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Eur J Cardiothorac Surg 2002;21:918-923
© 2002 Elsevier Science NL

Results of surgical treatment for pulmonary aspergilloma

Chang Kwon Parka, Sanghoon Jheonb*

a Department of Thoracic and Cardiovascular Surgery, Dongsan Medical Center, School of Medicine, Keimyung University, 194, Dong San Dong, Daegu 700-712, South Korea
b Department of Thoracic and Cardiovascular Surgery, School of Medicine, Catholic University of Daegu, 3056-6, Daemyung-4 Dong, Namgu, Daegu 705-718, South Korea

Received 10 September 2001; received in revised form 8 February 2002; accepted 13 February 2002.

* Corresponding author. Tel.: +82-53-650-4567; fax: +82-53-629-6963
e-mail: jheon{at}cataegu.ac.kr


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Comments
 Appendix A. Conference...
 References
 
Objectives: The purpose of this retrospective study is to analyze the results of the surgical treatment for pulmonary aspergilloma and to confirm that aggressive surgical resection can provide effective outcome for these patients. Patients and method: From 1987 to 2000, 110 patients underwent thoracotomy for treatment of pulmonary aspergilloma in two hospitals. The most common indication for operation was hemoptysis (82%). Underlying diseases were tuberculosis (89%), bronchiectasis (5%), carcinoma (3%), lung tumor (1%) and none (2%). The procedures were lobectomy (74%), segmentectomy (12%), wedge resection (9%), pneumonectomy (4%) and cavernoplasty in two patients. Twenty-nine patients (26%) had severe underlying intrathoracic pathologies. Results: Postoperative complications occurred in 23.6% of the patients including: empyema (n=13), bleeding (n=6), respiratory insufficiency (n=2), wound infection (n=4) and bronchopleural fistula (n=1). There was one hospital death due to panperitonitis after gastric ulcer perforation. Conclusions: We recommend early surgical resection of symptomatic aspergilloma and even asymptomatic cases with reasonable complication.

Key Words: Pulmonary aspergilloma • Hemoptysis • Surgery


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Comments
 Appendix A. Conference...
 References
 
Pulmonary aspergilloma generally forms from saprophytic colonization of pre-existing pulmonary cavities of Aspergillus fumigatus, the most common saprophytic species of Aspergillus in human disease, producing a fungus ball or a mycetoma [1,2]. After formation of fungus ball in pre-existing cavities, antifungal agents are very hard to control. Surgical resection offers the only realistic chance of a permanent cure for aspergilloma [3–5]. But surgical indication is still a controversy because of the high incidence of postoperative complications [6,7]. The purpose of this study is to evaluate our indications and results in the surgical treatment of aspergilloma with specific attention to surgical resection in pulmonary aspergilloma without symptoms.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Comments
 Appendix A. Conference...
 References
 
During a 13-year period from 1987 to 2000, 110 patients in two institutes underwent thoracotomy for resection of pulmonary aspergilloma. There were 70 male and 40 female patients, with an average age of 46±12 years (ranging from 23 to 73 years). One hundred and eleven operations were performed, because one patient with bilateral aspergilloma sequentially underwent operations on both sides.

The clinical records of these 110 patients were reviewed for preoperative symptoms and signs, preoperative chest X-ray and computed tomographic (CT) findings, underlying lung diseases, indications for operation, operative procedure, postoperative complications, mortality, and short-term follow-up. All aspergillomas were retrospectively classified into two groups on the basis of medical imaging and operative findings. Group A includes patients with severe pleural thickening; pulmonary parenchymal destruction of at least one lobe or cavity involves apex chest wall (Fig. 1 ). Other patients with minor intrathoracic pathologies were classified as group B. If cavity is surrounded with normal pulmonary parenchyma, it is also classified as group B (Fig. 2 ). Results were expressed as median value or mean±SD. Comparisons between patients were made by unpaired Student's t-test for continuous variables and by chi square test for categorical variables. A P value of less than 0.05 was considered statistically significant.



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  		Fig. 1. Group A aspergilloma with extensive pulmonary destruction and pleural thickening.

 


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  		Fig. 2. Group B aspergilloma surrounded with relatively healthy lung tissue.

 

   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Comments
 Appendix A. Conference...
 References
 
3.1. Symptom and signs
Hemoptysis, the most frequent symptom, occurred in 90 patients (82%). The degree of hemoptysis was categorized by the amount of blood lost in 24 h. Hemoptysis was considered major if the amount was more than 200 cm3 and minor if less than 200 cm3. Eight and nine patients in each group, respectively, had major hemoptysis. Twelve of these patients (71%) had recurrent major episodes of hemoptysis with increasing frequency. Two patients required emergency operation for treatment of hemoptysis. Cough and chest pain were primary symptoms in 71 patients (64.5%) and 37 patients (33.6%) in each (Tables 1 and 2).


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  		Table 1. Symptoms and signs in 100 patients with aspergilloma

 

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  		Table 2. Hemoptysis status in patients with aspergillomaa

 
3.2. Underlying lung disease
Underlying lung diseases were present in 28 patients (96.6%) in group A and 80 patients (98.8%) in group B (Table 3). Pulmonary aspergillomas formed in patients with various underlying lung diseases, except in two. Tuberculosis in 98 patients (89%), bronchiectasis in six patients (5%), carcinomas (two lung cancer and one esophageal cancer) in three patients (3%), and one patient with benign lung tumor were observed. There was no patient with immunodepression.


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  		Table 3. Underlying lung diseases in 110 patients with aspergilloma

 
3.3. Radiologic findings and diagnosis
Chest radiographic and CT findings were abnormal in all 110 patients. Twenty-nine patients (26.4%) were included in group A and 81 patients (73.6%) in group B. Fifty-four patients (49%) had a preoperative diagnosis of aspergilloma considering their radiological examination only, demonstrating the characteristic fungus ball with the air crescent sign. The cavities were situated in the upper lobes in 81 patients (77%) or in the superior segment of the lower lobe. Cavities were present bilaterally in one patient in group A. The cavity diameter varied from 1.5 to 10 cm (average, 3.6 cm).

Bronchoscopic examination or percutaneous needle biopsy was tried on patients with undetermined mass.

3.4. The indications for operation
The indications for operation are hemoptysis in 90 patients (82%) and undetermined mass or infiltrate lesion in 12 (11%) patients (Table 4). Hemoptysis was the most frequent symptom and also the surgical indication. Group A and group B showed 76 and 84% hemoptysis rate, respectively. Eight patients in group A and nine patients in group B had major hemoptysis. Twelve of these patients had recurrent major episodes of hemoptysis of increasing frequency. Eleven patients preoperatively needed bronchial artery embolization and major hemoptysis was not completely controlled in most of the patients but the amount and frequency of hemoptysis were decreased. Preoperative pulmonary function tests showed a mean forced expiratory volume in 1 s of 2.09±0.77 l in group A whereas it was of 2.65±0.85 l in group B (P=0.008), and % predictive FEV1 of 77.5±21 in group A and 103±28 in group B (P=0.01). We could not obtain data of pulmonary function in 30 cases, nine in group A and 21 in group B because of hemoptysis.


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  		Table 4. Indications for surgery in 100 patients with aspergilloma

 
3.5. Operative procedure
Lobectomy was the most common procedure performed (Table 5). The 110 primary surgical procedures consisted of 81 lobectomies (associated with a wedge resection in ten cases, four bilobectomies and one sequential lobectomies), four pneumonectomies, 13 segmentectomies, ten wedge resections, and two cavernoplasties. Frozen biopsy was made after resection for patients with undetermined mass. There were three concomitant procedures, two decortications, and one esophageal resection and reconstruction for esophageal cancer. Histological examinations with Gomori's Methanamine Silver staining identified Aspergillus in all resected specimens.


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  		Table 5. Surgical procedures performed in 110 patients with aspergilloma

 
Two cavernoplasties were performed for the patients with severe underlying tuberculous lesions and large cavities. The two patients developed empyema postoperatively and needed prolonged chest tube drainage. Out of the 81 lobectomies, one sequential bilateral lobectomy was successfully performed in a patient who had bilaterally tuberculous cavities and fungus ball in the upper lobes with massive hemoptysis but the previous bleeding focus was not confirmed.

3.6. Operative morbidity and mortality
Postoperative course was uneventful in 84 cases (76.4%), and postoperative complications occurred in 26 cases (23.6%) (Table 6). Postoperative complications occurred more frequently among group A. There were nine patients (31%) in group A and 17 in group B (21%). Three patients in group A were reoperated due to excessive postoperative bleeding. Empyema occurred in 13 cases after lobectomy and these with one case of bronchopleural fistula were successfully managed with prolonged tube drainage. All complications developed in group B were successfully managed conservatively.


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  		Table 6. Postoperative complications in 26 patients with aspergilloma

 
There was no direct operative mortality but one hospital death occurred among the 110 patients (0.9%). A patient in group B died of panperitonitis due to gastric ulcer perforation on the 42th day after lobectomy. There was no significant statistical difference of the postoperative morbidity between groups A and B (P=0.274). We could not find the significant statistical difference of complications according to procedures in all cases either.

3.6. Follow-up
Follow-up was completed in the 109 patients, except one who died, and ranged from 1 to 133 months, with a median of 35 months. The surgical result was evaluated from the relief of preoperative symptom, mainly hemoptysis, and the findings on serial chest radiographs. All the patients did well without hemoptysis after operation except for two who still have brochopneumonia pattern on chest radiographs. During follow-up, none of the patients died of pulmonary problem nor had recurrent hemoptysis.


   4. Comments
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Comments
Appendix A. Conference...
 References
 
The spores of Aspergillus fumigatus are widespread in the environment and the organism is commonly found in sputum cultures. Saprophytic colonization of pre-existing pulmonary cavities predominantly in the upper lobes leads to the formation of a fungus ball, aspergilloma. The aspergilloma is a rounded necrotic mass of matted hyphae, fibrin, and inflammatory cells which usually lies free within the cavity. Radiographic and CT scanning show a diagnostic crescentic radiolucency. The cavitary disease results from previous chronic lung diseases such as tuberculosis, sarcoidosis, histoplasmosis, bronchiectasis, bronchogenic cyst, chronic lung abscess, or cavitating carcinoma. Rarely, any obvious evidence of pre-existing pulmonary damage exists. The most common preceding lung lesion in all series is an open healed tuberculous cavity, up to 17% of patients developing an aspergilloma in a 3 year observation period [8]. In most European reports [7,9] patients with pulmonary aspergillomas had a history of previous tuberculosis as a basis for underlying lung disease, as opposed to North American reports, which showed lower incidence of tuberculosis [1]. In our experience, tuberculosis was the cause of cavitary lung disease with fungus ball in 89% of the cases.

The clinical picture of aspergilloma ranges from an incidental radiologic finding to life-threatening hemoptysis. During the 13 years of study period, two different surgeons managed apparently similar cases. We have confirmed that the upper lobes are the predominant sites of aspergillomas. The size of the aspergillomas was variable and bore no relation to the severity of hemoptysis. Eighteen patients (16.4%) were asymptomatic, like those in the series published by Babatasi et al. [10] in which 18% of the patients had no symptoms. The natural history of aspergilloma is not well documented. Few long-term follow-up reports have been published, and in many of the reports, it is difficult to distinguish between the course of the underlying disease and that of the aspergilloma [11–14].

The most common symptom, however, is hemoptysis, which may be mild or severe, even exsanguinating especially in the intracavitary type. In the previous series [14–16], the incidence of hemoptysis in patients with an aspergilloma has ranged from 50 to 83% and is severe or recurrent in 10% [14] which is corresponding to our data, 82 and 15%, respectively. Bleeding classically occurs from bronchial arteries and usually stops spontaneously. Several mechanisms for the hemoptysis have been proposed and included erosion of the vascular cyst wall by motion of the mycetoma, elaboration of endotoxin by the fungus, and the patient's underlying disease [17]. Bleeding could be from intercostal arteries. Extension of the mycotic process with parenchymal destruction at the periphery of the lung invading the adjacent chest wall may lead to erosion of the intercostal arteries [16]. Bleeding from such large arteries is unlikely to stop spontaneously and could be fatal. Neither the size, the complexity of the lesion, the presence of a warning minor hemoptysis, nor the type of underlying disease can predict those patients who will progress to life-threatening hemoptysis [4].

We tried bronchial artery embolization in 11 patients. All patients except one had recurrent episode of hemoptysis suggesting that the roles of bronchial artery embolization are time sparing and better conditioning for surgery, not for permanent intention.

Surgery usually offers three potential benefits: control of symptoms, prevention of recurrent hemoptysis, and possible prolongation of life. However, the technique involved ranks among the most complex in thoracic surgery. Previous series reported mortality rates of up to 25% and morbidity including excessive hemorrhage, residual pleural space, bronchopleural fistula, and empyema of up to 60% [18].The fluctuating nature of the disease process and the modest surgical results restricted surgery to those patients with significant symptoms. But recent reports [19,20] showed a dramatic reduction in both mortality and morbidity. In the absence of effective medical treatment, early surgery in all patients with pulmonary aspergilloma is now recommended.

All patients consulted from the pulmonology department were considered as surgical candidates. For some patients, we performed surgery without their spirometry data because it could cause hemoptysis. So, mean pulmonary function of our series must be lower than the data presented. Even though postoperative pulmonary function could not be expected exactly, we could guess it with CT films and performances before hemoptysis. Those patients with critical bilateral pulmonary destruction with very poor performance before hemoptyisis, such as repeated bronchial arterial embolization, are managed conservatively.

Postoperative complications mainly depend on underlying pulmonary condition. Except minor complications such as wound infection, most major complications are mainly caused by bleeding or dead space. Bleeding is dependent on the severity of pleural thickening or symphysis and dead space is dependent on parenchymal condition. Transfusion is needed for excessive bleeding and can cause ARDS which could be fatal. We believe that the thickness of the cavity wall is not an important factor in the event of excessive bleeding. Pleural thickening especially apex of the lung with cavity invading chest wall makes surgery extremely difficult. Usually, full posterolateral thoracotomy is employed. But in some instances, anterolateral thoracotomy could be selected if tight adhesion is confined only on the apex. Some authors [6] recommended to spare lattissimus dorsi muscle for potential use for close of bronchopleural fistula or filling residual space in second surgery. But it could hinder operative field of first surgery which is most important.

From chest wall incision, every effort should be made toward meticulous hemostasis. Extrapleural approach is not always helpful. After small area dissection with electrocautery, we tightly packed the dissected area with gauze and moved to the other site for dissection. After dissecting and packing, we moved to the previous gauze packed site for further dissection. Using this method, we could minimize loss of blood to avoid transfusion. Dissection is targeted to mediastinal side first which has usually no tight adhesion. After freeing mediastinal side just cephalad to hilum, we can continue dissection of apex bidirectionally, mediastinal side and chest wall side. At the apex, if the cavity invades chest wall, we did not hesitate opening the cavity. If cavity is opened, curettage is needed until necrotic tissues are completely removed. Before completing pulmonary resection, we packed adhesiolysis sites tightly with gauze. After completing the procedure, we again make cauterization of chest wall with Argon beam.

Another point of surgery we suppose is to minimize dead space. After the lung is freed from the chest wall and mediastinum, interlobar fissue which usually has no tissue plane, is divided. If the remaining lung volume does not seem enough, the use of stapler, which could reduce lung volume, is not preferred. After deciding the proper resection level, division is performed with electrocautery. Major air leakage sites are sutured leaving minor leakage sites. Sometimes, we clamp phrenic nerve to induce temporary paralysis. If large volume of dead space is encountered, concomitant thoracoplasty is employed. Some dead space in apex usually does not cause problem. Special attention should also be given when placing two draining chest tubes properly. We did extensive postoperative chest physiotherapy. Bronchoscopy was also frequently employed.

Seventeen patients in group B had complications. Ten patients had postoperative empyema, eight of them were managed by prolonged chest tube drainage and two of them discharged with opened chest tubes which were removed in outpatient clinic after the shortening procedure. Three patients of postoperative bleeding were managed without reoperation. Three patients of wound infection were also managed without difficulty. Even though postoperative morbidity is up to 21% in group B, troublesome complications were in the acceptable range. Furthermore, no major complication developed in 18 patients of asymptomatic cases. We also believe that 31% morbidity rate in group A is acceptable considering the underlying conditions. One case of mortality is not directly related to pulmonary surgery. From these results, we recommend aggressive surgical resection for pulmonary aspergilloma in both symptomatic and asymptomatic patients.


   Footnotes
 
Presented at the joint 15th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 9th Annual Meeting of the European Meeting of the European Society of Thoracic Surgeons, Lisbon, Portugal, September 16–19, 2001.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Comments
 Appendix A. Conference...
References
 
Dr S. Halezeroglu (Istanbul, Turkey): How do you explain your very, very low mortality rate for pulmonary resection for aspergilloma, because I think your mortality rate is lower than that of wedge resection for another simple disease?

Dr Park: We had very good surgical candidates for selection and the experience of the surgeon and postoperative management and localized the lung disease. So they were very carefully selected.

Dr I. Bellenis (Athens, Greece): How long do you cover your patients with antifungal treatment pre and postoperatively and if you have any follow-up for recurrences?

Dr Park: It is not my job. It is the pulmonologist's. I don't know.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Comments
 Appendix A. Conference...
 References
 

  1. Faulkner S.L., Vemon R., Brown P.P., Fisher R.D., Bender H.W. Hemoptysis and pulmonary aspergilloma: operative versus non-operative treatment. Ann Thorac Surg 1978;25:389-392.[Abstract]
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  3. Belcher J.R., Plummer N.S. Surgery in bronchopulmonary aspergillosis. Br J Dis Chest 1960;54:335-341.
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  5. Battaglini J.W., Murray G.F., Keagy B.A., Starck P.J., Wilcox B.R. Surgical management of symptomatic pulmonary aspergilloma. Ann Thorac Surg 1984;39:512-516.[Abstract]
  6. Daly R.C., Pairolero P.C., Pichler J.M., Trastek V.F., Payne W.S., Bermatz P.E. Pulmonary aspergilloma (results of surgical treatment). J Thorac Cardiovasc Surg 1986;92:981-988.[Abstract]
  7. Massard G., Roeslin N., Wihlm J.M., Dumont P., Witz J.P., Morand G. Pleuropulmonary aspergilloma: clinical spectrum and results of surgical treatment. Ann Thorac Surg 1992;54:1159-1164.[Abstract]
  8. British Thoracic and Tuberculosis Association. Aspergilloma and residual tuberculous cavities — the results of a re-survey. Tubercle 1970;51:227-245.[Medline]
  9. Csekeo A., Agocs L., Egervary M., Heiler Z. Surgery for pulmonary aspergillosis. Eur J Cardiothorac Surg 1997;12:876-879.[Abstract]
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  11. Chatzimichalis A., Massard G., Kessler R., Barsotti P., Claudon B., Ojard-Chillet J., Wihlm J. Bronchopulmonary aspergilloma: a reappraisal. Ann Thorac Surg 1998;65:927-996.[Abstract/Free Full Text]
  12. Salerno C.T., Ouyang D.W., Pederson T.S., Larson D.M., Shake J.P., Johnson E.M., Maddaus M.A. Surgical therapy for pulmonary aspergillosis in immunocompromised patients. Ann Thorac Surg 1998;65:1415-1419.[Abstract/Free Full Text]
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  16. Young V.K., Maghur H.A., Luke D.A., McGovern E.M. Operation for cavitating invasive pulmonary aspergillosis in immunocompromised patients. Ann Thorac Surg 1992;53:621-624.[Abstract]
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