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Infectivity of Microsporidia Spores Stored in Water at Environmental Temperatures

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Infectivity of Microsporidia Spores Stored in Water at Environmental Temperatures RESEARCH NOTES 185 human philophthalmosis was reported from the United States (Gutierrez 1981. Ein ausgereifter saugwurm der gattung Philophthalmus unter et al., 1987). The patient was a 66-yr-old man, and the parasite obtained der Bindehaut des Menschen. Klinische Monatsblatter fur Augen- from his left eye was identi®ed as P. gralli, although the position of heilkunde 179: 373±375. the cirrus sac in the specimen was not the same as that described for KANEV, I., P. M. NOLLEN,I.VASSILEV,V.RADER, AND V. D IMITROV. this species. A case was also reported from Israel (Lang et al., 1993). 1993. Redescription of Philophthalmus lucipetus (Rudolphi, 1819) The patient was a 13-yr-old girl, and the worm obtained from her right (Trematoda: Philophthalmidae) with a discussion of its identity and eye was apparently mature, but the species was not identi®ed. Our case characteristics. Annals of the Naturalist Museum, Wien. 94/95 B: is the ®rst in Mexico, the ®rst human case of P. lacrimosus infection 13±34. in the world, and the 24th case of human philophthalmosis overall. LANG, Y., Y. WEISS,H.GARZOZI,D.GOLD, AND J. LENGY. 1993. A ®rst The authors are grateful to Dr. A. Villegas-Alvarez, who extracted instance of human philophthalmosis in Israel. Journal of Helmin- the worm; QFB Javier Sedano Millan for his collaboration; and Dr. thology 67: 107±111. Scott Monks, Universidad Autonoma del Estando d Hidalgo, Dra. Vir- MARKOVIC, A. 1939. Der erste fall von Philophthalmose beim Mensch- ginia Leon Regagnon and M. en C. Luis Garcia Prieto, Instituto de en. Albrecht von Graefes Archives fur Ophthalmologie 140: 515± Biologia, UNAM, and Biol. Maria Antonieta Arizmendi, Facultad de 526. Ciencias, UNAM, for their valuable help and advice. MIMORI, T., H. HIRAI,T.KIFUNE, AND K. INADA. 1982. Philophthalmus sp. (trematoda) in a human eye. American Journal of Tropical Med- LITERATURE CITED icine and Hygiene 31: 859±861. NASIR,P.,AND M. T. DIAZ. 1972. Avian ¯ukes of Venezuela. Rivista di BRAUN, M. G. C. C. 1902. Fascioliden der Vogel. Zoologische Jahr- Parasitologica, Roma 33: 245±276. bucher 16: 1±162. NOLLEN,P.M.,AND I. KANEV. 1995. The taxonomy and biology of DISSANIKE,A.S.,AND D. P. BILIMORIA. 1958. On an infection of a human Philophthalmid eye ¯ukes. Advances in Parasitology 36: 206±271. eye with Philophthalmus sp. in Ceylon. Journal of Parasitology 32: TEIXEIRA DE FREITAS, J. F. 1955. Sobre dois trematodeos parasitos de 115±118. aves Philophthalmus lacrimosus Braun, 1902 e Renicola miran- GUTIERREZ, Y., H. E. GROSSNIKLAUS, AND W. L. ANNABLE. 1987. Human daribeiroi n. sp. Arquivos do Museu Nacional 42: 585±610. conjunctivitis caused by the bird parasite. American Journal of YAMAGUTI, S. 1958. Systema Helminthum. The digenetic trematodes of Ophthalmology 104: 417±419. Vertebrates, Vol. I, Parts 1±2. Interscience Publications, New York, KALTHOFF, H., K. JANITSCHKE,S.MRAVAK,W.SCHOPP, AND H. WERNER. New York, 1575 p. J. Parasitol., 89(1), 2003, pp. 185±188 q American Society of Parasitologists 2003 Infectivity of Microsporidia Spores Stored in Water at Environmental Temperatures X. Li, R. Palmer, J. M. Trout, and R. Fayer*, Animal Waste Pathogen Laboratory, Agricultural Research Service, United States Department of Agriculture, 10300 Baltimore Avenue, Beltsville, Maryland 20705-2350. *To whom correspondence should be addressed. e-mail: [email protected] ABSTRACT: To determine how long waterborne spores of Encephali- al., 1998). Although the actual routes of transmission are not well tozoon cuniculi, E. hellem, and E. intestinalis could survive at environ- known, it is possible that the infective spore stage in urine or feces can mental temperatures, culture-derived spores were stored in water at 10, contaminate the environment and enter surface water used for recreation 15, 20, 25, and 30 C and tested for infectivity in monolayer cultures of or drinking water (Sparfel et al., 1997; Dowd et al., 1998; Cotte et al., Madin Darby bovine kidney (MDBK) cells. At 10 C, spores of E. in- 1999; Fournier et al., 2000). Isolation of spores and molecular detection testinalis were still infective after 12 mo, whereas those of E. hellem of microsporidia in ditch water and river water along with circumstantial and E. cuniculi were infective for 9 and 3 mo, respectively. At 15 C, evidence of waterborne transmission is accumulating (reviewed by Bry- spores of the same species remained infective for 10, 6, and 2 mo, and an and Schwartz, 1999). The longevity of insect-infecting microsporidia at 20 C, for 7, 5, and 1 mo, respectively. At 25 C, spores of E. intes- stored under different conditions has been studied (Oshima, 1964; Hen- tinalis and E. hellem were infective for 3 mo, but those of E. cuniculi ry and Oma, 1974; Fuxa and Brooks, 1979; Teetor-Barsch and Kramer, were infective for only 3 wk. At 30 C, the former 2 species were in- 1979), but data on the effect of environmental temperatures on longevity fective for 3 wk and 1 mo, respectively, and the latter species for only of spores of species that infect animals and humans are sparse. Such 1 wk. These ®ndings indicate that spores of different species of En- information can be extremely helpful in understanding the epidemiology cephalitozoon differ in their longevity and temperature tolerance, but at and evaluating the risk of transmission. The present study was designed temperatures from 10 to 30 C, all 3 have the potential to remain infec- to investigate the effect of temperature and storage in water on infec- tive in the environment long enough to become widely dispersed. tivity of spores of E. cuniculi, E. hellem, and E. intestinalis by testing in cultured mammalian cells. Of the 13 species of microsporidia that infect humans, Encephalito- Spores of E. cuniculi and E. hellem were purchased from the Amer- zoon cuniculi, E. hellem, E. intestinalis, and E. bieneusi have been re- ican Type Culture Collection, Manassas, Virginia (ATCC Nos. 50502 ported in a variety of domesticated animals (Deplazes et al., 1996; and 50451, respectively). Spores of E. intestinalis originally isolated Mans®eld et al., 1997; Mathis et al., 1999; Rinder et al., 2000) and from an acquired immune de®ciency syndrome (AIDS) patient and wildlife (Hersteinsson et al., 1993; Mathis et al., 1996; Thomas et al., grown in culture (Didier et al., 1996) were provided by Elizabeth Didier, 1997). Encephalitozoon cuniculi has been identi®ed in wild, laboratory, Tulane Regional Primate Research Center, Covington, Louisiana. En- and pet rabbits, wild and laboratory rats and mice, dogs, cats, foxes, cephalitozoon cuniculi and E. intestinalis were propagated in monolayer mink, and a variety of monkeys (reviewed by Bryan and Schwartz, cultures of MDBK cells, and E. hellem was propagated in human lung 1999; Deplazes et al., 2000). Encephalitozoon hellem and E. hellem± ®broblasts (WI-38) in T-75 ¯asks. The MDBK cells were cultured in like microsporidia have been found in psittacine birds in the United Dulbecco modi®ed Eagle medium (DMEM) supplemented with 1% States and Australia as well as in budgerigar chicks and wild, yellow- nonessential amino acids (NEAA), 2% N-2-hydroxyethylpiperazine-N9- streaked lory (reviewed by Bryan and Schwartz, 1999; Deplazes et al., 2-ethane-sulfonic acid (HEPES), 5% fetal calf serum (FCS), and 1% 2000). Encephalitozoon intestinalis spores were identi®ed in feces of penicillin or streptomycin in a 5% CO2 atmosphere incubator at 35 C. farm animals in Mexico (dog, pig, cow, and goat) (Bornay-Llinares et WI-38 cells were similarly cultured in minimum essential medium 186 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO. 1, FEBRUARY 2003 TABLE I. Number of cultures with intracellular development of microsporidia out of 2 inoculated with spores of Encephalitozoon intestinalis (I), E. hellem (H), and E. cuniculi (C) after storage for 1 wk to 12 mo at environmental temperatures from 10 to 30 C. Temperature 10 C 15 C 20 C 25 C 30 C Time IHC IHC IHC IHC IHC 1wk ND* ND 2 ND ND 2 ND ND 2 ND ND 2 2 ND 2 2wk ND ND 2 ND ND 2 ND ND 2 ND ND 2 2 ND 0 3wk ND ND 2 ND ND 2 ND ND 2 ND ND 2 2 ND 0 1mo 2 2 2 2 2 2 2 2 2 2 2 0 0 2 0 2mo 2 2 2 2 2 2 2 2 0 2 0 0 0 0 0 3mo 2 2 1 2 2 0 2 2 0 2 1 0 0 0 0 4mo 2 2 0 2 2 0 2 2 0 0 0 0 0 0 0 5mo 2 2 0 2 1² 0 2 1 0 0 0 0 0 0 0 6mo 2 2 0 2 1² 0 2 0 0 0 0 0 0 0 0 7mo 2 2 ND 2 0² ND 1 0 ND 0 0 ND 0 0 ND 8mo 2 2 ND 1 0² ND 0 0 ND 0 0 ND 0 0 ND 9mo 2 1 ND 2 0² ND 0 0 ND 0 0 ND 0 0 ND 10 mo 2 0 ND 2 0² ND 0 0 ND 0 0 ND 0 0 ND 11 mo 2 1 ND 0 0² ND 0 0 ND 0 0 ND 0 0 ND 12 mo 2 ND ND 0 ND ND 0 ND ND 0 ND ND 0 ND ND * ND, not done. ² Results based on observation of 1 culture inoculated with spores. (MEM) supplemented with 1% NEAA, 2%HEPES, 10% FCS, 1% pen- chromotrope method and examined by bright®eld microscopy. Enceph- icillin or streptomycin, 1% L-glutamine, and 1% sodium pyruvate.
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