fusions contributed to renal failure and coagulopathy. Pseudornonas sepsis developed, and the patient died on the twelfth postoperative day.

Transcription

1 Surgical Management of Symptomatic Pulmonary Aspergilloma James W. Battaglini, M.D., Gordon F. Murray, M.D., Blair A. Keagy, M.D., Peter J. K. Starek, M.D., and Benson R. Wilcox, M.D. ABSTRACT Pulmonary aspergilloma is a potentially lifethreatening disease resulting from the colonization of lung cavities by the ubiquitous fungus Aspergillus fumigatus. Complex aspergilloma, characterized by thick-walled cavities with surrounding parenchymal inflammation, is a risk factor for increased morbidity and mortality. Fifteen patients with symptomatic aspergilloma underwent major thoracic procedures at North Carolina Memorial Hospital between January 1, 1972, and December 31, Twelve of the patients had hemoptysis; in 7 it was recurrent and in 5, life threatening. Tuberculosis and sarcoidosis were the most common underlying causes of lung disease, and more than half of the patients had other coexistent serious medical illness. Eleven of the 15 patients were seen with complex aspergilloma; all of the 4 major complications and the 2 deaths occurred in these patients. Bronchopleural fistula with persistent air space was the most common serious complication, and required thoracoplasty in 3 patients. Nine patients, including 5 with complex aspergilloma, had no postoperative complications, and there were no recurrent symptoms in any of the 13 operative survivors over a mean follow-up of five years. It is concluded that aggressive pulmonary resection can provide effective long-term palliation in critically ill patients with symptomatic pulmonary aspergilloma. Aspergilhs, a fungal genus that is ubiquitous in nature, was identified by Micheli in 1729 [l], and its pathogenicity in human beings was described by Bennett [2] in Since the original pathological description by Virchow [2a] of human aspergillosis in 1856, several forms of Aspergillus infection have been recognized, the most unusual of which is aspergilloma. In 1847, Sluyter [31 demonstrated that Aspergi/lus has the capability of colonizing preexisting lung cavities to form a mycetoma, which consists of tangled, septate hyphae, debris, and blood elements. This lesion has a characteristic radiographic appearance described by Deve [4] in Surgical resection of a fungus ball, performed in 1947 and reported in 1948 by Gerstl and co-workers [5], may become necessary when the lesion causes hemoptysis. From the Divisim of Cardiac and Thoracic Surgery, tlenry Ford Hospital, Detroit, MI, and the Division of Cardiothoracic Surgery, University of North Carolina, Chapel Hill, NC. Presented at the Thirty-first Annual Meeting of the Southern Thoracic Surgical Association, Hilton Head Island, SC, Nov 1-3, Address reprint requests to Dr. Murray, 108 Burnett-Womack Building 229H, University of North Carolina, Chapel Hill, NC At present, there is considerable controversy about the optimal treatment for aspergilloma, primarily because the natural history of the lesion is not well defined. Moreover, high morbidity and mortality have been reported from some surgical series. This study reviews the results for all patients who underwent pulmonary resection for aspergilloma at North Carolina Memorial Hospital over a twelve-year period. Material and Method Between January 1, 1972, and December 31, 1983, 15 patients underwent operation for pulmonary aspergilloma on the thoracic surgery service at North Carolina Memorial Hospital. There were 11 male and 4 female patients with an average age of 40 years (range, 22 to 70 years). Follow-up ranged from 6 to 120 months with a mean of five years (60.9 months). Nine of the 12 patients for whom a smoking history could be assessed were heavy cigarette smokers, and 4 patients had a history of heavy alcohol abuse. All patients were symptomatic, with chronic productive cough and hemoptysis being the most common symptoms. Shortness of breath, malaise, weight loss, fever, and chest pain were other presenting complaints. In all patients, chest roentgenograms revealed the classic picture of an intracavitary mass surrounded by a crescent of air. With one exception, the cavities were in the upper lobe or superior segment of the lower lobe. The most common causes of the preexisting pulmonary disease were tuberculosis (5 patients) and sarcoidosis (3 patients). Other causes included leukemia, congenital cysts, tularemia, and pneumonia. In 2 patients, the cause of the cyst could not be determined. Aspergillus was grown from sputum or from bronchoscopy specimens obtained before operation in 6 patients, and serum precipitins were positive in 6 of 7 patients tested. The diagnosis of aspergilloma was confirmed by histopathology in all 15 patients, with the typical findings of branched, septate hyphae. Based on pathological examination, 11 patients had complex aspergilloma (i.e., occurring in a thick-walled cavity with surrounding parenchymal disease) and 4 had simple aspergilloma (i.e., occurring in an epithelium-lined cyst without severe surrounding parenchymal disease). The indications for operation were recurrent gross hemoptysis (7 patients), life-threatening hemoptysis (5 patients), chronic cough with systemic symptoms (2 patients), and progressive infiltrate around a mycetoma cavity in 1 immunosuppressed patient. Surgical procedures included 11 lobectomies, 2 pneumonectomies, 1 wedge resection, and 1 pneumonotomy for removal of 512

2 513 Battaglini et al: Surgical Management of Aspcrgilloma the aspergilloma. In 2 of the lobectomies, segmental resection of the superior segment of the lower lobe was also necessary. Follow-up data were obtained from hospital records, referring physicians, telephone contact with the individual patients, or a combination of these. Results Nine patients, 5 of whom had complex aspergilloma, had no postoperative complications. The average postoperative hospital stay for these patients was 9.2 days, and no patient has had recurrent symptoms over a mean follow-up of 60.1 months. There have been no late deaths in this group. Seven major postoperative complications occurred in 4 patients, all of whom had complex aspergilloma. A bronchopleural fistula with persistent air space developed in 3 patients. Thoracoplasty was required in all 3 and was successful in each. One patient had postoperative empyema, which was successfully managed by initial tube thoracostomy followed by a Clagett procedure. Early postoperative hemorrhage necessitated reexploration in 1 patient who subsequently made an uneventful recovery. Respiratory insufficiency requiring tracheostomy and two weeks of mechanical ventilation occurred in 1 patient in whom a bronchopleural fistula and Serratia pneumonia also developed. The mean postoperative hospital stay for these 4 patients was 30.5 days. Over a mean follow-up of 62.2 months, these patients have had no recurrent hemoptysis. One patient died of atherosclerotic coronary artery disease three years after resection of the aspergilloma. There were 2 deaths in the immediate postoperative period. Both patients had a long history of sarcoidosis and had been on a regimen of steroids for many years. One patient was seen with extensive infiltrates in the right lung as well as a fungus ball in the right upper lobe. She had marked systemic symptoms, and a tension pneumothorax developed preoperatively. Amphotericin B therapy prior to operation had been ineffective, and she was critically ill at the time of operation. A right pneumonectomy was performed, and pathological examination of the lung revealed an aspergilloma as well as invasive aspergillosis (she was the only patient in this series to have invasive disease). The postoperative course was complicated by arrhythmias and signs of sepsis. The patient died of sudden cardiac arrest on the fifth postoperative day. Postmortem examination revealed aspergillosis involving the right pleural cavity and the left lung. The other postoperative death occurred in a woman who underwent a left pneumonectomy. She had recurrent hemoptysis preoperatively as well as an episode of life-threatening hemoptysis. Left upper lobectomy had been planned, but at the time of operation, extensive fibrosis and sarcoid involvement of the hilar nodes made dissection very difficult. Massive hemorrhage from the pulmonary artery occurred, requiring intrapericardial control. Intraoperative hypotension and massive trans- fusions contributed to renal failure and coagulopathy. Pseudornonas sepsis developed, and the patient died on the twelfth postoperative day. Comment Aspergillus infections have been classified into three types: bronchial, invasive, and mycetoma. The bronchial or allergic form is a noninvasive process characterized by productive cough, fever, episodic wheezing, pulmonary infiltrates, and eosinophilia. It is not a condition requiring surgical intervention unless bronchiectasis results. Invasive aspergillosis arises in the lungs, spreads through diseased tissue, and disseminates to other organs under the proper host conditions. Aspergilloma is a saprophytic infection of a preexisting cavity and is the only type of infection that is of surgical importance. When Aspergillus colonizes a preexisting cavity, the result is a fungus ball, or mycetoma, consisting of tangled, branched, septate hyphae with an admixture of blood elements. The great majority of mycetomas are caused by Aspergillus; however, Nocardia, Candida, and Mucor species have also been reported to cause fungus balls [6]. McPherson [7] estimated the prevalence of aspergilloma at 0.01% based on a ten-year survey of chest roentgenograms in a population of 60,000, and a British cooperative study [8] found that patients with a history of tuberculosis and thick-walled lung cavities of more than seven years duration had the highest risk of aspergilloma. In most series involving aspergillomas, tuberculosis-either healed or active-has been the most common cause of the cavitary lung disease, with sarcoidosis, bronchiectasis, congenital cysts, lung abscess, and pulmonary infarct being the other common causes [l, 6, 9-20]. Although Flye and Sealy [21] reported that an aspergilloma developed without an apparent preexisting cavity in 2 patients with cyanotic congenital heart disease, virtually all patients in reported series have had cavitary lung disease. The 15 patients in this series all had preexisting pulmonary cavitary disease. The diagnosis of aspergilloma can usually be made on the basis of its characteristic appearance on the chest roentgenogram, as described by Deve [4] in 1938-a rounded density surrounded partially by a crescent of air (Fig 1). Tomograms are helpful in defining the fungus ball within a cavity (Fig 2), and changes in the position of the patient cause the density to move within the cavity. Radiographically, the differential diagnosis includes blood clot in a cyst, necrotic tumor, abscess with debris, and hydatid cyst after the parasite has sloughed [9, 221. Aspergilloma can often be distinguished from blood clot by the fact that the latter usually lyses over a relatively short period. Spontaneous lysis of an aspergilloma has been observed over long-term follow-up, but this is probably the exception rather than the rule [23]. A 1Y81 report by Fahey and colleagues [24] suggested that the rate of spontaneous resolution may be higher in acutely damaged but previously healthy lung tissue. Cultures grown from sputum or from specimens obtained at bronchoscopy can be helpful in making the

3 514 The Annals of Thoracic Surgery Vol 39 No 6 June 1985 Fig 1. Radicigrapli sliozciing tzc~o typiail asp2r~yillrirtias iri left upper 10fJC CLlZlitk. Fig 2. Toriiogrnrir of sniiic pticvit sliowirig typicnl crrscciit of nir owr C W l? rnycetonm. diagnosis of aspergilloma, especially when combined with typical chest roentgenographic findings. However, a single positive sputum culture has little value because of the ubiquitous nature of Aspergillus [17], and sputum cultures may be falsely negative if the cavity does not communicate with the bronchial tree [l]. Serum precipitins for Aspergillus can help to establish the diagnosis, as they may be positive in as many as 90% of patients with aspergilloma [ 11, 171. Although some surgeons have suggested that the presence of an aspergilloma is an indication for resection [IS], most would agree that an asymptomatic fungus ball requires no treatment. However, there is much less agreement on the management of an aspergilloma that produces symptoms. Hemoptysis is the most common and dangerous symptom of a mycetoma. In reported series, the incidence of hemoptysis in patients with an aspergilloma has ranged from 50 to 83% [17]. Several mechanisms for the hemoptysis have been proposed, including erosion of the vascular cyst wall by motion of the mycetoma, elaboration of endotoxin by the fungus, and the patient s underlying pulmonary disease [ll]. The risk of massive hemoptysis does not seem to be related to the size or duration of the aspergilloma, type of underlying disease, or previous major or minor episodes of hemoptysis [19]. Faulkner and associates [25] argued that most patients with hemoptysis have minor recurrent episodes that can be managed medically with bed rest, humidified oxygen, postural drainage, and appropriate antibiotics for any associated infection. In 1983, Jewkes and co-workers [19] reported a series of 85 patients with aspergillomas, and their data support nonsurgical management of the patient with minor hemoptysis. However, the fact that as many as 30% of patients with minor hemoptysis may subsequently have life-threatening hemoptysis [ 171 lends support for resection of such lesions in good-risk patients. Certainly in most series, including this one, hemoptysis has been the major indication for operative treatment of aspergilloma [l, 6, 9, 11, 12, 201. As was true for our patients, resection has proven to be extremely effective in preventing recurrent hemoptysis in all series. The relatively high morbidity and mortality associated with resection of an aspergilloma have probably contributed to the present controversy over optimal management. The average reported mortality for resection is approximately 10% with a range of 0 to 43% [l, 6, 9, 11, 12, 14-20], and a similar wide variability has been reported for postoperative complications. Many patients with aspergillomas have other serious medical problems, especially pulmonary insufficiency, which make them high-risk surgical candidates; undoubtedly that has been partly responsible for the relatively high mortality. The most common complications have been bronchopleural fistula, persistent air space, and empyema. The great technical difficulty often encountered in resecting aspergillomas results from the dense fibrous tissue around the wall of the cavity, obliteration of the

4 515 Battaglini et al: Surgical Management of Aspergilloma pleural space and fissures, and diseased surrounding lung parenchyma. Lobectomy is the most commonly performed procedure for aspergilloma, and the scarreddown remaining lung will often not expand completely to fill the thorax. Belcher and Plummer [26] divided aspergillomas into simple and complex types. Simple aspergillomas occur in an epithelium-lined cyst without substantial surrounding parenchymal disease, while complex ones occur in a thick-walled cavity with surrounding parenchymal disease. These authors noted that postoperative morbidity was significantly higher in patients with complex mycetomas, and our series confirms that finding, as all major complications and both deaths occurred in patients with the complex type. This also is certainly a reflection of the greater technical difficulty of the operation in those patients. Nonoperative methods of treating symptomatic aspergilloma have been described. In 1968, Henderson and Pearson [27] discussed 3 patients successfully treated by instillation of the antifungal agent natamycin into the aspergilloma cavity. Ramirez [28] used percutaneously placed catheters to instill amphotericin B or sodium iodide into the aspergilloma cavity. There was no systemic toxicity, and the mycetomas resolved. Aslam and colleagues [29] also described successful management of an aspergilloma by intracavitary infusion of sodium iodide. Intracavitary instillation of brilliant green and natamycin were employed in some patients discussed by Jewkes and co-workers [19]. Hammerman and associates [23] demonstrated that intravenous administration of amphotericin B has no efficacy in the treatment of aspergilloma, probably because it does not penetrate the cavity. The disadvantages of these techniques include the need for prolonged instillation and the persistence of the cavity even with successful lysis of the aspergilloma. However, nonoperative management should be considered in the patient who is at great risk for pulmonary resection. Hemoptysis can also be controlled by bronchial artery embolization, which may be used as a temporary or definitive mode of treatment in selected patients [30]. Our present approach to patients with symptomatic aspergilloma is outlined in Figure 3. Based on our experience, we conclude that pulmonary resection is effective management for hemoptysis associated with an asper- ASYMPTOMATIC I OBSERVATION DOCUMENTED / ASPERGILLoMA \.c R1r / HEMoPTYSIS \ POOR GOOD RISK t RESECTION BRONCHIAL EMBOLIZATION INTRACAVITARY INSTILLATION Fig 3. Sugestcd cliriicul appro~?ch to the ptioit 70ith uspqiliorm. gilloma. The patients are often critically ill, have serious underlying medical problems, and have had multiple hospital admissions for hemoptysis. In spite of this, they can be operated on with an acceptable morbidity and mortality, and can remain free from recurrent hemoptysis over long-term follow-up. References 1. Saab SB, Almond C: Surgical aspects of pulmonary aspergillosis. J Thorac Cardiovasc Surg 68:455, Bennett JH: On the parasitic vegetable structures found growing in living animals. Trans R Soc Edinb 15:277, a. Virchow R: Beitrage zur Lehre von den bcim Mcnschen vorkommenden pflanzlichen Parasiten. Virchows Arch [Pathol Anat] 9:557, Sluyter FT: De vegetalibus organismi animalis parasitis ac de movo Epiphyto in pitgreasi versicolors obvio. Diss Inaug Berolini, 1847, p Deve F: Une nouvelle forme anatomoradiologique de mycose pulmonaire primitive: le megamycetome intra bronchiectatique. Arch Med Chir Appar Respir 13:337, Cerstl B, Weidman WH, Newmann AV: Pulmonary aspergillosis: report of two cases. Ann Intern Med 28:662, Eastridge CE, Young JM, Cole F, et al: Pulmonary aspergillosis. Ann Thorac Surg 13:397, McPherson P: Pulmonary aspergillosis in Argyll. Br J Dis Chest 59148, Research Committee of the British Tuberculosis Association: Aspergillus in persistcnt lung cavities after tuberculosis. Tubercle 49:1, Kilman JW, Ahn C, Andrews NC, Klassen K: Surgery for pulmonary aspergillosis. J Thorac Cardiovasc Surg 57642, Reddy PA, Christianson CS, Brasher CA, et al: Comparison of treated and untreated pulmonary aspergilloma. Am Rev Respir Dis 101:928, Solit RW, McKeown JJ, Smullens S, Fraimow W: The surgical implications of intracavitary mycetomas (fungus balls). J Thorac Cardiovasc Surg 62:411, Strutz GM, Rossi NP, Ehrenhaft JL: Pulmonary aspergillosis. J Thorac Cardiovasc Surg 64:963, Hammerman KJ, Sarosi GA, Tosh FE: Amphotericin B in the treatment of saprophytic forms of pulmonary aspergillosis. Am Rev Respir Dis 10957, Henderson RD, Deslauriers J, Ritcey EL, et al: Surgery in pulmonary aspergillosis. J Thorac Cardiovasc Surg 70:1088, Karas A, Hankins JR, Attar S, et al: Pulmonary aspergilhis: an analysis of 41 patients. Ann Thorac Surg 221, 1Y Varkey B, Rose HD: Pulmonary aspergilloma: a rational approach to treatment. Am J Med 61:826, Garvey J, Crastnopol P, Weisz D, Khan F: The surgical treatment of pulmonary aspergillosis. J Thorac Cardiovasc Surg 74:542, Soltanzadeh H, Wychulis AR, Sadr F, et al: Surgical treatment of pulmonary aspergilloma. Ann Surg 186:10, Jewkes J, Kay PH, Paneth M, et al: Pulmonary aspergilloma: analysis of prognosis in relation to hemoptysis and survey of treatment. Thorax 38572, Rafferty P, Biggs B, Crompton GK, et al: What happens to patients with pulmonary aspergilloma? Analysis of 23 cases. Thorax 38:579, Flye MW, Sealy WC: Pulmonary aspergilloma: report of its

5 516 The Annals of Thoracic Surgery Vol 39 No 6 June 1985 occurrence in 2 patients with cyanotic heart disease (case report). Ann Thorac Surg 20:196, Irwin A: Radiology of the aspergilloma. Clin Radio1 18:432, Hammerman KJ, Christianson CS, Huntington 1, et al: Spontaneous lysis of aspergillomata. Chest 64:697, Fahey PJ, Utell MJ, Hyde RW: Spontaneous lysis of mycetomas after acute cavitating lung disease. Am Rev Respir Dis 123:336, Faulkner SL, Vernon R, Brown PP, et al: Hemoptysis and pulmonary aspergilloma: operative versus nonoperative treatment. Ann Thorac Surg 25:389, Belcher JR, Plummer NS: Surgery in bronchopulmonary aspergillosis. Br J Dis Chest 54:335, Henderson AH, Pearson JEG: Treatment of bronchopulmonary aspergillosis with obser vations on the use of natamycin. Thorax 23:519, Ramirez J: Pulmonary aspergilloma: endobronchial treatment. N Engl J Med 271:1281, Aslam PA, Larken J, Eastridge CE, Hughes FA: Endocavitary infusion through percutaneous endobronchial catheter. Chest 57:94, Magilligan DJ Jr, Ravipati S, Zayat P, et al: Massive hemoptysis: control by transcatheter bronchial artery embolization. Ann Thorac Surg 32:392, 1981 REVIEW OF RECENT BOOKS Vascular Surgery. Second Edition Editcd hy Robc-rt B. Rir therford Philudelphin, Snirtiders, ,660 pp, illirsfmtcvf, $ Rrnieiocd /n/ H. V. Liddlc, M.D The second edition of Vosculnr S urpq is a Comprehensive text that addresses all aspects of this discipline. One hundred fifteen recognized authorities have contributed 156 chapters, of which 73 are either new or newly revised. The chapters vary in length and detail from introductory overviews to in-depth discussions. The sections on noninvasive testing for arterial and venous disease provide very inclusive and readable coverage that includes a detailed description of the hemodynamics of normal and altered blood flow. The chapters on vasospastic diseases, causalgia, aneurysms, liver disease and varices, renovascular hypertension, and cerebral ischemia are thorough discussions of the pathophysiology, natural history, treatment (including medical and surgical alternatives), and expected outcome of each condition. The book has some shortcomings. For instance, I believe that the overview essays are often unnecessary and could well be replaced by introductory paragraphs in their respective chap ters. Several chapters are relatively superficial in content, seem to be directed to a medical student audience, and fail to provide source information. The chapter on extraanatomical grafts omits important technical details and pitfalls of operation that should be discussed in depth. The section on deep venous incompetence is superficial, alludes only briefly to the Linton procedure, and, although it describes several surgical approaches, does not defend a definitive mode of treatment for this disorder. However, other chapters, such as the one on hemodynamics and pathophysiology of arterial disease (chapter 4), are basic enough for the student reader yet sophisticated enough to be informative to the clinician. All sections are well referenced and provide the reader with sufficient resource material. In addition to the text references, many authors present an additional selected reference list that pertains to the essential issues discussed in their chapters. This text is sufficiently comprehensive to become a standard for the specialty. Salt Lnkc City, UT