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Ann Thorac Surg 2000;69:898-903
© 2000 The Society of Thoracic Surgeons

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Original Articles

Aspergilloma: a series of 89 surgical cases

^a Department of Thoracic Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, France

Address reprint requests to Dr Regnard, Service de Chirurgie Thoracique, Centre Chirurgical Marie Lannelongue, 133 Ave de la Résistance, Le Plessis Robinson, 92350, France

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Surgery for pleuropulmonary aspergilloma is reputed to be risky. We reviewed our results, focusing attention on the postoperative complications.

Methods. During a 20-year period, 87 patients were operated on for pulmonary (86) or pleural (3) aspergillomas. Seventy-two percent of patients were complaining of hemoptysis. Eighty-nine resections were performed because there were two bilateral cases. Seventy percent of aspergillomas had developed in cavitation sequelaes from tuberculosis disease. Thirty-four patients had severe respiratory insufficiency that allowed us to perform only lobectomy (18), segmentectomy (2), or cavernostomy (14).

Results. Thirty-seven lobectomies (five with associated segmentectomies), two bilobectomies, 21 segmentectomies, 10 pneumonectomies, and 17 cavernostomies were performed. Total blood loss exceeded 1,500 mL in 14 cases, and 71% of patients required blood transfusion. There were five postoperative deaths (5.7%), related to respiratory failure (2), infectious complication (1), pulmonary embolus (1), and cardiorythmic disorder (1). Incomplete reexpansions were frequently seen in patients undergoing lobectomies or segmentectomies. No death or major complications occurred in asymptomatic patients. During follow-up, none of the patients had recurrent hemoptysis.

Conclusions. Surgical resection of aspergilloma is effective in preventing recurrence of hemoptysis. It has low risk in asymptomatic patients and in the absence of underlying pulmonary disease. Incomplete reexpansion is frequent after lobectomy and segmentectomy, especially when there is underlying lung disease. Cavernostomy is an effective treatment in high-risk patients. Long-term prognosis is mainly dependent on the general condition of patients.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Aspergilloma generally results from colonization of an existing lung cavity by Aspergillus fumigatus, the most common saprophytic species of Aspergillus in human disease, producing a fungus ball or a mycetoma [1, 2]. Patients with aspergillomas should undergo surgical treatment, because there is a risk of sudden life-threatening hemoptysis, and because there is no effective alternative medical therapy. Patients with poor general condition and those with pulmonary insufficiency related to extended underlying lung disease are especially at risk for postoperative complications [3–10]. The aim of this work was to study our indications and results in the surgical treatment of aspergilloma over the last two decades, with specific attention to the analysis of postoperative complications.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
During a 20-year period (1977 to 1997), 87 patients were operated on for pulmonary aspergilloma. There were 61 male and 26 female patients with a mean age of 49 years (ranging from 13 to 73 years). Eighty-nine operations were performed, because 2 patients with bilateral aspergillomas underwent operations on both sides.

Charts were reviewed for clinical presentation, underlying lung disease, operative procedure, postoperative mortality, complications, and long-term outcome. According to previous reports [2, 6, 7, 9, 10], patients were classified as having simple or complex aspergilloma on the basis of medical imaging and of operative findings: simple aspergilloma was defined as a thin-wall cavitation occurring in an otherwise healthy lung, whereas complex aspergilloma occurred either in a thick-walled cavitation or in the presence of severe underlying parenchymal and pleural sequelae, or both. Clinical data as well as postoperative mortality were compared between subgroups of patients with the Student’s t and the ² test. Survival rates were obtained according to the actuarial method derived from the Kaplan-Meir method [11]. Operative mortality was included in the survival statistics, and survival differences between subgroups were compared by the log-rank test. Statistical significance was obtained for any value of p less than 0.05.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Underlying disease
Except for 7 patients without any underlying lung disease, pulmonary aspergillomas arose on various underlying lung disease, which are indicated in Table 1. Tuberculosus represented the main underlying disease (69%). Its incidence decreased significantly in a recent period 1987 to 1997 (p < 0.05) (Table 2). Among the 60 patients presenting lung sequellaes from tuberculosis, we observed 35 cases of cavitations and bronchectasies, 20 cases of destroyed lungs or lobes (13 of them had undergone previous segmentectomies), 2 cases of lung abscess cavities, and 3 cases of pleural empyemas. Four patients had received intensive courses of chemotherapy for treatment of extrapulmonary cancers. Two patients with a past history of lung cancer presented Aspergillus colonization on radiation pneumonitis sequelaes, and received amphothericin B administration for several weeks before operation without any positive effect. Moreover, 2 other patients had received long-term corticosteroid administration in the years before operation.

Diagnosis of aspergillomas
Sixteen patients had a preoperative diagnosis of aspergilloma considering their radiological examination only, demonstrating the characteristic fungus ball with the air crescent sign. Fifty-six patients had, in addition, a positive serodiagnosis of aspergillosis disease with more than three precipitin reactive archs, whereas 6 other patients had also the presence of A fumigatus on culture after broncho-alveolar lavage or bronchial brushing. Finally, serodiagnosis was positive in 62 patients, negative in 10 patients, and equivocal in 6, whereas 9 patients did not have this preoperative serological examination. Eleven aspergillomas (those occurring among asymptomatic patients) were only diagnosed on tissue sample cultures and on histological examinations of resected lung masses. Cultures of intracavitary material identified A fumigatus in all but 2 cases, where the specific species could not be stated. Histological examinations with periodic acid-Schiff staining identified Aspergillus in all resected specimens. In regard to the aspects of radiological imaging and of operative finding, there were 8 cases of simple aspergillomas (9%) and 82 cases (92%) of complex aspergillomas. The 8 cases of simple aspergillomas included all 7 cases occurring in the lungs without underlying disease and 1 case occurring inside a congenital cyst. Seven of 8 (87.5%) patients presenting simple aspergillomas were operated on these last 10 years. Only 1 patient in this group was possibly immunocompromised, receiving long-term corticosteroid administration in the years before operation.

Symptoms and rationale for operations
Eleven patients (12%) were free of symptoms, demonstrating radiological chest lesions only. In such patients, operation was decided upon to determine the etiology of their lesions. Nine out of these 11 asymptomatic patients have been operated on these last 10 years. In the 76 other patients, surgical treatment was decided because of the following symptoms: 63 patients (72%) were complaining of hemoptysis (10 with cough and bronchitis in association), and 13 (15%) were complaining of chronic cough only or associated with low-grade fever. Forty-seven of the 63 patients presenting hemoptysis had a history of minor and recurrent hemoptysis in the weeks or months before operation, whereas the remaining 16 patients had a single episode of bleeding. Eighteen of the hemoptysis cases were severe, demonstrating bleeding exceeding 200 mL. Preoperative embolization was performed in these 18 cases; it was successful in 9 cases, stopping recurrence of bleeding, unsuccessful in 6 cases, and it diminished severity of hemoptysis in the remaining 3 cases, but without complete disappearance. Forty-four patients (51%) had loss of weight, which exceeded 10% of the usual total body weight in 14 of them. Thirty-four patients (38.2%) with severe respiratory insufficiency (predicted postpneumonectomy forced expiratory volume in 1 second [FEV1] less than 33% of the theoretical values) underwent 18 lobectomies, two segmentectomies, and 14 cavernostomies because we thought they would not have tolerated larger resections.

Sixteen patients underwent antifungal therapy before operation, with no response in 12 cases, and with an incomplete response in 4 cases. As indicated in Table 2, the incidence of asymptomatic forms significantly increased in the recent period (1987 to 1997) when compared with that of the previous period (1977 to 1987) (p < 0.05).

Surgical procedure, operative findings, and blood loss
Eighty-nine surgical procedures were performed, because 2 patients had bilateral aspergillomas occurring on chronic tuberculous bronchectasies. These 2 patients were managed as follows. One patient underwent lobectomy on one side and segmentectomy on the opposite side 2 months later, with simple postoperative recovery. The second patient, with limited respiratory function, underwent segmentectomy first, and an emergency contolateral lobectomy 20 months later, because he suffered from recurrent hemoptysis that was not controlled by embolization. Unfortunately, he died on day 29 because of respiratory failure with lung sepsis. The 89 primary surgical procedures consisted in 37 lobectomies (associated with a segmentectomy in 5 cases), two bilobectomies, 21 segmentectomies, 10 pneumonectomies, 17 cavernostomies, and two open drainage through thoracostomy for treating two pleural empyemas. In 63 patients, severe pleuro-pulmonary bleeding adhesions led us to perform an extrapleural dissection with decortication before resection of lesions. In 5 patients who demonstrated a limited predicted postoperative FEV1 less than 1 L, a tracheostomy was performed at the end of the operation, to avoid mechanical ventilation and to prevent, as much as possible, postoperative pulmonary complications related to prolonged ventilation. The 3 patients with pleural localization of aspergillomas were operated on as follows. Two patients with poor general status and low pulmonary condition precluding any parenchymal resection underwent external drainage through thoracostomy, whereas the third patient underwent pleuropneumonectomy. After cavernostomy and thoracostomy, patients have daily bandage with insertion of gauze, sometimes impregnated with amphothericin B in the cavity, for several weeks.

All 8 patients presenting simple aspergillomas underwent either lobectomy (in 5 cases) or segmentectomy (in 3 cases).

Mean intraoperative and postoperative blood loss within the first 24 hours was 820 ± 660 mL (range 100 to 2,600 mL). Total blood loss (preoperative and postoperative) exceeded 1,500 mL in 14 patients, and a total of 62 patients (71%) required blood transfusion. Hemorrhage exceeding 1,500 mL was noticed at a 40% rate after pneumonectomy (4 of 10) and at a 21.6% (8 of 37) rate after lobectomy (NS).

Operative mortality, postoperative complications, and reoperations
There were five postoperative deaths (postoperative mortality: 5.6% [5 of 89]). All these deaths occurred in patients who had undergone lobectomy. Two of these patients had limited pulmonary function and were considered liable to support no more than a lobectomy, one of them being operated on in an emergency for recurrent hemoptysis after failure of embolization. Both patients died of pulmonary insufficiency with sepsis after 29 and 35 days of prolonged ventilation, respectively. One patient died of empyema with bronchial fistula on day 20. Two other patients died suddenly, 1 of cardiorythmic disorders on day 1, and the other of pulmonary embolus on day 12.

Postoperative course was uneventful in 54 cases (60.6% [54 of 89]), and postoperative nonfatal complications occurred in 30 cases (33.7%). These nonfatal complications, which were sometimes associated, are depicted in Table 3 according to the surgical procedure. Five patients were reoperated on for excessive postoperative bleeding. Prolonged air leaks occurred in 9 cases and were successfully managed with prolonged drainage. There were 15 incomplete reexpansions with residual pleural spaces, which required prolonged drainage in 3 cases, and intensive physiotherapy in the remaining 11 cases. There were also seven empyemas, which were treated with open drainage through thoracostomy in 3 cases, and with surgical evacuation of infected fluid and irrigation drainage in 2 cases. The remaining 2 cases of empyema were associated with bronchial fistulas, one occurring after lobectomy and the other after pneumonectomy. They were successfully managed with prolonged irrigation and drainage, followed by secondary thoracoplasty. Two patients required a prolonged postoperative ventilation, of 14 and 15 days, respectively. Three other patients presented various nonlethal but severe cardiorythmic disorders. In total, 12 patients were reoperated on: 5 for excessive bleeding, and 7 for treating empyemas as aforementioned. These reoperations are depicted in Table 4 according to the initial surgical procedure.

Long-term outcome
Follow-up was completed in the 82 patients who survived their operations, and ranged from 8 to 168 months, with a median of 40 months. During follow-up, none of the patients had recurrent hemoptysis. During the follow-up period, 9 patients had another operation. There were three thoracoplasties, three reenlargements of cavernostomy, three closures of cavernostomy, and one closure of open thoracostomy. Twenty-one patients died: 14 of miscellaneous diseases, 4 of respiratory failure, and 3 of cachexia. Among the 61 patients remaining alive, 33 had no symptoms, 19 had moderate symptoms related to mild chronic pulmonary insufficiency, and 9 had severe chronic pulmonary insufficiency. The 5-year actuarial survival rate for the entire group was 66%. No difference in survival was observed according to the surgical procedure. The survival of patients with preoperative loss of weight exceeding 10% of their usual body weight was significantly diminished. Their 5-year actuarial survival rate was only 30% (p < 0.05).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Diagnosis
Although more than 1,000 species of Aspergillus organisms have been identified, very few species may cause human disease, A fumigatus being the most common type [1, 7]. Usually, the spores are of low virulence in an immunocompetent host but can produce aspergilloma that results from saprophytic colonization of an existing lung or pleural cavity, producing a fungus ball [1, 2]. The spore can also be a source of necrotizing bronchopneumonia in immunocompromised patients, leading to an invasive form with dissemination [7, 11–14]. In our series, all cases concerned true aspergillomas. In a few cases, colonization may have been facilitated by transitory immunosuppression due to chemotherapy or corticosteroid administration. All kinds of cystic and of cavitary parenchymal or pleural disease sequelae may be involved, such as old cavities occurring in the course of sarcoidosis, lung cancers, and bacterial abscess. However, old chronic tuberculosis cavities remain the most frequent underlying disease, and was recorded in 70% of our cases. Like other authors [10], we observed in recent years an increased incidence of asymptomatic forms of cases occurring on the lungs without any underlying disease. However, we have still observed in recent years a 60.4% rate of aspergillomas occurring in tuberculous lung sequelae, which is a higher rate incidence than the 17% rate reported by Chatzimichalis and associates [9] during an equivalent period (1992 to 1997).

As demonstrated in our study, and according to other series [4, 5, 7, 9], the diagnostics is based on various signs. Among those, the presence of radiological opacity with the air crescent sign is of specific importance. This air crescent sign reflects the presence of a fungus ball in a parenchymal cavity. The presence of Aspergilli on cultures must be interpreted by the physician, who may decide whether they are of pathological significance, knowing that spores of Aspergilli are easily inhaled and then identified in sputum and secretion. The serodiagnosis may be negative or doubtful, as we have observed in 20.5% of cases in our series.

Indications of surgical treatment
The most frequent symptom indicating surgery is hemoptysis, because of the risk of massive and fatal hemoptysis [4, 5]. In the series of Karas and associates [4], of 10 patients with hemoptysis who were not treated surgically, mainly because they were poor operative risks, 4 died. Seventy-two percent (63 of 87) of our indications concerned patients who suffered from hemoptysis, which was severe in 25% of cases and recurrent in 75% of cases. Our results confirm that surgery is effective for stopping hemoptysis; none of our patients presented with recurrence of hemoptysis after the operation, even if it was a cavernostomy only. Bronchial artery embolization was effective in 50% of the cases where it was attempted in our series, allowing immediate cessation of life-threatening hemoptysis. Therefore, surgical treatment was planned without emergency. However, because we considered embolization as a temporizing measure, and because recurrent fatal hemoptysis has been reported in the weeks after embolization [15], we recommend not delaying the operation too long. Because, in asymptomatic patients, some authors [5, 16] have estimated that major hemoptysis may occur with a rate incidence of 20%, surgery is also indicated to prevent hemoptysis in such patients. In our study, like others [10], operation was more and more often indicated to determine the etiology of a lung lesion, most often incidentally discovered, in asymptomatic patients, without past history of tuberculous disease. As demonstrated in our study, like in other recent studies [9, 10], the risk of surgical resection is minimal in such asymptomatic patients. Intervention is necessary not only to treat symptoms and prevent fatal hemoptysis, but also to prevent deterioration of patients’ condition with profound cachexia [17]. When patients have limited respiratory function or poor general condition, the risk for major complications after lung resection is obvious. Our study demonstrates that minimal surgical management with cavernostomy is safe in such patients, and that it is an effective method to prevent recurrences of hemoptysis. Consequently, we think surgery remains, to date, the mainstay of treatment of aspergillomas, being more effective than antifungal medical treatments, which are often not satisfactory, even when recent drugs such as itraconazole are administered or when intracavitary injection of drugs is attempted [18–20], the intracavitary diffusion of drugs being hampered by fibrosis. In patients who seem able to tolerate lung resection, key questions remain to determine what is the amount of lung parenchyma that is necessary to safely resect the lesion, and how the remaining lung parenchyma is able to reexpand, avoiding any postoperative space problems.

Operative risk and factors of postoperative complications
Our postoperative mortality rate of 5.6% is comparable with those reported in the literature, ranging from 7% to 10% [9, 21, 22] (Table 5). According to previous authors [6, 7, 9, 10], patients with simple forms, who have either normal lungs or simple cysts, are likely to present simpler and better postoperative recovery, when compared with patients who have complex forms. In such cases, the residual lung parenchyma after lobectomy or segmentectomy may be too altered and too insufficiently compliant to expand and obliterate residual pleural space, with the risk of prolonged air leak, fluid collection, and empyema. As a matter of fact, as shown in Table 5, the mortality rate ranged in the literature from 0% to 34% in complex forms. In our series, the mortality rate was 0% for simple forms and 6.2% for complex forms, confirming the prognosis significance of this classification. However, simple forms were infrequent in our experience. In our study, postoperative mortality occurred only in patients who underwent lobectomy, with a 13.5% rate. Moreover, up to 30% of the patients who underwent lobectomy suffered from incomplete lung reexpansion, and 16% from prolonged air leak. These complications were managed as usual, with prolonged chest tube drainage and physiotherapy, whereas some cases required reoperation for thoracoplasty. Two cases of empyema with broncho-pleural fistula were successfully managed with irrigation-drainage followed by secondary thoracoplasty. In these 2 cases, alternative treatment could have been plombage of the chest cavity using either muscle or omental flap [8]. These postoperative space complications are particularly feared when important pleural and parenchymal sequellae are observed on radiological examinations and computed tomography scanning. In up to 25% of their cases, Personne and associates [23] performed additional thoracoplasty after lobectomy in order to prevent postoperative space problems. We are considering this approach for the near future.

Primary pleural aspergilloma infection is rare, described in 3 cases in the current series. Shirakusa and associates [8] have previously reported 5 such cases, whereas most of the 16 cases reported by Massard and associates [9] were fungal empyemas that occurred secondarily, after surgical treatment of various non-Aspergillus diseases. Decortication or pleuropneumonectomy when lung destruction is associated, may be required, as in 1 of our cases. However, we agree with other authors [8] that open-window thoracostomy followed by daily insertion of gauze impregnated with amphotericin B is a good alternative option in the treatment of A empyemas, as we performed in 2 physically weak patients in our series. As for cavernostomy, the thoracostomy can be secondarily closed by muscle flap.

Conclusion
Surgical resection is effective in preventing recurrence of hemoptysis. In the postoperative period, incomplete reexpansions after lung resections are frequent and responsible for severe complications. The realization of a thoracoplasty immediately after lung resection should be considered any time lung reexpansion appears too insufficient to fill the residual cavity. In debilitated patients who are at risk for lung resection, cavernostomy is an effective and well-tolerated procedure, and could be secondarily closed by muscle plombage.

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