic dysfunction after open heart surgery: treatment with a rocking bed. Ann Intern Med 1989;111:881-886.
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  4. Benjamin J.J., Cascade P.N., Rubenfire M., et al. Left lower lobe atelectasis and consolidation following cardiac surgery: the effect of topical cooling on the phrenic nerve. Radiology 1982;142:11-14.[Abstract/Free Full Text]
  5. Scannell S.C. In discussion: McGoon DC, Mankin HT, Kirlin JW. Results of open heart operation for acquired aortic valve disease. J Thorac Cardiovasc Surg 1964;45:47-66.
  6. Dimopoulou I., Daganou M., Dafni U., et al. Phrenic nerve dysfunction after cardiac operation: electrophysiologic evaluation for risk factors. Chest 1998;113:8-14.[Abstract/Free Full Text]
  7. Efthimiou J., Butler J., Woodham C., Benson M., Westaby S. Diaphragm paralysis following cardiac surgery: Role of phrenic nerve cold injury. Ann Thorac Surg 1991;52:1005-1008.[Abstract]
  8. Cohen A., Katz M., Katz R., Hauptman E., Schachner A. Chronic obstructive pulmonary disease in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 1995;109:574-581.[Abstract/Free Full Text]
  9. Efthimiou J., Butler J., Benson M.K., et al. Bilateral diaphragm paralysis after cardiac surgery with topical hypothermia. Thorax 1991;46:351-354.[Abstract/Free Full Text]
  10. Kohors W.R., Schonfeld S.A., Altman M. Bilateral diaphragmatic paralysis following topical cardiac hypothermia. Chest 1984;85:65-68.[Abstract/Free Full Text]
  11. Norris A.H.N., Shock W., Wagman I.H. Age changes in the maximal conduction velocity of motor fibers of human ulnar nerves. J Appl Physiol 1959;5:589-593.
  12. Lytle B.W., Blackstone E.H., Loop F.D., et al. Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
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  17. Williams PL, Warwick R, Dyson M, Bannister LH. Gray’s anatomy. 37th ed. Edinburgh: Churchill Livingstone, 1989
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