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Ann Thorac Surg 1996;61:170-173
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Diaphragmatic Paralysis: A Complication of Lung Transplantation

Departments of Surgery and Medicine, University of Toronto, The Toronto Hospital, Toronto, Ontario, Canada

Accepted for publication August 16, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. Damage to the phrenic nerve, either unilaterally or bilaterally, is a well-documented complication of cardiac operation, but less commonly reported after lung transplantation.

Methods. A retrospective review of 185 single and sequential single lung transplant procedures was performed at The Toronto Hospital. Objective confirmation (fluoroscopy or ultrasound) of diaphragmatic paralysis was found in 6 patients. Paralysis was unilateral in 5 patients (all were left sided) and bilateral in 1 patient.

Results. The average length of ventilation was 8.2 ± 9.2 days with an average intensive care unit stay of 11.2 ± 10.6 days. Mean duration in the hospital was 37.5 ± 11.1 days. The average length of intensive care unit stay and hospitalization were compared with all other sequential single transplantations performed from approximately the time of the first documented case of diaphragmatic paralysis. Intensive care unit stay and hospitalization for the other (no diaphragmatic paralysis) transplant recipients were significantly shorter (5.3 ± 2.7 and 29.1 ± 12.9 days, respectively; p < 0.05). One patient required noninvasive ventilatory assistance via bilevel positive airway pressure in the hospital. One other patient used bilevel positive airway pressure in the hospital and overnight for 6 months after discharge. All patients obtained acceptable lung function and were ambulatory upon discharge from the hospital.

Conclusions. Clinically detectable diaphragmatic paralysis is an infrequent complication of lung transplantation and is associated with longer intensive care unit stay and hospitalization, but is not associated with significant adverse outcomes.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Diaphragmatic paralysis is a well-documented complication of open heart operations. Phrenic nerve injury during operation has been proposed to result from stretching during retraction of the sternum and manipulation of the pericardium, or from ice slush hypothermic injury to the phrenic nerves [1].

Lung transplantation involves dissection of the mediastinum and manipulation of the pericardium. Cardiopulmonary bypass is occasionally required during double-lung transplantation. One might presume, therefore, that phrenic nerve injury would occur as a complication of lung transplantation, yet postoperative diaphragmatic paralysis has rarely been reported. Upon review of our experience with approximately 185 lung transplant procedures, we uncovered 6 cases of clinically detectable diaphragmatic paralysis after lung transplantation and assessed the outcome following this complication.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Population
The records of 185 patients who underwent single or sequential single-lung transplantation between 1983 and 1994 at The Toronto Hospital were retrospectively reviewed for the diagnosis of diaphragmatic paralysis in the physician notes. Only patients who had confirmation of diaphragmatic paralysis by an imaging technique (fluoroscopy or ultrasound) were included in the study.

Morbidity
Duration of mechanical ventilation, stay in the intensive care unit, and hospitalization was calculated from the medical records. The operative note was reviewed for any unusual occurrences that may have predisposed the patient to phrenic nerve injury.

Spirometry
Flow-volume curves were obtained by maximal forced expiratory maneuvers using a Morgan Spiroflow 12 L dry rolling seal spirometer (P.K. Morgan, England). The best of three expiratory maneuvers was used to obtain for forced expiratory volume in 1 second and forced vital capacity. Lung volumes were obtained by the helium dilution method.

Data Analysis
The data are presented as absolute values or means ± standard deviation. The average length of intensive care unit stay and hospitalization were compared with all other single sequential lung transplant recipients from approximately the time of the first documented case of diaphragmatic paralysis using the unpaired t test. Statistical significance was considered at p less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Patients Identified
Six patients with diaphragmatic paralysis were identified. There were 2 men and 4 women with a mean age of 44.0 ± 6.0 years (range, 36 to 52 years). The indications for lung transplantation were cystic fibrosis in 1, lymphangioleiomyomatosis in 1, emphysema in 3, and eosinophilic granuloma in 1. No patient had abnormal elevation of the hemidiaphragms on chest radiograph preoperatively.

Operative Review
All 6 patients underwent bilateral sequential single-lung transplantation through a clam-shell incision. Three patients required cardiopulmonary bypass during the operation. All patients had bilateral right and left internal jugular lines inserted, 1 of which was a cordis. The lowest recorded temperature on bypass was 33.4°C (average, 34.1°C). Four patients had extensive pleural adhesions bilaterally, with 2 of the 4 having had previous pleurectomies and talc for pneumothoraces. In all cases the phrenic nerve was identified and preserved. Cold saline sponges were used to pack the chest as the donor lung was anastomosed. No ice or slush was used in the chest.

Morbidity
The average length of ventilation was 8.2 ± 9.2 days (range, 2 to 25 days) with a length of stay of 11.2 ± 10.6 days (range, 2 to 30 days) in the intensive care unit and an average hospitalization of 37.5 ± 11.1 days (range, 26 to 56 days). In comparison, the average length of stay in the intensive care unit for all other sequential single-lung transplant patients was 5.3 ± 2.7 days (p < 0.001) (range, 1 to 12 days) with an average length of hospitalization of 29.1 ± 12.9 days (p < 0.05) (range, 8 to 59 days).

The average length of days to suspect abnormal diaphragmatic movement was 12.0 ± 7.8 days (range, 4 to 20 days). Diaphragmatic paralysis was suspected in only 2 patients before extubation. The method of diagnosis of a paralyzed diaphragm was by fluoroscopy in 4 patients and by ultrasound in 2. In 5 patients the left hemidiaphragm was paralyzed and in 1 patient there was bilateral paralyzation of the diaphragm. Two patients required noninvasive ventilatory assistance via bilevel positive airway pressure: 1 patient used bilevel positive airway pressure in the hospital only, and the other (with bilaterally paralyzed diaphragms) required bilevel positive airway pressure in the hospital and overnight for approximately 6 months after discharge.

The respiratory symptoms and signs (excluding imaging procedures) of the patients at time of diagnosis are listed in Table 1. Three of 6 patients did not have any of the listed signs or symptoms. Of the 3 with clinical manifestations, 2 (patients 5 and 6) fully recovered before discharge from the hospital. There were no notations in the medical records of paradoxical abdominal motion; however, this does not exclude the possibility that it was simply overlooked. One patient required a tracheostomy (patient 1) after being ventilated for 11 days and was extubated 14 days later.

The pulmonary function tests of these 6 patients at 1, 3, and 6 months after transplantation are listed in Table 2. At 6 months, all patients had a forced expiratory volume in 1 second of at least 60% and total lung capacities exceeding 78%. However, 2 patients had vital capacities of less than 60%.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Diaphragmatic paralysis may first be suspected because of failure to be weaned from mechanical ventilatory support or by paradoxical movement of the diaphragms on clinical examination. Symptoms may include dyspnea, orthopnea, nocturnal arterial oxygen desaturation, and desaturation on exercise. Methods to evaluate diaphragmatic function include assessment of movement of hemidiaphragms by physical examination of chest wall and abdominal movement during inspiration, measurement of vital capacity differences from the upright and supine positions, fluoroscopy or ultrasound, transdiaphragmatic pressures by an esophageal balloon, and phrenic nerve stimulation and diaphragmatic electromyography.

In Griffith and co-workers' [10] 10-year review of 232 lung transplantations in Pittsburgh, only 2 patients had documented diaphragmatic paralysis, both of whom had poor outcomes (death). Sheridan and associates [7] evaluated 29 consecutive lung transplant recipients for evidence of phrenic nerve dysfunction and recovery by transcutaneous electrical stimulation of cervical phrenic nerve. Evidence of phrenic neuropathy was uncovered in 10 patients (34%), the majority being on the right side. In our group of 185 lung transplant patients, only 6 had symptomatic problems with documented phrenic nerve paralysis (incidence of 3.2%), all of which affected the left phrenic nerve, and 1 patient had bilateral involvement. The left phrenic nerve is more commonly affected in cardiac operations secondary to the cold fluid being directed over the left ventricle and, therefore, falling onto the left side of the pericardium first. In our case, the injury to the phrenic nerve is more likely due to stretching, as ice or slush was not used. With stretching of the phrenic nerve, the axons are stretched but the integrity of the nerve remains intact. The implication is that the time for recovery depends on the distance of the nerve injury to the diaphragm, as well as the rate of regeneration.

Knowledge of the anatomy and course of the phrenic nerve also serves to avoid traumatizing this nerve. It arises mainly from the third through fifth cervical nerves. Starting at the upper part of the lateral border of scalenus anterior, it descends into the neck anterior to it, and deep to the sternocleidomastoid muscle. It then runs anterior to the subclavian artery and posterior to the subclavian vein into the thorax. The right phrenic nerve, shorter with a more vertical position, runs lateral to the brachiocephalic vein and superior vena cava and between the fibrous pericardium and mediastinal pleura to the diaphragm. On the left, the nerve passes medially to the left vagus nerve, superficial to the arch of the aorta, anterior to the root of the left lung, to lie between the fibrous pericardium covering the left ventricle and the mediastinal pleura.

In the neck, each nerve receives variable communicating filaments from the cervical sympathetic ganglia and may communicate with the internal mammary sympathetic plexus. During its course in the chest, the phrenic nerve gives off pleural and pericardial branches as well as terminal branches through the diaphragm. Of importance to note are the accessory phrenic nerves (usually from the fifth cervical nerve, but may be as well from the fourth, sixth, or from the ansa cervicalis) that lie lateral to the main phrenic nerve and descend posterior or anterior to the subclavian veins. They usually join the main phrenic nerve at the level of the first rib but may do so only at the level of the root of the lung, or even lower.

Despite knowledge of the anatomy, quite often at the time of lung transplantation there are extensive adhesions secondary to previous surgical procedures, pleurodesis, or even the underlying disease process, which may complicate the dissection. However, we believe with good exposure, attention to detail, and meticulous dissection of adhesions, possible trauma to the phrenic nerve can be minimized. We also attempt to identify the phrenic nerve and to avoid the use of forceps for retraction or the use of electrocautery for dissection. The vein retractor serves as an excellent instrument and can be used to retract the nerve and prevent it from being injured during the application of the DeBakey clamp on the atrium for the pulmonary venous anastomosis. Keeping this in mind, we believe that trauma to the phrenic nerve can be kept at a minimum.

The actual incidence of diaphragmatic dysfunction in our patients may be higher than reported, as many patients may have been asymptomatic or had only a brief period of phrenic nerve dysfunction. The patients with diaphragmatic dysfunction that we identified required longer intensive care unit and hospital stays, suggesting that diaphragmatic dysfunction should be considered when there are difficulties in weaning and there are no readily available explanations. Fortunately, of those we have documented, all have had acceptable lung function, although 2 patients had a forced expiratory volume in 1 second between 60% and 70% at 6 months. Although a prospective evaluation examining preoperative and postoperative diaphragmatic function would determine the true incidence, rate of recovery, and consequence of phrenic nerve injury, our review suggests that given the favorable outcome, it is unlikely that clinically useful information would be obtained.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Kesten, General Division, The Toronto Hospital, 200 Elizabeth St, 10-NU-122 Toronto, ON, Canada M5G 2C4.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

1. Chandler KW, Roxas CJ, Kory RC, Goldman AL. Bilateral diaphragmatic paralysis complicating local cardiac hypothermia during open-heart surgery. Am J Med 1984;77:243–9.[Medline]
2. Esposito RA, Spencer FC. The effect of pericardial insulation on hypothermic phrenic nerve injury during open heart surgery. Ann Thorac Surg 1987;43:303–8.[Abstract/Free Full Text]
3. Large SR, Heywood LJ, Flower CD, Pearce RC, Wallwork J, English TAH. Incidence and etiology of a raised hemidiaphragm after cardiopulmonary bypass. Thorax 1985;40:440–7.
4. Martland ON, Moorthy SS, Mahomed Y, King RD, Brown JW. Postoperative phrenic nerve palsy in patients with open heart surgery. Ann Thorac Surg 1985;39:68–73.[Abstract/Free Full Text]
5. Olopade CO, Staats BA. Time course of recovery from frostbitten phrenics after coronary artery bypass graft surgery. Chest 1991;99:1112–5.[Abstract/Free Full Text]
6. Dajee A, Pellegrini J, Cooper G, Karlson K. Phrenic nerve palsy after topical cardiac hypothermia. Int Surg 1983;68:345–8.[Medline]
7. Sheridan P, Cheriyan A, Doud J, et al. Incidence of phrenic neuropathy following isolated lung transplant. J Heart Lung Transplant 1994;13:S91.
8. Marco JD, Hahn JW, Barner HB. Topical cardiac hypothermia and phrenic nerve injury. Ann Thorac Surg 1977;23:235–7.[Abstract/Free Full Text]
9. Armengaud MH, Trevoux-Paul J, Boucherie JC, Cousin MT. Diaphragmatic paralysis after puncture of the internal jugular vein. Ann Fr Anesth Reanim 1991;10:77–80.[Medline]
10. Griffith BP, Hardesty RL, Armitage JM, Hattler BG, Pham SM, Keenan RJ. A decade of lung transplantation. Ann Surg 1993;218:310–20.[Medline]

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Donna E. Maziak Janet R. Maurer Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Maziak, D. E. Articles by Kesten, S. Search for Related Content PubMed PubMed Citation Articles by Maziak, D. E. Articles by Kesten, S.