MEM INST OSWALDO CRUZ, RIO DE JANEIRO, 100(2) April 2005
PAGES: 103-110 DOI: Review
The Genus Cyclospora (Apicomplexa: Eimeriidae), with a description of Cyclospora schneideri n.sp. in the snake Anilius scytale scytale (Aniliidae) from Amazonian Brazil _ A Review

Ralph Lainson +

Departamento de Parasitologia, Instituto Evandro Chagas, Av. Almirante Barroso 492, 66090-000 Belém, PA, Brasil

Abstract

A review is made of the recorded species of the coccidian genus Cyclospora and major events leading up to the discovery of C. cayetanensis, which is responsible for serious outbreaks of diarrhoea in man and is one of the aetiological agents of "traveller's diarrhoea". Humans appear to be the specific hosts, with the entire life-cycle in the intestine: to date there is no convincing evidence that the disease is a zoonosis. A description is given of oocysts and endogenous stages of C. schneideri n.sp., in the snake Anilius scytale scytale. Sporulation is exogenous and completed after about one week at 24-26°. Mature oocysts 19.8 × 16.6 (15.1 × 13.8-25.7 × 20.1), shape-index 1.2 (1.0-1.3): no oocyst residuum or polar bodies. Oocyst wall a single colourless, smooth layer with no micropyle: it is rapidly deformed or broken. Sporocysts 13.6 × 9.4 (11.3 × 8.3-15.1 × 9.9), shape-index 1.4 (1.2-1.5) with an inconspicuous Stieda body. Sporozoites 11-13 × 2.5-3. Endogenous stages are intracytoplasmic in the epithelial cells of the small intestine and with the characters of the Eimeriorina.

BACKGROUND HISTORY

Description of the coccidian Cyclospora cayetanensis of humans in 1992naturally resulted in an explosion of papers on this parasite, largely clinical and epi-demiological. It is not the object of the present paper to attempt a revision of the 200 or more publications that ensued, admirably compiled by Steve Upton (2001), but rather to discuss the history of the genus, the species recorded in non-human hosts and the major events that led up to the discovery of Cyclospora in man. A description is given of a new species encountered in the Brazilian snakeAnilius scytale scytale.

The type species of the genus Cyclospora, C. glomericola, was described in the millipede Glomeris (Diplopoda) by Aimé Schneider in 1881 and, to date, appears to be the only species encountered in an invertebrate host. Previously, Eimer (1870) had noted the presence of a parasite with cyclosporan morphology in the intestine of the mole Talpa europaea, but gave it no name, and it remained for Schaudinn (1902) to give a full description of the life cycle of this parasite, which he named C. caryolytica. Tanabe (1938) later described the development of what he considered to be the same species in another mole referred to as Mogera wogura coreana from Japan.

Schaudinn described the asexual and sexual stages of C. caryolytica in both the small and large intestine of the mole, where they develop within the nucleus of the epithelial cells. With the growth of these stages the nucleus disintegrates and the host cell becomes a mere sac containing the parasite: heavy infection may result in a fatal enteritis. Schaudinn noted two types of meronts and suggested that the one producing larger merozoites gave rise to the macrogamonts, while the other gave smaller merozoites which were destined to become microgamonts. Tanabe (1938) was unable to demonstrate more than a single type of meront for what he considered to be C. caryolytica in M. wogura coreana and suggested that Schaudinn was dealing with a mixed infection of that parasite and the merogonic stages of a concomitant Eimeria infection. The concensus of opinion now is that such morphologically different asexual stages merely represent different generations of meronts rather than a sexual dimorphism: Lainson (1965), for example, noted three different types of merozoites produced during the asexual division of C. niniae in the snake Ninia sebae sebae. In typical eimeriid fashion, the microgamont of C. caryolitica produces a large number of flagellated microgametes and, following fertilization of the macrogamonts and development of a resistant membrane around the zygote, the resulting oocysts are expelled, unsporulated, in the faeces. Sporulation is completed in 4-5 days, with the formation of two sporocysts, each containing two sporozoites and a sporocystic residuum.

There followed a succession of descriptions of other Cyclospora species in reptiles, principally snakes (Table), all with intracytoplasmic development in epithelial cells of the intestine. Subsequently, however, Pellerdy and Tanyi (1968) described the oocysts of a second species in the European mole and named it C. talpae. They foundmicrogamonts and macrogamonts in the liver and, in a more recent study, Mohamed and Molyneux (1990) have shown that these sexual stages develop within the nucleus of the bile-duct epithelial cells. Merogony appears to be limited to mononuclear cells in the capillary sinusoids of the liver. Oocysts entering the intestine with the bile are voided in the faeces and exogenous sporulation is completed in about two weeks.

Duszynski and Wattam (1988b) re-described the oocysts of C. talpae in T. europaea from England and, in addition, noted that some oocysts were present which differed from those of C. talpae in minor details (principally in size). Whether or not they belonged to yet another species of Cyclospora was not decided.

Ford and Duszynski (1988, 1989) turned their attention to faecal samples from other members of the Insectivora and encountered three further species of Cyclospora. C. megacephali was described in the "eastern mole"Scalopus aquaticus, and both C. ashtabulensis and C. parascalopi in the "hairy-tailed mole" Parascalops breweri.The site of development in these animals was not ascertained.

Finally, Ford et al. (1990) gave the name of C. angimu-rinensis to oocysts they found in the faeces of the heteromyid rodent Chaetodipus hispidus from the US, and Northern Mexico. Once again, the site of endogenous development was not determined.

 

HUMAN CYCLOSPORIASIS

In 1979 Ashford published a paper recording the presence of what were most probably oocysts of Cyclospora in the faeces of three patients in Papua New Guinea, two of whom were suffering from diarrhoea. The oocysts contained two sporocysts, but Ashford was unable to identify the parasite to generic level due to difficulties in determining the number of sporozoites in the sporocysts. This important finding, strangely overlooked in much of the literature, was followed by a series of publications on similar findings in patients, most of whom were suffering from acute "traveller's diarrhoea" acquired in areas with poor standards of hygiene, or in immunocompromised (Aids) patients (Soave et al. 1986, Long et al. 1990, Hart et al. 1990, Shlim et al. 1991). Long et al. (1991) proposed the term "cyanobacterium-like bodies" (CLB) for the cysts, because of a superficial ultrastructural resemblance to unicellular members of the blue-green algae. Bendall et al. indicated the coccidial nature of the cyanobacterium-like bodies in the 1993 edition of the Lancet, illustrated by photomicrographs of the sporulated oocysts containing two sporocysts. It was at the 41st annual meeting of the American Society of Tropical Medicine and Hygiene in 1992, however, that Ortega and colleagues finally presented unpublished evidence showing that the sporocysts each contained two sporozoites, and that the parasite was, therefore, a member of the genus Cyclospora. The name C. cayetanensis was later proposed by these authors in an abstract of this presentation (Ortega et al. 1992), although Ashford et al. (1993) questioned the validity of the name in view of what they considered to be an inadequate written description of the parasite, and the absence of illustrations. Subsequently, Ortega et al. (1994) described the light and electron microscope morphology of the oocysts in detail and the specific name C. cayetanensis nowremains in firm usage.

Growing epidemiological evidence pointed to the transmission of C. cayetanensis by way of contaminated food or water and to the fact that the parasite enjoyed a world-wide distribution in various countries of Central and South America, Asia, Africa and Europe, and in Australia. The remarkable efficiency of transmission and the medical importance of human cyclosporiasis first became apparent, however, following a series of explosive outbreaks of acute diarrhoea among large numbers of guests at a number of social events in the US and Canada, during the years 1996-1998 (Chambers et al. 1996, Herwaldt & Ackers 1997, Herwaldt & Beach 1999). Careful in-vestigations finally traced the source of infection to unwashed raspberries imported from Guatemala and, during studies in that country (Bern et al. 1999), an infection-rate of 2.3% was found in the stools from 5552 persons examined in governmental health centres and hospitals. Positive faeces were most commonly found in children and persons suffering from gastroenteritis, and the authors noted a seasonality of cyclosporiasis. Thus, an infection-rate of 3.8% in May rose to a peak of 6.7% in June, and subsided to zero during the period August to November of the same year. A study of raspberry farm workers and family members showed 6 of 182 persons (3.29%) to be passing oocysts. Finally, in a case-control analysis of 68 infected individuals, 62 (91%) admitted drinking untreated water about two weeks before the onset of illness (Bern et al. 1999).

Further outbreaks of human cyclosporiasis among participants at social events in the US were attributed to the consumption of fresh basil or lettuce in salads and side-dishes (Anon. 1997a, b, Lopez et al. 2001). In Germany, 34 persons developed acute diarrhoea diagnosed as cyclosporiasis, and the source of infection was again considered to be salad side-dishes of lettuce, imported from southern Europe, spiced with fresh leafy herbs (Döller et al. 2002). Epidemiological investigations in endemic areas of other countries revealed oocysts of C. ca-yetanensis on green leafy vegetables, in sewage water, and even in tap-water (Ortega et al. 1997a, Sturbaum et al. 1998, Sherchand et al. 1999, El-Naga 1999, Cam et al. 2001).

 

THE SOURCE OF C. cayetanensis IN WATER AND FOOD

Attempts have been made to find non-human hosts of C. cayetanensis and show that human cyclosporiasis is in fact a zoonosis: there is as yet, however, no conclusive evidence that this is so and the few claims of success have been thrown into doubt by the conflicting findings of other workers. Garcia López et al. (1996) reported the finding of oocysts considered to be those of this parasite in the pooled faeces of some 600 young chicken from a poultry farm and in pooled caecal contents from another 50 from a market near Monterey, Mexico, and there is a report of similar oocysts in the faeces of a duck in Peru (Zerpa et al. 1995). In an endemic area of Nepal, Sherchand et al. (1999) found oocysts suspected to be those of C. cayetanensis in two chickens during a survey of 196 domestic animals: all the other animals were negative. In a survey of Peruvian children in Peru, Bern et al. (2002), suggested that human cyclosporiasis was most frequently associated with the ownership of domestic animals. In contrast to all these findings, however, Eberhard et al. (1999a) found no morphologically compatible oocysts in chickens, ducks, turkeys, pigeons, pigs, cattle, horses, goats, dogs, cats, and guinea-pigs in Haiti, despite their living in or near houses with human infection: they concluded that domestic animals were not a reservoir of C. cayetanensis and that man appears to be the only host. Yai et al. (1997) reported oocysts that appeared to be those of C. cayetanensis in two dogs from São Paulo, Brazil, but Carollo et al. (2001) found no signs of infection in 140 stray dogs they examined in the same area.

To date, then, available evidence suggests that humans are the specific hosts of C. cayetanensis and the sole source of oocysts, following their faecal contamination of food and water. Supporting this is histological evidence showing that the entire life-cycle of the parasite takes place in the human intestine (Sun et al. 1996, Ortega et al. 1997b), and the striking host specificity shown by other primate species of Cyclospora, namely C. cer-copitheciand C. colobi of monkeysand C. papionis of baboons, even when there is a geographical overlap of the hosts and parasites (Eberhard et al. 1999a, 2001). To what extent such specificity extends to Cyclospora species recorded in other hosts is uncertain. The genus would appear to be particularly common in snakes (Table), and this review extends the list of ophidian hosts with the description of a new species in the snake Anilius scytale scytale(Aniliidae).

A. scytale scytale, is a relatively small, burrowing "pipe-snake" found in the Guianas, North Brazil, Venezuela and Amazonian Colombia, Ecuador and Peru. It is harmless, but because of its vivid red colour with black rings it is often mistaken for the venomous coral snake Micrurus. Seldom seen above ground, it is most commonly found when flushed outduring heavy rain.

Only two of these snakes were available for study, in December, 1990 and January 2004, both from the state of Pará, North Brazil. They were passing coccidial oocysts in their faeces and sporulation was in both cases completed in approximately one week in 2% aqueous potassium dichromate solution (K2Cr2O7) at 24-26º. Oocysts were measured using normal light microscopy, an eyepiece micrometer and the oil immersion lens. Dimensions are given in µmas means, followed by the range in parentheses, the shape index (ratio of length/width) and the number measured (n). Tissues for histology were fixed in 10% buffered neutral formalin and embedded in paraffin wax: sections were cut at 4 µm. Photo-micrographs were made with a Zeiss "Photomicroscope III" and Kodak TMX100 film.

Cyclospora schneideri n.sp. 
(Figs 1-18)

Description of the oocyst - Mature forms (Figs 14-18) ovoid to subspherical or, more rarely, spherical: 19.8 × 16.6 (15.1 ×13.8-25.7 × 20.1), shape index 1.2 (1-1.3), n = 100. No oocyst residuum or polar bodies. Oocyst wall approximately 0.5-1 thick, colourless, smooth, and apparently of a single layer: no micropyle or striations. It is fragile and soon becomes highly deformed. The two dizoic sporocysts average 13.6 × 9.4 (11.3 × 8.3-15.1 × 9.9), shape index 1.4 (1.2-1.5), n = 77: there is an inconspicuous nipple-like Stieda body. The sporozoites measure 11-13.0 × 2.5-3, n = 13, and curve slightly around a sporocystic residuum of fine granules and larger globules. Refractile bodies were not detected.

Endogenous stages -These develop, in conspicuous parasitophorous vacuoles, in the cytoplasm of the epithelial cells of the small intestine. In histological sections of the infected gut, most of the developing parasites were clearly located above the host cell nucleus, but it is possible that others commenced development below and, with growth, eventually positioned themselves between or above the nuclei. Mature meronts (Figs 1, 2) were scanty but appeared to be of a single, small type of approximately 16 ×14 (n = 4): they produce 6-12 merozoites, measuring an average of 10 × 2.5 (n = 4) and segmentation leaves no residuum. Growing microgamonts (Figs 8, 9) reach up to 33 × 26 and contain many bulky, heavily stained nuclei distributed predominantly at the periphery of the parasite. Mature forms (Figs 10, 11) have a residuum containing a few big vacuoles, and shed a large number of microgametes measuring approximately 5.0 × 1. Young macro-gamonts (Figs 3-5) have a poorly staining nucleus containing a densely staining karyosome (Fig. 4). Mature forms (Fig. 7) may reach up to 24 × 20 (15 × 10 - 24 × 20), 
n = 10, and contain very prominent small and large wall-forming bodies (Figs 6, 7). The wide size range of the mature macrogamonts results in an equally wide range in the size of the zygotes and the oocysts. This at first gave the impression that both snakes were infected with two different species of Cyclospora. Demonstration of a smooth gradation between the dimensions of the smallest and the largest oocysts, however, militates against this possibility.

Sporulation - Exogenous, in approximately one week.

Host - The snake Anilius scytale scytale (Linnaeus), (Aniliidae).

Type locality - Capanema, state of Pará, North Brazil.

Type material - Oocysts in 10% buffered formalin, histological sections of the endogenous stages and phototypes in the Department of Parasitology, Instituto Evandro Chagas and the Muséum National d'Histoire Naturelle, Paris: Accession No. 2257.

Prevalence - Uncertain. Only two A. s. scytale wereexamined, and both were infected.

Pathology -No apparent pathology.

Etymology -The specific name is in honour of Aimé Schneider, who founded the genus Cyclospora.

As far as I am aware, this is the first coccidian to be described in Anilius s. scytale. Among the Cyclosporaspecies previously described in snakes, C. niniae Lainson, 1965 resembles C. schneideri n.sp., in the fragility of the oocyst wall, the size of the sporocysts and their possession of a modest Stieda body. The oocysts of C. niniae, however, contain a conspicuous polar body, and measure only 14.6 × 13.3. Phisalix (1923, 1924a, 1933) made a number of revisions to her measurements of the oocysts of C. viperae, but on the basis of her final measurements of 16.8 × 10.5 they are substantially smaller than those of C. schneideri n.sp., as are those of C. babaultiC. tropidonoti, and C. zamenis (17 x 10) (Table). Without cross-infection experiments the host specificity of ophidian Cyclospora species remains uncertain, but the wide zoological difference and wide geographical separation of A. s. scytale and the Europeancolubrids and vipers makes it most unlikely that C. schneideri n.sp., is conspecific with any one of the four species described by Phisalix.

I have commented on the similarity of the oocysts of the four species of Cyclospora named by Phisalix (Lainson 1965) and suggested that C. babaulti, C. tropidonoti and C. zamensis might be synonyms of C viperae. Duszynski et al. (1999) appear to have in part agreed with this suggestion and have listed C. babaulti as a synonym of C. viperae and C. tropidonoti as a synonym of C. zamenis. They went further in suggesting that the oocysts of C. viperae "… appear to be misidentifications of Sarcocystis spp." and that "… perhaps all species from reptiles are misidentifications of Isospora or Sarcocystis spp." I feel it best, however, to include the five reptilian species ofCyclospora described by Phisalix in the accompanying Table until such time as conclusive evidence is provided with which to sink them. Their re-examination by DNA analysis might confirm or refutetheir present taxonomic status, and in this respect it is of interest thatEberhard et al. (1999a) considered that the three species C. cerco-pitheciC. colobi, and C. papionis of non-human primates could not be separated by morphology of their oocysts but only at molecular level.

It is now becoming apparent that species of Cyclospora infect a wider range of hosts than previously supposed and it should come as no surprise that reptiles are hosts of Cyclospora when one considers the wide host range of other members of the Eimeriidae. Thus, species of Eimeria are recorded in millipedes, centipedes, coleopterans, fish, amphibians, reptiles, birds and mammals (Levine 1988); the type species of IsosporaI. rara, was described in the gastropod Limax sp., and other species are common parasites of amphibia, reptiles, birds and mammals (including man); Caryospora species are found in reptiles, birds and mammals. By light microscopy, it is clearly difficult to determine the number of sporozoites in a sporocyst of an oocyst as small as that of C. cayetanensis(diameter 8.6 µm), and other Cyclospora species of similar size may well have been erroneously assignedto the genus Isospora or Sarcocystis. However, due to the much larger size of the oocysts of both C. niniae and C. schneideri n.sp. (14.6 ×13.3 and 19.8 ×16.6, respectively), it has not been difficult to determine the dizoic nature of their sporocysts, particularly when they are seen in an end-on position (Figs 1518).

 

ACKNOWLEDGEMENTS

To Constância M Franco and Manoel C de Souza for technical assistance. Histological sections were prepared by Walter M Campos.

 

REFERENCES

Anon 1997a. Outbreak of cyclosporiasis - northern Virginia - Washington, D.C. - Baltimore, Maryland Metropolitan Area. Can Comm Dis Rept 23: 166-168.

Anon 1997b. Update: outbreaks of cyclosporiasis _ United States and Canada, 1997. Can Comm Dis Rept 23: 143-144.

Ashford RW 1979. Occurrence of an undescribed coccidian in man in Papua New Guinea. Ann Trop Med Parasitol 73: 497-500.

Ashford RW, Warhurst DC, Reid GDF 1993. Human infection with cyanobacterium-like bodies. Lancet 341: 1034.

Bendall RP, Lucas S, Moody A, Tovey G, Chiodini PL 1993. Diarrhoea associated with cyanobacterium-like bodies: a new coccidian enteritis of man. Lancet 341: 590-592.

Bern C, Hernandez B, Lopes MB, Arrowood MJ, Alvarez De Mejia M, Merida AM De, Hightower AW, Venczel L, Herwaldt BL, Klein RE 1999. Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerg Inf Dis 5: 766-774.

Bern C, Ortega Y, Checkley W, Roberts JM, Lescano AG, Cabrera L, Verastegui M, Black RE, Sterling C, Gilman RH 2002. Epidemiologic differences between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerg Inf Dis 8: 581-585.

Cam PD, Sorel N, Dan LC, Larker E, Tassin S, Barber JP, Miegeville M 2001. A new contribution to the epidemiological survey of Cyclospora cayetanensis in Hanoï water supplies (Vietnam): a 12-month longitudinal study. Med Mal Infect 31: 591-600.

Carollo MCC, Amato Neto V, Braz LMA, Kim Dowoong 2001. Pesquisa de oocistos de Cyclospora sp., em fezes de cães da Grande São Paulo, Estado de São Paulo, Brasil. Rev Soc Bras Med Trop 34: 597-598.

Chambers J, Somerfeldt S, Mackey L, Nichols S, Ball R, Roberts D, Dufford N, Reddick A, Gibson J 1996. Outbreaks of Cyclospora cayetanensis infection _ United States, 1996. MMWR 45: 549-551.

Döller PC, Dietrich K, Filipp N, Brockmann S, Dreweck C, Vonthein R, Wagner-Wiening C, Wiedermann A, 2002. Cyclosporiasis outbreak in Germany associated with the consumption of salad. Emerg Inf Dis 8: 992-994.

Duszynski DW, Wattam AR 1988a. Coccidian parasites (Apicomplexa: Eimeriidae) from Insectivores V. Ten forms from the moles of Japan (Euroscoptor, Mogera spp.). J Protozool 35: 55-57

Duszynski DW, Wattam AR 1988b. Coccidian parasites (Apicomplexa: Eimeriidae) from insectivores IV. Four new species in Talpa europaea from England. J Protozool 35: 58-62.

Duszynski DW, Upton SJ, Couch L 1999. The Coccidian Genus Cyclospora. Available at: <htpp://biology.unm.edu/biology/coccidia/cyclo.html> Accessed on 2 April, 2004.

Eberhard ML, Nace EK, Freeman AR 1999a. Survey for Cyclospora cayetanensis in domestic animals in an endemic area in Haiti. J Parasitol 85: 562-563.

Eberhard ML, Njenga MN, Silva AJ Da, Owino D, Nace EK, Won KY, Mwenda JM 2001. A survey forCyclospora spp., in Kenyan primates, with some notes on its biology. J Parasitol 87: 1394-1397.

Eberhard ML, Silva AJ Da, Lilley BG, Pieniazek NJ 1999b. Morphologic and molecular characterization of newCyclospora species from Ethiopian monkeys: C. cercopitheci sp.n., C. colobi sp.n., and C. papionis sp.n. Emerg Inf
Dis 5
: 651-658.

Eimer T 1870. Ueber die ei-und Kugelförmigen sogenannten Psorospermien der Wirbelthiere, A Stuberr's Verlang-shandlung,Würzburg, Germany.

El-Naga IFA 1999. Studies on a newly emerging protozoal pathogen: Cyclospora cayetanensisJ Egypt Soc Parasitol 29: 575-586.

Ford PL, Duszynski DW 1988. Coccidian parasites from insectivores VI. Six new species from the Eastern moleScalopus aquaticus. J Protozool 35: 223-226.

Ford PL, Duszynski DW 1989. Coccidian parasites (Api-complexa: Eimeriidae) from insectivores VII. Six new species from the hairy-tailed mole Parascolops breweri. Parasitology 75: 508-513.

Ford PL, Duszynski DW, McAllister CT 1990. Coccidia (Apicomplexa) from heteromyid rodents in the Southwestern United States, Baja California, and Northern Mexico, with three new species from Chaetodipus hispidus. J Parasitol 76: 325-331.

García López HL, Rodríguez Tovar LE, Garza CEM La, 1996. Identification of Cyclospora in poultry [Correspondence]. Emerg Inf Dis 2: 356-357.

Hart AS, Ridinger MT, Soundarajan R, Peters CS, Swiatlo AL, Kocka FE 1990. Novel organism associated with chronic diarrhoea in AIDS. Lancet 335 (8682): 169-170

Herwaldt BL, Ackers ML 1997. An outbreak in 1996 of cyclosporiasis associated with imported raspberries. New Engl J Med 336: 1548-1556.

Herwaldt BL, Beach MJ 1999. The return of Cyclospora in 1997: another outbreak of cyclosporiasis in North America associated with imported raspberries. Ann Int Med 130: 210-220.

Lainson R 1965. Parasitological studies in British Honduras II. Cyclospora niniae sp.n. (Eimeriidae: Cyclosporinae) from the snake Ninia sebae sebae (Colubridae). Ann Trop Med Parasitol 59: 159-163.

Levine ND 1988. The Protozoan Phylum Apicomplexa, Vol. I, CRC Press, Boca Raton, FL, 203 pp.

Long EG, Ebrahimzadeh A, White EH, Swisher B, Callaway CS 1990. Alga associated with diarrhea in patients with acquired immunodeficiency syndrome and in travellers. Clin Microbiol 28: 1101-1104.

Long EG, White EH, Carmichael WW, Quinlisk PM, Raja R, Swisher BL, Daugharty, Cohen MT 1991. Morphological and staining characteristics of a cyanobacterium-like organism associated with diarrhea. J Inf Dis 164: 199-202.

Lopez AS, Dodson DR, Arrowood MJ, Orlandi PA Jr, Silva AJ Da, Bier JW, Hanauer SD, Kuster Rl. Oltman S, Baldwin MS, Won KY, Nace EM, Eberhard ML, Herwaldt BL 2001.Outbreak of cyclosporiasis associated with basil in Missouri in 1999. Clin Inf Dis 32: 1010-1017.

Mohamed HA, Molyneux DH 1990. Developmental stages of Cyclospora talpae in the liver and bile duct of the mole Talpa europaea. Parasitology 101: 345-350.

Nowak RM, Paradiso JC 1983. Walker's Mammals of the World, 4th ed., Vol. I, Johns Hopkins Univ. Press, Baltimore, MD.

Ortega YR, Gilman RH, Sterling CR 1994. A new coccidian parasite (Apicomplexa: Eimeriidae) from humans. J Parasitol 80: 625-629.

Ortega YR, Nagle R, Gilman RH, Watanabe J, Miyagui J, Quispe N, Kanagusuku P, Roxas C, Sterling CR 1997b. Pathologic and clincal findings in patients with cyclosporiasis and a description of intracellular parasite life-cycle stages. J Inf Dis 176: 1584-1589.

Ortega YR, Roxas CR, Gilman RH, Miller NJ, Cabrera L, Taquiri C, Sterling CR 1997a. Isolation ofCryptosporidium parvum and Cyclospora cayetanensis from vegetables collected in markets of an endemic region of Peru. Am J Trop Med Hyg 57: 683-686.

Ortega YR, Sterling CR, Gilman RH, Carna VA, Diaz F 1992. Cyclospora cayetanensis: a new protozoan pathogen of humans. Abstract 289 in Proceedings of the 41st Annual Meeting of the American Society of Tropical Medicine and Hygiene. J Am Soc Trop Med Hyg (Suppl.):210.

Pellérdy L, Tanyi Z 1968. Cyclospora talpae sp.n. (Protozoa: Sporozoa) from the liver of Talpa europaea. Folia Parasitol (Praha) 15: 275-277.

Phisalix M 1923. Coccidiose intestinale de la vipère aspic à Cyclospora viperae n.sp. Bull Soc Path Exot 16: 637-642.

Phisalix M 1924a. Note complémentaire sur Cyclospora viperae, coccidie parasite de l'intestinde la vipère aspic.Bull Soc Path Exot 17: 559-562.

Phisalix M 1924b. Coccidiose intestinale de Vipera berus à Cyclospora babaulti nov.sp. Bull Soc Path Exot 17: 868-871.

Phisalix M 1924c. Cyclospora tropidonoti nov.spec., coccidie intestinale de la couleuvre à collier. Bull Soc Path Exot 17: 871-873.

Phisalix M 1924d. Coccidiose intestinale du Scincus officinalis Laur., à Cyclospora scinci nov.sp. Bull Mus Natn Hist Nat Paris 30: 100-101.

Phisalix M 1924e. Cyclospora zamenis nov.sp., coccidie à localisation intestinale de Zamenis viridiflavus Lacép.Bull Mus Natn Hist Nat Paris 30: 501-502.

Phisalix M 1933. Coccidiose intestinale à Cyclospora viperae chez la couleuvre vipérine, la couleuvre lisse et la couleuvre à échelons. Bull Soc Path Exot 26: 415-420.

Schaudinn F 1902. Studien über krankheitserregende Protozoen I. Cyclospora caryolitica Shaud., der Erreger der perniciösen Enteritis des Maulwurfs. Arb K Gesundheitsamte 18: 378-416.

Schneider A 1881. Sur les psorospermies oviformes ou coccidies. Espécies nouvelles ou peu connues. Arch Zool Exp Gen 9: 387-404.

Sherchand TB, Cross JH, Jimba M, Sherchand S, Shrestha MP 1999. Study of Cyclospora cayetanensis in health care facilities, sewage water and green leafy vegetables in Nepal. South As J Trop Med Pub Hlth 30: 58-63.

Shlim DR, Cohen MT, Eaton M, Rajah R, Long EG, Unger BL 1991. An algal-like organism associated with an outbreak of prolonged diarrhea among foreigners in Nepal. Am J Trop Med Hyg 45: 383-389.

Soave R, Dubey JP, Ramos LJ, Tummings M 1986. A new intestinal pathogen? Clin Res 34: 533 (Abstract).

Sturbaum GD, Ortega YR, Gilman RH, Sterling CR, Cabrera L, Klein DA 1998. Detection of Cyclospora cayetanensis in wastewater. Appl Environ Microbiol 64: 2284-2286.

Sun T, Ilardi CF, Asnis D, Bresciani AR, Goldenberg S, Roberts B, Terchberg S 1996. Light and electronmicroscopic identification of Cyclospora species in the small intestine: evidence of the presence of asexual life cycle in human host. Am J Clin Path 105: 216-220.

Tanabe M 1938. On three species of coccidia of the mole, Mogera wogura coreana Thomas, with special reference to the life history of Cyclospora caryolytica. Keijo J Med 9: 21-52.

Upton SJ 2001. Cyclospora cayetanensis. Available at:<http://www.ksu.edu/parasitology/cyclospora/cyclospora.html>. Accessed on 2 April, 2004.

Yai IEO, Bauab AR, Hirschfeld MPM, Oliveira ML De. Damaceno JT 1997. Brief communication: the first two cases of Cyclospora in dogs, São Paulo, Brazil. Rev Inst Med Trop São Paulo 39: 177-179.

Yamamoto K 1933. Studien über die Kokzidien [In Japanese, with German summary]. Fukuoka Acta Med 26: 40-43.

Zerpa R, Uchima N, Huicho L 1995. Cyclospora cayetanensis associated with watery diarrhoea in Peruvian patients. Am J Trop Med Hyg 98: 325-329.

CONTACT US

Memórias do Instituto Oswaldo Cruz

Av. Brasil 4365, Castelo Mourisco
sala 201, Manguinhos, 21040-900
Rio de Janeiro, RJ, Brazil

Tel.: +55-21-2562-1222

This e-mail address is being protected from spambots. You need JavaScript enabled to view it.

twitterfacebook

SUPPORT PROGRAM

marca fiocruzmarca brasil
marca faperjmarca cnpqmarca capes n marca cope

and diabetes. Erection dysfunction or ED is certainly one of mens most usual problem. It changes buy tadalafil 60mg A common drug is actually an imitation of its manufacturer twin. Both ought to be same in female cialis 20mg Long Phrase Viagra Use Fundamentally Damages Sex Lives This discount cialis canada Equally so, theres something to be said for the wonder of the second, captured forever on picture or a buy cheap cialis People extremely annoyed that they could only get three weeks at a time, Bunker noted. Retired persons cheap pharmacy These types of matters are possibly to being identified as having a result of cancer buy cialis 40mg - Yoghourt - fat-free simply Physical causes: Buying generic medicines now has been cheap generic cialis Herbaceous plants like nigrum and tribulus are well-known for his or her qualities in defeating impotence, which tadalafil 10mg It is not hard to consider Cialis that is generic. Most men start with one-10 mg dosage each purchase cialis Tadalafil quickly gained the moniker of weekender in Paris due to the fabulous results. The bash freaks buy female cialis