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Granulomatous Amoebic Meningoencephalitis in an Immunocompetent Patient

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Granulomatous Amoebic Meningoencephalitis in an Immunocompetent Patient OBSERVATION Granulomatous Amoebic Meningoencephalitis in an Immunocompetent Patient Rodrigo Alencar e Silva, MD; Stanley de Almeida Arau´jo, MD; Izabela Faria de Freitas e Avellar, MD; Jose´ Eymard Homem Pittella, MD, PhD; Jose´ Teotoˆnio de Oliveira, MD; Paulo Pereira Christo, MD, PhD Objective: To report a case of granulomatous amoebic Results: This study shows the diagnosis of B mandril- encephalitis caused by Balamuthia mandrillaris. laris encephalitis suspected from a cerebral biopsy speci- men and confirmed by immunohistochemical and poly- Design: Case report. merase chain reaction studies. Conclusions: This study demonstrates that the diagno- Setting: University hospital. sis of amoebic encephalitis represents a clinical chal- lenge and confirming diagnoses are made, in most cases, Patients: An adult female patient without any appar- after death. High suspicion, histopathologic examina- ent suppressor immune system factor had central ner- tion, and indirect immunofluorescence, polymerase chain vous system infection caused by B mandrillaris. reaction, and cytokine studies from tissue and cerebro- spinal fluid are the main devices to reach the diagnosis. Main Outcome Measures: Clinical, neuroimaging, and pathology findings. Arch Neurol. 2010;67(12):1516-1520 RANULOMATOUS AMOEBIC ache in the frontal region that had started encephalitis (GAE) is a 8 days earlier and evolved into a holocra- rare and sporadic central nial headache, whose intensity progres- nervous system infection sively worsened. The patient had had vom- caused by free-living iting over the previous 2 days. There was Gamoeba. However, the disease has gained no report of fever at the onset of symp- importance because of the growing num- toms, alcohol abuse, diabetes mellitus, or ber of immunodepressed patients, its diffi- other comorbidities, except for systemic ar- cult diagnosis, lack of adequate treatment, terial hypertension. Additional examina- and high level of mortality. tion revealed mild neck stiffness but no cra- Most cases have been reported in the nial nerve abnormalities or focal signs. United States, Australia, and Europe, Funduscopy was normal. The patient had which might be because of better identi- no lymphadenomegaly, fever, or skin al- fication of patients at these centers and/or terations. A cranial computed tomo- publication bias. To our knowledge, only graphic scan showed discrete sulcus oblit- 2 cases have been described in Brazil, one eration (Figure 1A). The patient had a associated with AIDS and the other, with 1 lumbar puncture for analysis of the cere- alcoholism as a risk factor. brospinal fluid, which showed the follow- Most cases of GAE are related to host im- ing results: elevated opening pressure (44 munosuppression and are caused by amoe- 2,3 cm of water), protein level of 131 mg/dL, bae of the genus Acanthamoeba. A case of glucose level of 57 mg/dL, and 39 nucle- Author Affiliations: GAE caused by Balamuthia mandrillaris in ated cells (69% lymphocytes, 12% neutro- Departments of Clinical an adult immunocompetent patient is re- Neurology (Drs Silva, Oliveira, phils, 15% monocytes, and 4% plasma ported herein. The radiologic and histo- and Christo) and Pathology and cells). Results of gram staining, acid-fast pathologic findings are also described. Forensic Medicine (Drs Arau´ jo, staining, and oncotic cytologic analysis were Avellar, and Pittella), Clinics negative. The VDRL test results were non- Hospital, and Program of REPORT OF A CASE reactive and the cultures for fungi and My- Infectious Diseases and Tropical Medicine, Medical School cobacterium tuberculosis were negative. (Dr Arau´ jo), Federal University A 47-year-old woman from Belo Hori- The initial diagnostic hypothesis was vi- of Minas Gerais, Belo zonte, Minas Gerais, Brazil, was admitted ral meningitis. The patient was kept un- Horizonte, Minas Gerais, Brazil. to the emergency service reporting a head- der observation and showed stabilization (REPRINTED) ARCH NEUROL / VOL 67 (NO. 12), DEC 2010 WWW.ARCHNEUROL.COM 1516 ©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 A B C A L 5 cm A D A E L L 5 cm Figure 1. Cranial computed tomography and magnetic resonance imaging. A, Cranial computed tomography showing discrete obliteration of the sulci. B, Cranial computed tomography showing hypodensity in the left cerebellar hemisphere. C and D, Fluid-attenuated inversion recovery magnetic resonance imaging showing hyperintensity in the left cerebellar hemisphere and frontal, temporal, and occipital lobes. E, Heterogeneous contrast enhancement. of clinical symptoms over the subsequent 2 days. On the treatment was maintained. The patient had a decreased third day after admission, the patient developed focal signs level of consciousness and underwent orotracheal intu- characterized by horizontal nystagmus, ataxic gait, and bation on the same day. dysmetria on the left side. A cranial computed tomo- A left lateral suboccipital craniectomy was per- graphic scan was repeated and showed hypodensity in formed to obtain a biopsy specimen of a lesion in the left the left cerebellar hemisphere (Figure 1B). The diagnos- cerebellar hemisphere. Blood cell count, coagulogram, tic hypothesis of herpes encephalitis was raised and treat- erythrocyte sedimentation rate, renal and hepatic func- ment with acyclovir, ampicillin, and dexamethasone was tion test results, antinuclear factor results, chest radiog- introduced. The headache improved after 24 hours, but raphy, transthoracic echocardiogram, and serologic test the cerebellar signs persisted. The patient developed results for human immunodeficiency virus were nega- drowsiness after 3 days and underwent nuclear mag- tive and/or showed no alterations. After the procedure, netic resonance imaging of the brain, which showed mul- the patient had an increase in intracranial pressure, loss tiple brain lesions on both cerebral hemispheres, rang- of brainstem reflexes, and hemodynamic instability and ing in diameter from 0.5 to 3 cm. Heterogeneous contrast died 15 days after hospital admission. enhancement was observed especially in the left cerebel- The histopathologic analysis revealed extensive areas lar hemisphere (Figure 1C, D, and E). An empirical treat- of necrosis and hemorrhage in the cerebellum, fibrinoid ment for neurotuberculosis and neurotoxoplasmosis was necrotizing panarteritis, some thrombosis, granuloma- tried. Treatment with rifampicin, isoniazid, pyrazin- tous lymphoplasmacytic inflammatory infiltrate, foamy amide, ethambutol, sulfadiazine, and pyrimethamine was macrophages, isolated multinucleated giant cells, and in- introduced. Ampicillin, acyclovir, and dexamethasone cipient formation of perivascular granulomas. The in- (REPRINTED) ARCH NEUROL / VOL 67 (NO. 12), DEC 2010 WWW.ARCHNEUROL.COM 1517 ©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 A B C D Figure 2. Histopathologic examination of the cerebellum. A, Fibrinoid necrotizing panarteritis, with thrombosis, granulomatous lymphoplasmacytic inflammatory infiltrate, and foamy macrophages (hematoxylin-eosin, original magnification ϫ100). B, Isolated multinucleated giant cells and incipient perivascular granulomas (hematoxylin-eosin, original magnification ϫ200). C, Presence of diverse structures (isolated or forming small clusters, marked by asterisks) with morphologic characteristics of amoeba trophozoites seen in the vessel wall and areas with and without an inflammatory reaction (hematoxylin-eosin, original magnification ϫ200). D, Detail showing a vessel completely filled with trophozoites (hematoxylin-eosin, original magnification ϫ400). flammatory infiltrate extended focally to the adjacent lep- drill baboon that died of encephalitis at the San Diego tomeninges. Different structures (isolated or forming small Zoo.7 This species causes encephalitis in both immuno- clusters) with the morphological characteristics of amoeba depressed and immunocompetent individuals as well as trophozoites were identified in the vascular wall and in in animals.4,8 B mandrillaris and various species of Acan- areas with and without an inflammatory reaction thamoeba are opportunistic agents that cause the clini- (Figure 2). Part of the material was sent to the Armed cal presentation of GAE in debilitated and malnour- Forces Institute of Pathology, Washington, DC. Immu- ished patients; different types of immunocompromised nohistochemical and polymerase chain reaction studies patients, including those with AIDS; and children.5 In con- were then performed and revealed the presence of tro- trast with Acanthamoeba, which preferentially occurs in phozoites of the free-living amoeba B mandrillaris. immunocompromised patients, Balamuthia is also seen in immunocompetent patients, particularly children.9 By COMMENT 2007, approximately 150 cases of infection with Bala- muthia had been reported worldwide since the recogni- The involvement of free-living amoebae in human dis- tion of the disease in 1990.8 eases was only recognized after 1965, when the first fa- Balamuthia and Acanthamoeba species show a ubiq- tal cases of meningoencephalitis were described in Aus- uitous distribution, with organisms being found in soil, tralia and, almost at the same time, the United States.2 water, heaters, and air-conditioning units.10 The former Free-living amoeba species causing central nervous sys- species is probably transmitted by inhalation of air- tem injury include Naegleria fowleri,
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