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Ann Thorac Surg 2005;80:1067-1072
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Clinical Profile and Surgical Outcome for Pulmonary Aspergilloma: A Single Center Experience

Jayesh Gopal Akbari, MS a , Praveen Kerala Varma, MCh a , * , Praveen Kumar Neema, MD b , Madathipatt Unnikrishnan Menon, MCh a , Kurur Sankaran Neelakandhan, MCh a

a Department of Cardiovascular and Thoracic Surgery, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
b Department of Anesthesiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India

Accepted for publication March 16, 2005.

* Address reprint requests to Dr Varma, B-8, New Faculty Quarters, Chitra Staff Quarters, Poonthi Road, Thiruvananthapuram, Kerala 695 011, India (Email: pkvarma{at}sctimst.ker.nic.in; varmapk{at}gmail.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: This retrospective study was designed to study the clinical profile, indications, postoperative complications and long-term outcome of pulmonary aspergilloma operated in our institute.

METHODS: From 1985 to 2003, 60 patients underwent surgery for pulmonary aspergilloma at Sree Chitra Tirunal Institute for Medical Sciences and Technology.

RESULTS: The group consisted of 36 male patients and 24 female patients with a mean age of 42.7 ± 11.8 years. The most common indication for surgery was hemoptysis (93.3%). The common underlying lung diseases were tuberculosis (45%), bronchiectasis (28.3%), and lung abscess (11.6%). Fourteen patients (23%) had simple aspergilloma (SA) and 46 (77%) had complex aspergilloma (CA). The procedures performed were lobectomy (n = 55), pneumonectomy (n = 2), segmental resection (n = 2), and cavernoplasty (n = 2). One patient underwent bilateral lobectomy at 14 months interval. The operative mortality was 4.3% and 0% in CA and SA, respectively (p = 1.0). Major complications occurred in 26.1% patients of CA, whereas none occurred in SA (p = 0.052). The complications included bleeding (n = 2), prolonged air leak (n = 4), empyema (n = 4), repeated pneumothorax (n = 1), and wound dehiscence (n = 1). Three patients needed thoracoplasty. The mean follow-up period was 40 ± 24 months. The actuarial survival at 10 years was 78% and 92% for CA and SA, respectively. There was no recurrence of disease or hemoptysis.

CONCLUSIONS: Surgical resection of pulmonary aspergilloma prevents recurrence of hemoptysis. Complex aspergilloma resection was associated with low mortality but significant morbidity, whereas SA had no associated early mortality and morbidity. Long-term outcome is good for SA and satisfactory for CA.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Aspergillus organisms colonize preexisting lung cavities and produces a fungus ball, or aspergilloma [1]. Healed tuberculous lesions, benign lung abscess, and cavitary bronchiectasis are fertile grounds for Aspergillus to smolder. After formation of fungus ball, antifungal agents are usually ineffective [2], and often surgical treatment is required. The goals of the surgery are prevention hemoptysis with preservation of lung parenchyma. Although successful lobectomy for pulmonary aspergilloma (PA) was described in 1948 [3], surgical resection was infrequent because of the high incidence of complications and mortality. Nevertheless, studies have shown that surgery for PA can be undertaken with a low complication rate, and surgical resection is now accepted as the treatment for PA [4–6]. Some authors [4–6], because of the risk of massive hemoptysis, recommend prophylactic resections of PA. The benefits of the surgery are prevention of hemoptysis and growth of mycetoma, eradication of the pyogenic component, and probable prolongation of life. In this study, we review the indications for and short- and long-term outcome of all patients who underwent surgery for PA.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Population
During a 19-year period (1985 to 2003), 60 patients were surgically treated for PA at Sree Chitra Tirunal Institute for Medical Sciences and Technology. The group consisted of 36 male patients and 24 female patients with a mean age of 42.7 ± 11.8 years. The clinical record of these patients were reviewed for preoperative symptoms, chest radiography, computed tomography (CT) findings, preoperative preparation, technique of anesthesia and postoperative analgesia, surgical procedure performed, postoperative complications encountered, and long-term follow-up status.

Diagnosis and Classification
The diagnosis was suspected on chest radiography in all the patients. In the initial part of the study, tomography (13.3%, n = 8) and more recently CT scan (86.7%, n = 52) had confirmed the classical picture of an intracavitary mass surrounded by air crescent. All aspergillomas were retrospectively classified based on medical imaging and operative findings as either simple aspergilloma (SA) or complex aspergilloma (CA), according to the description reported by Belcher and Plummer [7]. Simple aspergilloma had a thin-walled cavity with little or no surrounding parenchymal disease (Fig 1). In contrast, CA had a thick-walled cavity, surrounding parenchymal disease, and greater pleural thickening (Fig 2A and 2B). Immunologic tests were not done in any case. Aspergillus organisms were histologically confirmed on all resected specimens.



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  		Fig 1. Computed tomography scans of a simple aspergilloma patient, showing a cavitary lesion with an air crescent (arrow) with minimal pleural thickening. The rest of the lung parenchyma was normal.

 


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  		Fig 2. Computed tomography scans of a complex aspergilloma patient showing cavitary lesion with an air crescent in the (A) supine and (B) lateral decubitus with pleural thickening. The rest of the lung parenchyma was destroyed.

 
The degree of hemoptysis was categorized by the amount of blood lost in 24 hours. Hemoptysis was considered massive if the amount lost was more than 300 mL, severe if between 150 to 300 mL, moderate if less than 150 mL, and minimal if sputum was blood stained. Preoperative pulmonary function tests were done in all cases except those who had recent bout of hemoptysis.

Operative Preparation
Preoperative preparation of the patients included cessation of smoking, improvement of nutritional status, and a short course of antibiotics, if required. Antifungal agents were not used. All patients, including patients undergoing cavernoplasty, were operated on under general anesthesia. The lung isolation was ensured by the use of a double-lumen endobronchial tube. All patients received intermittent lumbar epidural buprenorphine 3 to 5 µg/kg in 7.5 mL of normal saline for postoperative analgesia and for ensuring active participation in postoperative chest physiotherapy.

Operative Technique
In all patients, the surgical procedure was performed through posterolateral thoracotomy. The pleural space was entered through the fifth space. Initially, minimal adhesiolysis was done to permit the placement of a small blade retractor; further adhesiolysis was done with electrocautery. The practice was to dissect at one place and then pack the dissected area with sponges and continue dissection at another place. It was observed that, once the entire lung was released this way, the oozing stopped. In case of posttuberculous sequel with cavity in the apex of the chest and dense fibrosis with adhesion to subclavian vessels, after quarantining the area of the lung, the cavity was opened, taking care to prevent spillage. After evacuating the content of the cavity and removing the diseased lobe, only a minimum amount of cavity wall was left on the surface of the subclavian vessels. In this way, major bleeding from injury to the subclavian vessels was avoided. The pulmonary vessels were ligated with silk tie and then transfixed with nonabsorbable suture. The lung was transected using vascular clamps through the relatively healthy lung and sealed by running fine polypropylene sutures. The policy was to underrun the area of major air leak with pledgetted fine suture. The bronchial stump was closed with two figure-of-eight stitches of polypropylene, and an extra stitch was taken only if air leak was present on water seal testing. However, stapler or sealant like fibrin glue was not used. Primary thoracoplasty or latissimus dorsi muscle flap for filling the dead space were not done in any case. Extrapleural dissection was also not performed. Two chest tubes, one anterior apical and the other posterior basal, were placed in all cases. In patients who underwent cavernoplasty, the cavity was incised and the fungus ball was removed, and the area of air leak was underrun with suture. Thereafter, the chest wall was closed after inserting two chest drains.

Postoperative Care
All patients were shifted to a dedicated thoracic surgery intensive care unit and were extubated after ensuring complete lung reexpansion and recovery from anesthesia. The majority of the patients were extubated within 2 to 6 hours. During the immediate postoperative period, continuous low suction in the range of 15 to 20 cm H2O was applied to the chest tube bottle in all cases. Postoperative analgesia by the epidural route was continued for a minimum of 48 hours, and the patients were given intensive chest physiotherapy. Bronchospic clearance of retained secretions was undertaken if required. Patients were shifted to the ward only if the air leak was minimal and chest radiograph showed satisfactory expansion of the ipsilateral lung.

Postoperative bleeding was considered excessive when total drainage in the first 24 hours exceeded 1 liter. Prolonged air leak was defined as any air leak lasting more than 10 days. Operative death was defined as any death occurring in the first 30 days or during the initial hospital admission. All operative deaths and death due to any other cause were included for survival statistical analysis.

Follow-Up
Follow-up data were completed from the case records; in addition, a letter was sent to all survivors operated on before 2002, requesting them to attend our outpatient department. The patients were evaluated by clinical history and physical examination by the first and second author. Chest radiographs, posteroanterior and lateral views, were evaluated. Patients operated on after 2002 were followed up at 6 months. Follow-up was completed in February 2004.

Statistical Analysis
Analysis was done using SPSS for Windows (version 11.0; SPSS, Chicago, Illinois) by a biostatistician. Continuous variable were expressed as mean ± SD, and proportions were compared with Fisher’s exact test. Survival probability was calculated by the Kaplan-Meier method, plotted at monthly intervals with the day of surgery as the starting point.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Symptoms and Indication for Surgery
Table 1 denotes the symptoms. Hemoptysis was the most frequent indication for surgery. Hemoptysis was massive in 3 patients (5.3%) and severe in another 8 patients (14.2%); 10 of them underwent successful bronchial artery embolization, and 1 required emergency surgery for failed embolization. Moderate to minimal hemoptysis was seen in 45 patients (80.3%). Twenty patients (33.3%) had superimposed infection proven by sputum culture and received antibiotic therapy according to antibiotic sensitivity.


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  		Table 1. Symptoms in 60 Patients
 
Underlying pulmonary pathology was detected in 91.6% of patients (Table 2).


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  		Table 2. Underlying Pulmonary Pathology
 
Radiology and Spirometry
The location of cavities is denoted in Table 3. Cavity diameter varied from 2 to 8 cm (mean 4.5 cm). Computed tomography scan was effective in differentiating SA and CA (Fig 1 and 2) and gave an overall picture of lung pathology. Preoperative pulmonary function tests showed a restrictive pattern in 36 patients (60%), obstructive in 2 patients (3.3%), and normal in 5 patients (8.3%). In 17 patients (28.3%; 5 SA and 12 CA), pulmonary function testing was not done because of a recent bout of hemoptysis.


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  		Table 3. Chest Radiography Findings
 
Operative Procedures
The operative procedures were as shown in Table 4. One patient underwent bilateral upper lobectomy at 14 months interval. Another patient previously operated on for right classic Blalock-Tausig’s shunt for tetralogy of Fallot underwent right upper lobectomy. Cavernoplasty was performed in 2 patients (3.2%); both of them presented with severe hemoptysis and bilateral severe lung destruction. Two CA patients underwent pneumonectomy for destroyed lung.


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  		Table 4. Procedures in 60 Patients
 
Operative Mortality
In-hospital death occurred in 2 patients of CA. The first patient, who underwent cavernoplasty, died on the 50th day of surgery because of respiratory failure. The second patient, a case of tetralogy of Fallot with right classic Blalock-Taussig’s shunt, underwent right upper lobectomy and died on the 10th day of surgery of bronchopneumonia. No perioperative mortality occurred in the SA patients. There was no statistical difference in mortality between the two groups (p = 1.0).

Postoperative Morbidity
Twelve complications developed (26.1%) in CA patients (Table 5), whereas none occurred in SA patients (p = 0.05). Major blood loss occurred in 2 patients, who required reexploration. Overall, mean postoperative blood loss was 340 ± 150 mL (range, 150 to 1,200 mL). Prolonged air leak existed in 4 cases, and 2 of them were reexplored; pnuemostasis was achieved with muscle pledgetted sutures in the one patient; the second patient required decortication. Four patients had empyema; in 3 of them thoracoplasty was required, and the fourth patient underwent decortication. One case each had repeated pneumothorax and wound dehiscence.


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  		Table 5. Complications
 
Long-Term Outcome
The mean follow-up period was 40.7 ± 24 months (range, 6 to 194). One patient in the SA group was lost to follow-up at 3 months. Five others were lost to follow-up in the CA group, 2 patients after 3 months and 3 patients after 1 year. Four patients died in the intervening period in the CA group, 3 of miscellaneous causes and 1 because of respiratory failure. Personal follow-up was completed in the remaining 48 patients (80%). There was no recurrence of hemoptysis or PA in any patient. Forty patients (83.3%) are in functional class I, 6 patients (12.6%) are in functional class II, and 2 patients (4%) are in functional class III. Chest radiography did not show any abnormality in 44 cases; in 2 cases it showed infiltrates, and in 2 cases there was residual insignificant apical airspace. Ten-year actuarial survivals in the SA and CA groups were 92% and 78%, respectively (Fig 3).



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  		Fig 3. Kaplan-Meier actuarial survival curve. At 5 years and 10 years for patients with simple aspergilloma ([SA]Group A), it was 92% and 92%, respectively; whereas for patients with complex aspergilloma ([CA] Group B), it was 85% and 78%, respectively. The number of patients at risk is shown below the curve. (Cum. = cumulative.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Pulmonary tuberculosis is highly prevalent in developing countries. One study [8] reported development of PA in 21% of patients after chronic pulmonary disease, of which pulmonary tuberculosis was the most common underlying pathology. Aspergilloma occurs in preexisting pulmonary cavities, predominantly in the upper lobes. The most common cavitary lesion in all series is tuberculosis; in one series [9], aspergilloma developed in as many as 17% of the patients during a 3-year observation period. In most European and Asian reports, the incidence of previous tuberculous lesion is high, as opposed to North American reports [10]. In our series also, tuberculosis (45%) was the leading cause for the development of PA. However, no underlying lung pathology could be detected in 8.4% of patients, which was similar to other reports [11].

Indications for Surgery
Like other series, the most common indication for surgery was hemoptysis. In previous series, the incidence of hemoptysis ranged from 50% to 83% and was severe or recurrent in 10% [12]; the respective figures in our series were 93% and 8%. The bleeding usually occurs from bronchial arteries and is self-limiting. Extension of the mycotic process with parenchymal destruction may invade the chest wall, leading to erosion of the intercostal arteries and bleeding [13] and can be fatal [2]. The outcome of the patients treated conservatively for massive hemoptysis was poor; in one series, 4 of 10 patients who were not operated on died [14]. In our series, bronchial artery embolization was performed in 11 patients, and was successful in 10 patients. This modality was used to tide patients over the crisis and prepare the patient for surgery and not for permanent intention. As recurrent and fatal hemoptysis can occur in patients thus palliated, and the results of bronchial artery embolization are variable [11]; these patients underwent surgery during the same hospital admission. No patient was asymptomatic, as opposed to the 18% and 22% prevalence of asymptomatic patients reported by Jewkes and colleagues [2] and Babatasi and coworkers [11], respectively. This can be explained by the fact that our center is a tertiary referral center to which only symptomatic patients are referred for surgical options.

Surgical Technique, Complications, and Early Outcome
In our series, the commonest surgical procedure performed was lobectomy (90%). Lobectomy in PA was found to be difficult in view of extensive adhesions between the lung, pleura, diaphragm, and mediastinum. The fissure was often obliterated. Segmentectomy was done in 2 cases of SA with limited disease. Cavernoplasty was considered for poor-risk candidates based on spirometric data and CT scan findings. Of the 2 cavernoplasties performed, 1 patient died of respiratory failure whereas the other patient is alive after 72 months of the surgery in functional class III. Percutaneous cavernostomy may have been a better option in these patients as it carries less risk of postoperative respiratory failure. Pneumonectomy was performed in 2 cases—in 1 patient with posttuberculous destroyed lung and in 1 patient with multiple PA involving multiple lobes. One patient is in functional class III after 184 months, and other patient is in functional class II after 12 months of surgery. Widespread disease, multiple unilateral aspergilloma, or destroyed lungs because of the primary underlying condition were the common indications for pneumonectomy in other reports [4]. Pneumonectomy was difficult in view of the extensive adhesions, mediastinal shift, and indurated hilar structures. However, in centers that often deal with posttuberculous destroyed lung, this procedure can be undertaken safely. In the present series, in 3 patients thoracoplasty was performed for empyema as a subsequent procedure—2 after lobectomy and 1 after cavernoplasty. Decortication was required in another patient. The outcome after the secondary procedures was good without further mortality or morbidity.

Previous series [15] reported overall mortality rates of 22% and as high as 34% for CA. But recent reports showed significant reduction in morbidity and mortality [11, 16–19]. The overall operative mortality rate in our series was 3.3%, death occurred only in CA (4.34%). In our series, the overall morbidity rate was 20%, which was similar to other series [20]. We attribute this to proper preoperative preparation of the patients, our experience in the operative management of posttuberculous complications, and aggressive postoperative chest physiotherapy.

Contrary to the earlier report [13], pleural space problems were minimal in our series, we believe that the reasons are (1) full mobilization of the lung through the transpleural route, (2) effective hemostasis, (3) lung resection through the healthy lung, (4) judicious use of crushing of the phrenic nerve, (5) aggressive postoperative chest physiotherapy, and (6) continuous low suction to keep the lung expanded. For similar reasons, the problems of bleeding and empyema were minimal, and bronchopleural fistula was not encountered.

Limitations
Selection bias could have occurred, as only patients who they thought would be benefited by surgery were referred by chest physicians for surgical options. As this was a retrospective study, cardioarrhythmic events were not analyzed.

In summary, we recommend aggressive surgical resection for pulmonary aspergilloma. Preoperative preparation of the patient, meticulous surgical technique, and postoperative care reduced the rate of complications, which was absent for simple aspergilloma. Complications still occurred in complex aspergilloma and were largely related to the underlying lung pathology; however, the overall long-term outcome was good.

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   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We wish to thank Mr Lijji Kumar of the Medical Illustration Department for all illustrations, and Dr P. S. Mathuranath, DM (Neurology), and Prabhakaran Sankara Sarma, PhD, for their statistical assistance.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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