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Eur J Cardiothorac Surg 1998;14:191-196
© 1998 Elsevier Science NL

Lung transplantation for cystic fibrosis – a single center experience over 8 years¹

^a Division of Thoracic and Cardiovascular Surgery, Hannover Medical School (Medizinische Hochschule Hannover), 30623 Hannover, Germany
^b Division of Pulmonary Medicine, Hannover Medical School (Medizinische Hochschule Hannover), 30623 Hannover, Germany
^c Division of Pediatric Pulmonary Medicine, Hannover Medical School (Medizinische Hochschule Hannover), 30623 Hannover, Germany

Received 18 November 1997; received in revised form 7 May 1998; accepted 12 May 1998.

Corresponding author. HTG-Chirurgie, Medizinische Hochschule Hannover, 30623 Hannover, Germany. Tel.: +49 511 5326580; fax: +49 511 5325404.

	Abstract

Top Abstract Introduction Patients and methods Results Appendix A. Conference... References

 
Objective: Colonization of the lung and mediastinal lymphnodes with multi-resistent bacteria, diabetes and malnutrition represent potential risk factors for lung transplantation in cystic fibrosis. We therefore reviewed our experience in this patient population. Methods: Between December 1988 and March 1997, 219 lung and heart–lung transplantations were performed at our institution. Of these, 39 procedures were done in 35 patients with cystic fibrosis. All candidates (mean age 26 years) were oxygen dependent (preoperative mean PO₂: 44.8±9.1 Torr, preoperative mean PCO₂: 53.4±10.5 Torr, one patient on respirator). Of the primary operations, 34 were performed as bilateral sequential lung transplants, one as a heart–lung transplantation. Results: Mean duration on respirator for survivors was 3.1 (1–12) days, mean ICU and hospital stay were 4.7 (1–13) and 28 (12–79) days, respectively. The 3-month mortality rate was 5.7% (two patients died due to acute graft failure on days 36 and 73). Other causes of death in the follow-up were cerebral bleeding (one patient) and chronic graft failure (three patients). The survival rates were 91% at 1 year, 83% at 3 years and 76% at 5 years. In eight patients, a bronchiolitis obliterans syndrome (BOS) developed (in four cases grade 3). The freedom of BOS (grade 1 or more) at 1, 3 and 5 years was 87, 79 and 55%, respectively. Four retransplantations were performed. Of the 29 patients alive, only seven are physically limited. Conclusion: Bilateral lung transplantation for cystic fibrosis allows for acceptable early- and long-term results. Postoperative survival is not impaired by infection, diabetes and malnutrition. Long-term functional outcome seems to be comparable to lung transplantation in patients without infectious pulmonary disease.

Key Words: Lung transplantation • Cystic fibrosis

	Introduction

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Life expectancy for patients with cystic fibrosis is limited. Due to advances in medical care the third and fourth decade of life can be reached, but the intractability of broncho-pulmonary disease remains the major cause of morbidity and mortality. More than 95% of patients die from pulmonary failure [1] [2] [3]. Predominant pathogens are multiresistant gram negative strains of pseudomonas aeruginosa or burkholderia cepacia [4] [5] [6]. In addition colonization of airways with aspergillus is frequent [7] [4]. Because of the underlying genetic exocrine defect, several other organ dysfunctions are associated with infectious pulmonary disease in this population. These include exocrine pancreatic insufficiency, glucose intolerance and diabetes mellitus, a variety of gastrointestinal problems, intestinal malabsorbtion, severe nutritional deficiency, liver disease and chronic sinusitis [2] [8] [9] [10]. Pleural adhesions due to frequent pulmonary infections and previous pleurodesis for recurrent pneumothoracis are often seen in transplant candidates. Due to these challenges in patients with cystic fibrosis, it has been suggested that this group of patients may be at higher risk for complications than other lung transplant recipients, especially with regard to pulmonary infections [6].

The first lung transplantation for cystic fibrosis was realized in 1984 as a heart–lung-transplantation. With growing experience operative techniques, postoperative management, and survival rates improved. After the introduction of a lung transplantation program in Hannover in 1988, a total of 239 lung and heart–lung transplantations have been performed. Of these, 39 procedures were done in 35 patients with cystic fibrosis.

	Patients and methods

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Patient selection
Preoperative evaluation of patients with cystic fibrosis is routinely performed in cooperation with the divisions of pulmonary medicine and pediatrics. Indication for transplantation is based on several clinical and laboratory aspects of the disease, including lung function tests, oxygenation, carbon dioxide retention, nutritional status, concurrent diseases, course of disease, frequency and severity of respiratory decompensations and infectious complications. Although FEV1 (forced expiratory volume per second) is known to be the best indicator for prognosis [11], all factors listed are evaluated. Previous lung surgery, pleurodesis, or pleurectomy are not considered contraindications. No candidate is rejected for reduced general or nutritional status, or colonization of the lungs by multiresistant bacteria. Aspergilloma or invasive aspergillosis and severe liver dysfunction, however, remained contraindications [3] [12]. Currently, two candidates are listed for combined liver and lung transplantation.

Patients
Since 1988, 35 patients with cystic fibrosis underwent lung transplantation. The mean age of the recipients was 26 years with a range of 12–34 years. There were 21 male and 14 female candidates. All recipients were depending on oxygen supplementation via nasal tube, one patient was on mechanical ventilation prior to surgery. The majority of patients were hypoxic and hypercarbic with a mean PO₂ of 44.7±9 mmHg and a PCO₂ of 53.9±11 mmHg. Lung function tests were severely compromised. Vital capacity was reduced to 1509±442 ml (35% of predicted value), FEV1 was 654±167 ml (24% of predicted value). In four cases cardiac decompensations occurred due to right heart dysfunction. All patients had recurrent pulmonary infections with strains of pseudomonas and other highly resistant bacteria. Aspergillus was identified in the sputum of eight candidates, and allergic broncho-pulmonary aspergillosis treated in seven patients.

The general condition and nutritional status of the recipients was markedly reduced. The mean weight was 48±9 kg (22–63 kg) at a mean height of 168±11 cm (131–187 cm). In six patients a percutaneous entero gastric tube was implanted for their inability to gain weight. A total of six patients was suffering from insulin-dependent diabetes.

Of the 35 primary transplantations, 34 were done as bilateral sequential transplantations, one as a heart–lung transplantation.

Procedures
Donor organs were selected from size-matched and ABO blood group compatible individuals with established brain death. No matching for CMV serological status was performed. One heart–lung transplantation and 34 bilateral sequential lung transplantations were done.

Cardio-pulmonary bypass was applied when required. Double lung transplantations were done via a clamp shell incision (bilateral anterolateral thoracotomy with transverse sternotomy) [12], bronchial anastomoses were not secured by omentum and bronchial arteries not anastomosed.

Immunosuppression
Postoperative management included a triple drug immunosuppressive therapy (cyclosporine A, azathioprine, prednisolon). In addition nine of the 35 patients received an induction therapy using anti-thymocyte-globuline (ATG, Biotest). Since 1993, ATG has not been applied routinely, but in selected cases. Acute rejection was treated with methylprednisolon (1 g i.v./day, on 3 consecutive days).

Antibiotic and CMV prophylaxis
For postoperative antibiotic prophylaxis a combination of tobramycine, ceftazidim and flucloxacillin was applied for a minimum of 7 days at high dosages, as considered for cystic fibrosis patients. Thereafter, the antibiotic therapy was adjusted based on the findings in the broncho-alveolar lavage. All patients inhaled nebulized colistin.

Prophylactic postoperative CMV treatment consisted of 10 g/day of immunoglobuline preparations for 3 days and i.v. ganciclovir (10 mg/kg) for 2 weeks. Therapy with a 3-week course of ganciclovir for CMV infection was initiated, when CMV immediate early antigen (pp 65) was identified or in any case of suspected infection.

Additional prophylactic agents in maintenance therapy of patients with cystic fibrosis were pancreatic enzyme supplementation, ursodeoxycholic acid, acetyl-cysteine, itraconazol, nebulized colistin, and amphothericine B.

Surveillance
Bronchoscopy was performed at least once a week in the early postoperative period.

All recipients were regularly seen in our out patient transplant clinic following discharge. Appointments were made weekly, after 1 month every 2 weeks, after 3 months every 4 weeks and after 1 year every 3 months. The diagnosis of bronchiolitis obliterans syndrome (BOS) was made according to the ISHLT criteria, when a decrease of more than 20% of a baseline FEV1 developed.

Statistics
The actuarial survival and freedom of BOS curves were calculated using the method of Kaplan Meier. Values are expressed as mean±SD. For comparison of groups ² and Wilcoxon tests were applied.

	Results

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Procedures
From December 1988 to February 1997 35 patients with cystic fibrosis underwent lung transplantation. Time on waiting list was 12 (1–37) months for these patients. The first operation was performed as a heart–lung transplantation, the following 34 procedures were done as bilateral sequential double lung transplantations via a clamp shell incision. Mean operating time was 253±66 min. Twelve procedures were performed with the use of cardio-pulmonary bypass for pulmonary hypertension, or intraoperative instability of hemodynamics or oxygenation. In the 34 double lung transplantations ischemic times for the first and second lung implanted were 262±42 min and 344±55 min, respectively.

Postoperative course
Two patients died postoperatively, one on day 53 and one on day 79, for a perioperative (90 days) mortality rate of 5.7%. Of the 35 patients, 33 were discharged from hospital. In these patients the mean time on the ventilator was 3.1±3 days (1–12 days). An average of 4.7±3 days (1–13 days) were spent on the ICU, and the hospital stay ranged from 12–79 days with a mean of 28±12 days.

Postoperative complications are listed in Table 1. Four patients developed a significant reperfusion injury of the lungs with prolonged ventilation periods. Rethoracotomies for persisting hemorrhage were necessary in three patients, all of whom had an operation with the use of cardio-pulmonary bypass. Acute renal failure was observed in one case. Two patients died from acute organ failure. In both cases rejection was found on autopsy. One recipient developed an intestinal obstruction requiring surgical intervention. During the postoperative period 1 (0–2) rejection episodes per patient were treated. Complicated healing of bronchial anastomoses was observed in nine patients, including bronchial dehiscence and late stenosis. All cases could be managed conservatively.

Colonization of airways with pseudomonas developed in all recipients. Broncho-pulmonary infection with pseudomonas had to be treated in 25 of 35 patients in the postoperative course, however no patient died due to infection. On recipient developed an empyema due to pseudomonas aruginosa infection. In four patients other bacterial pneumonias and in one severe CMV infection with pulmonary impairment occurred. Fungal infection with aspergillus fumigatus developed in two cases. Both fungal infections were acquired postoperatively in patients without a history of aspergillus infection.

Long-term outcome
Recipients with cystic fibrosis had a mean follow-up period of 39 (1–98) months. The actuarial survival was 91% at 1 year, 83% at 3 years and 76% at 5 years. Causes of death in the six patients lost were, acute organ failure in the postoperative period in two, a cerebrovascular accident in one and BOS in three recipients. The mean FEV1 in the 29 patients alive increased from a preoperative value of 654±167 (410–1000) ml to a baseline of 3217±1006 (1200–5280) ml within the first year following transplantation ( Fig. 1 ). The current FEV1 value remained at 2800±1199 (590–4910) ml after a follow-up period of 39 months. Twenty two (76%) of the 29 survivors were without limitations of their physical activity ( Fig. 2 ). Five patients (17%) had moderate and two (7%) severe impairment of respiratory function.

View larger version (46K): [in this window] [in a new window]   Fig. 1. FEV1 in patients with cystic fibrosis (n=29) preoperatively, baseline value post transplantation, and at the end of the follow-up period.

View larger version (46K): [in this window] [in a new window]   Fig. 2. Physical activity in patients with cystic fibrosis (n=29) after lung transplantation. Subjective classification in no, moderate, or severe limitations.

View larger version (19K): [in this window] [in a new window]   Fig. 3. Freedom from BOS (grade 1 or more) following lung transplantation, in cystic fibrosis (n=32) and in other indications (n=114) for patients at risk (follow-up/survival of more than 6 months).

View larger version (20K): [in this window] [in a new window]   Fig. 4. Actuarial survival after double lung transplantation for cystic fibrosis (n=34) and for other indications (n=43). (method of Kaplan Meier, Wilcoxon test, P=0,036).

The major concern in lung transplantation for cystic fibrosis used to be the threat of overwhelming infection, if transplantation is performed in a state of chronic multifocal infection due to multi-resistant bacteria in combination with the necessity of heavy postoperative immunosuppressive therapy [15]. The sinus cavities, upper airways, trachea and remaining bronchi may well serve as a basis for colonization of the transplanted lungs with preexisting bacteria. More than 10 years after the first successful lung transplantation in cystic fibrosis the influence of this potential source of infection on graft function is still under debate. In all 35 patients we found a colonization of the lung allografts with strains of pseudomonas during the first 6 weeks. In the majority of cases, these were bacteria that had been identified prior to transplantation. For prevention of recurrent broncho-pulmonary infections all recipients received nebulizied colistin for 3 months. In case of persisting identification of pseudomonas strains the inhalative antibiotic was applied as maintenance therapy. The management of chronic sinusitis in transplant candidates is discussed controversially. Based on our experience, we do not recommend operative drainage of chronic affection of sinus cavities prior to transplantation, unless there is significant obstruction of airways [5]. Two of our patients, however, had to undergo antrostomy several months post-transplantation for recurrent broncho-pulmonary infection with pseudomonas.

Colonization of airways with strains of burkholderia cepacia (formerly pseudomonas cepacia) is associated with a high mortality rate following lung transplantation [6]. In our recipients, pseudomonas cepacia was identified in only one case prior to transplantation, and in another patient this bacterium was acquired postoperatively. None of our 35 transplanted patients died from pulmonary infection. This is one important finding in this study, reflecting the necessity of appropriate prophylactic and therapeutic strategies. In 71% of patients antibiotic treatment for clinical signs of pseudomonas infection was required in the postoperative course. Even when in vitro testing revealed resistance to antibiotics, the application of these drugs, most often applied in combination, proved effective in our clinical experience. Thus, infections of the transplanted lungs with multi-resistant gram negative bacteria were well tolerated. Corresponding to our results, other groups [4] [16] also found no increased rate of pulmonary infections, when transplants for cystic fibrosis were compared with transplants in non-infectious diseases.

Fungal infection with aspergillus in lung-transplanted patients is a dangerous and often lethal complication. In cystic fibrosis colonization of airways with aspergillus is a common feature that has been reported in up to 63% of transplant candidates [7]. Allergic broncho-pulmonary aspergillosis may result, but invasive infection with a rapid decline of pulmonary function and general status of the patient remains rare. In 23% (eight cases) of transplanted patients in our cohort colonization with aspergillus was present prior to transplantation. These candidates received steroids, but no anti-fungal treatment. After transplantation none of these recipients had persisting identification of aspergillus. Two pulmonary infections with aspergillus seen post transplantation were acquired in recipients with no previous history of fungal disease. All lung transplants in our institution receive a postoperative prophylactic treatment with itraconazol for 6 weeks, in patients with cystic fibrosis this is continued permanently.

In the early nineties acceptable results for heart–lung transplantation in cystic fibrosis with 1 year survival rates of more than 70% were reported [15] [17]. After introduction of bilateral sequential lung transplantation, this operation became the favorite procedure [14] [16] [18] [19]. For both adolescent and adult patients with cystic fibrosis we prefer double lung transplantation, as an organ sparing procedure with respect to donor hearts. The heart can be used for a different recipient and shortage of heart–lung blocks is avoided. Airway healing in bilateral lung transplantation is however known to be more complicated than in heart lung transplantation [13]. Out of 35 cystic fibrosis recipients nine patients (25%) developed a complicated healing of bronchial anastomoses due to necrosis and, or dehiscence. But no intervention was necessary and no stents for later stenosis of anastomoses had to be implanted. Thus, we consider bilateral sequential lung transplantation as the procedure of choice in cystic fibrosis patients.

We were able to keep postoperative mortality low (9% mortality at 1 year). But long-term survival is mainly determined by the incidence of BOS. The improved rate in annual loss of patients, compared with other series, however, is well explained by our retransplantation activity. Retransplantation for BOS is still debated controversially, due to a poor outcome in these patients. We did, however, perform four retransplantations (11%) in the 35 patients with cystic fibrosis. Only one patient died due to recurrence of BOS.

Perioperative mortality in cystic fibrosis was even less than in other indications for double lung transplantation at our institution (5.7 vs. 23%). Because of the difference in postoperative mortality long-term outcome in cystic fibrosis was statistically superior (5 year survival of 76 vs. 64%). Freedom from BOS, the most frequent reason for late death, in patients with cystic fibrosis (54% at 5 years) was comparable with the rate in other indications (43% at 5 years). One of the reasons why the group of cystic fibrosis patients, despite underlying infectious lung disease, have a favorable outcome might be, that they represent an ideal age group (mean age of 26 years in our patients) for surgical procedures. In lung transplantation, pediatric patients and recipients above the age of 55 years have a less favorite outcome [14] [20]. Although often in extremely reduced general condition, postoperative recovery is faster and complications are better tolerated in these most often very compliant and disciplined patients.

Further we found, that a team approach of surgeons, physicians and pediatricians for the management of cystic fibrosis patients is essential throughout the entire pre- and postoperative course. Within our surgical transplant group there are four experienced cardiothoracic transplant surgeons, performing both cardiac and general thoracic surgery on a regular basis. Indication for and application of cardio-pulmonary bypass in case of an intraoperative emergency situation are therefore readily done. A high volume of both cardiac and pulmonary transplants has resulted in a very experienced team of residents and nurses for postoperative care especially on the ICU. A close follow-up of transplanted patients in our outpatient clinic, run with the cooperation of surgeons and pulmonologists, proved very effective in managing surviving recipients.

In conclusion, lung transplantation is a safe procedure for end-stage pulmonary disease in cystic fibrosis patients. Despite colonization of the allografts with multiresistant bacteria and subsequent infections of airways, mortality at 1 year was only 9%. Long-term results are comparable with lung transplantation for other indications. Although mid-term quality of life is excellent in these patients, BOS does represent the major obstacle to true long-term rehabilitation after lung transplantation.

	Footnotes

 
Presented at the 11th Annual Meeting of The European Society for Cardio-thoracic Surgery, Copenhagen, Denmark, September 28 – October 1, 1997.

	Appendix A. Conference discussion

Top Abstract Introduction Patients and methods Results Appendix A. Conference... References

 
Dr G. Petterson (Copenhagen, Denmark): I would like to ask you about your bronchial complications. You had nine incidents with bronchial complications, but they obviously had very little consequences. What kind of complications did you have?

Dr Wiebe: The majority of problems were bronchial dehiscence and two of the patients developed stenosis at the bronchial anastomosis in the long run. No interventions had to be made for the bronchial healing problems.

Dr Petterson: What do you mean by the concept of reperfusion injury? When do you say it is reperfusion injury and when do you say that you have some other problem? How do you separate reperfusion injury infections and so on?

Dr Wiebe: When the clinical situations as well as the radiologic pictures deteriorated within the first 2 days following transplantation with no other diagnosis made, then we considered that a reperfusion injury of the lung, and those patients typically needed longer periods of intubation.

Dr E. Birnbaum (Regensburg, Germany): Could you state your perioperative antibiotic regimen? Did you particularly administer Pseudomonas sensitive antibiotics prophylacitcally?

Dr Wiebe: The postoperative antibiotic regimen was conducted for 7 days as a standard regimen, no matter what kind of pseudomonas strains or patterns of resistance were known prior to transplantation. There after antibiotic therapy was modified according to the results of the bronchial lavages. The only long-term prophylactic treatment was an inhalation therapy with nebulized colistin in patients with evidence of colonization with pseudomonas.

Dr D.R. Metras (Marseille, France): I want to congratulate the Hannover group for spectacular results that, as I will show you later, we have not been able to match, at least for mid- and long-term results, in particular due to infectious problems and in particular to viral problems.

I would like to know your policy towards CMV matching and CMV prophylaxis, which, in our experience, as in others, seems to be a major problem and not in yours, and also a little word about cepacia and your attitude towards the presence of Burkholderia cepacia in the bronchus.

Dr Wiebe: First, we did not conduct any matching for CMV. The prophylaxis for CMV consisted of antibody treatment with IgG fractions for 3 days postoperitively and the patients received an antiviral agent, ganciclovir, for 2 weeks following transplantation. Thereafter it was continued or started when the immediate early antigen for CMV (pp 65) turned positive. We did not reject any patients who had a Pseudomonas cepacia strain. In one of our patients this was found preoperatively and two patients developed this infection postoperatively.

	References

Top Abstract Introduction Patients and methods Results Appendix A. Conference... References

 

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This Article Abstract Full Text (PDF) 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 Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wiebe, K. Articles by Haverich, A. Search for Related Content PubMed PubMed Citation Articles by Wiebe, K. Articles by Haverich, A.