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Acta Tropica 115 (2010) 181193
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Acta Tropica
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Review
Epidemiology of Cyclospora cayetanensis: A review focusing in endemic areas
Leonor Chacn-Bonilla
Postgrado de Inmunologa, Instituto de Investigaciones Clnicas, Facultad de Medicina, Universidad del Zulia, Apartado Postal 23, Maracaibo, Venezuela
a r t i c l e i n f o
Article history:
Received 23 December 2009
Accepted 1 April 2010
Available online 9 April 2010
Keywords:
Cyclospora cayetanensis
Cyclosporiasis
Epidemiology
Risk factors
Transmission
Review
a b s t r a c t
Cyclospora cayetanensis is an intestinal coccidian protozoon that has emerged as an important cause
of endemic or epidemic diarrhoeal illness in children and adults worldwide. Humans appear to be the
only natural hosts. However, the role of animals as natural reservoirs is uncertain but of increasing
concern. Human-to-human spread of the parasite occurs indirectly via the environment through oocysts
in contaminated water, food or soil. In endemic areas, risk factors associated with the infection include
contaminatedwater or food, contact withsoil or animals, type of sanitationandlowsocioeconomic status.
Infections linked to soil contact provide reasons to believe that this route of spread may be more common
than realised in disadvantaged community settings. C. cayetanensis is an important cause of travellers
diarrhoea and numerous large foodborne outbreaks associated with the globalisation of the food supply
andimportationof fruits andvegetables fromdeveloping countries have occurred. Waterborne outbreaks
have also been reported. Implementation of measures to prevent or control the spread of Cyclospora
oocysts in the environment is critical. In endemic areas, the most important steps to prevent infection are
improving environmental sanitation and health education. Signicant gaps remain in our understanding
of the epidemiology of human cyclosporiasis that highlight the need for continued research in several
aspects of C. cayetanensis.
2010 Elsevier B.V. All rights reserved.
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
1.1. Historical perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
1.2. Human cyclosporiasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
1.3. Aim of this review. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
2. Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
2.1. Current taxonomy and phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
2.2. Life cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183
2.3. Structure and survival of the infective stage. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183
2.4. Infectivity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183
2.5. Environmental occurrence of oocysts and transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
3. Epidemiology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
3.1. Distribution of human cyclosporiasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
3.2. Geographic distribution and prevalence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
3.3. Age and sex distribution. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186
3.4. Seasonal distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
3.5. Reservoirs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
3.6. Sources and routes of transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
3.6.1. Waterborne transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
3.6.2. Foodborne transmission. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188
3.6.3. Soil transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188
3.6.4. Zoonotic transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
3.6.5. Airborne transmission. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
4. Prevention and control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
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0001-706X/$ see front matter 2010 Elsevier B.V. All rights reserved.
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182 L. Chacn-Bonilla / Acta Tropica 115 (2010) 181193
5. Future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190
1. Introduction
1.1. Historical perspective
Coccidian protozoa of genus Cyclospora are obligate intracellu-
lar apicomplexan parasites that infect the mucosal epithelium of
the intestine or bile duct of a variety of hosts, mostly vertebrates
(Lainson, 2005). The genus Cyclospora was rst characterised and
namedby Schneider (1881), who recognisedandidentiedC. glom-
ericola in millipedes. This appears to be the only species found
in invertebrates. Subsequently, C. caryolytica was named and its
life cycle was described (Schaudinn, 1902). Since this time, several
Cyclospora species have been described in reptiles, mostly snakes,
insectivores, rodents and primates, including humans. There are
currently 19 recognised species (Lainson, 2005).
Cyclospora was rst identied as a human pathogen in three
patients from Papua, New Guinea but it was thought to be a
coccidium, probably a new species of Isospora (Ashford, 1979).
Subsequently, several reports on similar ndings in patients with
diarrhoea, mostly travellers to endemic areas and AIDS patients,
were published (Soave et al., 1986; Hart et al., 1990; Long et
al., 1990; Shlim et al., 1991; Wurtz et al., 1993). The term
cyanobacterium-like bodies was proposed for the organism
because of an ultrastructural resemblance to unicellular members
of theblue-greenalgae(Longet al., 1991). Later, thecoccidial nature
of this organism was pointed out (Bendall et al., 1993). Subse-
quently, the parasite was described from human faecal material
in Peru and was identied as a coccidian of the genus Cyclospora
because when the oocysts were induced to sporulate, they yielded
two sporocysts, each containing two sporozoites. The parasite was
namedC. cayetanensis (Ortegaet al., 1993, 1994). This species differs
signicantlyfromall other Cyclosporaspecies not onlyinits host but
also in its oocyst stage, which is much smaller and spherical rather
than oblong. The recovery from non-human primates of C. cerco-
pitheci, C. colobi and C. papionis that produce also small, spherical
oocyts seems tosuggest twodifferent groupings: species that infect
insectivores and rodents and produce large, oblong oocysts and
those that infect primates, including humans, and produce small,
spherical oocysts (Eberhard et al., 1999a).
1.2. Human cyclosporiasis
Cyclospora cayetanensis is an important emerging cause of diar-
rhoea worldwide that leads to signicant morbidity and mortality.
In immunocompetent hosts, mild-to-moderate, self-limiting diar-
rhoea is common. In immunocompromised hosts, severe intestinal
injury and prolonged diarrhoea is observed (Shields and Olson,
2003). In developed countries, the disease has been associated
with cases of travellers diarrhoea; the parasite is commonly iso-
lated fromtravellers to Latin America, the Indian subcontinent and
Southeast Asia (Long et al., 1990; Shlim et al., 1991; Clarke and
McIntyre, 1996; Drenaggi et al., 1998; Manseld and Gajadhar,
2004; Boure et al., 2006; Puente et al., 2006; Ramrez-Olivencia
et al., 2008). However, the coccidium has only been documented
as a signicant human pathogen in the early 1990s when it was
recognised as the causative agent of numerous outbreaks of diar-
rhoeal illness in the developed world, mostly associated with fresh
foodproduce, suchas soft fruits andleafyvegetables importedfrom
the developing world (Chambers et al., 1996; Anonymous, 1997;
Herwaldt and Ackers, 1997; Herwaldt and Beach, 1999; Herwaldt,
2000; Dawson, 2005). Waterborne disease has also been identied
(Huang et al., 1995; Dawson, 2005; Karanis et al., 2007). Unlike the
United States and Canada, most cases of cyclosporiasis in Europe
andAustralia have beenlinkedwithinternational travel inendemic
areas (Shlimet al., 1991; Clarke and McIntyre, 1996; Drenaggi et al.,
1998; Manseld and Gajadhar, 2004; Puente et al., 2006; Boure et
al., 2006, 2007). Exposure to contaminated drinking or recreational
water or to sewage have been involved in the spread of the infec-
tion to a lesser extent (Wurtz et al., 1993; Hale et al., 1994; Ooi et
al., 1995; Dawson, 2005).
Indevelopednations, the risk factors andmodes of transmission
for the cases of cyclosporiasis that have been identied and studied
are well dened. Most of the cases have been related to interna-
tional travel or tofoodborneoutbreaks causedbyimportedproduce
from endemic regions (Herwaldt and Ackers, 1997; Herwaldt and
Beach, 1999; Herwaldt, 2000; Gascon et al., 2001; Manseld and
Gajadhar, 2004; Dawson, 2005; Puente et al., 2006; Boure et al.,
2006, 2007). In contrast, the risk factors and routes of spread and
other epidemiologic features for C. cayetanensis in developing areas
remain poorly understood.
1.3. Aim of this review
This paper reviews the current status of knowledge of the
epidemiology of human cyclosporiasis, focusing in developing
countries andemphasisingfeatures of theparasitethat areessential
to understanding the surveillance and risk factors for the infection,
in order to institute appropriate risk management, control systems
andpreventionof transmission. Areviewof thepathogenic, clinical,
diagnostic and therapeutic features of the infection is not provided.
There are several major reviews that have described in detail these
aspects (Eberhard et al., 1997; Shields and Olson, 2003; Manseld
and Gajadhar, 2004).
2. Biology
Basic knowledge of the biologic features of C. cayetanensis is
crucial to understanding the complex epidemiology of human
infection as well as the difculty to develop successful control
strategies.
2.1. Current taxonomy and phylogeny
C. cayetanensis is taxonomically classied as follows: subphy-
lumApicomplexa, subclass Coccidiasina, order Eucoccidiorida, family
Eimeriidae (Sterling and Ortega, 1999; Shields and Olson, 2003).
Within the subphylum Apicomplexa there are several related gen-
era referred to collectively as coccidia including ve that have been
described from humans: Sarcocystis, Toxoplasma, Isospora, Cryp-
tosporidium and Cyclospora (Ortega et al., 1994).
Relatively little is known regarding the genome organisation
or gene sequences of C. cayetanensis. However, the small-subunit
rRNA (SSU-rRNA) sequence was obtained by PCR amplication
using primers based on the highly conserved regions of the SSU-
rRNA (Adam et al., 2000). Analysis of this sequence revealed that
C. cayetanensis is closely related to Eimeria spp. and supports the
conclusion that both genera belong to the same family of coccid-
ian parasites (Relman et al., 1996). The inclusion of an additional
SSU-rRNA sequence of E. falciformis, a parasite of mice, in the phy-
logenetic tree claried the resolutionof the tree into three different
L. Chacn-Bonilla / Acta Tropica 115 (2010) 181193 183
clades: mammalian Eimeria, avian Eimeria and Cyclospora. With the
addition of molecular data of more species, particularly the species
of Cylospora described from mammals other than primates, it may
be reasonably to consider reclassifying the Cyclospora of primates,
including humans, and either the bird or mammalian Eimeria to
a new genus (Eberhard et al., 1999a). It has been suggested that
SSU-rRNA sequences of Isospora should be compared with those
of Cyclospora to help clarify taxonomic issues (Sterling and Ortega,
1999). C. cayetanensis and the recognised Cyclospora spp. infecting
lower primates (C. cercopitheci, C. papionis, and C. colobi) group as a
single branch intermediate between mammalian and avian Eime-
ria (Eberhard et al., 1999a). It is not yet known whether all human
Cyclospora isolates belong to the same species and whether the
closely related Cyclospora species described from lower primates
infect humans.
2.2. Life cycle
C. cayetanensis is an obligate intracellular parasite with a life
cycle not fully characterised. It appears to be monoxenous, requir-
ing a single human host to complete the entire life cycle, since both
asexual and sexual stages have been observed in this host (Sun et
al., 1996; Ortega et al., 1997a; Connor et al., 1999). The life cycle is
complex and follows the patterns described for other enteric coc-
cidia, which involves a merogonic cycle with two generations of
meronts, a gametogonic cycle with macro- and microgametes and
zygotes, and a sporogony (Schaudinn, 1902).
The life cycle begins upon the ingestion of the transmissible
stage, the sporulated oocyst, which excysts in the gut releas-
ing infective sporozoites. These invade the epithelial cells of the
small intestine (Sun et al., 1996; Ortega et al., 1997a). The sporo-
zoites and subsequent stages are located within the cytoplasm in
a supranuclear position and are surrounded by parasitophorous
vacuoles (Sun et al., 1996). The sporozoites transform into tropho-
zoites which undergo asexual proliferation by merogony to form
meronts which contain merozoites. Two types of meronts develop.
Type I meronts contain 812 merozoites which penetrate host cells
and form type II meronts containing four merozoites. Once lib-
erated, these merozoites enter host cells and start sexual phase
by differentiating into either male (microgametocyte) or female
(macrogametocite) stages. The former forms numerous agellated
microgametes. The fertilised macrogametocite develops into a
zygote. A resistant wall is then formed around the zygote and
develops into an oocyst which contains the sporont (Tran Van
Nhieu et al., 1996; Ortega et al., 1997a; Connor et al., 1999). Even-
tually, the unsporulated oocysts are passed in the stool and the
sporont divides into two sporocysts, each containing two sporo-
zoites (Ortega et al., 1994). The environmental conditions for
sporulationare not yet fully understood. Oocysts require a fewdays
to weeks, depending on climatic factors, to mature in the environ-
ment into the infective sporulated oocysts (Ortega et al., 1998).
Under experimental conditions, sporulation has been carried out
using 2.5% potassium dichromate (Ortega et al., 1993) and occurs
in 713 days at temperatures between 22 and 32
C within 14 days
(Ortega et al., 1998).
2.3. Structure and survival of the infective stage
Oocysts are small and spheroidal in shape with a diameter of
7.79.9m. With the modied acid-fast stain, some oocysts are
open and others not opened to the stain. Some stain dark red and
have variable number of dark inclusion bodies, whereas others do
not stain at all and appear as transparent spheres. Under epiuo-
rescence illumination, they have the ability to autouoresce blue
or green under a 365nm or a 490nm dichromatic lter (Ortega et
al., 1993; Sterling and Ortega, 1999). From transmission electron
microscopy studies, a sporulated oocyst is described as possessing
a two-layered oocyst wall (63 and 50nm thick, respectively) sur-
roundingtwosporocysts, eachwith62-nm-thickwalls surrounding
a plasma membrane. Sporocyst has Stieda and substieda bodies
and a residuum with spherical globules. Each sporocyst has two
sporozoites (Ortega et al., 1993, 1994).
Coccidia oocysts can persist for long periods of time in the
environment, maintaining their infectivity even under harsh envi-
ronmental conditions (Manseld and Gajadhar, 2004; Sinski and
Behnke, 2004). Naturally occurring Cyclospora oocysts may survive
for extendedperiods inthe environment, giventhe markedseason-
ality of infection in endemic regions (Herwaldt and Beach, 1999).
Cyclospora oocysts survive inwater at 4
Cfor 2 months and at 37
C
for 7 days (Smith et al., 1997; Ortega et al., 1998). Oocysts cannot
be induced to sporulate after freezing at 18
C for 24h and after

heating at 60
C for 1h (Sterling and Ortega, 1999). They are resis-

tant to many disinfectants, including chlorination at levels used
in water treatment (Rabold et al., 1994; Soave et al., 1998), but
they are very sensitive to desiccation; oocyst wall ruptures after
15min (Long et al., 1991). The oocysts require time, moisture and
moderate temperature to become infective. It has been established
that water facilitates both the development and transmission of
coccidian oocysts (Manseld and Gajadhar, 2004).
Eimeria acervulina, a chicken coccidium with similarities to
Cyclospora, has been used as a surrogate to develop decontami-
nation treatments for fruits imported from endemic areas for C.
cayetanensis. Freezing and heat treatment and gamma irradiation,
at a dose of 1.0 kGy or higher, were effective against the coccidium
(Lee and Lee, 2001). Sporulation of C. cayetanensis oocysts, as an
indicator of viability, has been determined on produce. Unsporu-
lated oocysts were subjected to freezing and heating conditions
in dairy and basil substrates and then placed in 2.5% potassium
dichromate. Sporulation occurred when oocysts resuspended in
dairy substrates were stored at 15
C within 24h and when they

were placed in water or basil at 20
C for up to two days and at 37
C
for up to 4 days. Few oocysts sporulated at 50
C for 1h. Sporula-

tion did not occur at 70, 70, and 100
C in water or basil leaves

(Sathyanarayanan and Ortega, 2006). High-hydrostatic-pressure
processing and UV light radiation have been suggested to reduce
the risk of cyclosporiasis associated with produce (Kniel et al.,
2007). C cayetanensis sporulation was not affected after microwave
heating for up to 45s (Ortega and Liao, 2006) and after the use of
gaseous chlorine dioxide at 4.1mg/l for 20min (Ortega et al., 2008).
2.4. Infectivity
The actual infectious dose of Cyclospora oocysts is unknown but
based on data from outbreak studies and extrapolations to other
coccidia, it is generally thought to be relatively low (Sterling and
Ortega, 1999; Dixon et al., 2005), probably between 10 and 100
oocysts (Adam and Ortega, 1999). Factors that allow C. cayeta-
nensis oocysts become infectious in the environment are not fully
understood. Researchers have been unable to establish the para-
site in a wide variety of animal models (Eberhard et al., 2000) and
humans (Alfano-Sobsey et al., 2004). Host susceptibility, risk fac-
tors and virulence are factors that inuence the host response to
a pathogen exposure. Virulence and features of the coccidium to
infect human hosts are unknown. Nucleotide sequence variability
intherst internal transcribedspacer regions withinC. cayetanensis
fromdifferent geographic areas has beenobservedandsuggests the
existence of multiple strains (Adamet al., 2000; Olivier et al., 2001);
it is possible that many human Cyclospora infections are charac-
terised by multiclonality of the infecting coccidia. The triggers and
conditions necessary for Cyclospora oocysts to become infectious in
the environment are not fully understood.
Table 1
Biologic and epidemiologic features of Cyclospora cayetanensis that are relevant to
its epidemiology.
Feature Epidemiologic signicance
Relative small size Difcult to lter
Resistent, chlorine oocysts Spread in chlorinated water or
swimming pools
Likely, low infective dose Easily acquired
Probably, humans are the
only host
Likely, lack of zoonotic
potential
Oocysts shed in
non-infective form
Person-to-person transmission
is highly unlikely
Oocysts need external
maturation
A vehicle of transmission is
needed
Marked seasonality Oocysts survive for long
periods in the environment
Environmental dispersal
can contaminate water,
food and soil
Widely spread with
water-food-soilborne
transmission
2.5. Environmental occurrence of oocysts and transfer
Little information is available on C. cayetanensis in the environ-
ment and in animal population. The parasite has been detected on
fresh vegetables from markets in Peru (Ortega et al., 1997b) and
Costa Rica (Calvo et al., 2004), and from farms in Nepal (Sherchand
and Cross, 2001). The relationship between numbers of organisms
found on fresh produce and numbers in the environments in which
crops were grown is unclear (Dawson, 2005). In Egypt, the coccid-
ium was identied in bivalves from markets in Alexandria (Negm,
2003). C. cayetanensis was describedindrinkingwater inGuatemala
(Dowd et al., 2003) and Nepal (Rabold et al., 1994). In Vietnam, the
parasite was identied in drinking water and in 63.6% of rivers and
lakes samples (Miegeville et al., 2003). In Egypt, the coccidiumwas
isolated in ve residential areas from several water sources used
for consumption, such as a drain, an irrigation canal, underground
water and piped water, reecting the high environmental contam-
ination of the area (El-Karamany et al., 2005). In other study, the
parasite was observed in 0.24% of 840 potable water samples from
sevendistricts (Elshazlyet al., 2007). InPer, (Sturbaumet al., 1998)
and Nepal (Sherchand and Cross, 2001), Cyclospora oocysts were
detected in sewage water. Since there is little or no monitoring for
Cyclospora in the environment, it is unknown whether the parasite
is widespread.
Critical to the epidemiology and transmission of C. cayetanensis
are some biologic and epidemiologic features that determine the
medical and public health importance of this coccidium. These are
presented in Table 1 and discussed below.
3. Epidemiology
3.1. Distribution of human cyclosporiasis
As a result of the increased awareness of infection and
the development of diagnostic screening techniques, widespread
investigation of the frequency of cyclosporiasis has ensued
throughout the world. C. cayetanensis infection has been described
worldwide, in developed and developing countries and in urban
and rural areas (Ortega et al., 1998; Shields and Olson, 2003).
However, prevalence rates of Cyclospora are often underestimated
Table 2
Prevalence of Cyclospora cayetanensis, in immunocompetent individuals from developing countries
a
.
Country Population Infected % (no./no. tested) Controls % (no./no. tested) References
Mexico Children 3.3 (18/541) NR
b
Bernal Redondo et al. (1998)
Guatemala All ages 2.3 (126/5552) NR Bern et al. (1999)
Honduras All ages 2.0 (96/4698) NR Kaminsky (2002)
Brazil Adults 0.3 (14/4869) NR Do Nascimento et al. (2005)
Peru All ages 0.7 (2/272) NR Rodriguez-Alarcn et al. (2007)
All ages 7.8 (7/90) 0 (0/50) Zerpa et al. (1995)
All ages 7.3 (217/2968) NR Burstein Alva (2005)
Children 13.0 (64/489) NR Cordova et al. (2006)
Venezuela Children 5.3 (7/132) NR Chacn-Bonilla et al. (2001)
Cuba 07 yr 4.4 (5/113) 0 (0/288) Nu nez et al. (2003)
Children 0.2 (20/7956) NR Martnez Silva et al. (2002)
Turkey All ages 0.5 (23/4660) 0 (0/326) Turgay et al. (2007)
All ages 0.4 (2/554) NR Aksoy and Tuncay (2007)
Jordan All ages 6.0 (12/200) NR Nimri (2003)
Saudi Arabia <5 yr 11.1 (7/63) 4.2 (8/190) Al-Braiken et al. (2003)
China All ages 5.6 (10/178) 0.2 (1/400) Wang et al. (2002)
Nepal 5 yr 5.0 (6/124) 2.0 (2/103) Hoge et al. (1995)
Children 1.0 (18/1790) NR Easow et al. (2005)
All ages 9.2 (128/1397) NR Kimura et al. (2005)
Bangladesh 5 yr 0 (0/814) 0 (0/814) Albert et al. (1999)
25 yr 0 (0/289) NR Haque et al. (2003)
Lao PDR All ages 0.1 (1/686) NR Kimura et al. (2005)
Thailand <5 yr 0 (0/1230) 0 (0/1230) Echeverra et al. (1989)
<5 yr 1.3 (3/236) 2.1 (5/236) Wongstitwilairoong et al. (2007)
Indonesia School children 0.6 (2/348) NR Fryauff et al. (1999)
Egypt Children 9.0 (7/80) NR Nassef et al. (1998)
Adults 10.0 (5/50) NR
Nigeria All ages 1.0 (11/1109) NR Alakpa et al. (2003)
Uganda <5 yr 0.1 (1/650) NR Tumwine et al. (2003)
Kenya <5 yr 0 (0/4899) NR Gatei et al. (2006)
Tanzania Children 0 (0/76) NR Cegielski et al. (1999)
Mozambique <5 yr 0 (0/529) NR Mandomando et al. (2007)
a
Based on conventional faecal examination.
b
Not reported.
Table 3
Prevalence of Cyclospora cayetanensis in immunocompromised individuals from developing countries
a
.
Country Population Infected % (no./no. tested) Controls % (no./no. tested) References
Guatemala Malnourished children 0.9 (1/111) NR
b
Pratdesaba et al. (2001)
HIV/AIDS patients 3.8 (6/157) NR Pratdesaba et al. (2001)
Honduras HIV patients 6.8 (9/133) NR Kaminsky (1997)
AIDS patients 3.6 (2/56) NR Kaminsky et al. (2007)
Colombia 1063 yr 2.6 (1/38) NR Arzuza et al. (2003)
Venezuela AIDS adults 9.8 (7/71) NR Chacn-Bonilla et al. (2001)
HIV adults 6.8 (5/74) 3.4 (1/29) Chacn-Bonilla et al. (2006)
Brazil Immunocompromised patients 1.0 (5/393) NR De Souza and Garca Zapata (2006)
Cuba AIDS adults 3.0 (2/67) 0 (0/136) Escobedo and Nu nez (1999)
HIV adults 3.5 (6/170) NR Capo de Paz et al. (2003)
Haiti HIV adults 11.3 (51/450) NR Pape et al. (1994)
AIDS adults 36.0 (27/74)
c
NR Raccurt et al. (2008)
China Immunocompromised patients 9.4 (3/32) 0.2 (1/400) Wang et al. (2002)
India HIV adults 1.0 (1/100) 0 (0/50) Kumar et al. (2002)
HIV adults 0 (0/298) NR Becker et al. (2007)
HIV adults 2.9 (1/113) 0 (0/113) Gupta et al. (2008)
Thailand AIDS adults 2.2 (1/45) NR Manatsathit et al. (1996)
Indonesia HIV/AIDS adults 4.4 (14/318) NR Kurniawan et al. (2009)
Egypt Immunocompromised patients 4.0 (6/150) NR Abou el Naga (1999)
Malnourished children 5.6 (2/36) 2.8 (1/36) Rizk and Soliman (2001)
Cameroon HIV adults 0 (0/154) NR Sarfati et al. (2006)
Kenya HIV adults 0 (0/88) NR Gatei et al. (2006)
Tanzania AIDS patients 1.2 (1/86) NR Cegielski et al. (1999)
HIV children 2.6 (1/38) 0 (0/20) Cegielski et al. (1999)
Zimbabwe HIV adults 0 (0/88) NR Gumbo et al. (1999)
a
b
Not reported.
c
PCR method.
because of the low sensitivity of conventional detection methods,
thefact that theparasitemaybepresent at subclinical levels andthe
intermittent nature of oocysts shedding. Surveys have had several
limitations. Theyhavedependedonevaluationof singlefaecal spec-
imens by techniques that might have missed light infections and
are subjected to variable levels of technical expertise. Most of the
studies have been based on selective populations, such as patients
with gastrointestinal symptoms or diarrhoea who are hospitalised
or seek medical attention or simply on faecal samples submitted
to diagnostic laboratories. The resulting survey data may be biased
toward children since medical intervention is more likely to result
from gastrointestinal symptoms appearing in younger patients.
Despitetheselimitations, surveys providevaluabledataconcerning
the ubiquitous nature of infection in various populations world-
wide, and may detect changing trends and signal the probability of
an epidemic.
3.2. Geographic distribution and prevalence
From a review of 47,642 apparently immunocompetent indi-
viduals from endemic areas attending health care centres, most of
them with diarrhoea, infection rates ranged from 0 to 13% (aver-
age 1.7%), whereas the isolation rates frommatched asymptomatic
controls varied from0 to 4.2% (average 0.4%) (Table 2). The surveys
suggest that C. cayetanensis is associated with diarrhoea. Among
3340 immunocompromised persons, mostly HIV/AIDS patients
with diarrhoea, the percentages of Cyclospora infections presented
estimates that differ from one another, ranging from 0 to 36%
(average 4.5%) (Table 3). Variations in prevalence of Cyclospora
infections may be inuenced by study design, geographic area, age
and immunologic status of the population studied, seasonal vari-
ability of the parasite, methods of detection used, and expertise of
the microscopist. It is interesting to note the scarcity of Cyclospora
reports in African populations. In immunocompetent individuals,
with the exception of one study (Nassef et al., 1998), very low
infection rates of 1% have been observed (Table 2). In immuno-
compromisedpersons, prevalences of 05.6%have beenfoundwith
an average percentage of 1.6% (10/640) (Table 3). It has been pos-
tulated that the amount of sulpha drugs administered as drugs of
choice for malaria and other infectious diseases may suppress the
parasite (Eberhard and Arrowood, 2002).
In community based studies, prevalence rates from 0 to 41.6%
(average 4.2%) have been found (Table 4). Whether the high infec-
tion rate (41.6%) observed in a Peruvian community reects an
endemic high risk of exposure to the parasite by the popula-
tion of the area or an epidemic is not known. High percentages
of asymptomatic carriers (68.298.7%, average 87.1%) have been
noted. Infected children are often asymptomatic or have relatively
mild illness (Madico et al., 1997; Ortega et al., 1997a; Eberhard
et al., 1999b; Chacn-Bonilla et al., 2003, 2007). Thus, in endemic
settings, C. cayetanensis may not play a consistently pathogenic
role. It appears that in endemic areas, the situation at the gen-
eral population level is quite different than that observed in health
centre populations in whom a strong association of the parasite
with diarrhoea has been recognised (Zerpa et al., 1995; Fryauff et
al., 1999; Al-Braiken et al., 2003; Nu nez et al., 2003; Manseld
and Gajadhar, 2004). This nding suggests that cyclosporiasis is
common in impoverished areas and that very early and persistent
exposure may be associated with immunity to illness and asymp-
tomatic excretion (Madico et al., 1997; Ortega et al., 1997a; Bern et
al., 2002). In fact, after an initial episode of cyclosporiasis, the like-
lihood of diarrhoea decreases signicantly with each subsequent
infection (Bern et al., 2002).
The prevalence of C. cayetanensis is unknown in some develop-
ing countries. However, the reports of sporadic cases of infection
in local residents or foreign visitors reect the endemicity of infec-
tion in these nations. Such is the case of Costa Rica (Chinchilla et al.,
1999; Cede no, 2002), Argentina (Velasquez et al., 2004), Dominican
Table 4
Prevalence of Cyclospora cayetanensis in communities from developing countries
a
.
Country Population Infected % (no./no. tested) Asymptomatic % (no./no. tested) References
Mexico Children 3.3 (9/272) NR
b
Daz et al. (2003)
Guatemala Raspberry farm workers and family members 3.3 (6/182) NR Bern et al. (1999)
Raspberry farm workers 0 (0/206) NR Pratdesaba et al. (2001)
Venezuela All ages 6.1 (13/212) 84.6 (11/13) Chacn-Bonilla et al. (2003)
All ages (Indians) 11.9 (19/160) 98.7 (158/160) Devera et al. (2005)
All ages 8.3 (43/515) 86.0 (37/43) Chacn-Bonilla et al. (2007)
Peru 02.6 yr 10.9(41/377) 73.2 (30/41) Ortega et al. (1993)
Children 1.1 (63/5836) 68.2 (43/63) Madico et al. (1997)
All ages 41.6 (121/291) NR Burstein Alva (2005)
Children 2.6 (22/845) NR Perez Cordn et al. (2008)
Adults 4.3 (11/256) NR Roldan et al. (2009)
Brazil All ages (Indians) 10.8 (9/83) NR Das Borges et al. (2009)
Haiti Children and mothers 7.9 (59/741) 86.8 (46/53) Eberhard et al. (1999b)
All ages 6 (24/402) NR Lpez et al., 2003
a
b
Not reported.
Republic (Green et al., 2000; Estran et al., 2004), Bangladesh (Albert
et al., 1994), Vietnam (Naito et al., 2009), New Guinea (Ashford,
1979), Morocco (Kansouzidouet al., 2004) and Madagascar (Boure
et al., 2007). In Chile (Madrid et al., 1998) and Uruguay (Salvatella
et al., 2000), one case was reported from each country. However,
the patients presented cyclosporiasis after visiting Cuba or Peru,
respectively, that are endemic areas.
Occurrence of C. cayetanensis outbreaks has mostly been
reported in the developed world (Herwaldt and Beach, 1999;
Herwaldt, 2000; Ho et al., 2002; Doller et al., 2002; Hoang et
al., 2005). Whereas their occurrence in endemic settings are lim-
ited (Table 5). Only, 11 outbreaks appear to have been published
with detection of infection in 10.386% of diarrhoeal cases. Six
of them have involved foreign residents or visitors. This may be
explained by the protective immunity induced by repeated expo-
sure of natives from endemic regions to the parasite (Madico et
al., 1997; Ortega et al., 1997a; Bern et al., 2002). However, it has
been demonstrated recently that outbreaks of cyclosporiasis do
occur in the developing world among local populations. At least
ve have been published from Mexico, Brazil, Colombia and Peru
(Table 5). Other three from Brazil have been reported in ofcial
records (Do Nascimento et al., 2005). The explanation for these epi-
demics inlocal adult populations is that acquiredimmunityinthese
areas is not long lasting and fades over time (Torres-Slimming et
al., 2006) or that geographic distribution, prevalence and spread
of the parasite in one region may vary from one place to another
leaving some populations unprotected, particularly those fromthe
upper social class (Mundaca et al., 2008). Other factors that could
explainthe limitedoutbreaks of cyclosporiasis reportedinendemic
areas are the indiscriminate use of antibiotics effective against C.
cayetanensis and the lack of adequate diagnostic capability (Torres-
Slimming et al., 2006). Greater awareness of the parasite in these
areas and increased familiarity with the disease it causes, along
with improved surveillance programmes for Cyclospora, increase
the probability that future outbreaks will be detected.
3.3. Age and sex distribution
In developing countries, risk categories for cyclosporiasis
include immunocompromised patients, foreigners and children.
It is well known that the infection causes signicant morbidity
and mortality in immunodepressed individuals, in particular those
with HIV infection. The risk of faecal carriage and severity of ill-
ness are related to the state of immunosuppression of the patients.
Among expatriates, the disease is common (Clarke and McIntyre,
1996; Drenaggi et al., 1998; Shields and Olson, 2003; Puente et al.,
2006; Boure et al., 2006, 2007) and outbreaks have been reported
(Table 5).
Cyclosporiasis has been found to be common in children. Most
of the studies on prevalence of the infection and association with
disease have been conducted in children that have attended clin-
ics, hospitals or laboratories and have been skewed towards those
with clinical manifestations. The highest risk of infection and diar-
rhoea occur in the rst ve years of life (Hoge et al., 1995; Madico
et al., 1997; Ortega et al., 1998; Chacn-Bonilla et al., 2001; Bern et
al., 2002). In children less than 18 months of age, Cyclospora infec-
Table 5
Outbreaks of cyclosporiasis in developing countries
a
.
Country Year Population Disease cases Infected % (no.) Probable source of exposure References
Nepal 1989 Foreigners 535 10.3 (55) UK
b
Shlim et al. (1991)
1989 Foreigners 14 86.0 (12) Drinking water Rabold et al. (1994)
1992 Foreigners 964 11.2 (108) Drinking water Hoge et al. (1993)
Indonesia 19951998 Foreigners 558 11.8 (66) Fruits, vegetables Fryauff et al. (1999)
2001 Foreigners 29 48.3 (14)
c
UK Blans et al. (2005)
Mexico 2001 Party attendees 92 78.5 (55/70) Watercress Ayala-Gaytn et al. (2004)
Brazil 19992002 Laboratory attendees 132 12.1 (16) UK Zini et al. (2004)
Colombia 2002 University employees 56 55.4 (31) Salads, juices Botero-Garces et al. (2006)
Guatemala 2003 Foreigners 11 63.6 (7) Raspberry juice Puente et al. (2006)
Peru 2004 Recruits 77 31.2 (24) Vegetables sauces Torres-Slimming et al. (2006)
2005 Recruits 35 57.1 (20)
c
Food, water Mundaca et al. (2008)
a
b
Unknown.
c
PCR method.
tions were undetected in Nepal (Hoge et al., 1995), uncommon in
Guatemala (Bern et al., 1999) and Venezuela (Chacn-Bonilla et al.,
2001) and present but asymptomatic in Peru (Ortega et al., 1993).
It is not known if it is due to weaning maternal antibodies or to
limited environmental exposure in this age group.
The community based studies of Cyclospora age distribution are
scarce. In a 2-year cross sectional study in Peru, the prevalence of
the coccidiumwas highest among children aged 24 years (Madico
et al., 1997). In this study and other fromthe same region (Ortega et
al., 1998), the infection was not detected among persons older than
11years. Inseveral studies fromGuatemala (Bernet al., 1999), Hon-
duras (Kaminsky, 2002), Hait (Lpez et al., 2003), Cuba (Nu nez et
al., 2003), Venezuela (Chacn-Bonilla et al., 2007), Nepal (Kimura et
al., 2005) and Turkey (Turgay et al., 2007) the infection was more
frequent in school children <10 years of age. The causes for this
age distribution pattern are not clear but may be related to pre-
dominant modes of exposure. C. cayetanensis is usually transmitted
by exposure to contaminated environmental sources from which
young children are relatively protected (Bern et al., 2002). Signi-
cant differences of Cyclospora infection rate by sex have not been
reported.
3.4. Seasonal distribution
In addition to geographic variability, a marked seasonality of
the prevalence of Cyclospora infection has been described in sev-
eral endemic countries. However, it is not uniformamong different
regions and dees easy explanation (Herwaldt, 2000). The sea-
sonal trenddescribedinvarious nations oftencoincidewithperiods
of maximal rainfall. In Guatemala (Bern et al., 1999), Honduras
(Kaminsky, 2002), Jordan (Nimri, 2003), Nepal (Hoge et al., 1993,
1995; Sherchand and Cross, 2001; Kimura et al., 2005) and Indone-
sia (Fryauff et al., 1999), the prevalence of Cyclospora markedly
increases during the warm and rainy season. In USA and Canada,
nearly all the cases of foodborne outbreaks, which has been mostly
related to Guatemalanraspberries, have occurred during the spring
and early summer, a warm and rainy season (Herwaldt, 2000;
Shields and Olson, 2003). In contrast, infection has been reported
more prevalent in seasons of less rainfall in Haiti (Eberhard et al.,
1999b) and Peru (Ortega et al., 1993; Bern et al., 2002), during the
cooler anddrier months of the year. Inthese countries, temperature
uctuations appear to be the moderator of the infection seasonal-
ity (Eberhard et al., 1999b). However, in Turkey, the prevalence
of cyclosporiasis has been noted during the hot and dry weather
(Turgay et al., 2007). The seasonal variation of C. cayetanensis sug-
gests that environmental factors are important in the life cycle of
this parasite.
3.5. Reservoirs
The role of animals as natural reservoirs of C. cayetanensis is
uncertain but of increasing concern.
Effort toestablishthe coccidiuminanimal models toculture it in
vitrohavebeenunsuccessful andatrueanimal reservoir host for the
parasite in the environment has not yet been conrmed (Eberhard
et al., 2000). These ndings suggest the strict host specicity of the
parasite and that humans are the only natural host for C. cayetanen-
sis. However, oocysts resembling those of C. cayetanensis have been
described in several animals, including chickens, ducks, mice, rats,
dogs and primates (Zerpa et al., 1995; Garca-Lpez et al., 1996;
Smith et al., 1996; Yai et al., 1997; Lpez et al., 1999; Eberhard et
al., 2001; Sherchand and Cross, 2001). Identication of the coccid-
ium has been based on conventional microscopic techniques and
the reports are controversial. Thus, the ndings of the presence of
C. cayetanensis in animals have been met with uncertainty.
Oocysts considered to be those of C. cayetanensis were observed
in a duck from Peru (Zerpa et al., 1995), in the pooled faeces of
some 600 young chicken from poultry farms and in pooled caecal
contents from another 50 from a market of Mexico (Garca-Lpez
et al., 1996) and in two chickens of 196 domestic animals in Nepal
(Sherchandet al., 1999). InGuatemala (Bernet al., 1999), Peru(Bern
et al., 2002), Jordan (Nimri, 2003), Nepal (Sherchand and Cross,
2001) and Egypt (El-Karamany et al., 2005), domestic animals were
signicant risk factors for infection. In contrast to these ndings,
the parasite was not detected in Haiti from 327 domestic animals,
including pigeons, chickens, ducks, turkeys, guinea pigs, cats, dogs,
goats, pigs, horses, and cattle (Eberhard et al., 1999c). In Brazil,
Cyclospora-like oocysts were noted in two dogs (Yai et al., 1997).
However, in the same area, these oocysts were not identied in
140 stray dogs (Carollo et al., 2001).
Cyclospora-likeoocysts werefoundinbaboons andchimpanzees
(Smith et al., 1996) and non-human-primates (Eberhard et al.,
2001) suggesting the existence of another host and reservoir for C.
cayetanensis. However, a subsequent study pointed out that these
isolates were three different species of Cyclospora (Eberhard et al.,
1999a). Recently, the presence of C. cayetanensis was demonstrated
by PCR in one chicken, two dogs and one monkey (Chu et al., 2004).
Whether this nding represents either the shedding of ingested
oocysts through the gastrointestinal tract or a natural infection in
an animal host other than humans needs to be determined.
3.6. Sources and routes of transmission
Direct person-to-persontransmissionof C. cayetanensis is highly
unlikely because of the period needed by the oocysts outside the
host to sporulate and become infectious (Manseld and Gajadhar,
2004). Thus, a transmission vehicle must be involved. Cyclospora
oocysts can be transmitted in humans through exposure to faecally
contaminated environmental water, food or soil. In areas where
environmental sanitation may be compromised, such as disadvan-
taged community settings, the frequency of transmission may be
high.
The biologic and epidemiologic features of C. cayetanensis that
encourage transmission to humans might produce an interplay
between the different routes of spread but the relative rates of
the various modes of transmission are unknown. In developing
countries, few studies have been conducted to address the routes
of spread of infection. However, multiple routes of transmission
almost certainly exist in these areas.
3.6.1. Waterborne transmission
Waterborne oocysts are a common source of infection, but
denitive documentation is lacking (Manseld and Gajadhar,
2004). In a case-control study from Guatemala, several variables
related to water were associated with risk for Cyclospora infec-
tion. Drinking of untreatedwater, water source, swimming inrivers
or springs were all found to signicantly increase risk of infection
(Bern et al., 1999). In rural areas from this country, various water
sources used for public consumption were screened for C. cayeta-
nensis. Three of ve water samples allowed for amplication of
Cyclospora18S-rDNAwere conrmedtobe C. cayetanensis (Dowdet
al., 2003). In Peru, the parasite was associated with consumption of
unchlorinated water (Zerpa et al., 1995) and identied in wastewa-
ter (Sturbaum et al., 1998). In Haiti, the only factor associated with
infection was drinking water from an artesian well (Lpez et al.,
2003).
InAsia, Nepal, theinfectionwas associatedwithuntreatedwater
or milk mixed with water (Hoge et al., 1993). An outbreak among
foreignsoldiers was linkedwithdrinking water inwhichCyclospora
oocysts were detected. This water was a mixture of river and
municipal water that was chlorinated and ltered but the organ-
isms were not completely removed (Rabold et al., 1994). In other
study, drinking water and sewage water were identied as possible
sources of cyclosporiasis (Sherchand and Cross, 2001). In Vietnam,
Cyclospora oocysts were identied in drinking water, rivers and
lakes (Miegeville et al., 2003).
In Africa, a study designed to address the prevalence and risk
factors for infection in a village from Egypt showed that water
was an important source of infection. Cyclospora oocysts were
detected in several water sources suggesting water as the main
vehicle of transmission. The densities of water contamination by
the oocysts indicated sewage contamination (El-Karamany et al.,
2005). In Alexandria, the parasite was identied in different water
sources, including swimming pools (Youseff et al., 1998). Of partic-
ular recent concernis theidenticationof C. cayetanensis inbivalves
in this city (Negm, 2003). The roles of the marine ecosystem itself
and of freshwater run-off from land in the presence and mainte-
nance of this coccidium in marine hosts are unknown. However,
using the sea for recreation is a potential risk factor. In endemic
areas, at least three outbreaks have been related to drinking water
(Table 5).
These ndings all together suggest that C. cayetanensis has the
potential to be spread by drinking water, including chlorinated
water, recreational water, or via irrigation water with wastewater
in endemic areas. Contaminated water used for food crops that are
consumed raw may represent a route of infection. It is considered
that waterborne oocysts are likely to mediate food contamination,
but conclusive evidence is lacking (Manseld and Gajadhar, 2004).
In the developed world, several outbreaks of waterborne
Cyclospora disease have been documented, but large epidemics like
those caused by Cryptosporidium and Giardia have not occurred
(Dawson, 2005). Therst reportedoutbreakof cyclosporiasis inUSA
was inChicago, where 23 cases were linked to a hospital water sup-
ply (Huang et al., 1995). At least 325 water-associated outbreaks of
protozoandisease have beenreportedworldwide andC. cayetanen-
sis has been the causative agent in six (1.8%) (Karanis et al., 2007).
The presence of C. cayetanensis in aquatic ecosystems suggests the
importance of waterborne oocysts in the spread of infection.
3.6.2. Foodborne transmission
Inthe developing world, cyclosporiasis has beenassociatedwith
eating vegetables in Nepal (Sherchand and Cross, 2001) and Jordan
(Nimri, 2003). C. cayetanensis was identied in 1.8% of market veg-
etables samples from Peru (Ortega et al., 1997b), in lettuce from
agricultural markets in Costa Rica (Calvo et al., 2004) and from
green leafy vegetables in Nepal (Sherchand and Cross, 2001). In
Egypt, thecoccidiumwas isolatedfromlettuce(Abouel Naga, 1999)
and bivalves collected in markets fromAlexandria (Negm, 2003). In
a study of travellers to endemic areas, affected by diarrhoea, straw-
berries, buffalos milk and marinated sh were identied as risk
factors for infectioninvecases (Gasconet al., 2001). Thesendings
suggest that C. cayetanensis has the potential to be transmitted by
foods. Manyoutbreaks of foodbornediseasehavebeendocumented
worldwide. In developing countries, at least six epidemics have
been linked to fruits or vegetables in Mexico, Guatemala, Colombia,
Peru and Indonesia (Table 5).
Increasing globalisation of the fresh food supply and world
travel and a trend towards eating outside home have contributed
to the spread of C. cayetanensis from endemic to non-endemic
areas. In the developed world, several epidemics have occurred
which have been traced to fresh foods that are difcult to clean
thoroughly and are consumed without further processing that
can inactivate or remove the coccidium. The parasite has not
been shown to be an important problem for industrially manufac-
tured foods or those that are enough heated before consumption
(Dawson, 2005). C. cayetanensis has been responsible for numer-
ous high-prole epidemics of foodborne disease from Guatemalan
contaminatedraspberries inUSAandCanada(Herwaldt andAckers,
1997; Herwaldt and Beach, 1999; Herwaldt, 2000; Ho et al., 2002;
Shields and Olson, 2003; Dawson, 2005). Further outbreaks of
cyclosporiasis in USA, Canada and Europe were associated to the
consumption of basil, mesclun lettuce, eld greens and snowpeas;
the countries of origin of these products remain unclear (CDC,
1997a,b; Herwaldt, 2000; Brockmannet al., 2001; Lpezet al., 2001;
Doller et al., 2002; Anonymous, 2004; CDC, 2004; Hoang et al.,
2005). In USA, 90% of cases of cyclosporiasis has been food related
(Mead et al., 1999). Foodborne cyclosporiasis has been shown to
be a great concern in food production and a signicant problemfor
public health worldwide.
3.6.3. Soil transmission
In developing countries, contact with soil has been a risk fac-
tor for cyclosporiasis. Studies from Peru (Madico et al., 1997),
Guatemala (Bern et al., 1999) and Africa (El-Karamany et al., 2005)
showed this factor as an important source of infection among chil-
dren. In developed regions, this factor appears to play a role in
the spread of infection. A study of an outbreak of cyclosporiasis
in Florida, USA suggests that contact with soil may be a risk factor
(Koumans et al., 1998). In Germany, an outbreak was associated
to lettuce from farms in France and Italy. Likely, oocysts may have
been transmitted by workers fromendemic areas through local soil
or water contact (Doller et al., 2002).
Variables associated with low socioeconomic status could pre-
dispose persons to infection. In endemic countries, in areas where
indiscriminate human defaecation can contaminate soil, this could
be a mayor source of infection. In a study conducted to deter-
mine the prevalence and potential risk factors for cyclosporiasis in
a western island from Venezuela, multivariate logistic regression
model strongly implied risk factors that included living in areas of
extreme poverty (odds ratio (OR) =1.77, 95% CI 1.691.84), living
in huts or small residences (OR=10, 95% CI 6.8914.5), using an
area of the backyard for defaecation (OR=2.64, 95% CI 2.103.31)
and contact with soil contaminated with human faeces (OR=3.32,
95% CI 2.554.32) (Chacn-Bonilla et al., 2007). The main nd-
ing of this study was the strong correlation of stool positivity for
Cyclospora with environments conducive to human faecal contam-
ination (p<0.001), which suggests that contact with contaminated
soil is an important mode of transmission in this area. Indeed, this
factor was strongly linked to infection (p<0.01). The ndings indi-
cated an inverse relationship between socioeconomic status and
infection and showed that cyclosporiasis, as for other commu-
nicable infections, affects families living in substandard housing
developments. In Haiti, where the use of the water from an arte-
sian well was linked to infection, it was considered that one of the
causes for contamination of the well water might have been indis-
criminate defaecation since latrines were uncommon in the area
(Lpez et al., 2003). In China, in Anhui province, signicant higher
rates of infectionwere notedinrural areas, where decient sanitary
facilities and personal hygiene and frequent faeces contamination
of soils were present (Wang et al., 2002).
The reasons for a higher prevalence of infection in children <10
years of age (Bern et al., 1999, 2002; Kaminsky, 2002; Lpez et
al., 2003; Nu nez et al., 2003; Chacn-Bonilla et al., 2007; Turgay
et al., 2007) are not clear. It would appear that these children har-
bour signicantly higher infection rates due to other exposure and
behavioural subfactors stronglycorrelatedwithsocioeconomic sta-
tus rather thanagealone. Indevelopingareas, thedramatic increase
of populationdensityandthe massive rural tourbanmigrationover
the last decades has meant the rapid evolution of unplanned urban
centres with crowding, inadequate sanitation and garbal disposal
and poor health awareness. In these environments, contamination
of soils by inadequate defaecation practices might be signicant
determinants for infection, as was the case in the Venezuelan
study (Chacn-Bonilla et al., 2007). Since many persons defaecate
outdoors, in the backyard or in the vicinity of human dwellings
where children play, non-supervised children may be more prone
to defaecating in places that are already contaminated with faeces
and therefore be exposed to more frequent infection than adults.
Under these conditions, direct faecal-oral transmission without
passage into the water supply is possible. This situation highlights
the key role of unadequate sanitation as a risk factor for cyclospo-
riasis in low-income countries. In these areas, soilborne Cyclospora
might be an important route of transmission.
It has been hypothesised that contamination of Guatemalan
raspberries has been through the dilution of insecticides and fungi-
cides made withcontaminatedriver water or throughtransfer from
hands of pickers or handlers of crops (Sterling and Ortega, 1999;
Sathyanarayanan and Ortega, 2004). However, the exact route of
contamination remains a matter of speculation. C. cayetanensis can
contaminate crops through different pathways, via water contam-
inated by faeces that is used for irrigation or spraying of crops,
by contact with contaminated soil, or by infected food handlers
(Dawson, 2005) through unwashed hands after contact with con-
taminated soil. Thus, soilborne transmission might be one of the
routes of contamination of raspberry crops. Currently, C. cayeta-
nensis is considered a food- and waterborne parasite. However,
infections linked to contact with soil provide reasons to believe
that this route of spread could be a mayor source of infection in
areas of poor environmental sanitation and poverty a predisposing
factor. However, how frequent this mode of transmission occurs
and under what circumstances have yet to be determined.
3.6.4. Zoonotic transmission
The link between human and animal infections has been part of
the research effort on C. cayetanensis. The role that animals may
play in its epidemiology remains controversial and needs to be
resolved. C. cayetanensis appears to be the only species found in
humans and restricted to this host. However, contact with animals
has been pointed out as a risk factor for infection in Guatemala
(Bern et al., 1999), Peru (Bern et al., 2002), Jordan (Nimri, 2003),
Nepal (Sherchand and Cross, 2001) and Egypt (El-Karamany et al.,
2005) and oocysts resembling those of C. cayetanensis have been
reported in animals (Zerpa et al., 1995; Smith et al., 1996; Yai et al.,
1997; Sherchand et al., 1999; Eberhard et al., 2001; Sherchand and
Cross, 2001).
The recent nding of C. cayetanensis, conrmed by PCR, in two
dogs, one monkey and one avian (Chu et al., 2004) raises the ques-
tion if they are simple transport hosts or natural reservoir hosts.
Although this result is probably the most valuable result from
zoonotic perspective, currently there is not evidence of zoonotic
transmission of C. cayetanensis and the role of animals as natural
reservoir hosts remains to be determined.
3.6.5. Airborne transmission
Concernfor airborne spreadwas raisedwhenCyclospora oocysts
were identied in the sputum of two HIV negative adults from
Argentina and Egypt, both patients had cough with purulent spu-
tum, dyspnea and weight loss. One of them had a history of a
successfully treated TB (Di Gliullo et al., 2000); the other had an
active TB infection (Hussein et al., 2005). Whether the parasite
interacts with TB or has only been noted in TB patients because the
use of acid-fast stained smears serves as the standard for detecting
both pathogens is unknown. Although evidence of airborne trans-
mission of Cyclospora is lacking, the presence of the parasite in
the sputum of these patients raises the question about the pos-
sibility that this type of spread of the coccidium to humans can
exist; how frequent such transmission can occur and under what
circumstances have to be determined.
4. Prevention and control
Preventive measures are by far the most effective approach to
control C. cayetanensis. Because the mainsource of humaninfection
is contaminated water, food and soil, implementation of measures
to decrease or avoid the spread of Cyclospora oocysts in the envi-
ronment is critical. Endemicity of cylosporiasis is often linked to
developing countries where population growth and unplanned
urbanisation, rural to urban migration, poverty, inadequate san-
itation and poor health education contribute to the increasing
prevalence of infection. Improving environmental sanitation may
reduce exposure to humanfaeces and contaminationof water, food
and soil. The most important steps to prevent infection are health
education including personal hygiene, changing eating habits,
proper sanitary infrastructures and safe drinking water. However,
these steps are difcult challenges for developing regions. Prevent-
ing geophagia in children is important because of the potential
soilborne transmission of infection.
Specic instructions, regulations andrecommendations for con-
trolling waterborne protozoa have been proposed or developed by
international organisations that could be used for Cyclospora. From
a public health perspective, potential spread of C. cayetanensis from
water can be avoided only by adequate treatment of household
water sources. Studies to assess water quality of stored water and
household practices which stimulate post-treatment contamina-
tion are highly recommended.
For the developed world, the increasing globalisation of fresh
food supply and international trade is a complicating factor in
prevention and control of cyclosporiasis. Development, implemen-
tation and monitoring of on-farm control measures in endemic
areas are necessary to diminish or avoid future epidemic in
non-endemic areas. Improvement and application of disinfection
techniques for decontaminating imported produce will improve
food quality and safety. Treatment methods for removing Cryp-
tosporidium oocysts (Fayer, 2004) should be effective also for C.
cayetanensis. Control methods should be devised for the potential
routes used by the coccidium to enter the food production pro-
cess. It is necessary to establish preventive or control measures in
the processing and production operation to attenuate the impact
on human health of contaminated raw foods entering a factory or
contamination of food products inside the factory (Dawson, 2005).
Prevention of infection is particularly important for groups
at high risk for developing life-threatening infections such as
AIDS patients. Common sense prevention strategies would include
drinking boiled or bottled water and adequate hand-washing. For-
eign residents or visitors from non-endemic regions should also
have safe drinking water and avoid fresh produce.
5. Future perspectives
Currently, signicant gaps remain in our knowledge of the biol-
ogy and epidemiology of C. cayetanensis. In order to get a better
understanding of the parasite and its impact on human health, a
great deal of research is necessary.
Recently, molecular biologic tools havebeendevelopedtodetect
and differentiate Cyclospora at the species levels but they are not in
widespread use for routine testing. Molecular techniques must be
applicable to clinical and environmental samples.
The poor sensitivity and specicity of diagnostic methods
suggest that Cyclospora infection and illness have been underes-
timated. In the developing world, great awareness of the parasite
and increased familiarity with it or with the disease would improve
surveillance programmes for the coccidiumandwouldincrease the
likelihood that future epidemics would be detected. In these areas,
it is necessary to implement detection techniques in the labora-
tories and in the eld that would help to control the infection and
prevent outbreaks locallyandassociatedtoimportedcontaminated
produce in the developed world.
Little is knownregardingthe environmental biologyof C. cayeta-
nensis. It is necessary to determine its basic biology to develop
methods for prevention, control andtreatment of infection. Oocysts
of coccidiaareabletoendureandsporulateafter exposuretostress-
ful environmental conditions (ManseldandGajadhar, 2004; Sinski
and Behnke, 2004). Whether Cyclospora oocysts are as resistant or
if another host exists is unknown. Our understanding of the sur-
vival of this organism in the environment is developing. However,
studies are required to address why Cyclospora infectionis seasonal
with different patterns in different areas of the world.
There is little monitoring for Cyclospora in the environment.
Thus it is not known whether the coccidium is widespread. Com-
plex methods are used for isolation of the parasite from food and
water. There are no commercial paramagnetic beads coated with
antibody or labelled antibodies for the detection of Cyclospora
by immunomagnetic separation and ow cytometry (Dixon et
al., 2005). Further developments in the methods and systems of
epidemiology and diagnosis of the parasite would allow a bet-
ter assessment of the epidemiology and actual risks presented by
the coccidium which would lead to better prevention and con-
trol measures. Effective molecular methods for identication of
parasite in environmental samples must have increased sensitiv-
ity, specicity and discrimination. Molecular characterisation of
isolates in environmental matrices along with source and disease
tracking would greatly improve our knowledge of contamination
routes.
The lack of an in vitro method of growing C. cayetanensis and of
animal experimental models have limited studies of laboratory and
risk assessment models (Eberhard et al., 2000). An in vitro method
of culturing Cyclospora oocysts is needed for laboratory research.
Studies of the coccidium in primates as animal models have added
newknowledge on infection but also newquestions about the biol-
ogy of C. cayetanensis (Eberhard and Arrowood, 2002).
In order to assess the potential risk of water contaminated
with the parasite, the viability and sporulation stage of Cyclospora
oocysts have been determined by the electron rotation method
(Dalton et al., 2001). Development of new methods for simple and
quickly determining the viability of C. cayetanensis is necessary.
Also, improvements in disinfection methods of contaminated pro-
duce are required. Application of these advance technologies will
improve water and food quality and safety.
The modes of transmission and their relative rates of cyclospo-
riasis are not well known. Understanding howthese routes interact
andthefrequencyof transmissionrequires molecular epidemiolog-
ical studies in dened endemic locations. In developing countries,
infections linked to soil contact provide reasons to believe that this
route of spread may be more common that realised. How frequent
soilborne transmission occurs and whether variables associated
with socioeconomic status could predispose people to infection
remain to be determined. Environmental studies must include the
examination of soil samples.
Direct evidence of airborne transmission of C. cayetanensis is
lacking. However, the implications of respiratory tract infection
to the spread of the parasite remains to be determined. Also,
the zoonotic potential of Cyclospora requires elucidation. Further
molecular studies are needed to demonstrate whether Cyclospora
spp. identied in lower primates occur in humans or conrm
whether C. cayetanensis can occur in monkeys. Much research is
needed to identify and establish the role of animals as a part of the
life cycle development of this parasite. Research focus toward this
issue seems warranted. Despite new data on the parasite, impor-
tant uncertainties remain in our knowledge which highlight the
need for increasing research in several areas.
6. Conclusions
C. cayetanensis has emerged as a global public health problem.
There are several gaps in our understanding of the epidemiology
of cyclosporiasis. These deciencies seriously challenge our efforts
to implement effective surveillance and prevention and control
strategies for infection.
In the developing world, improving environmental sanitation
and health education could be the most practical intervention for
controlling the infection. For the developed world, the increas-
ing globalisation of fresh food supply and international trade is
a complicating factor in prevention and control of cyclosporiasis.
Signicant public interest has beengeneratedfromnumerous food-
borne outbreaks and the parasite has become a concern to the food
industry. The biology and ecology of C. cayetanensis make its con-
trol in food manufacturing and food service operations difcult.
Prevention and control of waterborne disease depends upon our
ability to avoid, remove or kill coccidian contaminant.
The numerous deciencies in our knowledge of epidemiol-
ogy and other basic issues of C. cayetanensis, warrant continued
research efforts of this parasite.
References
Abouel Naga, I.F., 1999. Studies ona newlyemergingprotozoal pathogen: Cyclospora
cayetanensis. J. Egypt Soc. Parasitol. 29, 575586.
Adam, A., Ortega, Y.R., 1999. Cyclospora. In: Robinson, R.K., Batt, C.A., Patel, P.D.
(Eds.), Encyclopaedia of Food Microbiology. Academic Press Limited, London,
United Kingdom, pp. 502513.
Adam, R.D., Ortega, Y.R., Gilman, R.H., Sterling, C.R., 2000. Intervening transcribed
spacer region 1. Variability in Cyclospora cayetanensis. J. Clin. Microbiol. 38,
23392343.
Aksoy, U., Tuncay, S., 2007. Short communication: investigationof intestinal coccidia
in patients with diarrhea. Mikrobiyol. Bul. 41, 127131.
Alakpa, G.E., Clarke, S.C., Fagbenro-Beyioku, A.F., 2003. Cyclospora cayetanensis in
stools submittedtohospitals inLagos, Nigeria. Clin. Microbiol. Infect. 9, 731733.
Albert, M.J., Kabir, I., Azim, T., Hossain, A., Ansaruzzaman, M., Unicomb, L., 1994.
Diarrhea associated with Cyclospora sp. in Bangladesh. Diagn. Microbiol. Infect.
Dis. 19, 4749.
Albert, M.J., Faruque, A.S.G., Faruque, S.M., Sack, R.B., Mahalanabis, D., 1999. Case-
control study of enteropathogens associated with childhood diarrhea in Dhaka,
Bangladesh. J. Clin. Microbiol. 37, 34583464.
Al-Braiken, F.A., Amin, A., Beeching, N.J., Hommel, M., Hart, C.A., 2003. Detection of
Cryptoporidiumamongst diarrhoeic and asymptomatic children in Jeddah, Saudi
Arabia. Ann. Trop. Med. Parasitol. 97, 505510.
Alfano-Sobsey, E.M., Eberhard, M.L., Seed, J.R., Weber, D.J., Won, K.Y., Nace, E.K., Moe,
C.L., 2004. Human challenge pilot study with Cyclospora cayetanensis. Emerg.
Infect. Dis. 10, 726728.
Anonymous, 1997. Update: outbreaks of cyclosporiasis United States and Canada.
Can. Comm. Dis. Rep. 23, 143144.
Anonymous, 2004. Salad implicated in US Cyclospora outbreak. Food safety and
security. Page 7, www.pjbames.co.uk/fss/foodsafety.hhm.
Arzuza, O.S., Arroyo, B.J., Villegas, S., Rocha, A., Daz, H., 2003. Infecciones parasitarias
intestinales enpacientes positivos para el virus de la inmunodeciencia humana
(VIH) en la ciudad de Cartagena de Indias, Colombia. Infectio 7, 5863.
Ashford, R.W., 1979. Occurrence of an undescribed coccidian in man in Papua New
Guinea. Ann. Trop. Med. Parasitol. 73, 497500.
Ayala-Gaytn, J.J., Daz-Olachea, C., Riojas-Montalvo, P., Palacios-Martnez, C., 2004.
Cyclosporidiosis: clinical anddiagnostic characteristics of anepidemic outbreak.
Rev. Gastroenterol. Mex. 69, 226229.
Becker, M.L., Cohen, C.R., Cheang, M., Washington, R.G., Blanchard, J.F., Moses, S.,
2007. Diarrheal disease among HIV-infected adults in Karnataka India: evalua-
tion of risk factors and etiology. Am. J. Trop. Med. Hyg. 76, 718722.
Bendall, R.P., Lucas, S., Moody, A., Tovey, G., Chiodini, P.L., 1993. Diarrhea associated
with cyanobacterium-like bodies: a new coccidian enteritis of man. Lancet 341,
590592.
Bern, C., Hernandez, B., Lopez, M.B., Arrowood, M.J., Alvarez de Meja, M., de Merida,
A.M., Hightower, A.W., Venczel, L., Herwaldt, B.L., Klein, R.E., 1999. Epidemiologic
studies of Cyclospora cayetanensis in Guatemala. Emerg. Infect. Dis. 5, 766774.
Bern, C., Ortega, Y.R., Checkley, W., Roberts, J.M., Lescano, A.G., Cabrera, L., Verastegui,
M., Black, R.E., Sterling, C., Gilman, R.H., 2002. Epidemiologic differences
between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerg.
Infect. Dis. 8, 581585.
Bernal Redondo, R.M., Hernandez Sanchez, G., Ramirez Hernandez, E.C., Gamez
Aranda, A., Martinez Mendez, L., 1998. Protozoos emergentes Comparacin de
tres mtodos de identicacin. Rev. Mex. Patol. Clin. 45, 193199.
Blans, M.C.A., Ridwan, B.U., Verweij, J.J., Rozenberg-Aroka, M., Verhoef, J., 2005.
Cyclosporiasis outbreaks Indonesia. Emerg. Infect. Dis. 11, 14531455.
Botero-Garces, J., Montoya-Palacio, M.N., Barguil, J.I., Casta no-Gonzalez, A., 2006.
Brote epidmico por Cyclospora cayetanensis en Medelln Colombia. Rev. Salud
Publica 8, 258268.
Boure, P., Lancon, A., Bonnot, G., 2006. Une parasitose mergente: la cyclosporose
Revue propos de ve observations. Antibiotiques 8, 7378.
Boure, P., Lancon, A., Bisaro, F., Bonnot, G., 2007. Six human cyclosporiasis: with
general review. J. Egypt Soc. Parasitol. 37, 349360.
Brockmann, S., Dietrich, K., Doller, P.C., Dreweck, C., Filipp, N., Wagner-Wiening,
C., Wiedenmann, A., Kiehl, W., 2001. Cyclosporiasis in Germany. Euro Surveill.
Wkly. 5, 22.
Burstein Alva, S., 2005. Ciclosporosis: una parasitosis emergente (1) Aspectos clni-
cos y epidemiologicos. Rev. Gastroenterol. Per 25, 328335.
Calvo, M., Carazo, M., Arias, M.L., Chaves, C., Monges, R., Chinchilla, M., 2004. Preva-
lencia de Cyclospora sp., Cryptosporidiumsp., microsporidios y determinacin de
coliformes fecales en frutas y vegetales frescos de consumo crudo en Costa Rica.
Arch. Latinoam. Nutr. 54, 428432.
Capo de Paz, V., Barreto Brnguez, M., Velazquez Vamonte, B., Luzardo Suarez, C.,
Martinez Rodriguez, A., Alujas Martinez, Z., 2003. Diagnstico de coccidias y
microsporas enmuestras de heces diarreicas de pacientes cubanos seropositivos
al VIHPrimer reporte de microsporas enCuba. Rev. Cubana Med. Trop. 55, 1418.
Carollo, M.C., Amato Neto, V., Braz, L.M., Dowoong, K., 2001. Pesquisa de oocistos
de Cyclospora sp., em fezes de ces da Grande So Paulo, Estado de So Paulo,
Brasil. Rev. Soc. Bras. Med. Trop. 34, 597598.
CDC (Centers for Disease Control and Prevention), 1997. Update: outbreaks of
cyclosporiasis United States and Canada. MMWR Morb. Mortal. Wkly. Rep.
46, 521523.
CDC (Centers for Disease Control and Prevention), 1997. Update: outbreak of
cyclosporiasis Northern Virginia Washington, D.C. Baltimore, Maryland,
Matropolitan area. MMWR Morb. Mortal. Wkly. Rep. 46, 689691.
CDC (Centers for Disease Control and Prevention), 2004. Outbreak of cyclosporiasis
associated with snowpeas Pennsylvania. MMWR Morb. Mortal. Wkly. Rep. 53,
876878.
Cede no, T.C., 2002. Cyclospora cayetanensis: descripcin del primer caso en el Hos-
pital San Rafael de Alajuela. Acta Med. Costarric. 44, 7981.
Cegielski, J.P., Ortega, Y.R., McKee, S., Madden, J.F., Gaido, L., Schwartz, D.A., Manji, K.,
Jorgensen, A.F., Miller, S.E., Pulipaka, U.P., Msengi, A.E., Mwakyusa, D.H., Sterling,
C.R., Reller, L.B., 1999. Cryptosporidium, Enterocytozoon, andCyclosporainfections
in pediatric and adult patients with diarrhea in Tanzania. Clin. Infect. Dis. 28,
314321.
Chacn-Bonilla, L., Estevez, J., Monsalve, F., Quijada, L., 2001. Cyclospora cayetanensis
infections among diarrheal patients from Venezuela. Am. J. Trop. Med. Hyg. 65,
351354.
Chacn-Bonilla, L., Mejia de Young, M., Estevez, J., 2003. Prevalence and pathogenic
role of Cyclospora cayetanensis in a Venezuelan community. Am. J. Trop. Med.
Hyg. 68, 304306.
Chacn-Bonilla, L., Panunzio, A.P., Monsalve Castillo, F., Parra Cepeda, I.E., Martnez,
R., 2006. Microsporidiosis in Venezuela. Prevalence of intestinal microsporidio-
sis and its contribution to diarrhea in groups of human immunodeciency virus
infected patients from Zulia State. Am. J. Trop. Med. Hyg. 74, 482486.
Chacn-Bonilla, L., Barrios, F., Sanchez, Y., 2007. Epidemiology of Cyclospora cayeta-
nensis infection in San Carlos Island, Venezuela: strong association between
socio-economic status and infection. Trans. R. Soc. Trop. Med. Hyg. 101,
10181024.
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. MMWR Morb. Mortal. Wkly. Rep. 45, 549551.
Chinchilla, M.C., Guerrero, O.M., Reyes, L.L., Castro, A.C., 1999. Cyclospora cayeta-
nensis: revision e informe del primer caso humano en Costa Rica. Acta. Med.
Costarric. 41, 3942.
Chu, D.-M.T., Sherchand, J.B., Cross, J.H., Orlandi, P.A., 2004. Detection of Cyclospora
cayetanensis in animal fecal isolates from Nepal using an FTA lter-base poly-
merase chain reaction method. Am. J. Trop. Med. Hyg. 71, 373379.
Clarke, S.C., McIntyre, M., 1996. The incidence of Cyclospora cayetanensis in stool
samples submittedtoadistrict general hostipal. Epidemiol. Infect. 117, 189193.
Connor, B.A., Reidy, J., Soave, R., 1999. Cyclosporiasis: clinical and histopathological
correlates. Clin. Infect. Dis. 28, 12161222.
Cordova Paz, S.O., Vargas Vasquez, F., Gonzalez Varas, A., Prez Cordn, G., Velasco
Soto, J.R., Snchez-Moreno, M., Rodrguez Gonzalez, I, Rosales Lombardo, M.J.,
2006. Intestinal parasitismin Peruvian children and molecular characterization
of Cryptosporidium species. Parasitol. Res. 98, 576581.
Dalton, C., Goater, A.D., Pethig, R., Smith, H.V., 2001. Viability of Giardia intesti-
nalis cysts and viability and sporulation state of Cyclospora cayetanensis oocysts
determined by electrorotation. Appl. Environ. Microbiol. 67, 586590.
Dawson, D., 2005. Foodborne protozoan parasites. Int. J. Food Microbiol. 103,
207227.
De Souza Jr., E.S., Garca Zapata, M.T., 2006. Diagnstico laboratorial de enteropara-
sitoses oportunistas, comnfase nas microsporidioses humanas, emGoinia-Go.
Rev. Soc. Bras. Med. Trop. 39, 560564.
Devera, R., Blanco, Y., Cabello, E., 2005. Elevada prevalencia de Cyclospora cayeta-
nensis en indgenas del estado Bolvar, Venezuela. Cad. Saude. Publica 21,
17781784.
Das Borges, J., Rodriguez Alarcn, R.S., Amato Neto, V., Gakiya, E., 2009. Para-
sitoses intestinais de indgenas da comunidade Mapuera (Oriximin, Estado
do Par, Brasil): elevada prevalncia de Blastocystis hominis and nding of
Cryptosporidium sp. and Cyclospora cayetanensis. Rev. Soc. Brs. Med. Trop. 42,
348350.
Daz, E., Mondragon, J., Ramirez, E., Bernal, R., 2003. Epidemiology and control of
intestinal parasites with nitazoxanide in children in Mexico. Am. J. Trop. Med.
Hyg. 68, 384385.
Di Gliullo, A.B., Cribari, M.S., Bava, A.J., Cicconetti, J.S., Collazos, R., 2000. Cyclospora
cayetanensis in sputum and stool samples. Rev. Inst. Med. Trop. So Paulo 42,
115117.
Dixon, B.R., Bussey, J.M., Parrington, L.J., Parenteau, M., 2005. Detection of Cyclospora
cayetanensis oocysts in human fecal specimens by owcytometry. J. Clin. Micro-
biol. 43, 23752379.
Do Nascimento, E.M.G., Horroiva Uemura, I., Paglius, V.L., Pereira Corbett, C.E., 2005.
Retrospective study of the occurrence of Cyclospora cayetanensis at clinical hos-
pital of the University of Sao Paulo Medical School SP. Rev. Soc. Bras. Med. Trop.
38, 326330.
Doller, P.C., Dietrich, K., Filipp, N., Brockmann, S., Dreweck, C., Vonthein, R.,
Wagner-Wiening, C., Wiedermann, A., 2002. Cyclosporiasis outbreak in Ger-
many associated with the consumption of salad. Emerg. Infect. Dis. 8, 922994.
Dowd, S.E., John, D., Eliopolus, J., Gerba, C.P., Naranjo, J., Klein, R., Lopez, B., de Mejia,
M., Mendoza, C.E., Pepper, I.L., 2003. Conrmed detection of Cyclospora cayeta-
nensis, Encephalitozoon intestinalis and Cryptosporidium parvum in water used
for drinking. J. Water Health 1, 117123.
Drenaggi, D., Cirioni, O., Giacometti, A., Fiorentini, A., Scalise, G., 1998. Cyclosporiasis
in a traveler returning from South Amrica. J. Travel Med. 5, 153155.
Easow, J.M., Mukhopadhyay, C., Wilson, G., Guha, S., Jalan, B.Y., Shivananda, P.G.,
2005. Emerging opportunistic protozoa and intestinal pathogenic protozoal
infestation prole in children of Western Nepal. Nepal Med. Coll. J. 7, 134137.
Eberhard, M.L., Pieniazek, N.J., Arrowood, M.J., 1997. Laboratory diagnosis of
Cyclospora infections. Arch. Pathol. Lab. Med. 121, 792797.
Eberhard, M.L., Da Silva, A.J., Lilley, B.G., Pieniazek, N.J., 1999a. Morphologic and
molecular characterization of new Cyclospora species from Ethiopian monkeys:
C. cercopitheci sp.n., C. colobi sp.n, and C. papionis sp.n. Emerg. Infect. Dis. 5,
651658.
Eberhard, M.L., Nace, E.K., Freeman, A.R., Streit, T.G., Da Silva, A.J., Lammie, P.J., 1999b.
Cyclospora cayetanensis infections in Haiti: a common occurrence in the absence
of watery diarrhea. Am. J. Trop. Med. Hyg. 60, 584586.
Eberhard, M.L., Nace, E.K., Freeman, A.R., 1999c. Survey for Cyclospora cayetanensis
in domestic animals in an endemic area in Haiti. J. Parasitol. 85, 562563.
Eberhard, M.L., Ortega, Y.R., Hanes, D.E., Nace, E.K., Do, R.Q., Robl, M.G., Won, K.Y.,
Gavidia, C., Sass, N.L., Manseld, K., Gozalo, A., Grifths, J., Gilman, R., Ster-
ling, C.R., Arrowood, M.J., 2000. Attempts to establish experimental Cyclospora
cayetanensis infection in laboratory animals. J. Parasitol. 86, 577582.
Eberhard, M.L., Njenga, M.N., da Silva, A.J., Owino, D., Nace, E.K., Won, K.Y., Mwenda,
J.M., 2001. A survey for Cyclospora spp. in Kenyan primates, with some notes on
its biology. J. Parasitol. 87, 13941397.
Eberhard, M.L., Arrowood, M.J., 2002. Cyclospora spp. Opin. Infect. Dis. 15, 519522.
Echeverra, P., Taylor, D.N., Lexsomboon, U., Bhaibulaya, M., Blacklow, N.R., Tamura,
K., Sakazaki, R., 1989. Case-control study of endemic diarrheal disease in Thai
children. J. Infect. Dis. 159, 543548.
El-Karamany, E.M., Zaher, T.I., el-Bahnasawy, M.M., 2005. Role of water in the trans-
mission of cyclosporiasis in Sharkia Govemorate Egypt. J. Egypt. Soc. Parasitol.
35, 953962.
Elshazly, A.M., Elsheikha, H.M., Soltan, D.M., Mohammad, K.A., Morsy, T.A., 2007.
Protozoal pollution of surface water sources in Dakahlia Govemorate Egypt. J.
Egypt. Soc. Parasitol. 37, 5164.
Escobedo, A.A., Nu nez, F.A., 1999. Prevalence of intestinal parasites in Cuban
acquired immunodeciency syndrome (AIDS) patients. Acta Tropica 72,
125130.
Estran, C., Chaillou, S., Marty, P., 2004. Un risque parasitaire pour le touriste en
Rpublique Dominicaine: la cyclosporose. Med. Trop. 64, 9899.
Fayer, R., 2004. Cryptosporidium: a water-borne zoonotic parasite. Vet. Parasitol. 126,
3756.
Fryauff, D.J., Krippner, R., Prodjodipuro, P., Ewald, C., Kawengian, S., Pagelow, K., Yun,
T., von Heydwolff-Wehnert, C., Oyofo, B., Gross, R., 1999. Cyclospora cayetanensis
among expatriate and indigenous populations of West Java Indonesia. Emerg.
Infect. Dis. 5, 585588.
Garca-Lpez, H.L., Rodriguez-Tovar, L.E., Medina-De la Garza, C.E., 1996. Identica-
tion of Cyclospora in poultry. Emerg. Infect. Dis. 2, 356357.
Gascon, J., Alvarez, M., Valls, E.M., Bordas, M.J., Jimenez de Anta, T.M., Corachan,
M., 2001. Cyclosporiasis: a clinical and epidemiological study in travellers with
imported Cyclospora cayetanensis infection. Med. Clin. (Barc) 116, 451464.
Gatei, W., Wamae, C.N., Mbae, C., Waruru, A., Mulinge, E., Waithera, T., Gatika, S.M.,
Kamwati, S.K., Revathi, C., Hart, C.A., 2006. Cryptosporidiosis: prevalence, geno-
type, analysis, and symptoms associated with infections in children in Kenya.
Am. J. Trop. Med. Hyg. 75, 7882.
Green, S.T., McKendrick, M.W., Mohse, A.H., Schmid, M.L., Prakasam, S.F., 2000. Two
simultaneous cases of Cyclospora cayetanensis enteritis returning from Domini-
can Republic. J. Travel Med. 7, 4142.
Gumbo, T., Sarbah, S., Gangaidzo, I.T., Ortega, Y., Sterling, C.R., Carville, A., Tzipori,
S., Wiest, P.M., 1999. Intestinal parasites in patients with diarrhea and human
immunodeciency virus infection in Zimbabwe. AIDS 13, 819821.
Gupta, S., Narang, S., Nunavath, V., Singh, S., 2008. Chronic diarrhea in HIV patients:
prevalence of coccidian parasite. Indian J. Med. Microbiol. 26, 172175.
Hale, D.W., Aldeen, W., Carroll, K., 1994. Diarrhea associated with cyanobacteria like
bodies in an inmunocompetent host: an unusual epidemiological source. JAMA
271, 144145.
Haque, R., Mondal, D., Kirkpatrick, B.D., Akther, S., Farr, B.M., Bradley Sack, R., Petri
Jr., W.A., 2003. Epidemiologic and clinical characteristics of acute diarrhea with
emphasis on Entamoeba histolytica infections in preschool children in an urban
slum of Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 69, 398405.
Hart, A.S., Ridinger, M.T., Soundarajan, R., Peters, C.S., Swiatlo, A.L., Kocka, F.E., 1990.
Novel organismassociated with chronic diarrihea in AIDS. Lancet 335, 169170.
Herwaldt, B.L., Ackers, M.L., 1997. An outbreak in 1996 of cyclosporiasis associated
with imported raspberries. N. Engl. J. Med. 336, 15481556.
Herwaldt, B.L., Beach, M.J., 1999. The return of Cyclospora in 1997: another outbreak
of cyclosporiasis in North America associated with imported raspberries. Ann.
Intern. Med. 130, 210220.
Herwaldt, B.L., 2000. Cyclospora cayetanensis: a review, focusing on the outbreaks of
cyclosporiasis in the 1990s. Clin. Infect. Dis. 31, 10401057.
Ho, A.Y., Lpez, A.S., Eberhart, M.G., Levenson, R., Finkel, S., da Silva, A.J., Roberts,
J.M., Orlandi, P.A., Johnson, C.C., Herwaldt, B.L., 2002. Outbreak of cyclosporiasis
associated with imported raspberries, Philadelphia, Pennsylvania, 2000. Emerg.
Infect. Dis. 8, 783788.
Hoang, L.M., Fyfe, M., Ong, C., Harb, J., Champagne, S., Dixon, B., Isaac-Renton, J., 2005.
Outbreak of cyclosporiasis in British Columbia associated to imported Thai basil.
Epidemiol. Infect. 133, 2337.
Hoge, C.W., Shlim, D.R., Rajah, R., Triplett, J., Shear, M., Rabold, J.G., Echeverra, P.,
1993. Epidemiology of diarrhoeal illness associated with coccidian-like organ-
ism among travellers and foreign residents in Nepal. Lancet 341, 11751179.
Hoge, C.W., Echeverra Rajah, R., Jacobs, J., Matthouse, S., Chapman, E., Jimenez,
L.M., Shlim, D.R., 1995. Prevalence of Cyclospora species and other enteric
pathogens among children less than 5 years of age in Nepal. J. Clin. Microbiol.
33, 30583060.
Huang, P., Weber, J.T., Sosin, D.M., Grifn, P.M., Long, E.G., Murphy, J.J., Kocka, F.,
Peters, C., Kallick, C., 1995. The rst reported outbreak of diarrheal illness asso-
ciated with Cyclospora in the United States. Ann. Intern. Med. 123, 409414.
Hussein, E.M., Abdul-Manaem, A.H., el-Attary, S.L., 2005. Cyclospora cayetanensis
oocysts in sputum of a patient with active pulmonary tuberculosis, case report
in Ismailia, Egypt. J. Egypt. Soc. Parasitol. 35, 787793.
Kaminsky, R.G., 1997. Cyclospora cayetanensis: nuevo apicomplexa intestinal, con
observaciones en el Hospital Escuela. Rev. Med. Hondur. 65, 6872.
Kaminsky, R.G., 2002. Comparacin epidemiolgica entre apicomplexa intestinales
en poblacin hospitalaria en Honduras. Rev. Med. Hondur. 70, 164172.
Kaminsky, R.G., Stovall, M.E., Mayer, M.L., Martin, A.D., Bowers, L.C., Didier, E.S., 2007.
Microsporidia intestinales en pacientes viviendo con SIDA en Honduras. Rev.
Med. Hondur. 75, 116123.
Kansouzidou, A., Charitidou, C., Varnis, T., Vavatsi, N., Kamaria, F., 2004. Cyclospora
cayetanensis inapatient withtravelers diarrhea: casereport andreview. J. Travel
Med. 11, 6163.
Karanis, P., Kourenti, C., Smith, H., 2007. Waterborne transmission of protozoan par-
asites: a worldwide review of outbreaks and lessons learnt. J. Water Health 5,
138.
Kimura, K., Rai, S.K., Rai, G., Insisiengmay, S., Kawabata, M., Karanis, P., Uga, S., 2005.
Study on Cyclospora cayetanensis, associated with diarrheal disease in Nepal and
Lao PDR. Southeast Asian J. Trop. Med. Public Health 36, 13711376.
Kniel, K.E., Shearer, A.E., Cascarino, J.L., Wilkins, G.C., Jenkins, M.C., 2007. Highhydro-
static preasure and UV light treatment of produce contaminated with Eimeria
acervulina as a Cyclospora cayetanensis surrogate. J. Food Prot. 70, 28372842.
Koumans, E.H.A., Katz, D.J., Malecki, J.M., Kumar, S., Wahlquist, S.P., Arrowood, M.J.,
Hightower, A.W., Herwaldt, B.L., 1998. An outbreak of cyclosporiasis in Florida
in 1995: a harbinger of multistate outbreaks in 1996 and 1997. Am. J. Trop. Med.
Hyg. 59, 235242.
Kumar, S.S., Ananthan, S., Lakshmi, P., 2002. Intestinal parasitec infection in HIV
infected patients with diarrhoea in Chennai. Indian J. Med. Microbiol. 20, 8891.
Kurniawan, A., Karyadi, T., Dwintasari, S.W., Sari, I.P., Yunihastuti, E., Djauzi, S., Smith,
H.V., 2009. Intestinal parasitic infections in HIV/AIDS patients presenting with
diarrhoea in Jakarta, Indonesia. Trans. R. Soc. Trop. Med. Hyg. 103, 892898.
Lainson, R., 2005. The genus Cyclospora: (Apicomplexa: Eimeriidae), with a descrip-
tion of Cyclospora schneideri n.sp. in the snake Anilius scytale (Anildae) from
Amazonian Brazil a review. Mem. Inst. Oswaldo Cruz 100, 103115.
Lee, M.B., Lee, E.H., 2001. Coccidial contamination of Rasberries: mock contamina-
tion with Eimeria acervulina as a model for decontamination treatment studies.
J. Food Prot. 64, 18541857.
Long, E.G., Ebrahimzadeh, A., White, E.H., Swisher, B., Callaway, C.S., 1990. Alga asso-
ciatedwithdiarrhea inpatients withacquiredimmunodeciency syndrome and
in travellers. Clin. Microbiol. 28, 11011104.
Long, E.G., White, E.H., Carmichael, W.W., Quinlisk, P.M., Raja, R., Swisher, B.L.,
Daugharty, H., Cohen, M.T., 1991. Morphological and staining characteristics
of a Cyanobacterium-like organism associated with diarrhea. J. Infect. Dis. 164,
199202.
Lpez, F.A., Manglicmot, J., Schimdt, T.M., Yeh, C., Smith, H.V., Relman, D.A., 1999.
Molecular characterization of Cyclospora-like organisms frombaboons. J. Infect.
Dis. 179, 670676.
Lpez, A.S., Dodson, D.R., Arrowood, M.J., Orlandi Jr., P.A., Silva, A.J.Da., Bier, J.W.,
Hanauer, S.D., Kuster, R.I., Oltman, S., Baldwin, M.S., Won, K.Y., Nace, E.M., Eber-
hard, M.L., Herwaldt, B.L., 2001. Outbreak of cyclosporiosis associated with basil
in Missouri in 1999. Clin. Infect. Dis. 32, 10101017.
Lpez, A.S., Bendik, J.M., Alliance, J.Y., Roberts, J.M., da Silva, A.J., Moura, I.N.S.,
Arrowood, M.I., Eberhard, M.L., Herwaldt, B.L., 2003. Epidemiology of Cyclospora
cayetanensis andother intestinal parasites ina community inHaiti. J. Clin. Micro-
biol. 41, 20472054.
Madico, G., McDonald, J., Gilman, R.H., Cabrera, L., Sterling, C.R., 1997. Epidemiology
and treatment of Cyclospora cayetanensis infection in Peruvian children. Clin.
Infect. Dis. 24, 977981.
Madrid, V.V., Torrejn, G.E., Rivera, F.N., Madrid, P.M., 1998. Ciclosporosis: informe
de un caso clnico en Concepcin, Chile. Rev. Med. Chile 126, 559562.
Manatsathit, S., Tansupasawasdikul, S., Wanachiwanawin, D., Setawarin, S., Suwana-
gool, P., Prakasvejakit, S., Leelakusolwong, S., Eampokalap, B., Kachintorn, U.,
1996. Causes of chronic diarrhea inpatients withAIDS inThailand: a prospective
clinical and microbiological study. Gastroenterology 31, 533537.
Mandomando, I.M., Macete, E.V., Ruiz, J., Sanz, S., Abacassamo, F., Valles, X., Sacar-
lal, J., Navia, M.M., Vila, J., Alonso, P.L., Gascon, J., 2007. Etiology of diarrhea in
children younger than 5 years of age admitted in a rural hospital of Southern
Mozambique. Am. J. Trop. Med. Hyg. 76, 522527.
Manseld, L.S., Gajadhar, A.A., 2004. Cyclospora cayetanensis a food-and waterborne
coccidian parasite. Vet. Parasitol. 126, 7390.
Martnez Silva, I., Ayllon Valds, L., Benitez Padron, X., 2002. Cyclospora cayetanensis.
Presentacin de 20 casos. Rev. Cub. Pediatr. 74, 178181.
Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Grifn, P.M.,
Tauxe, R.V., 1999. Food-related illness and death in the United States. Emerg.
Infect. Dis. 5, 607625.
Miegeville, M., Koubi, V., Dan, L.C., Barbier, J.P., Cam, P.D., 2003. Cyclospora cayeta-
nensis et sa presnce en milieu hydrique Hanoi (Vietnam) Etude dans
lenvironnement (eaux de forage, lacs et rivires). Bull. Soc. Path. Exot. 96,
149152.
Mundaca, C.C., Torres-Slimming, P.A., Araujo-Castillo, R.V., Moran, M., Bacon, D.J.,
Ortega, Y., Gilman, R.H., Blazes, D.L., 2008. Use of PCR to improve diagnostic
yield in an outbreak of cyclosporiasis in Lima Peru. Trans. R. Soc. Trop. Med.
Hyg. 102, 712717.
Naito, T., Mizue, S., Misawa, S., Nakamura, A., Isonuma, H., Kondo, S., Dambara, T.,
Yamamoto, N., 2009. Cyclospora infection in an immunocompetent patient in
Japan. Jpn. J. Infect. Dis. 62, 5758.
Nassef, N.E., el-Ahl, S.A., el-Shafee, O.K., Nawar, M., 1998. Cyclospora: a newly iden-
tied protozoan pathogen of man. J. Egypt. Soc. Parasitol. 28, 213219.
Negm, A.Y., 2003. Human pathogenic protozoa in bivalves collected fromlocal mar-
kets in Alexandria. J. Egypt. Soc. Parasitol. 33, 991998.
Nimri, L.F., 2003. Cyclospora cayetanensis and other intestinal parasites associated
with diarrhea in rural area of Jordan. Int. Microbiol. 6, 131135.
Nu nez, F.A., Gonzalez, O.M., Gonzalez, I., Escobedo, A.A., Cordovi, R.A., 2003. Intesti-
nal coccidia in Cuban pediatric patients with diarrhea. Mem. Inst. Oswaldo Cruz.
98, 539542.
Olivier, C., van de Pas, S., Lepp, P.W., Yoder, K., Relman, D.A., 2001. Sequence variabil-
ity in the rst internal transcribed spacer region within and among Cyclospora
species is consistent with polyparasitism. Int. J. Parasitol. 31, 14751487.
Ooi, W.W., Zimmerman, S.K., Needham, C.A., 1995. Cyclospora species as a gastroin-
testinal pathogen in inmunocompetent hosts. J. Clin. Microbiol. 33, 12671269.
Ortega, Y.R., Sterling, C.R., Gilman, R.H., Cama, V.A., Daz, F., 1993. Cyclospora species-
a new protozoan pathogen of humans. N. Engl. J. Med. 328, 13081312.
Ortega, Y.R., Gilman, R.H., Sterling, C.R., 1994. Anewcoccidian parasite Apicomplexa:
Eimeriidae from humas. J. Parasitol. 80, 625629.
Ortega, Y.R., Nagle, R., Gilman, R.H., Watanabe, J., Miyagui, J., Quispe, H., Kanagusuku,
P., Roxas, C., Sterling, C.R., 1997a. Pathologic and clinical ndings in patients
with cyclosporiasis and a description of intracellular parasite life-cycle stages.
J. Infect. Dis. 176, 15841589.
Ortega, Y.R., Roxas, C.R., Gilman, R.H., Miller, N.J., Cabrera, L., Taquiri, C., Sterling, C.R.,
1997b. Isolation of Cryptosporidium parvum and Cyclospora cayetanensis from
vegetables collected in markets of an endemic region in Peru. Am. J. Trop. Med.
Hyg. 57, 683686.
Ortega, Y.R., Sterling, C.R., Gilman, R.H., 1998. Cyclospora cayetanensis. Adv. Parasitol.
40, 339418.
Ortega, Y.R., Liao, J., 2006. Microwave inactivation of Cyclospora cayetanensis sporu-
lation and viability of Cryptosporidium parvum. J. Food Prot. 69, 19571960.
Ortega, Y.R., Mann, A., Torres, M.P., Cama, V., 2008. Efcacy of gaseous chlorine diox-
ide as a sanitizer against Cryptosporidium parvum, Cyclospora cayetanensis, and
Encephalitozoon intestinalis on produce. J. Food Prot. 71, 24102414.
Pape, J.W., Verdier, R.I., Boncy, M., Boncy, J., Johnson, W.D., 1994. Cyclospora infection
in adults infected with HIV. Clinical manifestations, treatment, and prophylaxis.
Ann. Intern. Med. 121, 654657.
Perez Cordn, G., Cordova Paz, S.O., Vargas Vasquez, F., Velasco Soto, J.R., Sempere
Bordes, L., Sanchez Moreno, M., Rosales, M.J., 2008. Prevalence of enteropara-
sites and genotyping of Giardia lamblia in Peruvian children. Parasitol. Res. 103,
459465.
Pratdesaba, R.A., Gonzalez, M., Piedrasanta, E., Mrida, C., Contreras, K., Vela, C., Cula-
jay, F., Flores, L., Torres, O., 2001. Cyclospora cayetanensis in three populations at
risk in Guatemala. J. Clin. Microbiol. 39, 29512953.
Puente, S., Morente, A., Garca-Benayas, T., Subirats, M., Gascon, J., Gonzalez-Lahoz,
J.M., 2006. Cyclosporiasis: a point source outbreak acquired in Guatemala. J.
Travel Med. 13, 334337.
Rabold, G., Hoge, C.W., Shlim, D.R.D.R., Kefford, C., Rajah, R., Echeverra, P., 1994.
Cyclospora outbreak associated with chlorinated drinking water. Lancet 344,
13601361.
Raccurt, C.P., Fouch, B., Agnamey, P., Menotti, J., Chouaki, T., Totet, A., Pape, J.W.,
2008. Presence of Enterocytozoon bieneusi associated with intestinal coccidia in
patients with chronic diarrhea visiting an HIV center in Haiti. Am. J. Trop. Med.
Hyg. 79, 579580.
Ramrez-Olivencia, G., Herrero, M.D., Subirats, M., Gonzalez, R., Puente, S., 2008.
Brote de Cyclospora cayetanensis en viajeros a Cuba. Enferm. Infecc. Microbiol.
Clin. 26, 558560.
Relman, D.A., Schmidt, T.M., Gajadhar, A., Sogin, M., Cross, J., Yoder, K., Sethabutr, O.,
Echeverra, P., 1996. Molecular phylogenetic analysis of Cyclospora, the human
intestinal pathogen, suggests that it is closely related to Eimeria species. J. Infect.
Dis. 173, 440445.
Rizk, H., Soliman, M., 2001. Coccidiosis among malnourished children in Mansoura,
Dakahlia Govemorate, Egypt. J. Egypt Soc. Parasitol. 31, 877886.
Rodriguez-Alarcn, R.S., Amato Neto, V., Gakiya, E., Bezerra, R.C., 2007. Observaces
sobre Blastocystis hominis e Cyclospora cayetanensis em exames parasitolgicos
efetuados rotineiramente. Rev. Brs. Md. Trop. 40, 253255.
Roldan, W.H., Espinoza, Y.A., Huapaya, P.E., Huiza, A.F., Sevilla, C.R., Jimnez, S., 2009.
Frequency of human toxocariasis in a rural population from Cajamarca Per
determined by dot-Elisa test. Rev. Inst. Med. Trop. S. Paulo 51, 6771.
Salvatella, R., Eiralle, C., Sundberg, F., 2000. Primera deteccin de Cyclospora cayeta-
nensis en Uruguay, a partir de un caso de diarrea del viajero adquirido en el
exterior. Rev. Urug. Pat. Clin. 32, 912.
Sarfati, C., Bourgeois, A., Menotti, J., Liegeois, F., Moyou-Somo, R., Delaporte, E.,
Derouin, F., Ngole, E.M., Molina, J.M., 2006. Prevalence of intestinal parasites
including Microspordia in human immunodeciency vrus-infected adults in
Cameroon: a cross-sectional study. Am. J. Trop. Med. Hyg. 74, 162164.
Sathyanarayanan, L., Ortega, Y.R., 2004. Effects of pesticide on sporulation of
Cyclospora cayetanensis and viability of Cryptosporidium parvum. J. Food Prot.
67, 10441049.
Sathyanarayanan, L., Ortega, Y.R., 2006. Effects of temperature and different food
matrices onCyclospora cayetanensis oocyst sporulation. J. Parasitol. 92, 218222.
Schaudinn, F., 1902. Studien ber krankheitserregende Protozoen I. Cyclospora cary-
olytica Shaud. der pernicisen Enteritis des Maulwurfs. Arb. K. Gesundheitsamte
18, 378416.
Schneider, A., 1881. Sur les psorospermies oviformes oucoccidies, espces nouvelles
ou peu connues. Arch. Zool. Exp. Gen. 9, 387404.
Sherchand, J.B., Cross, J.H., Jimba, M., Sherchand, S., Shrestha, M.P., 1999. Study of
Cyclospora cayetanensis in health care facilities, sewage water and green leafy
vegetables in Nepal. Southeast Asian J. Trop. Med. Public Health 30, 5863.
Sherchand, J.B., Cross, J.H., 2001. Emerging pathogen Cyclospora cayetanensis infec-
tion in Nepal. Southeast Asian J. Trop. Med. Public Health 32 (Suppl.), 143150.
Shields, J.M., Olson, B.H., 2003. Cyclospora cayetanensis: a review of an emerging
parasitic coccidian. Int. J. Parasitol. 33, 371391.
Shlim, D.R., Cohen, M.T., Eaton, M., Rajah, R., Long, E.G., Ungar, B.L., 1991. Analga-like
organism associated with an outbreak of prolonged diarrhea among foreigners
in Nepal. Am. J. Trop. Med. Hyg. 45, 383389.
Sinski, E., Behnke, J.M., 2004. Apicomplexan parasites: environmental contamina-
tion and transmission Pol. J. Microbial. 53 (Suppl.), 6773.
Smith, H.V., Paton, C.A., Girdwood, R.W., Mtambo, M.M., 1996. Cyclospora in non-
human primates in Gombe Tanzania (letter). Vet. Rec. 138, 528.
Smith, H.V., Paton, C.A., Mtambo, M.M., Girdwood, R.W., 1997. Sporulation of
Cyclospora sp. oocysts. Appl. Environ. Microbiol. 63, 16311632.
Soave, R., Dubey, J.P., Ramos, L.J., Tummings, M., 1986. A new intestinal pathogen?
Clin. Res. 34, 533.
Soave, R., Herwaldt, B.L., Relman, D.A., 1998. Cyclospora. Infect. Dis. Clin. N Am. 12,
112.
Sterling, C.R., Ortega, Y.R., 1999. Cyclospora: an enigma worth unraveling. Emerg.
Infect. Dis. 5, 4853.
Sturbaum, G.D., Ortega, Y.R., Gilman, R.H., Cabrera, C., Klein, D.A., 1998. Detection of
Cyclospora cayetanensis in wastewater. Appl. Environ. Microbiol. 64, 22842286.
Sun, T., Ilardi, C.F., Asnis, D., Bresciani, A.R., Goldenberg, S., Roberts, B., Teichberg,
S., 1996. Light and electron microscopic identication of Cyclospora species in
the small intestine. Evidence of the presence of asexual life cycle in human host.
Am. J. Clin. Path. 105, 216220.
Torres-Slimming, P.A., Mundaca, C.C., Moran, M., Quispe, J., Colina, O., Bacon, D.J.,
Lescano, A.G., Gilman, R.H., Blazes, D.L., 2006. Outbreak of cyclosporiasis at a
naval base in Lima Per. Am. J. Trop. Med. Hyg. 75, 546548.
TranVanNhieu, J., Nin, F., Fleury-Feith, J., Chaumette, M.T., Schaeffer, A., Bretagne, S.,
1996. Identication of intracellular stages of Cyclospora species by light micro-
scope of thick sections using hematoxylin. Hum. Pathol. 27, 11071109.
Tumwine, J.K., Kekithnwa, A., Nabukeera, N., Akiyoshi, D.E., Rich, S.M., Widmer, G.,
Feng, X., Tzipori, S., 2003. Cryptosporidium parvum in children with diarrhea in
Mulago Hospital, Kampala, Uganda. Am. J. Trop. Med. Hyg. 68, 710715.
Turgay, N., Yolasigmaz, A., Erdogan, D.D., Zeyrek, F.Y., Uner, A., 2007. Incidence of
cyclosporiasis in patients with gastrointestinal symptoms in western Turkey.
Med. Sci. Monit. 13, 3439.
Velasquez, J.N., Carnevale, S., Cabrera, M., Kuo, L., Chertcoff, A., Mariano, M., Bozzini,
J.P., Etchart, C., Argento, R., di Rissio, C., 2004. Cyclospora cayetanensis en
pacientes conSIDAy diarrea crnica. Acta Gastroenterol. Latinoam. 34, 133137.
Wang, K.-X., Li, C.P., Wang, J., Tian, Y., 2002. Cyclospora cayetanensis in Anhui China.
World J. Gastroenterol. 15, 11441148.
Wongstitwilairoong, B., Srijan, A., Serichantalergs, O., Fukuda, C.D., McDaniel, P.,
Bodhidatta, L., Mason, C.J., 2007. Intestinal parasitic infections among pre-school
children in Sangkhlaburi Thailand. Am. J. Trop. Med. Hyg. 76, 345350.
Wurtz, R.M., Kocka, F.E., Peters, C.S., Weldon-Linne, C.M., Kuritza, A., Yungbluth, P.,
1993. Clinical characteristics of seven cases of diarrhea associated with a novel
acid-fast organisms in the stool. Clin. Infect. Dis. 16, 136138.
Yai, L.E.O., Bauab, A.R., Hirschfeld, M.P.M., de Oliveira, M.L., Damaceno, J.T., 1997.
The rst two cases of Cyclospora in dogs, So Paulo Brazil. Rev. Inst. Med. Trop.
So Paulo 39, 177179.
Youseff, M.Y., Khalifa, A.M., el Azzouni, M.Z., 1998. Detection of Cryptosporidia in
different water sources in Alexadria by monoclonal antibody test and modied
ZiehlNeelsen stain. J. Egypt. Soc. Parasitol. 28, 487496.
Zerpa, R., Uchima, N., Huicho, L., 1995. Cyclospora cayetanensis associated with
watery diarrhoea in Peruvian patients. J. Trop. Med. Hyg. 98, 325329.
Zini, R.M., Santos, C.C., Almeida, I., Aparecida, Z.C., Peresi, J.T., Marques, C.C., 2004.
Atuaco do Laboratrio de Sade Pblica na elucidac o do surto de diarria
causado por Cyclospora cayetanensis no municpio de General Salgado-SP. Rev.
Inst. Adolfo Lutz 63, 116121.

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