Granulomatous amebic encephalitis in a child with acute. lymphoblastic leukemia successfully treated with
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1 JCM Accepts, published online ahead of print on 17 November 2010 J. Clin. Microbiol. doi: /jcm Copyright 2010, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved Granulomatous amebic encephalitis in a child with acute lymphoblastic leukemia successfully treated with combination antimicrobial therapy and hyperbaric oxygen Maritschnegg P 1, Sovinz P 1, Lackner H 1, Benesch M 1, Nebl A 1, Schwinger W 1, Walochnik J 2, Urban C 1. 1 Division of Pediatric Hematology/Oncology, Department of Pediatric and Adolescent Medicine; Medical University of Graz, Austria. 2 Department of Medical Parasitology, Institute of Specific Prophylaxis and Tropical Medicine; Medical University of Vienna, Austria. Corresponding author: Peter Maritschnegg, MD Department of Pediatrics and Adolescent Medicine Medical University of Graz; Graz, Austria. Auenbruggerplatz 30, 8036 Graz Phone: 0043/316/385/82906 Fax: 0043/316/385/3450 peter.maritschnegg@meduni-graz.at - 1 -
2 Acanthamoeba is the causative agent of granulomatous amebic encephalitis (GAE), a rare and usally fatal disease. We report a child with acute lymphoblastic leukemia (ALL) who developed brain abscesses caused by Acanthamoeba during induction therapy. Multimodal antimicrobial chemotherapy and hyperbaric oxygen therapy resulted in complete resolution of symptoms and MRI pathology. CASE REPORT: A 25-month-old boy was treated at our institution for acute lymphoblastic leukemia (ALL). Induction therapy consisted of prednisone, dexamethasone, vincristine, daunorubicin, l- asparaginase, methotrexate, cyclophosphamide and mercaptopurine. Infection prophylaxis included oral amphotericin B and trimethoprim-sulfamethoxazole (4mg/kg/day four days/week). Complete remission of ALL was achieved by day 15 of ALL treatment. 43 days after establishing diagnosis and starting therapy the boy developed fever followed by an increase of C-reactive protein (CRP) (maximum 87.8 mg/l [normal range 0-8 mg/l]). Therapy with meropenem and liposomal amphothericin B resulted in defeverescence. The patient suffered from mild headache and five days later he experienced left sided hemiparesis and a second elevation of CRP level (maximum: 37mg/dl). No other symptoms besides fever and hemiparesis were noted. Magnetic resonance imaging (MRI) revealed multifocal lesions up to 20 millimeters in diameter, partially necrotic with increased contrast medium enhancement and extended edema. The largest lesion was located in the right frontoparietal lobe. Morphology of these lesions were indicative for abscess formations (Fig.1)
3 Analysis of initially aquired cerebrospinal fluid (CSF) showed 0 erythrocytes/µl, 2 leukocytes/µl, increased protein (62 mg/dl), normal glucose and no bacteria. Extensive diagnostic workup on fungi, bacteria and parasites, known for causing brain abscesses in children (7), revealed positive PCR for Acanthamoeba two days after the first signs of hemiparesis. An Acanthamoeba-specific PCR amplifying a fragment of the 18S rdna was performed using the JDP1 and JDP2 primers (12) and Acanthamoeba strain ATCC PRA-105, genotype T4 as a positive control. For genotyping, amplicons were sequenced using a 310 ABI PRISM automated sequencer (Applied Biosystems, Langen, Germany) and the genotype was assessed with the model assumption of a <5% sequence dissimilarity within one genotype (3). Further specification revealed Acanthamoeba group II, genotype T4, known to be the predominant type that causes granulomatous amebic encephalitis (GAE) in humans (13). The GenBank accession number for the strain found in this case is HQ Cultures and PCR of CSF were negative for fungi and bacteria. Results of Acanthamoeba-PCR of nasal and respiratory discharge and sputum were negative. ALL therapy was stopped on treatment day 44 and empiric antimicrobial therapy was initiated consisting of meropenem, teicoplanin, fosfomycin, metronidazole and liposomal amphothericin B. Hyperbaric oxygen therapy (HBO) was started empirically for its known effect on brain abscesses as previously described (6,7), consisting of 36 applications in the pressure chamber once daily at 2.2 atmospheres absolute for 60 min at 12 m within 36 days. After confirmation of diagnosis two days after the first lumbar puncture treatment was changed to daily trimethoprim-sulfamethoxazole (6 mg/kg/d iv), fluconazole (10 mg/kg/d iv), pentamidine (4 mg/kg/d iv for 20 days) and miltefosine (2,5 mg/kg/d iv for 23 days) (13,15). Additional granulocyte-colony stimulating factor (G-CSF) was given in order to increase leukocyte count. Phenobarbital was administered as anticonvulsive prophylaxis
4 A repeated lumbar puncture 8 days later still showed positive PCR on Acanthamoeba-DNA and an elevated CSF leukocyte count (293 leukocytes/µl). 3 weeks after initiation of specific therapy, PCR in CSF on Acanthamoeba was negative. Subsequent MRI studies 14, 30 and 60 days as well as 90 days after the first symptoms showed regression of the lesions and oedema (Fig.2). Treatment was very well tolerated with only mild laboratory signs of pancreatitis. ALL polychemotherapy was resumed after 12 days. To date the patient completed maintenance therapy and is in complete remisson for 22 months. He achieved complete resolution of neurologic symptoms after four months. Acanthamoeba is a free-living amoeba distributed worldwide in soil, fresh and brackish water, dust, hot tubes and sewage (2). Most people seem to have been exposed to this organism during their life, since most of healthy individuals show serum antibodies against Acanthamoeba (8). Acanthamoeba causes three distinct clinical syndromes. First is Acanthamoeba keratitis following minor corneal trauma in immunocompetent patients, usually appearing in contact lens wearers. Second, disseminated Acanthamoeba infections involving skin, sinuses and lungs that typically occur in immunocompromised patients including those with AIDS, systemic lupus erythematodes, steroid use, malnutrition or liver disease, transplant recipients and patients receiving chemotherapy. And third is GAE, usually affecting immunocompromised patients. Acanthamoeba may enter through skin lesions or the respiratory tract and spread hematogenously to the central nervous system (CNS). The route of infection in our patient was not clear. The child lives in a rural region, however analysis of drinking water was negative for Acanthamoeba. Two other amebic genera are known to cause CNS infections, Naegleria fowleri and Balamuthia mandrillaris. While infections with Balamuthia mandrillaris are clinically very similar to - 4 -
5 infections with Acanthamoeba, Naegleria fowleri causes primary amebic meningoencephalitis, usually in immunocompetent individuals and children. Treatment is based on administration of amphotericin B in combination with other drugs (9,14), but results are poor in general. GAE in immunocompetent persons is extremely rare (16). Symptoms of GAE are generally non-specific and include headache (53%), meningism (40%), fever (53%), mental status changes (86%), visual disturbances (26%), ataxia (20%), hemiparesis (53%) and seizures (66%). The exact incubation period is unknown but is probably weeks to months. Disease duration is reported to range from days (average 39 days). The clinical course of GAE is often fatal (5). Diagnosis of GAE is based on CSF analysis including microscope examination, culture and PCR (11). PCR is especially useful in cases with low parasite density (16). Acanthamoeba grow in culture on non-nutritive agar overlaid with gram negative bacteria. If a culture is positive, susceptibility testing should be done (1). Acanthamoeba are sensitive to multiple antimicrobial agents (13). Ofori et al. reported on a 7-year-old girl with GAE who was treated successfully, after surgical intervention and treatment with ketoconazol neurological symptoms slowly resolved (10). A 17- year-old patient with ALL and amebic encephalitis was treated successfully with ketoconazole (5 mg/kg/day), trimethoprim / sulfamethoxazole (15 mg/kg/day) and rifampicin (10 mg/kg/day). Diagnosis of Acanthamoeba infection was confirmed by positive CSF culture. Nevertheless the patient died in consequence of the preexisting ALL (4). Another case of GAE occurring in a patient following liver transplantation was reported 2008 by Fung et al. Surgical intervention was performed as well as multimodal chemotherapy. Final diagnosis was established microscopically in a lobectomy specimen. Rifampicin (600 mg twice a day) and co-trimoxazol (960 mg twice a - 5 -
6 day) were added as specific therapy after identification of Acanthamoeba. The patient survived, however with massive neurological residuals (2). In the case reported here we initially instituted empiric therapy with meropenem, teicoplanin, and amphotericin B and added therapy with pentamidine, fluconazole, metronidazole, trimethoprimsulfamethoxazole and miltefosin, when infection with Acanthamoeba was established (13). Since recoveries on only antimicrobial therapy are rare and surgical intervention was not possible due to the location of the abscess formations we started additional hyperbaric oxygen therapy, a treatment modality recently described in patients with brain abscesses (6,7). To the best of our knowledge this is the first case of GAE in childhood occurring during treatment of ALL in which diagnosis was confirmed by CSF-PCR and with full recovery without any neurological deficits. Because there is no therapeutic guideline yet, antimicrobial therapy must be wide and aggressive. Single cerebral lesions should be excised if possible, and, especially if they are not surgically excisable, hyperbaric oxygen therapy might be an additional treatment option
7
8 1 2 Fig. 1: MRI on day 44 of ALL treatment showing multiple abscess formations, up to a diameter of 20 mm. Midline shift is 3-4 mm.
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10 1 2 Fig. 2: MRI 2 months after diagnosis of brain abscesses showing further regression. Maximum diameter of a lesion is 11 mm
11 1 References: ) Castellano-Sanchez A., A. C. Popp, F.S. Nolte, G. S. Visvesvara, M. Thigpen, I. Redei, and J. Somani Acanthamoeba castellani encephalitis following partially mismatched related donor peripheral stem cell transplantation. Transpl Infect Dis. 5(4): ) Fung, K.T., P. D. Amar, J. E. McLaughlin, S. B. Lucas, B. Davidson, K. Rolles, D. Patch, and A. K. Burroughs Cure of Acanthamoeba Cerebral Abscess in a Liver Transplant Patient. Liver Transplantation 14: ) Gast, R. J., D. R. Ledee, P. A. Fuerst, and T. J. Byers Subgenus systematics of Acanthamoeba: four nuclear 18S rdna sequence types. J Eukaryot Microbiol 43: ) Gupta, D., G. S. Panda, and S. Bakhshi Successful treatment of acanthamoeba meningoencephalitis during induction therapy of childhood acute lymphoblastic leukemia. Pediatr Blood Cancer 50(6): ) Kaul, D. R., L. Lowe, G.S.Visvesvara, S. Farmen,Y.A. Khaled, and G.A.Yanik Acanthamoeba infection in a patient with chronic graft-versus-host disease occurring during treatment with voriconazole. Transpl Infect Dis. 10: ) Kurschel, S., A. Mohia, V. Weigl, and H. G. Eder Hyperbaric oxygen therapy for the treatment of brain abscess in children. Childs Nerv Syst. 22(1):38-42.
12 ) Lackner H, Sovinz P, Benesch M, Smolle-Jüttner F, Mokry M, Schwinger W, Moser A, Urban C Management of brain abscesses in children treated for acute lymphoblastic leukemia. Pediatr Blood Cancer. 52(3): ) Marciano-Cabral, F., and G. Cabral Acanthamoeba spp. as Agents of Disease in Humans. Clinical Microbiology Reviews 16(2): ) McKellar, M. S., R. M. Lahar, J. E. Greenlee, D. C. Hale, G. C. Booton, D. J. Kelly, P. A. Fuerst, R. Sriram, and G. S. Visvesvara Fatal Granulomatous Acanthamoeba Encephalitis Mimicking a Stroke, Diagnosed by Correlation of Results of Sequential Magnetic Resonance Imaging, Biopsy, In Vitro Culture, Immunofluorescence Analysis and Molecular Analysis. J Clin Microbiol. 44(11): ) Ofori-Kwakye, S. K., D. G. Sidebottom, J. Herbert, E. G. Fischer, and G. S. Visvesvara Granulomatous brain tumor caused by Acanthamoeba. Case report. J. Neurosurg. 64: ) Petry F, Torzewski M, Bohl J, Wilhelm-Schwenkmezger T, Scheid P, Walochnik J, Michel R, Zöller L, Werhahn KJ, Bhakdi S, Lackner KJ Early diagnosis of Acanthamoeba infection during routine cytological examination of cerebrospinal fluid. J Clin Microbiol. 44(5): ) Schroeder, J. M., G. C. Booton, J. Hay, I. A. Niszl, D. V. Seal, M. B. Markus, P. A. Fuerst, and T. J. Byers Use of subgenic 18S ribosomal DNA PCR and sequencing for genus and
13 48 49 genotype identification of acanthamoebae from humans with keratitis and from sewage sludge. J Clin Microbiol 39: ) Schuster, F.L., and G. S. Visvesvara Opportunistic amoebae: challenges in prophylaxis and treatment. Drug Resist Updat. 7(1): ) Seidel, J. S., P. Harmatz, G. S. Visvesvara, A. Cohen, J. Edwards, and J. Turner Successful treatment of primary amebic meningoencephalitis. N Engl J Med. 306(6): ) Walochnik, J., M. Duchene, K. Seifert, A. Obwaller, T. Hottkowitz, G. Wiedermann, H. Eibl, and H. Aspock Cytotoxic activities of alkylphosphocholines against clinical isolates of Acanthamoeba spp. Antimicrob Agents Chemother. 46(3): ) Walochnik, J., and H. Aspöck Diagnostics of infections with free living amoeba. J Lab Med. 29(6):
ACCEPTED. Microbiology, Medical University of Vienna, Austria, II. Medical Dept., Pulmonological
JCM Accepts, published online ahead of print on November 00 J. Clin. Microbiol. doi:0./jcm.0-0 Copyright 00, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.
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