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* From the Services de Pneumologie (Drs. Plantier, Mal, Brugière, Taillé, and Fournier) and Chirurgie Thoracique (Drs. Castier and Lesèche), Hôpital Beaujon, Clichy, France.
Correspondence to: Hervé Mal, MD, Service de Pneumologie, Hôpital Beaujon, 92110 Clichy, France; e-mail: herve.mal{at}bjn.aphp.fr
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Abstract |
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Setting: A tertiary care university hospital.
Results: Of 197 LTx recipients, hemoptysis developed in 15 over a 16-year period. The pulmonary circulation as well as the systemic circulation were involved in the mechanism of hemoptysis. Six patients had moderate or minimal hemoptysis, while nine patients had life-threatening hemoptysis, which occurred during the first year after LTx in all cases. Active necrotizing ischemic airway injury was present in five of the nine patients with life-threatening hemoptysis. Eight of those nine patients died as a result of hemoptysis. Overall, hemoptysis was the cause of death in 4.5% of patients who underwent LTx at our institution.
Conclusion: In our series of transplant patients, hemoptysis was not rare and was associated with a high rate of mortality.
Key Words: airway • hemoptysis • transplants
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Introduction |
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Since the beginning of our LTx program, we have been confronted by several cases of hemoptysis in transplant recipients, and we have suspected that hemoptysis may have been underreported in LTx patients. Therefore, we aimed to describe the frequency, the cause, the severity, and the outcome of cases of hemoptysis that occurred in LTx recipients. In this article, we present a series of 15 patients who underwent LTx at our center, who developed hemoptysis postoperatively.
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Materials and Methods |
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Of those 216 LTx procedures, 164 (75%) were single-LTx procedures (left lung, 43%; right lung, 32%), and 52 (25%) were double-LTx procedures. The most frequent underlying diseases were emphysema without 
1-antitrypsin deficiency (n = 63; 32%), idiopathic pulmonary fibrosis (IPF) [n = 48; 24%], and emphysema associated with 1-antitrypsin deficiency (n = 32; 16%). The standard operative procedure did not include bronchial revascularization. Following LTx, patients received combination therapy with an anticalcineurin drug (eg, cyclosporine or tacrolimus) with a puric synthesis inhibitor (eg, azathioprine or mycophenolate mofetil) and low-dose prednisone. Perioperative cefamandole was prescribed routinely. If the patient or the donor had previously been colonized by cefamandole-resistant bacteria, specific antibiotics were chosen. IV ganciclovir was administered postoperatively when either the donor or the recipient was seropositive for cytomegalovirus.
The cases of hemoptysis were identified by reviewing all inpatient and outpatient reports concerning the 197 LTx patients. Cases in which hemoptysis was an immediate complication of an invasive medical procedure such as thoracocentesis, transbronchial biopsy, or bronchial dilation were excluded. Cases in which hemoptysis was due to diffuse alveolar hemorrhage were also excluded. The medical files of patients with hemoptysis were analyzed, and the following information was retrieved: underlying diagnosis; type of transplantation; time interval between LTx and hemoptysis; presence of severe ischemic airway injury (IAI); site of bleeding; abundance and etiology of hemoptysis; results of bronchial angiography procedure if performed; and outcome. The abundance of hemoptysis was described as "minimal," "moderate," and "life-threatening," as previously described.14 IAI was described as being severe when bronchial necrosis was present corresponding to grades 3a and 3b of the classification of Couraud et al15 of bronchial anastomotic healing. IAI was described as active when airway necrosis was present at the time of hemoptysis.
Data were expressed as the median (range), and as counts and percentage when appropriate. The time interval between LTx and hemoptysis in patients with life-threatening hemoptysis was compared to that observed in patients with moderate or minimal hemoptysis using the Mann-Whitney nonparametric U test. A p value of < 0.05 was considered to be significant.
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Results |
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1-antitrypsin deficiency (n = 5; 33%), emphysema without 1-antitrypsin deficiency (n = 4; 27%), IPF (n = 3; 20%), silicosis (n = 1), postembolic cor pulmonale (PECP) [n = 1], and fibrosing allergic alveolitis (n = 1). Eight left single-LTx procedures (60%), two right single-LTx procedures (13%), and four bilateral LTx procedures (27%) had been performed in these patients.
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Five of the nine patients (55%) with life-threatening hemoptysis had active severe IAI (patients 1 to 5). In three patients (cases 1, 2, and 3), bleeding originated from a fistula between the bronchus and the adjacent pulmonary artery (ie, bronchus-pulmonary artery [BPA] fistula), the latter developing at the site of active severe IAI. In two other patients with active severe IAI (cases 4 and 5), the cause of hemoptysis could not be determined. Autopsy was not contributive in patient 4 and could not be performed in patient 5.
Patient 6 had a history of severe IAI, resulting in right anastomotic stenosis, which required three bronchial dilation procedures with satisfying local results. This patient also had a concomitant mycotic infection at the site of bronchial anastomosis due to Absidia sp. This infection followed a protracted course until an apparent favorable outcome was obtained after treatment with posaconazole (Schering-Plough; Kenilworth, NJ). Fatal hemoptysis occurred 2 months after the Absidia infection was considered to be controlled. Autopsy was not performed in this patient.
Two patients (patients 8, 9) underwent bronchial artery angiography, demonstrating bronchial hypervascularization. In one patient (case 8), bronchial hypervascularization had developed at the site of the implantation of a metallic expanding airway stent. Bronchial artery embolization was performed and was initially successful, but hemoptysis recurred and the patient died. In the other case (patient 9), hemoptysis originated from the native lung and was attributed to the underlying disease (ie, PECP). In this patient, hemoptysis was controlled by bronchial artery embolization. Patient 7, who had no history of severe IAI, died at home due to unexplained massive hemoptysis.
Moderate or Minimal Hemoptysis
Six patients (3% of LTx recipients) had moderate or minimal hemoptysis. The delay between LTx and the onset of hemoptysis was much longer in patients who experienced moderate or minimal episodes (median duration, 899 days; range, 144 to 3,466 days) than in those who experienced life-threatening episodes (median duration, 61 days; range, 10 to 280 days; p = 0.003). One patient who had moderate hemoptysis concomitant with respiratory failure died (case 14).
Two patients underwent bronchial angiography, demonstrating bronchial hypervascularization (patients 11 and 12). In patient 11, hemoptysis was caused by an unexplained erosive bronchitis in the transplanted lung. In patient 12, hemoptysis was caused by an aspergilloma, which developed postoperatively in the native lung. Hemoptysis was controlled by bronchial artery embolization in both patients. In the remaining patients, bleeding originated from the transplanted lung in three cases (bronchiectasis complicating chronic rejection, patient 10; invasive aspergillosis, patient 13; and endobronchial granuloma, patient 15). The last patient experienced a pulmonary infarction in the native lung secondary to pulmonary embolism (patient 14).
Reperfusion of the Bronchial Circulation in Transplanted Lungs
Bronchial angiography was performed in four single-LTx patients (patients 8, 9, 11, and 12). In all cases, bronchial hypervascularization was documented. In two patients (patients 8 and 11) in whom hemoptysis originated from the transplanted lung, bronchial angiography showed the anterograde perfusion of the bronchial arteries of the graft by vessels developed from the bronchial arteries of the native lung. In two patients (patients 9 and 12) in whom hemoptysis came from the native lung, no reperfusion of the graft by native lung bronchial arteries was observed. No bronchial angiography was performed in double-LTx recipients.
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Discussion |
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The frequency of hemoptysis in LTx recipients is not known and is assumed to be low. Indeed, only eight cases of hemoptysis in LTx patients have been reported in the medical literature published in English between 1993 and 2002,678910111213 and hemoptysis is not listed among the complications of LTx in a recent review.4 The 7.6% incidence of hemoptysis in our series suggests that this complication is not rare after LTx. We suspect that hemoptysis may have been underreported by the other LTx groups so far.
Hemoptysis was frequently severe in our series. Nine patients had life-threatening hemoptysis, and eight of them (4% of LTx recipients) died as a result of this complication. This particular severity is in accordance with published data since hemoptysis was life-threatening in seven of the eight previously reported cases68910111213 and was lethal in four of them.69111213 Another feature that should be underlined is that life-threatening hemoptysis was an early event, with all cases occurring during the first year after transplantation. Similarly, life-threatening hemoptysis was observed early after LTx in the previously reported cases (median, 2 months; range, 1 to 26 months).
A majority of the nine patients (55%) who had life-threatening hemoptysis had concomitant active severe IAI. Severe IAI, which is not a rare event among LTx recipients, is associated with the development of airway complications.16 Besides the known link between severe IAI and the development of airway complications, notably anastomotic dehiscence or stenosis, our observation suggests that severe IAI may also sometimes play a role in the occurrence of life-threatening hemoptysis.
Surprisingly, only one in nine patients with life-threatening hemoptysis had an associated respiratory mycotic infection. By contrast, mycotic infection was causative in five of the eight previously reported cases of life-threatening hemoptysis, with Aspergillus sp being involved in four cases791113 and Candida albicans being involved in one case.6 This raises the question of whether mycotic infection was properly searched for in our patients. However, respiratory secretions recovered during bronchoscopy are systematically evaluated for the presence of fungi at our center. Therefore, it seems unlikely that mycotic infection may have been undiagnosed in our series.
In the general population, hemoptysis originates most often from the bronchial circulation via the development of bronchial hypervascularization while involvement of the pulmonary circulation is rare.17 Since surgical bronchial revascularization is not performed by most centers, including ours, it could be expected that hemoptysis in LTx recipients may have been less frequently related to bronchial hypervascularization than in non-LTx patients. The modifications of the bronchial circulation after LTx are not well-known in humans. In dogs, the reconstitution of an anterograde bronchial circulation has been shown to occur directly across the bronchial anastomosis as soon as 12 days after left lung allografting.18 In our series, two patients with hemoptysis originating from a transplanted single lung underwent bronchial arteriography showing bronchial hypervascularization in the transplanted lung fed by collateral vessels arising from the bronchial arteries of the native lung. In a previously reported7 case of hemoptysis related to bronchial hypervascularization in a double-LTx recipient, a right intercostobronchial arterial trunk was shown to vascularize a pathologic area of the right lung. In those three cases, no direct reperfusion of the bronchial vasculature of the transplanted lung was observed across the bronchial anastomosis. Besides the bronchial arterial circulation, the involvement of the pulmonary circulation was also observed. A fistula between the bronchus and pulmonary artery was documented in three of our patients and in four of the eight previously reported cases.9101112 This suggests that, in contrast to what is observed in the general population, hemoptysis in LTx recipients may frequently originate from the pulmonary circulation. Hemoptysis was massive in all reported cases of BPA fistula in LTx recipients. In those patients, BPA fistula was located at the site of bronchial anastomosis and involved the proximal pulmonary artery, which may explain the severity of hemoptysis despite the fact that it originated from a low-pressure system.
From a clinical point of view, the therapeutic options in cases of life-threatening hemoptysis in LTx patients are limited. This is illustrated by the high mortality rate associated with this complication. However, the successful treatment of life-threatening hemoptysis in LTx patients has previously been reported. Pinet et al11 and Guth et al10 reported two cases of massive hemoptysis related to BPA fistula treated by surgical repair of the fistula and bilobectomy, respectively. In the case of life-threatening hemoptysis arising from the bronchial circulation, arterial embolization may be successful, as was the case in one of our patients (patient 9). Carlsen et al8 and Schoenberger and Darcy7 also reported two cases of life-threatening hemoptysis related to bronchial hypervascularization, which was successfully treated by bronchial artery embolization.
The aim of the present study was to describe the cases in which hemoptysis was the main event, and in which it dominated the clinical scene from a diagnostic and prognostic point of view. Therefore, we chose to exclude cases in which hemoptysis was a manifestation of an otherwise well-defined condition. In particular, we excluded the cases of hemoptysis occurring in the setting of diffuse alveolar hemorrhage. Among the 197 patients in this series, 6 (3%) experienced diffuse alveolar hemorrhage during follow-up. Diffuse alveolar hemorrhage was attributed to thrombotic thrombocytopenic purpura in two cases, to acute vascular rejection in one case, and was of undetermined origin in the three remaining cases. In those six patients, hemoptysis was minimal and was observed after respiratory failure had developed.
In summary, hemoptysis was an often lethal complication in the patients who underwent LTx at our institution, with the most dramatic cases occurring during the first year after LTx. Our data suggest a possible role of severe IAI in the occurrence of life-threatening hemoptysis in LTx patients.
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Footnotes |
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Received for publication September 13, 2005. Accepted for publication November 18, 2005.
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