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ScienceDirect www.sciencedirect.com Médecine et maladies infectieuses 45 (2015) 128–132

Original article

Chronic pulmonary aspergillosis: A frequent and potentially severe disease L’aspergillose pulmonaire chronique : une pathologie fréquente et potentiellement grave H. Benjelloun a,∗ , N. Zaghba a , N. Yassine b , A. Bakhatar a , M. Karkouri b , M. Ridai c , A. Bahlaoui b a

Service des maladies respiratoires, hôpital Ibn Rochd, Casablanca, Morocco Service d’anatomie pathologique, hôpital Ibn Rochd, Casablanca, Morocco c Service de chirurgie thoracique, hôpital Ibn Rochd, Casablanca, Morocco

b

Received 5 November 2014; received in revised form 6 January 2015; accepted 29 January 2015 Available online 18 February 2015

Abstract Introduction. – Chronic pulmonary aspergillosis is a pulmonary fungal infection with various presentations that can occur on a pre-existing cavity, often a sequel of tuberculosis. The objective of our study was to report the diagnostic and therapeutic management of pulmonary aspergilloma in our structure. Patients and methods. – We retrospectively studied 81 cases of pulmonary aspergilloma having occurred in the respiratory diseases unit of the Casablanca Ibn Rochd hospital, over 11 years. Results. – We included 48 male and 33 female non-immunocompromised patients, with an average age of 51 years (27–75). A history of tuberculosis was recorded in 78 cases. Hemoptysis was the revealing symptom in 73 cases. A characteristic “bell-like” image was observed in 25 cases. The serological results were positive for aspergillus in 54 cases. The treatment was surgical in 50 cases and medical in 24 cases. Five patients died. Discussion. – A significant number of pulmonary aspergilloma cases were recorded in our study, occurring most frequently on sequels of tuberculosis. This disease is currently common in countries highly endemic for tuberculosis; early and adequate management is required. Conclusion. – Aspergillosis is a frequent and potentially severe disease occurring on pre-existing lesions, most often in our context sequels of tuberculosis. Surgical resection is the reference treatment but is the cause of a significant morbidity and mortality. Preventive measures are mandatory. © 2015 Elsevier Masson SAS. All rights reserved. Keywords: Aspergilloma; Mycosis; Sequel of tuberculosis; Hemoptysis

Résumé Introduction. – L’aspergillose pulmonaire chronique est une infection mycosique pulmonaire qui peut prendre différents aspects et survenir sur une cavité préexistante, le plus souvent séquellaire d’une tuberculose. L’objectif de ce travail est de rapporter la prise en charge diagnostique et thérapeutique des aspergillomes pulmonaires chez des patients non immunodéprimés dans notre structure. Patients et méthodes. – Nous rapportons une étude rétrospective portant sur 81 cas d’aspergillome pulmonaire colligés au service des maladies respiratoires du centre hospitalier universitaire Ibn Rochd de Casablanca, sur une période de 11 ans. Résultats. – Il s’agissait de 48 hommes et 33 femmes non immunodéprimés. La moyenne d’âge était de 51 ans (27–75). L’antécédent de tuberculose était noté dans 78 cas. L’hémoptysie était le symptôme révélateur dans 73 cas. L’image caractéristique en grelot était relevée dans 25 cas. La sérologie aspergillaire était positive dans 54 cas. Le traitement était chirurgical dans 50 cas et médical dans 24 cas. Cinq décès étaient rapportés. Discussion. – À travers cette étude, un nombre important d’aspergillome pulmonaire était recensé, survenant pour la plupart sur des séquelles de tuberculose. Cette affection est, à ce jour, fréquente dans les pays à forte endémie tuberculeuse d’où la nécessité d’une prise en charge précoce et bien adaptée. ∗

Corresponding author. E-mail address: hanane [email protected] (H. Benjelloun).

http://dx.doi.org/10.1016/j.medmal.2015.01.014 0399-077X/© 2015 Elsevier Masson SAS. All rights reserved.

H. Benjelloun et al. / Médecine et maladies infectieuses 45 (2015) 128–132

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Conclusion. – La greffe aspergillaire est une pathologie fréquente et potentiellement grave survenant sur des lésions préexistantes le plus souvent tuberculeuse. La chirurgie d’exérèse demeure la thérapeutique de référence mais la cause d’une morbimortalité non négligeable. Les mesures préventives restent indispensables. © 2015 Elsevier Masson SAS. Tous droits réservés. Mots clés : Aspergillome ; Mycose ; Séquelles de tuberculose ; Hémoptysie

1. Introduction Pulmonary aspergillosis is an opportunistic pulmonary mycosis pulmonary fungal infection with various presentations depending on the underlying condition and the patient’s immune status. Pulmonary aspergilloma is the development of Aspergillus hyphae in pre-existing cavities, usually sequels of tuberculosis [1–3]. It can present as simple pulmonary aspergilloma or chronic cavitary pulmonary aspergillosis (CCPA) [4]. Surgical resection is the only truly curative treatment and should be planned as soon as possible to prevent sometimes-fatal infectious and hemorrhagic complications. The severity of the disease is related to its morbidity and mortality [5]. The objective of this study is to describe the epidemiological, clinical, diagnostic and treatment of this fungus.

2. Patients and methods We conducted a retrospective descriptive study of 81 cases of pulmonary aspergilloma collected from August 2003 to September 2014, in the respiratory diseases unit, at the Casablanca Ibn Rochd Teaching hospital. We selected the records of all HIV-negative non-immunocompromised patients who were diagnosed with pulmonary aspergilloma according to radiological, clinical, and/or biological, and/or histological data. An information sheet was studied for each patient. It included epidemiological (age, gender), clinical (underlying condition or clinical history), and laboratory (chest imaging, bronchoscopy, aspergillus serology) data. The hospital morbidity and mortality, as well as the short and long-term outcome were also considered. The definition of aspergillus infection is not clearly defined and many entities have been described with various names. The classification of the Infectious Diseases Society of America (IDSA) distinguishes simple pulmonary aspergilloma (SPA) from chronic pulmonary aspergillosis (CPA) [6]. The latter is classified as: chronic cavitary pulmonary aspergillosis (CCPA), former complex aspergilloma; chronic necrotizing pulmonary aspergillosis (CNPA); and chronic fibrosing pulmonary aspergillosis (CFPA), with specific diagnostic criteria. This classification divides aspergilloma into 2 categories: SPA and CCPA. [6] SPA is a parenchymal cavity with well defined edges evolving without associated pleural parenchymal abnormalities [2]. CCPA is defined as the occurrence of multiple cavities that may or may not contain an aspergilloma, associated with pulmonary and systemic symptoms, and elevated inflammatory markers [6–8].

Table 1 Clinical presentation of pulmonary aspergilloma cases. Présentation clinique des cas d’aspergillomes pulmonaires.

History of tuberculosis Delay between onset of tuberculosis and aspergillosis 2–10 10–20 20–23 Hemoptysis Dyspnea Chronic bronchorrhea Thoracic pain Wasting Fever

Number

Percentage (%)

78

96.3

32 43 6 73 56 27 30 19 12

39.5 53.1 7.4 90 69.1 33.3 37 23.4 14.8

Our series is an illustration and a description of APCC in a non-immunocompromised population with a high prevalence of tuberculosis. 3. Results Forty-eight male and 33 female patients were diagnosed with pulmonary aspergilloma during the study period. The average age was 51 years (27 to 75 years). Seventy-eight (96.3%) patients had a history of treated pulmonary tuberculosis. The average delay between the onset of tuberculosis and aspergillosis was 12.87 years (2 to 23 years). Eighteen (22.2%) patients were smokers and 4 of these presented with chronic obstructive pulmonary disease (COPD), and 4 (5%) patients presented with well-controlled non-insulin dependent diabetes. No short or long-term oral or inhaled corticosteroid therapy was documented. The reasons for consulting were: hemoptysis in 73 (90%) cases (Table 1), with an average delay since the onset of symptoms of 3 months (2 days to 7 months). The clinical examination revealed a retracted hemithorax in 11 (13.6%), stertorous breathing in 72 (89%) patients, and wheezing in 28 (34.5%) patients. Thoracic imaging (Table 2), including X-rays and CT scan performed in every cases, revealed pleural thickening in 38 (47%) patients, cavitary image in 26 (32%) patients, and a characteristic “bell-like” image in 25 (31%) patients. The lesions were predominant in the upper lobes, 74 (91.3%) patients. Laboratory tests results revealed an accelerated sedimentation rate in 28 (34.5%) patients, hypochromic microcytic anemia in 17 (21%) patients with a range of 6.4 to 11.1 g/dL, and leukocytosis with a predominance of PNN in 13 (16%) patients with

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Table 2 Thoracic imaging of pulmonary aspergilloma. Imagerie thoracique des aspergillomes pulmonaires. Number

Percentage (%)

Pleural thickening Image of cavities “Bell-like” image Lung necrosis

38 26 25 23

47 32.1 30.8 28.4

Uncomplicated pulmonary aspergilloma Chronic pulmonary aspergilloma Superior lobes Right side Image of cavities

8 73 74 62 26

9.8 90.2 91.3 76.5

a range of 9,700 to 14,500 cells/mm3 , without neutropenia, controlled by the prescription of empiric antibiotic therapy. The cytobacteriological direct examination of sputum, performed in 15 (18.5%) patients, was negative. A flexible bronchoscopy, performed in all our patients, revealed endobronchial bleeding in 20 (24.7%) patients, aspergillosis mycetoma in 4 (5%) patients, a bronchial inflammatory condition in 45 (55.5%) patients, and was substantially normal in 5 (6%) patients. Aspergillus fumigatus was isolated in the bronchial aspirate of 9 (11%) patients. Screening for the Koch bacillus by direct examination and culture of sputum and bronchial aspirate was negative in every case. The HIV serology was negative in every case, as well as the hydatid serology performed in 8 (9.8%) patients, all in good condition, from rural areas, presenting with histologically confirmed SPA. The aspergillus serology performed in all patients was positive in 54 (66.6%) cases. It was performed with the immuno-electrophoresis technique (IEP) in 62 (76.5%) patients, with a positive threshold > 3 precipitation arcs, and with the passive hemagglutination technique in the remaining patients, with a positive threshold > 1/320. The diagnosis of pulmonary aspergilloma was made for all patients according to radiological aspect, association of suggestive radiological signs and serology positive for Aspergillus, mycological samples, or postoperative histological findings, after ruling out some differential diagnoses mimicking pulmonary aspergilloma, including ruptured pulmonary hydatid cyst, a tubercular caseous focus, atypical mycobacteriosis, an excavated lung tumor, etc. (Table 3). The treatment was surgery in 50 (61.7%) cases; lobectomy was performed in 27 (54%) cases, pneumonectomy in 13 (26%) cases, segmentectomy in 8 (16%) cases, and cavernostomy in 2 (4%) cases. Table 3 Elements of positive diagnosis of pulmonary aspergilloma. Éléments du diagnostic positif des aspergillomes pulmonaires.

Typical “Bell-like” image Serology positive for Aspergillus fumigatus Isolation of Aspergillus fumigatus in bronchial aspiration fluid Histology

Number

Percentage (%)

25 54

30.8 66.6

9 50

11 61.7

An exclusively medical treatment based on itraconazole was prescribed in 24 (29.6%) patients presenting with CPA for an average of 7 months. This therapy was recommended for inoperable patients (severely altered lung and/or cardiac function, and/or extent of lesions). Seven patients refused any treatment after hemoptysis was stopped and were lost to follow-up. The aspergillus infection was classified as SPA in 8 (9.8%) patients, 2 of these were diabetic, the clinical symptoms were mild, the treatment was exclusively surgical, and the outcome was good with no recurrence of hemoptysis after an average follow-up of 2 years and 4 months. Aspergillosis was ranked CPA in other patients whose clinical symptoms were more severe and 42 (57.5%) patients underwent surgery. The postoperative outcome of patients presenting with CCPA, formerly known as complex aspergilloma, was good, with no recurrence of hemoptysis in 35 (83.3%) cases, including for 2 diabetic patients, after an average follow-up of 4 years and 2 months. Four patients presented with recurrence of hemoptysis after 6 to 24 postoperative months and a diagnosis of bacterial superinfection of tuberculosis sequels was made. Three patients died postoperatively, all presenting with COPD and CCPA. The outcome of patients treated with antifungals only was marked by the recurrence of hemoptysis in 12 (50%) cases. This could be explained by the unavailability of treatment in our context and the extent of lesions. Two patients presenting with non-operated CPA died from sudden hemoptysis.

4. Discussion Aspergillosis is one of the most frequent opportunistic pulmonary mycoses. The intracavitary aspergilloma is by far the most common presentation. Aspergillus fumigatus is the species most often implicated in human disease, in temperate countries. It is responsible for 80 to 90% of pulmonary aspergillosis cases [1,2,9,10]. Histologically, the aspergilloma is a saprophytic proliferation of aspergillus spores organized as in a dense mycelial felting, or “mycetoma” within a preformed cavity [9,11,12] that is often a sequel of tuberculosis [3,8,13–15]. This infection was observed in 96.3% of our patients. This rate is comparable to the literature data, 71.1% of cases as reported by Chen et al. [15], 79.4% by Zait et al. [2], or even 100% by Ade et al. [5]. Conversely, 11 to 17% of post-tuberculous cavities can be complicated by aspergilloma [7,12,16]. This high percentage could be explained in our study by the susceptibility of young Moroccan male patients to tuberculosis infection. This disease is still common in areas of high TB endemicity where the pandemic HIV infection helped to increase the spread of this disease. However, any parenchymal cavity is likely to be complicated by aspergillosis, including bronchiectasis, bullous emphysema, and sarcoidosis. Other conditions may also be complicated by aspergillosis such as pneumoconiosis, fibrosis of ankylosing spondylitis or scleroderma, excavated lung cancer, bacteriologically sterilized lung abscess, pulmonary infarction sequels, cysts, sequesters [2,3,8,10,16–19].

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Pasquier et al. reported a case of pulmonary aspergilloma in a patient presenting with severe thalassemia [19]. Hemoptysis remains the hallmark of pulmonary aspergilloma and is reported in 50 to 95% of cases, according to the authors [8,9,14,15,20,21]. This is what was observed in our series where 90% of our patients consulted for hemoptysis. That said, the recruitment of patients in our pneumology department probably explain the high rate of hemoptysis revealing the aspergillus infection. This infection is often recurrent, sometimes abundant, and life threatening [7,20]. Other nonspecific signs may be observed such as cough, sputum, chest pain, and dyspnea [3,22]. Chronic pulmonary or systemic symptoms lasting for more than 3 months suggest CPA [4,8]. The aspergilloma is discovered during systematic X-ray screening in 10 to 30% of cases [9]. Chest CT is the first-line examination for the positive topographic diagnosis, to look for other locations, and the monitoring of lesions [9]. It also allows discriminating between SPA and CPA or CCPA [1,3,9,22–24]. The characteristic image is a cavity containing a rounded or oval mass, well defined, dense, and homogeneous, declive, and mobile, which may contain calcifications [3,9,11,13,14]. The surrounding pleura is thickened and may be the earliest sign [6]. When the mycelial mass is large, the “meniscus sign” can be observed. When the mass is small, a “bell-like” image can be observed, typical of the aspergilloma. Other atypical aspects may be observed leading to misdiagnosis as lung abscess, cavitary carcinoma, or ruptured hydatid cyst [3,7,11,25,26]. The aspergilloma is usually located in the upper lobes [7,8,14], as reported by Mimouni et al. [27] in 79.1% of cases and in our study in 91.3% of cases. The characteristic “bell-like” image was observed in respectively 66% and 30.8% of cases compared to only 12.8% as reported by Zait et al. [2]. This preferential topography is related to tuberculosis that usually affects the upper lobes [9,22]. The aspergilloma is often unique, sometimes multifocal and bilateral [9,27]. Bronchoscopy is required. It allows: ruling out some differential diagnoses, including lung tumors; locating the source of bleeding; visualize an aspergillus mycetoma, performing mycological and histological samplings for diagnostic purposes. Some authors have even used it for therapeutic purposes, as for the intrabronchial administration of amphotericin [28]. Serodiagnosis is a key contributor for the positive diagnosis of aspergilloma [8]. It allowed diagnosing 66.6% of patients in our series, a percentage close to the 63% reported by Caidi et al. [21] and slightly lower than the 75.86% reported by al Ade. [5]. However, serology may be falsely negative in 5 to 10% of cases, due to the death of the fungus, to a luminal blood clot, to cases of aspergilloma related to other fungi, in case of corticosteroid therapy, or to dysfunction of the T cell response in immunocompromised patients [21,29,30]. The detection of serum galactomannan antigen has a good sensitivity for the early detection of invasive aspergillosis, especially in hematological malignancies [6]. The isolation of Aspergillus on iterative samples (sputum, endobronchial aspiration) is an additional but inconstant argument for the diagnosis in 50% of cases [5].

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The pathological examination of the surgical specimen may help correct the preoperative diagnosis and prove the diagnosis for most patients [5]. Finally, the diagnosis of pulmonary aspergilloma is based on a set of clinical, radiological, endoscopic, biological, and possibly histological elements [17]. The outcome may be a spontaneous resolution in 7 to 10% of cases, or stabilize without complications in 25% of cases [9,16,20]. However, the prognosis remains severe given the high risk of bleeding, which can be explained by local invasion of the cavity’s parietal vessels, mechanical irritation of vascularization exposed in the cavity, the presence of hemolytic endotoxins released by the fungus, or the alleged superimposed acute bacterial infection [3,31]. The death rate attributed to hemoptysis ranges from 2 to 14% or 30% depending on the series [20]. In patients with specific risks, chronic lung superinfection may lead to local parenchymal necrosis, hence the term of chronic necrotizing aspergillosis or semi-invasive aspergillosis [2,17,25]. The treatment of aspergilloma is controversial and non-consensual [3,15]. The IDSA recommends as the first indication either no treatment or surgical resection, in case of SPA [6]. According to some authors, although it is generally accepted that it is technically difficult [7], surgical treatment is considered as standard of care in case of persistent hemoptysis or to prevent serious infectious and hemorrhagic complications [6,9,16,31–33]. Conservative surgery with a minimally invasive approach can be proposed for simple small aspergilloma with a peripheral location with better postoperative results [1,15,20]. However, according to the authors of numerous retrospective surgical series, surgery comes with a significant mortality and morbidity [3,34,35]. Three deaths were reported postoperatively in our series. Cavernostomy combined with thoracoplasty could be proposed. However, this technique remains controversial and requires more testing [1,3,15,36]. Bronchial artery embolization allows immediately treating severe hemoptysis most of the time, and preparing the patient for a possible surgery [1,7,21,31]. In complex presentations or CCPA, short-term antifungal therapy would be the best treatment according to the IDSA, given the impaired immune status and the operative complications often associated [6]. Nevertheless, some teams suggest using planned surgery with a usual approach. A systemic antifungal therapy [9,15,34,35], or by CT scan guided intracavitary injections [1,21,31], does not seem to be sufficiently effective for this indication, in terms of radiological improvement, mycological sterilization, or control of hemoptysis. However, the systemic use of antifungals was suggested in the recommendations of experts to treat complex aspergilloma, perioperatively or exclusively for inoperable patients [6,9,20]. Antifungal chemotherapy with itraconazole, voriconazole, or possibly posaconazole, offers potential therapeutic benefits with relatively minimal risk [6,37]. Their action remains undocumented for SPA, itraconazole having a better intracavitary distribution [6]. Radiation therapy has also given good results as a last resort for patients with threatening hemoptysis or multiple locations [1].

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