Histoplasmosis diseminada con síndrome hemofagocítico en un paciente con sida: descripción de un caso y revisión de la literatura española

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Histoplasmosis diseminada con síndrome hemofagocítico en un paciente con sida: descripción de un caso y revisión de la literatura española

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  Disseminated histoplasmosis withhemophagocytic syndrome in apatient with AIDS: description of one case and review of the Spanishliterature Ana Gil-Brusola 1 , JavierPemán 1 , María Santos 1 , Miguel Salavert 2 , Jose Lacruz 2 y Miguel Gobernado 1 1 Servicio de Microbiología y  2 Unidad de Enfermedades Infecciosas, Hospital Universitario La Fe, Valencia, Spain We report a case of disseminated histoplasmosis in a 33-year old Ecuadorianpatient with AIDS and a CD4 lymphocyte count of 39 cells/µl. He presentedwith prolonged fever and cough, was diagnosed with hemophagocyticsyndrome and multiple organ failure and died 18 days after admission. Histoplasma capsulatum was isolated post-mortem from bone marrow biopsyand blood culture.In a literature review we found 22 published cases of disseminatedhistoplasmosis in patients with AIDS in Spain since 1988. All but two weremen under 50 years old. Nineteen had been born or had lived in endemicareas. The diagnosis of histoplasmosis was established by culture of bonemarrow biopsy in 10 cases. Itraconazole was introduced as a second drugafter amphotericin B in ten of the thirteen patients who survived. Histoplasma capsulatum , Disseminated histoplasmosis, HIV, Hemophagocytic syndrome Histoplasmosis diseminada con síndromehemofagocítico en un paciente con sida: descripciónde un caso y revisión de la literatura española Presentamos un caso de histoplasmosis diseminada en un pacienteecuatoriano de 33 años, con sida y recuento de linfocitos CD4 de 39 células/µl. Al llegar a nuestro hospital refería fiebre prolongada y tos, fue diagnosticado de síndrome hemofagocítico con fallo multiorgánico y falleció a los 18 días del ingreso. El diagnóstico se completó post-mortem,con el aislamiento de Histoplasma capsulatum en las muestras de sangre y biopsia medular.En la revisión de los casos de histoplasmosis diseminada en infectados por el VIH publicados en España desde 1988, encontramos 22 pacientes. Todos excepto dos eran varones menores de 50 años. Diecinueve habíannacido o vivido en áreas endémicas. El diagnóstico de histoplasmosis serealizó por cultivo de biopsia de médula ósea en 10 casos. Diez de los trecepacientes que sobrevivieron habían sido tratados con anfotericina B y,posteriormente, con itraconazol como segundo fármaco. Histoplasma capsulatum , Histoplasmosis diseminada, VIH, Síndrome hemofagocítico 312 Rev Iberoam Micol 2007; 24: 312-316 Corresponding author: Dra. Ana Gil BrusolaServicio de Microbiología, H.U. La Fe Av. Campanar 21, 46009-Valencia, SpainTe.l.: +34 699 944 448Fax: +34 961 973 177E-mail: agilbru@hotmail.com  Aceptado para publicación el 10 de julio de 2007  ©2007 Revista Iberoamericana de MicologíaApdo. 699, E-48080 Bilbao (Spain)1130-1406/01/10.00 󲂬 Summary Key words Resumen Palabras clave Note  Introduction Histoplasmosis is a mycosis caused by the dimor-phic fungus  Histoplasma capsulatum . This fungus hasbeen isolated from soil containing bird and bat feces(guano), especially in caves and next to chicken houses. Ithas been classified into three varieties, two of which arepathogenic to humans:  H. capsulatum var. duboisii , foundmainly in Africa, and  H. capsulatum var. capsulatum , dis-tributed worldwide, and endemic to the Mississippi andOhio River valleys and to Central and South America.Infection results from the inhalation of the fungal microco-nidia. The development of disease depends on the size of the inoculum and the immune status of the host. Around1% of infected people develop symptoms that can varyfrom acute or chronic pulmonary forms, to disseminatedhistoplasmosis in immunosuppressed hosts [17]. Since1985, disseminated histoplasmosis is a defining illness of AIDS and, even though highly active antiretroviral therapy(HAART) has reduced the number of infected patients, itremains a significant opportunistic infection in Central andSouth America. The number of cases, both in endemic andin non-endemic areas, has grown since the first casereports in the US around 1980 [28].Reactive hemophagocytic syndrome has multipleetiologies (infectious, malignant or autoimmune) and is, inmany cases, associated with organ failure [30]. It has alsobeen described in patients with severe forms of histoplas-mosis and is often underdiagnosed because clinicians areunfamiliar with it.We present a new case of disseminated histoplas-mosis with reactive hemophagocytosis in an immigrantpatient from Ecuador infected by HIVand a review of theSpanish literature. Case report A33-year-old man was admitted to our hospital inFebruary 2006 for evaluation of a 2-week intermittentfever. Born in Ecuador, he had been living in Spain for 5 years but had visited his home country several times.The most recent visit had been four months before this epi-sode. He was heterosexual and was employed as a truckdriver.The patient had been diagnosed of HIVinfection in2002 but was not treated with HAART. In November 2005, he presented at our hospital with fever and hae-moptysis and was diagnosed of microbiologically provendisseminated tuberculosis (TB) and AIDS, starting anti-TBtherapy and prophylaxis with co-trimoxazol. He had anHIVviral load higher than 100,000 copies/ml and a CD4lymphocyte count of 39 cells/µl.By the time he arrived to our hospital in February2006, the patient referred a daily productive cough withintermittent haemoptysis, but no chest pain, dyspnea, diar-rhea or weight loss. Findings on a physical examinationwere unremarkable, except for a temperature of 40 °C. Hehad been treated 10 days with azithromycin, with no appa-rent response.Laboratory tests revealed a leukocyte count of 2000/mm 3 , 73.3% polymorphonuclear neutrophils, 20.8%lymphocytes and 5.9% monocytes; 107,000 platelets/mm 3 ;a 12.3g/dl hemoglobin level; and elevated acute phase pro-teins (serum lactate dehydrogenase 1047 IU/l; fibrinogen413.5 mg/dl; C-reactive protein 92.7 mg/l). Chest radio-graphy was normal, but chest computed tomography sho-wed extensive paratracheal, periaortic and retroperitonealadenopathy. Bacterial and mycobacterial smears and cultu-res from blood, respiratory samples and bone marrowbiopsy were negative. Serologic tests for HCV, HBV, HSV,CMV, VVZ, EBV, Toxoplasma ,  Leishmania spp, Trepo-nemapallidum , Cryptococcus neoformans and  Brucellamelitensis were also negative.The bone marrow biopsy specimens demonstratedhemophagocytosis and, in one bone marrow sample, stai-ning with Giemsa showed extracellular rounded forms thatcould not be identified.The situation of the patient worsened, despite theadministration of levofloxacin and imipenem. Having beendiagnosed of hemophagocytic syndrome with multipleorgan failure, the patient was admitted to the intensive careunit on day 13, where he died 5 days later.On day 18 of admission, yeasts grew in the bloodsamples cultured in Bactec 13Avials for mycobacteria.Budding yeasts were also observed after 20 days of incu-bation of the bone marrow samples on Sabouraud dextroseagar at 37 °C. When left at room temperature, the yeaststurned into a white cottony mould. Microscopic observa-tion of the septate fungi hyphae and tuberculate macroco-nidia allowed the identification of  Histoplasma capsula-tum . The diagnosis was then confirmed morphologically(Microbiology Department, Rovira i Virgili University,Reus) and by PCR assay of three serum samples (Mico-logy Department, National Microbiology Laboratory, Ma- jadahonda).Atotal of 24 diagnoses of disseminated histoplas-mosis were registered in the AIDS National Epidemiologi-cal Database of Spain between 1998 and 2004 [37]. In areview of the literature using Medline and Google websi-tes, we found 22 reported cases of this disease in patientsinfected with HIVin our country since 1988 [1-5,9-10,12-13,21,25,29,31-33,35-36]. The characteristics of thesecases, together with those of the current patient, are pre-sented in table 1. Discussion Infection with  H. capsulatum results from the inha-lation of its microconidia through day-to-day activities inareas where it is endemic or while removing soil fromcaves and old buildings with guano [17]. The descriptionof some cases in non-endemic regions suggests the exis-tence of environmental spots that allow the growth of thefungus [38]. Other possible methods of transmission thathave been proposed are through inhalation of contamina-ted cocaine from South America [5], parenteral transmis-sion after organ transplantation [20] or by sharing needleswith an infected patient [35]. In countries such as Spain,where the fungus is not widespread, the disease affectsmainly immigrants or travelers who have lived in endemicareas and have either been exposed to a large inoculum of the fungus or are immunosuppressed. In the series revie-wed, all patients but two were men under 50 years old, andonly one case corresponded to an infant. Including our patient, 20 (87%) had been born or had lived in endemicareas or tropical countries. The occupational exposure riskof the 3 patients who had not traveled to endemic countriesis unspecified. One of them had inhaled cocaine. All 3 of them were injection drug users, and one of them had shared needles with a patient who died of disseminatedhistoplasmosis. These data support the idea of possibleparenteral transmission.In patients with disseminated histoplasmosis, fever is the most common symptom. They may present withweight loss, anorexia, cough, nausea, vomiting, diarrheaand abdominal pain. On physical examination, patients 313 Disseminated histoplasmosis and AIDSGil-Brusola A, et al.  may have adenopathy, hepatosplenomegaly and, less fre-quently, oral ulcers and a maculopapular rash affectingface and trunk [27]. Clinically, histoplasmosis can mimicTB [19], as was appreciated in our patient when he presen-ted with fever and intermittent hemoptysis, and should bepart of the differential diagnosis, together with differentnon-endemic mycoses, nocardiosis, rhodococcosis andnon-infectious diseases such as lymphoma or other neo-plasm, in a patient with symptoms compatible with TBthat does not respond to correct anti-TB treatment.Chest radiography findings may be normal or showa diffuse nodular infiltrate or cavitary lesions [14]. Labo-ratory evaluation may reveal abnormal liver function testresults and pancytopenia due to involvement of the liver and bone marrow. Reactive hemophagocytic syndrome inpatients with severe forms of histoplasmosis has also beendescribed, and the presence of fever and cytopenia inpatients with AIDS can be a clue to its diagnosis [18]. He-mophagocytosis is defined as the consumption of hemo-poietic cells by non-malignant phagocytes and can occur as a result of multiple etiologies (viral, bacterial, parasitic,malignant, autoimmune or familial). Hemophagocyticsyndromes are associated with a high mortality dependenton etiology and degree of associated organ failure. In someareas of South America, disseminated histoplasmosis is the most frequent opportunistic infection in severelyimmunosuppressed HIVinfected patients with fever andcytopenia [24]. Hemophagocytosis in these patients is fre-quent, although not specific of diagnosis, and disseminatedhistoplasmosis should be included in the causes of pancy-topenia in patients with AIDS [22]. To our knowledge, the case we report is the first case of hemophagocytosis inthe setting of disseminated histoplasmosis in an AIDSpatient published in Spain. Another case, in a patient fromEcuador, was reported in the 22nd Congress of the Spa-nish Society of Anatomic Pathology but has not beenpublished [7]. Both patients died in a short period of timeafter admission to the hospital.In the diagnosis of disseminated histoplasmosis, the “gold standard” is a culture of a body sample, mainlyof the skin lesions, bronchoalveolar lavage, bone marrowor blood.  H. capsulatum grows in living tissue or in cul-ture at 37 °C as a small, round to oval budding yeast, andin soil or cultures at temperatures below 30 °C as a white,cottony mould with a pale brown transverse on Sabouraudagar. The 4-week incubation period required for culture isnot practical in severe cases, so other diagnostic techni-ques have to be used. Furthermore, skin tests are not use-ful; fungal staining of tissue or blood has lower sensitivitythan culture, and serum antibody tests can yield false-posi-tive and false-negative results. The detection of antigen inurine sample is rapid, sensitive and can be useful in moni-toring therapy, but should be confirmed with other serolo-gic and culture data [17]. Even though no PCR assay for routine use is commercially available, real-time and semi-nested PCR assays have adequately identified  H. capsula-tum from cultures of bone marrow biopsies, bronchoal-veolar lavage and blood [23]. Anew real-time PCR-basedassay which detects up to 1 fg of  H. capsulatum DNAper µl of sample, particularly when respiratory secretionsor bone marrow samples are analyzed (less reliable inserum), has recently been described [6]. These findingsdemonstrate that PCR techniques could be useful as rapiddiagnostic and confirmation methods. In the series revie-wed, the diagnosis was established mainly by culture of bonemarrowbiopsy(11cases),skinlesions(7cases),bloodculture(5cases)andrespiratoryspecimens(4cases).The diagnosis was achieved on autopsy or after the deathof the patient in six cases, with the disease not being sus-pected while the patients were alive. The diagnosis of HIVinfection and histoplasmosis coincided in seven patients.Treatment is required in patients with disseminatedhistoplasmosis, especially in those with HIVinfection anda CD4 lymphocyte count below 150 cells/µl, in whom thedisease is often fatal if untreated [17]. Intravenous ampho-tericin B (0.5-1mg/kg daily) is the treatment of choice in 314 Rev Iberoam Micol 2007; 24: 312-316 Table 1. Epidemiological data, diagnosis and outcome of AIDS patients with histoplasmosis in Spain.CaseHome country/ Travel HistoryAgeSexCD4Fungus isolation specimenAntifungal treatmentOutcomeReference1Argentina44M98SB, RSAmBDeath[13]2Argentina38MNDSB, RS, BC, BMBAmB and ketoconazoleSurvival[29]3Uruguay51F6SB, BC, BMB, CSF, urineAmB and itraconazoleSurvival[3]4None24MNDBMB, CSF (postmortem)NoDeath[2]5Lived 2 years in Guatemala28MNDSBAmB and itraconazoleSurvival[10]6Lived 8 years in Guatemala31M39RS, adenopathyAmB and itraconazoleSurvival[32]7Argentina36M35SB, BMBAmBDeath[4]8Argentina39M38SB, tracheal biopsyAmB and itraconazoleSurvival[4]9Travels frequently to South America49M32Necropsy (lung, spleen, liver)NoDeath[4]10Gambia37M50Necropsy (brain)NoDeath[4]11None32M12BMBAmB and itraconazoleSurvival[33]12Venezuela38M9Liver biopsy (postmortem)NoDeath[31]13Travels frequently to South America and Africa44M10BMB, BCAmB and itraconazoleSurvival[5]14Argentina49MNDSBitraconazoleSurvival[5]15Caiman Islands (Caribe)35M16BC, supraclavicular adenopathyAmB and itraconazoleSurvival[1]16None43M30BMB, RSAmB and itraconazoleSurvival[35]17 a Travels frequently to NicaraguaNDMNDNDNDDeath[35]18Colombia25M63IBSurgery and itraconazoleSurvival[9]19Ecuador11M5NecropsyNoDeath[12]20Ecuador23M17BMB, BCAmBDeath[36]21Ecuador25M11BMBAmB and itraconazoleSurvival[25]22Nicaragua39F34BMB, cervical adenopathy, BCAmB and itraconazoleSurvival[21]23Ecuador33M39BMB, BCNoDeathcurrent M: male; F: female; SB: skin biopsy; RS: respiratory samples (includes bronchial aspirate, bronchoalveolar lavage and transbronchial biopsy); BC: blood culture; CSF: cerebral spinalfluid; BMB: bone marrow biopsy; IB: intestinal biopsy; ND: no data available; AmB: amphotericin B. a Brother of case number 16. Shared needles with him. Died of disseminated histoplasmosis.  severely ill or immunocompromised patients, switching tooral itraconazole (200 mg twice a day) once the conditionof the patient has stabilized. Liposomal amphotericin B,was less toxic than conventional amphotericin B in a double-blinded, multicenter clinical trial [16]. Duration of treatment depends on the severity of the disease and the immune status of the patient. Patients with AIDS anddisseminated disease typically need 12 months of initialtherapy followed by lifelong maintenance using itraco-nazole therapy to prevent relapse, although some studiessuggest that it is possible to interrupt secondary prophyla-xis when the patient has responded to HAART, is clini-cally asymptomatic and has a CD4 lymphocyte countabove150cells/µl[15,26,34].Othertreatmentoptionsin-cludefluconazoleasasecond-lineantifungalinpatientswhoareintoleranttobothitraconazoleandamphotericinB,and posaconazole, which has proven to be effective for pa-tients in whom therapy with amphotericin B, fluconazoleor itraconazole has failed [39]. In the series reviewed, theCD4 lymphocyte count was below 150 cells/µl in the 18cases in which this data is available, and below 50 cells/µlin fourteen of them. Treatment was established in 13 pa-tients with CD4 lymphocyte count below 150 cells/µl. Theclinical situation of the patient allowed the introduction of a second drug in eleven of the thirteen patients that survi-ved. The other patient who survived had previously beentreated surgically by resection of the small bowel and hadthen received itraconazole. Of the 5 patients whose CD4lymphocyte count is unknown, only the three who weretreated survived, one of them having received itraconazoletherapy alone. This data shows the importance of startingtherapy with amphotericin B as soon as possible and thencontinuing with itraconazole, since all the patients who didnot receive any antifungal therapy, or were treated withamphotericin B alone, died. Moreover, all those who recei-ved itraconazole survived and did not present relapse in atleast 6 months of secondary prophylaxis.The mortality observed in the series reviewed was43.5%. This high mortality rate is similar to that reportedin other two studies, in which 40% of a total of 25 casesand 32% of 164 HIV-infected patients with disseminatedhistoplasmosis died [8,11].In summary, disseminated histoplasmosis should bepart of the differential diagnosis in any patient with AIDSand a CD4 lymphocyte count below 150 cells/µl, who hasprolonged fever, and who has traveled or has lived in anendemic area. However, it should not be disregarded inintravenous drug users or patients with tuberculosis-likesymptoms who do not respond to anti-TB therapy, inde-pendently of travel history. In HIVpositive patients withlow CD4 lymphocyte count and fever, any new or unspe-cific skin lesion, bone marrow biopsy and blood samplesshould be cultured since this procedure can lead to thediagnosis of the disease. New PCR techniques are encou-raging and could be useful as rapid diagnostic and confir-mation methods. Since the diagnosis of the disease can bedelayed, antifungal therapy should be initiated as soon aspossible in these patients. Disseminated histoplasmosisshould be included in the causes of pancytopenia inpatients with AIDS, where the presence of hemophagocy-tosis correlates with poor prognosis.  Agradecemos a J. Gene (Microbiology Department, Rovira i Virgili University, Reus), M. Cuenca-Estrella(Micology Department, National Microbiology Laboratory) y a M. Montagud (Hematology Department, Vinaroz Hospital) 315 Disseminated histoplasmosis and AIDSGil-Brusola A, et al.  1.Abella ML, Laynez P, Perera A, Díez O,Linares M, Miguelez M, Padilla ML.Síndrome febril, poliadenopatías yhepatoesplenomegalia. Rev Clin Esp2002; 202: 617-618.2.Alados JC, Miranda C, Ortiz F, Cano R.Disseminated histoplasmosis in AIDSpatients in Spain. Eur J Clin MicrobiolInfect Dis 1993; 12: 793-794.3.Añón S, Blanes M, Evole M, López-Aldeguer J. Histoplasmosisdiseminada en un paciente con SIDA.Enferm Infecc Microbiol Clin 1993; 11:343-344.4.Bayés B, Romeu J, Vaquero M, Ribera M,Navarro JT, Rosell A, Sirera G, Clotet B.Histoplasmosis diseminada y SIDA. Aportación de 4 casos. Med Clin (Bar)1996; 106: 700-703.5.Benito N, García E, Blanco A, de Górgolas M, Gadea I, Escaloñilla P,Fernández ML. Histoplasmosisdiseminada en pacientes con SIDA.Estudio de 2 casos y revisión de labibliografía española. Enferm InfeccMicrobiol Clin 1998; 16: 316-321.6.Buitrago MJ, Gómez-López A, Monzón A,Rodríguez-Tudela JL, Cuenca-Estrella M. Assessment of a quantitative PCRmethod for clinical diagnosis of importedhistoplasmosis. Enferm Infecc MicrobiolClin 2007; 25: 16-22.7.Calatrava A, Paradís A, Peláez S, Gómez A, Arnal M, Montagud M.Histoplasmosis diseminada con síndrome hemofagocítico asociado. Available from the URL:http://www.seapcongresos.com/2005/ comunicacion.asp?id=116.8.Chang MR, Taira CL, Paniago AM, Taira DL, Cunha RV, Wanke B. 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