Paracoccidioidomycosis associated with human immunodeficiency virus infection

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1 Medical Mycology 2003, 41, 259 /263 Short Communication Paracoccidioidomycosis associated with human immunodeficiency virus infection Report of 10 cases M.L. SILVA-VERGARA, A.C. TEIXEIRA, V.G.M. CURI, J.C. COSTA JÚNIOR, R. VANUNCE, W.M. CARMO & M.R. SILVA Departamento de Clínica Médica, Disciplina de Doenças Infecciosas e Parasitárias, Faculdade de Medicina do Triângulo Mineiro, Uberaba, MG, Brasil We describe here the epidemiological and clinical characteristics of 10 HIV-infected patients with paracoccidioidomycosis. All patients were adult males from small towns in Brazil and had a previous history of work or residence in a rural area. The two infections were diagnosed concomitantly in six of the ten patients, and for six of the patients, the mycosis was the first clinical manifestation of HIV infection. Risk factors for HIV infection were injection in some patients and multiple sexual in others. Six patients died and autopsy revealed severe disseminated paracoccidioidomycosis in three. Exuberant and severe clinical pictures suggest an alteration in the natural history of this mycosis as a result of HIV immunosuppression. The frequency of paracoccidioidomycosis in the HIVinfected population is not known to differ from that reported for this mycosis in non-hiv patients. Keywords brasiliensis co-infection, HIV/AIDS, paracoccidioidomycosis, Paracoccidioides Introduction Paracoccidioidomycosis, caused by the dimorphic fungus Paracoccidioides brasiliensis, is one of the most prevalent mycoses in Latin America [1] and its association with HIV/AIDS has been reported since the end of the 1980s in those countries where the disease is endemic [2 /4], especially in Brazil where tens of patients have been diagnosed [5 /8]. The intersection of these two infections results in disseminated and relatively severe mycosis showing overlaps in characteristics between the two classical clinical forms described in non-hiv patients [9,10]. These are, firstly, the acute/ Received November 2001; Accepted 26 July 2002 Correspondence: Mario León Silva-Vergara MD PhD, Caixa postal 118, CEP , Uberaba, MG, Brasil. Tel.: / ; Fax: / ; dip_fmtm@mednet.com.br subacute form observed in young individuals, which manifests some weeks or months after fungal infection and affects mainly the reticuloendothelial system, the skin and the large bones. Second, the chronic form, which occurs mostly in male adults several years after initial contact with the fungus and frequently features respiratory and mucosal lesions [11,12]. At present, it is not known whether clinical paracoccidioidomycosis in HIV patients can, in at least some cases, be explained by reactivation of latent infection or whether it always begins from a recent exogenously acquired infection. The low levels of CD4 lymphocytes in HIV infection appear to alter the natural history of this mycosis [9,10]. However, paracoccidioidomycosis has not classically been regarded as an opportunistic infection of the immunosuppressed patient. The aim of the present report was to describe the epidemiological and clinical 2003 ISHAM DOI: /

2 2003 ISHAM, Medical Mycology, 41, 259 /263 Table 1 Patient age Diagnostic, clinical, pathological and therapeutic aspects of 10 male patients with paracoccidioidomycosis and HIV infection Year of mycosis diagnosis HIV risk factor Injection Multiple Injection Time during which signs and symptoms were evident (months)* Paracoccidioidomycosis- related symptoms and signs 18 Fever, weight loss, cough, expectoration, hoarseness, anorexia, skin and mucosal lesions, lymphadenomegaly, hepatosplenomegaly, shortness of breath, chest pain 8 Weight loss, expectoration, anorexia, cough, shortness of breath, hoarseness, skin lesions, lymphadenomegaly, hepatosplenomegaly 1 Fever, weight loss, anorexia, cough, expectoration, lymphadenomegaly Unknown 1 Fever, weight loss, lymphadenomegaly, headache, anorexia, cough, expectoration, shortness of breath, hepatosplenomegaly Multiple 2 Fever, weight loss, anorexia, cough, expectoration, shortness of breath, lymphadenomegaly, chest pain, hepatosplenomegaly CD4 count (cells/ mm 3 ) Medication Treatment time (months) Diseases related to HIV ND TMP/SMX 1 Candidiasis Death ND Itraconazole 3 Leprosy$ Death 8 ND Amphotericin B 90 Itraconazole Oropharyngeal candidiasis$ 18 Tuberculosis$ Death Pneumocystosis$ Retinitis due to CMV$ 4 (days) meningitis Evolution and comments Autopsy showed disseminated fungal disease: heart, lung, spleen, liver, lymph nodes, bladder, oropharynx Autopsy showed disseminated fungal disease: lung, spleen, liver, lymph nodes Autopsy showed cryptococcal meningitis and disseminated herpes virus infection Death 18 None Alive Autopsy showed paracoccidioidomycosis disseminated to lung, liver, spleen, kidney, mesenteric, cervical and thoracic lymph nodes; also cryptococcal meningitis 260 Silva-Vergara et al.

3 2003 ISHAM, Medical Mycology, 41, 259 /263 Table 1 (Continued) Patient age Year of mycosis diagnosis HIV risk factor Multiple Injection Injection Injection Multiple Time during which signs and symptoms were evident (months)* Paracoccidioidomycosis- related symptoms and signs 3 Fever, weight loss, anorexia, skin lesions 2 Fever, weight loss, anorexia, cough, expectoration, shortness of breath, skin and mucosal lesions, suppurative, lymphadenomegaly 6 Fever, weight loss, anorexia, cough, expectoration, mediastinal lymphadenomegaly 3 Fever, weight loss, anorexia, cough, expectoration, shortness of breath 4 Fever, weight loss, hyporexia, mucosal lesions CD4 count (cells/ mm 3 ) Medication 5 Itraconazole 323 Itraconazole Itraconazole/ Treatment time (months) Diseases related to HIV 24 Chronical diarrhea% Tuberculosis% Evolution and comments At present uses and itraconazole Death 2 Strongyloidiasis% Death 24 Tuberculosis$ Alive 24 Tuberculosis% Alive 12 None Alive At necropsy disseminated nocardiosis was observed No evidence of Paracoccidioides brasiliensis infection Necropsy not possible At present and TMP/SMX At present and TMP/SMX At present and TMP/SMX *Related to paracoccidioidomycosis. $Before diagnosis of paracoccidioidomycosis. %After diagnosis of paracoccidioidomycosis. Concomitant with the diagnosis of paracoccidioidomycosis. Previously published data (Ref. 7). CMV, cytomegalovirus;, high-active antiretroviral therapy; ND, not done; TMP/SMX, trimethoprim/sulfamethoxazole. HIV-Paracoccidioides brasiliensis co-infection 261

4 262 Silva-Vergara et al. characteristics of ten Brazilian patients with combined paracoccidioidomycosis and HIV infection or AIDS. Population and methods From 1990 to 2000, patients with combined paracoccidioidomycosis and HIV infection were followed-up prospectively at the Infectious and Parasitic Diseases Clinic of the teaching hospital of the Faculty of Medicine of Triângulo Mineiro, Uberaba, Minas Gerais, Brazil. Diagnosis of fungal infection was based on microscopic examination of sputum, smears and lymph node aspirates, as well as histopathological examination of dermal, mucosal or pulmonary lesions. Cultures were not made. The observation of birefringent yeast cells with multiple buds is characteristic of P. brasiliensis. Autopsy was performed after consent had been obtained from families. Results From 1990 to 2000, 104 cases of paracoccidioidomycosis were diagnosed in the teaching hospital in Uberaba. Meanwhile, 674 individuals were diagnosed as having confirmed HIV infection. Ten patients had both infections. The main epidemiological and clinical features characterizing these 10 patients are summarized in Table 1. Discussion The profile of the patients reported here is similar to that observed at other Brazilian centers with documented cases of combined paracoccidioidomycosis and HIV infection [5,6,8]. Most patients came from small towns with integrated urban and rural areas, a type of environment in which this mycosis is endemic [1]. In such areas, inhabitants may come into contact with the fungus during childhood, establishing primary infections that may stabilize for an indefinite period of time. Clinical reactivation can occur during any incident of immunosuppression [9,10]. Starting from the first reported cases of combined paracoccidioidomycosis and HIV infection, it has been established that the fungal infection in such cases shows a diversity of relatively exuberant clinical pictures, mainly featuring lung, spleen, liver, skin, mucosa and lymph node lesions [5,7,9]. This diversity sometimes confounds the established classification of paracoccidioidomycosis manifestations in that the severe clinical pictures, and the dissemination seen, simulate the signs and symptoms of both classical acute/subacute paracoccidioidomycosis and the chronic adult form [9]. In seven of our ten patients, signs and symptoms consistent with paracoccidioidomycosis developed less than 6 months before the diagnosis of this disease was made, a pattern consistent with the classical acute or subacute form of the disease. HIV immunodepression may shorten the latency period of paracoccidioidomycosis. A CD4 lymphocyte count was performed in seven patients, and five of them showed B/100 cells/mm 3,a level that predisposes to many AIDS-defining opportunistic infections. Also, the findings at necropsy in three of our cases included severe lymph node depletion, an exudative and necrotizing invasive process not accompanied by granuloma formations and fungal dissemination. These findings clearly reflect the patients HIV immunodepression, in that they show attenuation of cellular immunity, the basis of control of fungal infections, including paracoccidioidomycosis [13,14]. As shown in Table 1, most patients had one or more other opportunistic infections before, after or concomitant with their diagnosis of paracoccidioidomycosis. Whether any of the other opportunistic infections influenced the development of paracoccidioidomycosis or predisposed to it in any way is unknown. Patients with HIV infection commonly use sulfa and azole drugs (to which P. brasiliensis is susceptible) for the and prophylaxis of common opportunistic infections. Whether these medicaments can prevent paracoccidioidomycosis in individuals taking them is unknown. In Brazil, where highly active antiretroviral therapy () has been fully available since 1996, most opportunistic infections associated with HIV/AIDS are on the decline [15]. Some years ago, as the HIV epidemic began to reach small-urban and rural areas in Brazil, an increased number of patients with P. brasiliensis reactivation as a result of HIV immunodepression were expected [13]. The low number of cases registered to date, however, seems to show only coincidental epidemiological overlapping of the two infections. References 1 Wanke B, Londero AT. Epidemiology and paracoccidioidomycosis. In: Franco M, Lacaz CS, Restrepo-Moreno A, Del Negro G (eds). Paracoccidioidomycosis. Boca Raton, Fl: CRC Press, 1994: 109/ Pedro RJ, Aoki FH, Boccato RSBS, et al. Paracoccidioidomicose e infecção pelo vírus da imunodeficiência humana. Rev Inst Med Trop São Paulo 1989; 31: 119/ Goldani LZ, Martinez R, Landell GAM, Machado AA, Coutinho V. Paracoccidioidomycosis in a patient with acquired immunodeficiency syndrome. Mycopathologia 1989; 105: 71/74. 4 Tobon AM, Orozco B, Estrada S, et al. Paracoccidioidomycosis and AIDS: report of the first two Colombian cases. Rev Inst Med Trop São Paulo 1998; 40: 377/ ISHAM, Medical Mycology, 41, 259 /263

5 HIV-Paracoccidioides brasiliensis co-infection Goldani LZ, Sugar AM. Paracoccidioidomycosis and AIDS: an overview. Clin Infect Dis 1995; 21: 1275/ Figueiredo JFC, Martinez R, Silva GF, Gabelini GC, Silveira S. Paracoccidioidomicose e AIDS: características gerais dos casos ocorridos em Ribeirão Preto, SP, Brasil, no período de 1987 a 1991 [abstract C-1/0]. Rev Arg Micol 1992; 15: Lima MA, Silva-Vergara ML, Demachki S, Santos JAM. Paracoccidioidomicose em paciente com a infecção pelo vírus da imunodeficiência humana. Relato de necropsia. Rev Soc Bras Med Trop 1995; 28: 279/ Marques AS, Conterno LO, Sgarbi LP, et al. Paracoccidioidomycosis associated with acquired immunodeficiency syndrome. Report of seven cases. Rev Inst Med Trop São Paulo 1995; 37: 261/ Marques AS, Shikanai-Yasuda MA. Paracoccidioidomycosis associated with immunosuppression, AIDS and cancer. In: Franco M, Lacaz LC, Restrepo-Moreno A, Del Negro G (eds). Paracoccidioidomycosis. Boca Raton, FL: CRC Press, 1994: 394/ Bernard G, Duarte AJS. Paracoccidioidomycosis: a model for evaluation of the effects of human immunodeficiency virus infection on the natural history of endemic tropical diseases. Clin Infect Dis 2000; 31: 1032/ Brummer E, Castañeda E, Restrepo A. Paracoccidioidomycosis: An update. Clin Microbiol Rev 1993; 6: 89/ Franco M, Montenegro MR, Mendes RP, Marques AS, Dillon NL, Mota NGS. Paracoccidioidomycosis: a recently proposed classification of its clinical forms. Rev Soc Bras Med Trop 1987; 20: 129/ Karp CL, Neva FA. Tropical infectious diseases in human immunodeficiency virus-infected patients. Clin Infect Dis 1999; 28: 947/ Mota NGS, Peraçoli MTS, Mendes RP, Gatass CR, et al. Mononuclear cell subsets in patients with different clinical forms of paracoccidioidomycosis. J Med Vet Mycol 1988; 26: 105/ Guimarães MDC. Temporal trends in AIDS associated opportunistic infectious diseases in Brazil, 1980/1999. Cad Saúde Publ 2000; 16(Suppl 1): 21/ ISHAM, Medical Mycology, 41, 259 /263

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