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Disseminated Microsporidiosis Caused By Disseminated Microsporidiosis Caused by Encephalitozoon cuniculi III (Dog Type) in an Italian AIDS Patient: a Retrospective Study Antonella Tosoni, B.Sc., Manuela Nebuloni, M.D., Angelita Ferri, M.D., Sara Bonetto, M.D., Spinello Antinori, M.D., Massimo Scaglia, M.D., Lihua Xiao, D.V.M., Ph.D., Hercules Moura, M.D., Ph.D., Govinda S. Visvesvara, Ph.D., Luca Vago, M.D., Giulio Costanzi, M.D. Pathology Unit, “L.Sacco” Hospital and Institute of Biomedical Sciences, University of Milan, Italy (AT, AF, SB, LV, GC); Institute of Infectious Diseases and Tropical Medicine, University of Milan, “L. Sacco” Hospital, Milan, Italy (SA); Pathology Unit, Hospital of Vimercate, Milan, Italy (MN); Infectious Diseases Research Laboratories and Department of Infectious Diseases, University of Pavia—IRCCS, San Matteo, Italy (MS); and Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Public Health Service, Atlanta, Georgia (LX, GSV, HM) The prevalence of opportunistic microsporidial We report a case of disseminated microsporidiosis infections in humans greatly increased during the in an Italian woman with AIDS. This study was done AIDS pandemia, particularly before the advent of retrospectively using formalin-fixed, paraffin- HAART. At least 12 species, belonging to seven gen- embedded tissue specimens obtained at autopsy. era (Enterocytozoon, Encephalitozoon, Pleistophora, Microsporidia spores were found in the necrotic Trachipleistophora, Brachiola, Nosema,andVit- lesions of the liver, kidney, and adrenal gland and in taforma), have been identified. Additionally, a ovary, brain, heart, spleen, lung, and lymph nodes. catch-all genus, Microsporidium, of uncertain The infecting agent was identified as belonging to taxonomic status, is also known to infect humans the genus Encephalitozoon based on transmission (2, 3). electron microscopy and indirect immunofluores- The most frequently recognized species in hu- cence. Additional molecular studies, including se- mans is Enterocytozoon bieneusi. It is mainly found quence of the rDNA internal transcribed spacer re- in the upper gastrointestinal tract and associated gion, identified the agent as E. cuniculi, Genotype with diarrheal illness, although a couple of reports III. We believe that this is the first report of a human have identified E. bieneusi in respiratory samples case of disseminated microsporidial infection in- (4). Encephalitozoon intestinalis, the second most volving the ovary. frequently identified microsporidian, causes dis- seminated microsporidiosis, including the gastroin- KEY WORDS: Adrenal gland, AIDS, Brain, Dissemi- testinal tract (4). The two other species of Enceph- nated infection, Encephalitozoon cuniculi, Kidney, alitozoon, E. cuniculi and E. hellem, are also known Liver, Microsporidia, Ovary, Pathology. to cause disseminated infections including the uro- Mod Pathol 2002;15(5):577–583 genital, respiratory, and ocular organs. There are, however, two reports of enteric localization of E. Microsporidia are spore-forming obligate intracel- cuniculi (2, 5), and very recently, an E. hellem was lular protozoan parasites belonging to the phylum recognized for the first time in stools of two immu- Ͼ Microspora, which includes 100 genera and nocompetent travelers with diarrhea (6). Ͼ 1000 species. They infect a wide range of inverte- Encephalitozoonosis has been associated with a brate and vertebrate hosts (1). wide range of pathological features, including tu- bulointerstitial nephritis, ureteritis, cystitis, pros- tatitis, rhino-sinusitis, bronchiolitis, pneumonia, Copyright © 2002 by The United States and Canadian Academy of and keratoconjunctivitis (2, 7). Two cases of dis- Pathology, Inc. VOL. 15, NO. 5, P. 577, 2002 Printed in the U.S.A. seminated infections with brain involvement Date of acceptance: February 4, 2002. caused by E. cuniculi have also been reported (8, 9). This study was supported by a grant from Istituto Superiore di Sanità, Rome, Italy: National Program AIDS Research, Project 30B19. E. cuniculi is the prototype species of the Enceph- Address reprint requests to: Antonella Tosoni, B.Sc., Anatomia Patologica Ospedale “L.Sacco,” Via G.B. Grassi n°74, 20157 Milan, Italy; e-mail: alitozoon genus and a well-known agent of micros- [email protected]; fax: 39-2-38200385. poridiosis in various mammalian hosts (1, 10). 577 Other species of microsporidia have been only pleural and peritoneal effusion developed, and the sporadically reported in patients with ocular, mus- patient died in January 1996. A complete autopsy cle, and disseminated infections (1, 2). was performed 19 hours after death. Some stains, such as modified trichrome, Gram, and fluorochrome-based techniques, used by mi- croscopists, make it possible to detect the micros- MATERIALS AND METHODS poridia spores in various biological specimens (1, Formalin-fixed, paraffin-embedded tissues in- 11–13). To differentiate the microsporidian gen- cluding brain, lung, heart, breast, kidney, adrenal era and most of their species, a transmission elec- gland, liver, pancreas, spleen, small and large tron microscopy study is usually enough, but im- bowel, lymph nodes, ovary, uterus, and bone mar- munological, biochemical, or molecular analyses row were sectioned and stained. Sections were are required to distinguish E. cuniculi from E. stained with hematoxylin and eosin, Kinyoun’s hellem (1, 2). acid-fast, Giemsa, AFIP-modified Gram, and special stains for microsporidia (aniline blue modified trichrome, Ref. 13; “quick-hot” trichrome Gram- CASE REPORT chromotrope, Ref. 12). Tissues were also examined by means of trans- A 33-year-old Italian female, an injection drug mission electron microscopy using a ZEISS EM109 user who had been HIV seropositive since 1985, was electron microscope. Selected areas from formalin- hospitalized in November 1995 because of a fixed, paraffin-embedded blocks of kidney, adrenal 1-month history of fever, myalgia, and abdominal gland, liver, spleen, brain, lung, and small and large pain and was treated with co-trimoxazole as pri- bowel that were positive for microsporidia in the mary PCP prophylaxis. She had also received anti- corresponding histological sections were retrieved retroviral therapy with zidovudine from 1990 to and deparaffinized with xylene over a 12-hour pe- 1992 and had recurrent oropharyngeal candidiasis riod. After rehydration and fixation with osmium and lower respiratory Pseudomonas aeruginosa in- tetroxide, the samples were reembedded in araldite fection. In April 1995, an atypical disseminated my- (Durcupan ACM Fluka). Semithin and thin sections cobacteriosis was diagnosed and successfully were stained using conventional methods. treated with clarithromycin, rifabutin, and etham- Indirect immunofluorescence analyses were per- butol. A few months later, a human papillomavirus– formed on smears made from the two reference related high-grade cervical intraepithelial neoplasia strains, E. cuniculi CDC:V282 (14) and E. hellem was also diagnosed by means of cytological exam- CDC:V213 (15), as well as on sections from ination of cervical smear. Upon admission to L. ϩ formalin-fixed, paraffin-embedded tissue samples. Sacco Hospital (in Milan, Italy) her absolute CD4 Culture-derived spores of the two reference strains lymphocyte count was 4 per microliter. Results of were harvested from culture supernatants and pu- direct microscopic evaluation and blood, stool, and rified as described elsewhere (15, 16). Rabbit poly- urine cultures for microbial pathogens were repeat- clonal antibodies against the reference strains were edly negative. A stool examination with modified used in the indirect immunofluorescence test, as trichrome staining for microsporidia and immuno- described elsewhere (17). assay for Cryptosporidium parvum were also nega- Molecular analyses were performed on formalin- tive. An abdominal computed tomography scan re- fixed and paraffin-embedded tissue blocks of kid- vealed multiple lesions involving the ovaries, right ney. Paraffin-embedded renal sections were dew- adrenal gland, kidney, and intraperitoneal lymph axed with xylene, and DNA was extracted and nodes. At that time, a solid nodule appeared in the amplified from the retrieved tissue as described right breast, and cytological evaluation of a fine- elsewhere (18, 26). The E. cuniculi parasite present needle aspirate showed large immunoblastic cells was genotyped by sequence analysis of the poly- typical of non-Hodgkin’s lymphoma. A subsequent merase chain reaction (PCR) product of the internal bone marrow examination demonstrated a com- transcribed spacer (ITS) of the rRNA gene (26) and plete substitution of the parenchyma by the same confirmed by direct PCR analysis of the polar tube pathological cells. A cerebral computed tomogra- protein gene (18). phy scan showed dense brain lesions and cranial erosions, and a blood examination revealed pancy- topenia, a high level of lactate dehydrogenase (7850 RESULTS U/L), and hypercalcemia. Chemotherapy was started with vincristine, prednisone, etoposide, and Light Microscopy idarubicin, and the hypercalcemia was treated with Large necrotic lesions with a ring of macro- clodronate. Despite an initial response and a partial phages, fibrosis, and a few lymphocytes and gran- improvement of the general condition, bilateral ulocytes were found in the hematoxylin and eosin– 578 Modern Pathology stained sections of liver (Fig. 1), cortical kidney, and the adrenal medulla. The last two organs also
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