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Ann Thorac Surg 1996;62:839-843
© 1996 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Colon Perforation After Lung Transplantation

Thomas M. Beaver, MD, David A. Fullerton, MD, Martin R. Zamora, MD, David B. Badesch, MD, David Weill, MD, James M. Brown, MD, David N. Campbell, MD, Frederick L. Grover, MD

Divisions of General and Cardiothoracic Surgery and Pulmonary and Critical Care Medicine, University of Colorado Health Sciences Center, Denver, Colorado

Accepted for publication April 23, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background. Colon perforation has been previously described after solid organ transplantation. Since the inception of the lung transplant program at the University of Colorado 60 isolated lung transplantations have been performed. Four of these patients have suffered spontaneous colonic perforation.

Methods. The case history of each lung transplant patient with a colon perforation and the literature were reviewed.

Results. An increased incidence of colon perforation in lung transplant patients was identified. Diverticulitis was found to be the predominant cause, and an association with steroids was noted. The two deaths in this series were in patients receiving high-dose steroids in whom invasive Aspergillus infections developed.

Conclusions.Careful screening of the gastrointestinal tract before transplantation is advocated. A steroid-sparing immunosuppressive regimen is recommended. All lung transplant patients with abdominal complaints require an aggressive work-up, and surgeons should have a low threshold for laparotomy. Conservative surgical principles, including resection of the perforated segment of colon and proximal end-colostomy rather than primary anastomosis, are necessary for the optimal outcome.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Lung transplantation is an accepted mode of therapy for end-stage pulmonary parenchymal and vascular disease [1]. As with other solid organ transplants, gastrointestinal complications have been reported after lung transplantation [2]. We have recently observed four colon perforations in our first 60 lung transplant recipients.

The purpose of this study was to review these cases in an effort to prevent future morbidity from this complication. All four spontaneous colon perforations in this series were secondary to diverticulitis. Two of the 4 patients died of aspergillosis after extended hospitalizations, and both of these patients were receiving high doses of steroids at the time of their perforation.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
The chart of each isolated lung transplant recipient with a colon perforation was reviewed. Our selection criteria, preoperative work-up, and surgical technique for lung transplantation are consistent with published reports [3, 4]. No specific gastrointestinal work-up was undertaken before transplantation. All patients received our standard immunosuppressive regimen, consisting of preoperative cyclosporine and intraoperative methylprednisolone >500 mg intravenously at the time of pulmonary artery clamp removal) and postoperative triple-drug therapy with cyclosporine >whole blood levels, 350 to 450 mg/dL), azathioprine >to keep the white blood cell count approximately 5,000/µL and prednisone >tapered over 1 month to 0.15 to 0.25 mg•kg-1•day-1). Postoperative viral prophylaxis included ganciclovor, 5 mg•kg-1•day-1 for 30 days, followed by acyclovir, 800 mg three times daily for 6 months, and cytomegalovirus >CMV) hyperimmune globulin on postoperative days 1, 15, and 30.


   Results
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Clinical data on the 4 patients are shown in Table 1Go.


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  		Table 1. . Lung Transplant Patients With Colon Perforations
 
Patient 1
A 44-year-old woman with end-stage obstructive lung disease secondary to {alpha}1-antitrypsin deficiency underwent an uncomplicated left isolated lung transplantation in July 1993. Twenty-four months after transplantation she presented with a 30-hour history of crampy lower abdominal pain. She was found to have diffuse lower abdominal tenderness with rebound but no guarding. Cervical motion tenderness was present, and her white blood cell count was 22.9 x 109/L. A computed tomographic scan of the abdomen and pelvis suggested a left lower quadrant mass with fluid in the pelvis. Diagnostic laparoscopy was performed, and perforated sigmoid diverticulitis was found. A sigmoid colectomy with end-colostomy and Hartmann's pouch was performed. Pathologic evaluation confirmed perforated diverticulitis with no evidence of CMV. She made an uneventful recovery and was discharged home after 11 days. The colostomy was taken down 14 weeks later.

Patient 2
A 59-year-old woman underwent left isolated lung transplantation in January 1995. Transplantation was complicated by International Society for Heart and Lung Transplantation grade 3A mild acute rejection 10 days postoperatively, which responded to a steroid pulse. Four months after transplantation she presented with severe lower abdominal pain with rigidity and rebound tenderness; her white blood cell count was 14.6 x 109/L. She was taken emergently for exploratory laparotomy and was found to have a perforated left colon with a contained mesenteric abscess. A left hemicolectomy with end-colostomy and Hartmann's pouch was performed. Pathologic evaluation confirmed diverticulitis with no evidence of CMV. Her colostomy was taken down 14 weeks later.

Patient 3
A 59-year-old man with a remote history of diverticulitis and Gilbert's syndrome underwent an uncomplicated right isolated lung transplant for {alpha}1-antitrypsin deficiency and was discharged home on postoperative day 9. Eight days later he returned to the emergency room complaining of epigastric pain, diarrhea, and fever. His temperature was 37.1°C, his abdomen was benign, and laboratory values were significant for a white blood cell count of 12.8 x 109/L and a total bilirubin level of 2.1 mg/dL. He was admitted and treated with histamine antagonists. He was improving until 48 hours later, when he complained of lower abdominal pain, shaking chills, and a fever of 38.8°C. Free air was noted on a plain film of the abdomen. Emergent exploration revealed perforated sigmoid diverticulitis with diffuse peritonitis. Sigmoid colectomy with end-colostomy and Hartmann's pouch was performed. Pathologic evaluation confirmed perforated diverticulitis with no evidence of CMV. He initially did well and was extubated, and his diet was advanced. Progressive hyperbilirubinemia ensued, with a total bilirubin level peaking at 30.9 mg/dL. Abdominal ultrasound revealed no biliary obstruction, a computed tomographic scan revealed no abscess, and a radionuclide biliary scan showed poor uptake consistent with hepatic dysfunction. Hepatitis serologies were negative. Respiratory failure required reintubation, and renal and cardiogenic failure followed. A chest roentgenogram showed a cavitary lesion in the left upper lobe of his native lung; administration of amphotericin B was started empirically. Bronchoscopic cultures later grew Aspergillus. The patient died of multiple-system organ failure 67 days after his lung transplantation. Autopsy revealed necrotizing Aspergillus infection in both the native emphysematous and transplanted lungs, and a cirrhotic liver with intracellular granules typical of {alpha}1-antitrypsin deficiency. There was no evidence of systemic CMV infection.

Patient 4
This 56-year-old woman underwent left isolated lung transplantation for end-stage chronic obstructive pulmonary disease in December 1993. Four months after transplantation she was treated with a steroid pulse for clinical rejection >the biopsy was technically inadequate for interpretation). A week later she presented complaining of progressive abdominal pain. On examination she had diffuse tenderness, guarding, and rebound with free air on abdominal films. Exploration revealed perforated sigmoid diverticulitis and generalized peritonitis. A sigmoid colectomy with end-colostomy and Hartmann's pouch was performed. Pathologic evaluation confirmed perforated diverticulitis without evidence of CMV infection. She initially did well, and her diet was advanced. However, 14 days postoperatively mental status changes were noted. A head computed tomographic scan was normal, and a computed tomographic scan of her abdomen revealed no abscess. A right lower lobe infiltrate was noted on her chest roentgenogram, and amphotericin B was given empirically; bronchoalveolar lavage grew Aspergillus. Multiple-system organ failure developed, and she died 35 days after her colostomy. Autopsy identified necrotizing Aspergillus pneumonia in the native right lower lobe and transplanted left upper lobes with dissemination to the kidneys, thyroid, left ventricle, and brain. There was no evidence of CMV infection.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Lung transplantation has become an accepted method of treatment for end-stage lung disease. The 1-year >91%) and 3-year >76%) survival rates at the University of Colorado compare favorably with those at other centers. Cooper [1] reported a 90% one-year survival. Dark [3] reported international 1-year survival rates of 65% to 80%, and Davis and Pasque [4] reviewed several series and found 1- and 2-year survivals between 60% and 100% depending on the institution, with an overall 5-year survival approximating 50% to 60%.

In the present report, four colon perforations were diagnosed in 60 lung transplant recipients, for an incidence of 6.7% with a mortality of 50%. Smith and associates [2] have previously reported four colon perforations in 75 lung transplant patients >5.3%); none of their patients had CMV colitis or a previous history of diverticular disease. Colon perforation in renal, liver, and more recently heart and lung transplant patients has been well documented in several large series, with an incidence of 1% to 2% [5–22]. The mortality in the early series was as high as 100%; however, recent series report more favorable outcomes >Table 2Go).


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  		Table 2. . Colon Perforations In Transplant Patients
 
Steroids have been implicated as a contributing factor in colonic perforation. Several investigators have speculated that steroids cause intestinal atrophy, deplete submucosal lymphoid patches, and inhibit the normal inflammatory reaction, leading to bacterial invasion, lack of containment, and subsequent perforation [6–8,16,23]. Warshaw and associates [23] have suggested that steroids may cause direct colon mucosal injury. In a series of nontransplant patients with perforated diverticulitis, Canter and Shorb [24] found 22% were receiving steroids, and these patients were more likely to have a free perforation. Tyau and colleagues [25] also found immunocompromised patients had a much higher incidence of free perforation, morbidity, and death as compared with nonimmunocompromised patients. Other transplant centers have noted an increased incidence of colon perforation after steroid pulses for rejection [13, 18]. Two of the patients in our series were receiving high-dose steroids at the time of their perforation: patient 3 was receiving higher doses of steroids as he was being tapered from his transplant induction, and patient 4 had received a steroid pulse for rejection. A "steroid-sparing" approach is now part of our present immunosuppressive regimen.

The immunosuppression used in transplant patients can mask significant intraperitoneal pathology. Delays in diagnosis and mortality have been shown to increase as steroid dose increases [26]. Accordingly, a high index of suspicion for occult perforation, aggressive work-up of all abdominal complaints, and early use of laparotomy have been recommended for all immunocompromised patients; this has led to the improved mortality in recent years [2,6,7,10–13, 16–18,21,22,24,27]. Conservative surgical principles-removal of the infectious source with end-colostomy and avoiding primary anastomosis-are essential for the best outcome [2, 5, 11, 18, 24]. Despite early intervention >time from diagnosis to operation less than 6 hours), 2 of our patients died of their perforations.

The four spontaneous colon perforations in this series were secondary to diverticulitis, consistent with other reports showing diverticulitis as the predominant cause of colon perforation in solid organ transplantation [5, 6, 8, 11, 13, 17]. Colon perforation secondary to pseudoobstruction also has been reported in transplant patients [19, 20]; early colonoscopic decompression is advocated, with colectomy reserved for patients who do not respond to conservative measures. Fecal impaction secondary to the use of antacids also has been implicated in some earlier reports of colon perforation [5, 12, 17]. Immediately before his admission patient 4 had been taking large doses of antacids, which conceivably could have been a contributing factor. Although none of our patients was found to have CMV infection of the colon, it has been reported to cause mucosal inflammation, pneumatosis, bleeding ulceration, and perforation in transplant recipients [7, 27–29]; the ulcerations and perforations are thought to be caused by microvascular thrombosis secondary to a CMV occlusive vasculitis in the bowel wall [30, 31].

The two deaths in the present series were caused by invasive Aspergillus infections. Both patients were receiving increased doses of steroids, which may have facilitated superinfection by Aspergillus. However, these infections occurred late in the postoperative courses and may have been a reflection of the decompensated state of the transplant recipients.

Aspergillosis in lung transplant patients is an ominous finding. At the University of Colorado invasive Aspergillus infections have been found in 3 >5%) of our lung transplant patients with a 100% mortality >including the 2 patients in this series), although superficial Aspergillus bronchitis was noted in an additional 8% with no mortality. Bertocchi and associates [32] reported Aspergillus infections in 10% of their lung transplant recipients with a 57% mortality. Guillemain and colleagues [33] noted an increased Aspergillus infection rate in their lung >18%) as compared with their heart >4.5%) and renal >0.5%) transplants, with mortality between 60 and 75%. They recommend liposomal administration of amphotericin B and surgical resection of the infection focus if possible [33].

The incidence of colon perforation in lung transplant patients, 6.6% in our series and 5.3% in Smith and associates' series, appears to be higher than that in other solid organ transplants, which is typically 1% to 2% >see Table 2Go). In fact, only 2 of the 133 heart transplant patients >1.5%) at our institution have had colon perforations. Both of these occurred in the first postoperative week: one secondary to pseudoobstruction and the other after a methylprednisolone burst for early rejection. A possible explanation for an increased incidence of colon perforation in lung transplant recipients is that aggressive diuresis to reverse reperfusion edema leads to constipation and an exacerbation of underlying diverticular disease with subsequent perforation. An older patient population also could be implicated, as the incidence of colon diverticulosis increases with age. However, the average age of patients undergoing lung transplantation at the University of Colorado >48 years) is actually less than that of the heart transplant recipients >51 years).

Given the serious morbidity of colon perforation, barium enema examination has been recommended in the past for renal transplant candidates with a possibility of colon disease [11]. Colon resection for renal transplant candidates with symptomatic diverticulosis also has been advocated [5]. Routine examination of the alimentary tract in lung transplant patients also has been suggested; however, given the compromised pulmonary function of lung transplant candidates, the risks of perioperative mortality or prolonged ventilation would have to be weighed against the possible benefits from intervention [2]. Patient 3 in our series had a remote history of diverticulitis >15 years before transplantation) but was asymptomatic at the time of transplantation. Our present lung transplant evaluation protocol includes a barium enema and flexible sigmoidoscopy for all potential lung recipients with age greater than 50 years or a history of abdominal complaints. Patients with radiographic evidence or a clinical history of diverticulitis are presently excluded, as are patients with extensive diverticulosis and other relative contraindications to transplantation; however, we are exploring the feasibility of prophylactic colon resection in these subgroups. Patients with asymptomatic diverticulosis proceed to transplantation with close follow-up, and colon resection if symptoms arise.

In conclusion, an increased incidence of colonic perforation has been identified in lung transplant patients. Preoperative work-up should include careful investigation of any history of gastrointestinal complaints, with an individualized assessment to determine if pretransplantation intervention is warranted. An association between elevated steroid doses and colon perforation was noted; steroid-sparing immunosuppressive regimens may lessen the risk of colonic perforation. Both patients who died of their colon perforations in this series were receiving high-dose steroids and had invasive Aspergillus infections. All lung transplant recipients with complaints of abdominal pain require aggressive work-up and early laparotomy with resection of the perforated colon and proximal end-colostomy rather than primary anastomosis.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Beaver, Department of Surgery, University of Colorado Health Sciences Center, 4200 E Ninth Ave, Box C-312, Denver, CO 80262.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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