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Ann Thorac Surg 2005;79:294-298
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Good Long-Term Outcomes After Surgical Treatment of Simple and Complex Pulmonary Aspergilloma

Young Tae Kim, MD, PhDa,*, Moon Chul Kang, MDa, Sook Whan Sung, MD, PhDa, Joo Hyun Kim, MD, PhDa

a Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, Cancer Research Institute, Xenotransplantation Research Center, Clinical Research Institute, Seoul National University College of Medicine, Seoul, South Korea

Accepted for publication May 14, 2004.

* Address reprint requests to Dr Young Tae Kim, Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, 28 Yongon-Dong, Chongno-Gu, Seoul, 110–744, Republic of South Korea
ytkim{at}shu.ac.kr

Presented at the Poster Session of the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: The long-term outcomes of pulmonary aspergilloma have been known to depend on the underlying lung disease. We analyzed the surgical long-term outcomes for both simple and complex aspergilloma.

METHODS: From 1981 to 1999, 90 surgical procedures were performed on 88 patients with pulmonary aspergilloma. The patients included 44 men and 44 women with a median age of 41 years (range, 12 to 69 years). The underlying lung diseases in the 72 complex aspergilloma cases were 57 tuberculosis (65%), 14 bronchiectases (16%), and 1 emphysema (1.1%). Sixteen (18%) had no underlying lung disease. The procedures performed were 52 lobectomies, 33 segmentectomies or wedge resections, 3 pneumonectomies, and 2 cavernostomies.

RESULTS: One case of operative mortality (1.1%) occurred in complex aspergilloma. Among the other patients, 24 complications developed (27%): 11 prolonged air leaks (longer than 7 days), 7 persistent spaces, 3 postoperative bleedings, 2 empyemas, 2 pneumonias, and 1 wound infection. Risk factor analysis revealed old age and complex aspergilloma as significant risk factors for postoperative complication. One simple and 13 complex aspergilloma patients died during the follow-up period. Only 4 deaths were caused by pulmonary problems. The 10-year actuarial survival rates of simple and complex aspergilloma were 80.0% and 79.6%, respectively. There was no difference between the long-term survival of simple and complex aspergilloma.

CONCLUSIONS: Although the postoperative morbidity rate was higher in complex aspergilloma, surgical treatment for both simple and complex aspergilloma could achieve satisfactory long-term outcomes in selected groups of patients.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Since Belcher and Pulmmer [1] classified aspergilloma into simple and complex types, the decision to perform surgical resection has been controversial because the surgery for complex aspergilloma had been reported with high mortality and morbidity [2]. In cases of simple aspergilloma, the risk of hemoptysis is present but the surgical risk is minimal; therefore, resection is indicated. In cases of complex aspergillomas, resection should be recommended only in low-risk patients because of a potentially higher level of surgical complications. In high-risk patients, secondary procedures, such as cavernostomy with muscle flap transposition, may be used. Regarding long-term survival, patients with simple aspergilloma demonstrated good results for survival when compared with the general population. However, the long-term survival of patients with complex aspergilloma was poor because of their underlying lung disease [2]. We analyzed the surgical long-term outcomes for both simple and complex aspergilloma in Korea, where pulmonary tuberculosis is the main underlying disease of complex aspergilloma.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patient Profile
Between 1981 and 1999, 90 surgical procedures were performed on 88 patients with pulmonary aspergilloma at Seoul National University Hospital. Patients with invasive aspergillosis or allergic bronchopulmonary aspergillosis were excluded. The medical records of all patients were reviewed retrospectively for preoperative signs and symptoms, preoperative chest roentgenographic findings, diagnostic studies, indications for operation, surgical procedures performed, postoperative complications, and long-term follow-up status.

Diagnosis of aspergilloma was made on the basis of the clinical symptoms and radiologic findings, such as tomography or computed tomographic scans. Fiberoptic bronchoscopy was performed to identify the bleeding focus. Sputum cultures were not routinely performed preoperatively. Percutaneous needle aspiration biopsy was performed when malignancy was suspected. We did not routinely perform immunodiffusion tests or sputum culture for fungus.

Based on the roentgenographic finding and pathologic records, we classified the types of aspergilloma retrospectively, according to the classification of Belcher and Pulmmer [1]: the simple type when it developed in isolated thin-walled cysts lined by ciliated epithelium and the surrounding lung is normal, and the complex type when the lesion developed in cavities formed by gross disease in the surrounding lung tissue (Fig 1).



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  		Fig 1. Radiologic findings of simple (a) and complex (b) aspergilloma.

 
We selected patients for surgery if they exhibited symptoms or presented with undetermined mass lesions. In cases with poor pulmonary reserve or with high risk of undergoing a thoracotomy, we recommended conservative treatment such as bed rest, bronchial artery embolization, and antitussive medications. A pathologist reviewed the specimens and described specimen details such as the size of the fungus ball and gross findings of the surrounding lung disease. Histologic examinations with periodic acid-Schiff staining identified Aspergillus species in all resected specimens.

Follow-Up and Statistical Analysis
Follow-up data were obtained from the outpatient clinic chart reviews or by telephone calls to patients or families. The follow-up process ended in September 2001. Four patients were lost during the follow-up period. Operative mortality and death owing to all causes were included in the survival statistics. Statistical analyses for any correlation between the risk factors and the occurrence of complications were performed with the {chi}2 test or Fisher's exact test for univariate analysis and the logistic regression stepwise backward method for multivariate analysis. For survival analysis, Kaplan-Meier's product-limit method with log-rank test was used. Parametric variables were expressed with a mean ± standard error of the mean and nonparametric variables were expressed with frequency. A p value less than 0.05 was considered to be statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The patient sample included 44 men and 44 women with a median age of 41 years (range,12 to 69 years; mean, 41 ± 1 years). The main signs and symptoms were hemoptysis in 40 (45%), blood-tinged sputum in 30 (34%), cough or sputum in 8 (9%), chest pain in 5 (6%), and indeterminate pulmonary nodule in 5 patients (6%; Table 1). In 5 patients, the diagnosis was confirmed after surgical resection for solitary pulmonary nodule. The lesions were located in the right or left upper lobes in a majority of patients (Table 2). In 1 patient, lesions were found in both upper lobes.


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  		Table 1. Present Signs and Symptoms of 88 Patients With Aspergilloma

 

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  		Table 2. Location of Pulmonary Aspergilloma in 88 Patients

 
Sixteen patients (18%) had no underlying lung disease and were classified into the simple aspergilloma group (SA). Seventy-two patients (82%) were classified into the complex aspergilloma group (CA). The underlying lung diseases of the CA group were 57 tuberculosis (65%), 14 bronchiectases (16%), and 1 case of emphysema (1%). None of the patients were immunocompromised.

Lobectomy was the most common procedure performed. Other procedures included segmentectomy, wedge resections, pneumonectomies, and cavernostomies (Table 3). Wedge resection was required in patients with small peripheral lesions. Cavernostomy was performed in 2 patients with poor respiratory functional reserve.


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  		Table 3. Ninety Procedures Performed on 88 Patients With Aspergilloma

 
The size of the fungus ball was measured as a median of 2.25 cm (range, 2.0 to 4.0 cm; mean, 2.6 ± 1.6 cm) in the SA group, compared with a median of 3 cm (range, 1.5 to 6.5 cm; mean, 3.0 ± 1.0 cm) in the CA group. The difference was statistically significant (p = 0.05).

Twenty-six complications developed in 24 patients (27%); 11 prolonged air leaks, 7 incomplete reexpansion, 3 postoperative bleedings, 2 postpneumonectomy empyemas, 2 pneumonias, and 1 wound infection (Table 4). There was 1 case of operative mortality (1.1%) that occurred in the CA group. The patient underwent cavernostomy with latissimus dorsi myoplasty owing to poor pulmonary reserve and experienced complications of postoperative bleeding. He died of hypovolemic shock and respiratory failure. Risk factor analysis revealed old age (p = 0.032) and CA (p = 0.034) as significant risk factors for postoperative complication in univariate analysis (Table 5). These two variables remained as significant risk factors after stepwise backward logistic regression analysis (old age: odds ratio = 2.75, p = 0.044; CA: odds ratio = 3.40, p = 0.046; r2 = 0.140).


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  		Table 4. Postoperative Complications in 88 Patients

 

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  		Table 5. Risk Factors for Developing Postoperative Complications

 
We had four recurrences giving a recurrence rate of 5%. The first patient was a 57-year-old man, who underwent a left upper lobe wedge resection for CA. The postoperative course was complicated with pneumonia, which was successfully controlled with antibiotics. Hemoptysis recurred 16 months later, and the computed tomographic scan showed a recurred fungus ball located near the previous operation site. Because of poor respiratory reserve, bronchial arterial embolization was performed. Unfortunately, the patient died of recurrent massive hemoptysis 18 months later. The second patient was a 51-year-old man, who underwent a right upper lobectomy for CA. The postoperative course was uneventful, but the patient died of massive hemoptysis 5 years later. As the death was reported by telephone contact, the cause of recurrent hemoptysis remains uncertain. The third patient was a 46-year-old woman, who had a left upper lobectomy performed for CA. Postoperatively, the patient suffered from complications of a prolonged air leak lasting 50 days. Fiberoptic bronchoscopy revealed a small bronchopleural fistula, which was sealed up with fibrin glue. The patient did well until she revisited us for recurrent hemoptysis 4 years later. The computed tomographic scan showed multiple bronchiectasis and small granulomas. The patient refused bronchial artery embolization, and she remains alive today. The fourth patient was a 27-year-old woman who had a recurrence of hemoptysis 20 days after right lower lobe wedge resection. We performed a chest computed tomographic scan and found a residual fungus ball, which was treated by right lower lobectomy. The patient is alive without any symptoms.

Among 87 long-term survivors, 13 CA patients and one SA died during the follow-up period. The causes of late death were identifiable in 8 patients: 2 pneumonias, 2 hemoptyses, 2 malignancies, 1 acute myocardial infarction, and 1 traffic accident. We were not able to clarify the cause of death in 5 patients. Four patients experienced hemoptysis during the follow-up period. One of them was treated with further resection, 1 received bronchial artery embolization, and the other 2 patients were not treated. At the time of this study, 2 individuals died of hemoptysis and 2 remain alive, 1 with symptoms and the other without symptoms.

The 10-year actuarial survival rates of SA and CA were 80.0% and 79.6%, respectively. For 15-year rates, actuarial survival was 80.0% and 75.2%, respectively (Fig 2). There was no difference between the long-term survival of SA and CA (p = 0.21).



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  		Fig 2. Long-term survival curves of 87 aspergilloma patients. (CA = complex aspergilloma; SA = simple aspergilloma.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
In 1960, Belcher and Pulmmer [1] classified aspergilloma into two categories: simple and complex. Simple aspergilloma develops in isolated thin-walled cysts lined by ciliated epithelium while the surrounding lung is normal. Complex aspergilloma develops in cavities formed by gross disease in the surrounding lung tissue, such as chronic tuberculosis, chronic lung abscess, advanced sarcoidosis, or bronchiectasis. Patients with CA usually exhibit more severe symptoms and experience a greater number of postoperative complications. Our series indicated that 82% of the patients had an underlying lung disease and, thus, were classified as the complex form. The underlying lung parenchymal disease was not identified in 18% of the patients. Tuberculosis was the most common underlying lung disease in our series. There were many patients whose lung diseases were not that extensive even though there was some extent of disease. We classified patients with any evidence of thick cavity or underlying lung disease as the complex form. Because we included patients with borderline lung disease into the complex form, our series may have a lower rate of severe disease compared with other reports, especially in terms of reporting poor survival [2].

It has been reported that the most common symptom associated with aspergilloma is hemoptysis [3]. About 80% of our patients had either hemoptysis or blood-tinged sputum. Less common symptoms include chronic cough with sputum, clubbing, malaise, weight loss, and reactive airway disease, and our data showed similar results.

The apical portion of the upper lobe and superior segment of the lower lobe were the most common sites of disease in our study, which seems to reflect an association with pulmonary tuberculosis. It has been shown that a significant portion of patients with CA are also immunosuppressed. However, in our series, we did not identify any patient who showed evidence of immunosuppression. This factor may be another reason for our relatively good outcome.

The decision of patient selection for surgery depends on the balance between the risk of disease and risk of surgery. In our practice, we do not hesitate to resect in case of SA because the risk of hemoptysis is present and the surgical risk is minimal. However, owing to a higher surgical risk in CA, we carefully evaluate the patients and only recommended surgery for low-risk patients. We recommend bronchial artery embolization in high-risk patients, and if the procedure fails, we consider secondary procedures, such as cavernostomy with muscle flap transposition. Thus, our series would not represent the whole population of CA.

In a comparison study between medical and resectional therapy, Jewkes and colleagues [4] found a similar 5-year survival between the medical (65%) and resectional (75%) options in a patient group with minor or no hemoptysis. However, for patients with recurrent hemoptysis or a single major bleeding, the 5-year survival was 41% for medical and 84% for resectional treatment groups, suggesting the necessity of resectional therapy for this group of patients. Our surgical outcome of 93% overall survival was a comparable result to other studies.

Operations of CAs are often technically challenging because of the dense fibrosis around the cavity, the obliteration of pleural space and fissures, the enlarged and tortuous bronchial arteries, and the diseased pulmonary parenchyma surrounding the lesion. Inflammatory fibrosis of the pulmonary parenchyma and pleura may cause the remaining lung to be unable to fully expand to fill the pleural space after resection. Our series showed that 32% of the patients with CA experienced various postoperative complications, with prolonged air leak and residual space the most common problem. It has been suggested that various techniques, including a pleural tent, pneumoperitoneum, decortication, muscle flap, omental transposition, or, in rare condition, thoracoplasty, should be considered after resection [2, 5, 6]. However, we did not perform additional myoplasty other than in patients who received cavernostomy.

Mortality, morbidity, and long-term survival depend on patient selection and proper management. The average reported operative mortality ranges from 0% to 43% [1, 7–10]. Daly and associates [2] reported surgically treating 53 patients with aspergilloma. Their study showed a 23% rate of operative mortality with the majority of deaths happening in patients with CA (34% in CA versus 5% in SA). Postoperative morbidity was also significantly higher in cases of CA (78% in CA versus 33% in SA), and this could be the result of widespread pulmonary disease and the secondary bacterial infection. Our results of 1% mortality and 32% morbidity in CA are much better. A possible explanation for the improved results could be the differences of the underlying lung disease and its severity, as well as a more stringent patient selection.

The underlying pulmonary condition is an important factor in determining the outcome because most deaths are caused by chronic respiratory failure or pneumonia [11]. Patients with SA seem to have good results of comparable survival to the general population [2]. However, the long-term survival of CA has been reported to be poor as many individuals die owing to an underlying lung disease. In our series, however, there was no statistically significant difference of long-term survival rates between SA and CA. This result suggests that if patients are carefully selected, we may expect good long-term outcomes in the complex form comparable to that in SA.

Recurrence of aspergilloma has been reported in 7% of patients after resection [4]. We had four recurrences, for a recurrence rate of 5%. Therefore, careful long-term follow-up is recommended.

In conclusion, although postoperative morbidity was higher in CA, surgical treatment, for both SA and CA in a selected group of patients, could work to bring about positive long-term outcomes.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Belcher J, Pulmmer N. Surgery in broncho-pulmonary aspergillosis. Br J Dis Chest. 1960;54:335–341
  2. Daly RC, Pairolero PC, Piehler JM, Trastek VF, Payne WS, Bernatz PE. Pulmonary aspergilloma. Results of surgical treatment. J Thorac Cardiovasc Surg. 1986;92:981–988[Abstract]
  3. Kim YT, Trastek VF. Mycotic infection of the lung. Pearson FG, Cooper JD, Deslauriers J, et al. Thoracic surgery. New York: Churchill Livingstone; 2002. p. 577–612
  4. Jewkes J, Kay PH, Paneth M, Citron KM. Pulmonary aspergilloma: analysis of prognosis in relation to haemoptysis and survey of treatment. Thorax. 1983;38:572–578[Abstract/Free Full Text]
  5. al-Zeerah M, Jeyasingham K. Limited thoracoplasty in the management of complicated pulmonary aspergillomas. Thorax. 1989;44:1027–1030[Abstract/Free Full Text]
  6. Massard G, Roeslin N, Wihlm JM, Dumont P, Witz JP, Morand G. Pleuropulmonary aspergilloma: clinical spectrum and results of surgical treatment. Ann Thorac Surg. 1992;54:1159–1164[Abstract]
  7. Eastridge CE, Young JM, Cole F, Gourley R, Pate JW. Pulmonary aspergillosis. Ann Thorac Surg. 1972;13:397–403[Medline]
  8. Karas A, Hankins JR, Attar S, Miller JE, McLaughlin JS. Pulmonary aspergillosis: an analysis of 41 patients. Ann Thorac Surg. 1976;22:1–7[Abstract]
  9. Kilman JW, Ahn C, Andrews NC, Klassen K. Surgery for pulmonary aspergillosis. J Thorac Cardiovasc Surg. 1969;57:642–647[Medline]
  10. Saab SB, Almond C. Surgical aspects of pulmonary aspergillosis. J Thorac Cardiovasc Surg. 1974;68:455–460[Medline]
  11. Suen H, Wright C, Mathisen DJ. Surgical management of pulmonary aspergillosis. Chest Surg Clin N Am 1993;3:671–81



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