Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-23T13:43:43.631Z Has data issue: false hasContentIssue false
  • English
  • Français

Cyclospora cayetanensis infection in humans: biological characteristics, clinical features, epidemiology, detection method and treatment

Published online by Cambridge University Press:  08 November 2019

Junqiang Li ,
Rongjun Wang ,
Yuancai Chen ,
Lihua Xiao  and
Longxian Zhang Open the ORCID record for Longxian Zhang [Opens in a new window]
Junqiang Li
Affiliation:
International Joint Research Laboratory for Zoonotic Diseases of Henan Province China, College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou450046, China Scientific Research Experiment Center & Laboratory Animal Center, Henan University of Chinese Medicine, Henan, China
Rongjun Wang
Affiliation:
International Joint Research Laboratory for Zoonotic Diseases of Henan Province China, College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou450046, China
Yuancai Chen
Affiliation:
International Joint Research Laboratory for Zoonotic Diseases of Henan Province China, College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou450046, China
Lihua Xiao*
Affiliation:
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, Guangzhou510642, China
Longxian Zhang*
Affiliation:
International Joint Research Laboratory for Zoonotic Diseases of Henan Province China, College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou450046, China
*
Author for correspondence: Longxian Zhang, E-mail: zhanglx8999@henau.edu.cn; Lihua Xiao, E-mail: lxiao1961@gmail.com
Author for correspondence: Longxian Zhang, E-mail: zhanglx8999@henau.edu.cn; Lihua Xiao, E-mail: lxiao1961@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Cyclospora cayetanensis, a coccidian parasite that causes protracted and relapsing gastroenteritis, has a short recorded history. At least 54 countries have documented C. cayetanensis infections and 13 of them have recorded cyclosporiasis outbreaks. Cyclospora cayetanensis infections are commonly reported in developing countries with low-socioeconomic levels or in endemic areas, although large outbreaks have also been documented in developed countries. The overall C. cayetanensis prevalence in humans worldwide is 3.55%. Among susceptible populations, the highest prevalence has been documented in immunocompetent individuals with diarrhea. Infections are markedly seasonal, occurring in the rainy season or summer. Cyclospora cayetanensis or Cyclospora-like organisms have also been detected in food, water, soil and some other animals. Detection methods based on oocyst morphology, staining and molecular testing have been developed. Treatment with trimethoprim–sulfamethoxazole (TMP–SMX) effectively cures C. cayetanensis infection, whereas ciprofloxacin is less effective than TMP–SMX, but is suitable for patients who cannot tolerate co-trimoxazole. Here, we review the biological characteristics, clinical features, epidemiology, detection methods and treatment of C. cayetanensis in humans, and assess some risk factors for infection with this pathogen.

Keywords

Biological characteristicclinical featureCyclospora cayetanensisdetection methodepidemiologytreatment
Type
Review Article
Information
Parasitology , Volume 147 , Issue 2 , February 2020 , pp. 160 - 170
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abanyie, F, Harvey, RR, Harris, JR, Wiegand, RE, Gaul, L, Desvignes-Kendrick, M, Irvin, K, Williams, I, Hall, RL, Herwaldt, B, Gray, EB, Qvarnstrom, Y, Wise, ME, Cantu, V, Cantey, PT, Bosch, S, DA Silva, AJ, Fields, A, Bishop, H, Wellman, A, Beal, J, Wilson, N, Fiore, AE, Tauxe, R, Lance, S, Slutsker, L, Parise, M and Multistate Cyclosporiasis Outbreak Investigation Team (2015) 2013 multistate outbreaks of Cyclospora cayetanensis infections associated with fresh produce: focus on the Texas investigations. Epidemiology & Infection 143, 3451–3458.CrossRefGoogle ScholarPubMed
Aksoy, U, Marangi, M, Papini, R, Ozkoc, S, Bayram Delibas, S and Giangaspero, A (2014) Detection of Toxoplasma gondii and Cyclospora cayetanensis in Mytilus galloprovincialis from Izmir Province coast (Turkey) by real time PCR/high-resolution melting analysis (HRM). Food Microbiology 44, 128–135.CrossRefGoogle Scholar
Alakpa, G, Fagbenro-Beyioku, AF and Clarke, SC (2002) Cyclospora cayetanensis in stools submitted to hospitals in Lagos, Nigeria. International Journal of Infectious Diseases 6, 314–318.CrossRefGoogle ScholarPubMed
Alfano-Sobsey, EM, Eberhard, ML, Seed, JR, Weber, DJ, Won, KY, Nace, EK and Moe, CL (2004) Human challenge pilot study with Cyclospora cayetanensis. Emerging Infectious Diseases 10, 726–728.CrossRefGoogle ScholarPubMed
Al-Megrin, WA (2010) Intestinal parasites infection among immunocompromised patients in Riyadh, Saudi Arabia. Pakistan Journal of Biological Sciences 13, 390–394.Google ScholarPubMed
Ashford, RW (1979) Occurrence of an undescribed coccidian in man in Papua New Guinea. Annals of Tropical Medicine and Parasitology 73, 497–500.CrossRefGoogle ScholarPubMed
Barratt, JLN, Park, S, Nascimento, FS, Hofstetter, J, Plucinski, M, Casillas, S, Bradbury, RS, Arrowood, MJ, Qvarnstrom, Y and Talundzic, E (2019) Genotyping genetically heterogeneous Cyclospora cayetanensis infections to complement epidemiological case linkage. Parasitology 31, 1–33.Google Scholar
Behera, B, Mirdha, BR, Makharia, GK, Bhatnagar, S, Dattagupta, S and Samantaray, JC (2008) Parasites in patients with malabsorption syndrome: a clinical study in children and adults. Digestive Diseases and Sciences 53, 672–679.CrossRefGoogle ScholarPubMed
Bern, C, Hernandez, B, Lopez, MB, Arrowood, MJ, de Mejia, MA, de Merida, AM, Hightower, AW, Venczel, L, Herwaldt, BL and Klein, RE (1999) Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerging Infectious Diseases 5, 766–774.CrossRefGoogle ScholarPubMed
Bhandari, D, Tandukar, S, Parajuli, H, Thapa, P, Chaudhary, P, Shrestha, D, Shah, PK, Sherchan, JB and Sherchand, JB (2015) Cyclospora infection among school children in Kathmandu, Nepal: prevalence and associated risk factors. Tropical Medicine and Health 43, 211–216.CrossRefGoogle ScholarPubMed
Bhattachan, B, Sherchand, JB, Tandukar, S, Dhoubhadel, BG, Gauchan, L and Rai, G (2017) Detection of Cryptosporidium parvum and Cyclospora cayetanensis infections among people living in a slum area in Kathmandu valley, Nepal. BMC Research Notes 10, 464.CrossRefGoogle Scholar
Bilung, LM, Tahar, AS, Yunos, NE, Apun, K, Lim, YA, Nillian, E and Hashim, HF (2017) Detection of Cryptosporidium and Cyclospora oocysts from environmental water for drinking and recreational activities in Sarawak, Malaysia. BioMed Research International 2017, 4636420.CrossRefGoogle ScholarPubMed
Brennan, MK, MacPherson, DW, Palmer, J and Keystone, JS (1996) Cyclosporiasis: a new cause of diarrhea. Canadian Medical Association Journal 155, 1293–1296.Google ScholarPubMed
Brown, GH and Rotschafer, JC (1999) Cyclospora: review of an emerging parasite. Pharmacotherapy 19, 70–75.CrossRefGoogle ScholarPubMed
Burstein Alva, S (2005) Cyclosporosis: an emergent parasitosis. (I) Clinical and epidemiological aspects. Revista de Gastroenterologia del Peru 25, 328–335.Google ScholarPubMed
Casemore, DP (1994) Cyclospora: another ‘new’ pathogen. Journal of Medical Microbiology 41, 217–219.CrossRefGoogle ScholarPubMed
Casillas, SM, Bennett, C and Straily, A (2018) Notes from the field: multiple cyclosporiasis outbreaks – United States, 2018. American Journal of Transplantation 18, 3072–3074.CrossRefGoogle Scholar
Cazorla, D, Acosta, ME, Acosta, ME and Morales, P (2012) Clinical and epidemiological study of intestinal coccidioses in a rural population of a semiarid region from Falcon state, Venezuela. Journal of Clinical Investigation 53, 273–288.Google Scholar
Chacín-Bonilla, L (2008) Transmission of Cyclospora cayetanensis infection: a review focusing on soil-borne cyclosporiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 215–216.CrossRefGoogle ScholarPubMed
Chacín-Bonilla, L, Barrios, F and Sanchez, Y (2007) Epidemiology of Cyclospora cayetanensis infection in San Carlos Island, Venezuela: strong association between socio-economic status and infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 1018–1024.CrossRefGoogle Scholar
Chu, DM, Sherchand, JB, Cross, JH and Orlandi, PA (2004) Detection of Cyclospora cayetanensis in animal fecal isolates from Nepal using an FTA filter-base polymerase chain reaction method. American Journal of Tropical Medicine and Hygiene 71, 373–379.CrossRefGoogle ScholarPubMed
Cinar, HN, Gopinath, G, Jarvis, K and Murphy, HR (2015) The complete mitochondrial genome of the foodborne parasitic pathogen Cyclospora cayetanensis. PLoS One 10, e0128645.CrossRefGoogle ScholarPubMed
Clarke, SC and McIntyre, M (1996) Modified detergent Ziehl-Neelsen technique for the staining of Cyclospora cayetanensis. Journal of Clinical Pathology 49, 511–512.CrossRefGoogle ScholarPubMed
Connor, BA, Shlim, DR, Scholes, JV, Rayburn, JL, Reidy, J and Rajah, R (1993) Pathologic changes in the small bowel in 9 patients with diarrhea associated with a coccidia-like body. Annals of Internal Medicine 119, 377–382.CrossRefGoogle Scholar
Connor, BA, Reidy, J and Soave, R (1999) Cyclosporiasis: clinical and histopathologic correlates. Clinical Infectious Diseases 28, 1216–1222.CrossRefGoogle ScholarPubMed
Connor, BA, Johnson, EJ and Soave, R (2001) Reiter syndrome following protracted symptoms of Cyclospora infection. Emerging Infectious Diseases 7, 453–454.CrossRefGoogle ScholarPubMed
Cordón, GP, Prados, AH, Romero, D, Sánchez Moreno, M, Pontes, A, Osuna, A, Rosales, MJ (2008) Intestinal parasitism in the animals of the zoological garden ‘Peña Escrita’ (Almuñecar, Spain). Veterinary Parasitology 156, 302–309.CrossRefGoogle Scholar
Di Genova, BM and Tonelli, RR (2016) Infection strategies of intestinal parasite pathogens and host cell responses. Frontiers in Microbiology 7, 256.CrossRefGoogle ScholarPubMed
Di Gliullo, AB, Cribari, MS, Bava, AJ, Cicconetti, JS and Collazos, R (2000) Cyclospora cayetanensis in sputum and stool samples. Revista do Instituto de Medicina Tropical de Sao Paulo 42, 115–117.CrossRefGoogle ScholarPubMed
Diaz, E, Mondragon, J, Ramirez, E and Bernal, R (2003) Epidemiology and control of intestinal parasites with nitazoxanide in children in Mexico. American Journal of Tropical Medicine and Hygiene 68, 384–385.CrossRefGoogle ScholarPubMed
Dillingham, RA, Pinkerton, R, Leger, P, Severe, P, Guerrant, RL, Pape, JW and Fitzgerald, DW (2009) High early mortality in patients with chronic acquired immunodeficiency syndrome diarrhea initiating antiretroviral therapy in Haiti: a case-control study. American Journal of Tropical Medicine and Hygiene 80, 1060–1064.CrossRefGoogle ScholarPubMed
Dixon, BR, Bussey, JM, Parrington, LJ and Parenteau, M (2005) Detection of Cyclospora cayetanensis oocysts in human fecal specimens by flow cytometry. Journal of Clinical Microbiology 43, 2375–2379.CrossRefGoogle ScholarPubMed
Eberhard, ML, da Silva, AJ, Lilley, BG and Pieniazek, NJ (1999) Morphologic and molecular characterization of new Cyclospora species from Ethiopian monkeys: C. cercopitheci sp.n., C. colobi sp.n., and C. papionis sp.n. Emerging Infectious Diseases 5, 651–658.CrossRefGoogle Scholar
Eberhard, ML, Ortega, YR, Hanes, DE, Nace, EK, Do, RQ, Robl, MG, Won, KY, Gavidia, C, Sass, NL, Mansfield, K, Gozalo, A, Griffiths, J, Gilman, R, Sterling, CR and Arrowood, MJ (2000) Attempts to establish experimental Cyclospora cayetanensis infection in laboratory animals. Journal of Parasitology 86, 577–582.CrossRefGoogle ScholarPubMed
Eberhard, ML, Njenga, MN, DaSilva, AJ, Owino, D, Nace, EK, Won, KY and Mwenda, JM (2001) A survey for Cyclospora spp. in Kenyan primates, with some notes on its biology. Journal of Parasitology 87, 1394–1397.CrossRefGoogle ScholarPubMed
Erdogan, DD, Kurt, O, Mandiracioglu, A, Ahmet, U, Mucide, A and Hande, D (2012) Prevalence and associated factors of Cryptosporidium spp. and Cyclospora cayetanensis in Izmir province, Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 18, A105–A110.Google Scholar
Escobedo, AA, Almirall, P, Alfonso, M, Cimerman, S, Rey, S and Terry, SL (2009) Treatment of intestinal protozoan infections in children. Archives of Disease in Childhood 94, 478–482.CrossRefGoogle ScholarPubMed
Fletcher, SM, Stark, D, Harkness, J and Ellis, J (2012) Enteric protozoa in the developed world: a public health perspective. Clinical Microbiology Reviews 25, 420–449.CrossRefGoogle ScholarPubMed
Fryauff, DJ, Krippner, R, Prodjodipuro, P, Ewald, C, Kawengian, S, Pegelow, K, Yun, T, von Heydwolff-Wehnert, C, Oyofo, B and Gross, R (1999) Cyclospora cayetanensis among expatriate and indigenous populations of West Java, Indonesia. Emerging Infectious Diseases 5, 585–588.CrossRefGoogle ScholarPubMed
Ghozzi, K, Marangi, M, Papini, R, Lahmar, I, Challouf, R, Houas, N, Ben Dhiab, R, Normanno, G, Babba, H and Giangaspero, A (2017) First report of Tunisian coastal water contamination by protozoan parasites using mollusk bivalves as biological indicators. Marine Pollution Bulletin 117, 197–202.CrossRefGoogle ScholarPubMed
Giangaspero, A and Gasser, RB (2019) Human cyclosporiasis. The Lancet Infectious Diseases 19, e226–e236.CrossRefGoogle ScholarPubMed
Giangaspero, A, Marangi, M, Koehler, AV, Papini, R, Normanno, G, Lacasella, V, Lonigro, A and Gasser, RB (2015) Molecular detection of Cyclospora in water, soil, vegetables and humans in southern Italy signals a need for improved monitoring by health authorities. International Journal of Food Microbiology 211, 95–100.CrossRefGoogle ScholarPubMed
Goldberg, E and Bishara, J (2012) Contemporary unconventional clinical use of co-trimoxazole. Clinical Microbiology and Infection 18, 8–17.CrossRefGoogle ScholarPubMed
Gonçalves, EM, Uemura, IH, Castilho, VL and Corbett, CE (2005) Retrospective study of the occurrence of Cyclospora cayetanensis at Clinical Hospital of the University of São Paulo Medical School, SP. Revista da Sociedade Brasileira de Medicina Tropical 38, 326–330.CrossRefGoogle Scholar
Graczyk, TK, Ortega, YR and Conn, DB (1998) Recovery of waterborne oocysts of Cyclospora cayetanensis by Asian freshwater clams (Corbicula fluminea). American Journal of Tropical Medicine and Hygiene 59, 928–932.CrossRefGoogle Scholar
Guo, Y, Roellig, DM, Li, N, Tang, K, Frace, M, Ortega, Y, Arrowood, MJ, Feng, Y, Qvarnstrom, Y, Wang, L, Moss, DM, Zhang, L and Xiao, L (2016) Multilocus sequence typing tool for Cyclospora cayetanensis. Emerging Infectious Diseases 22, 1464–1467.CrossRefGoogle ScholarPubMed
Guo, Y, Wang, Y, Wang, X, Zhang, L, Ortega, Y and Feng, Y (2019) Mitochondrial genome sequence variation as a useful marker for assessing genetic heterogeneity among Cyclospora cayetanensis isolates and source-tracking. Parasites & Vectors 12, 47.CrossRefGoogle ScholarPubMed
Helenbrook, WD, Wade, SE, Shields, WM, Stehman, SV and Whipps, CM (2015) Gastrointestinal parasites of Ecuadorian Mantled Howler Monkeys (Alouatta palliata aequatorialis) based on fecal analysis. Journal of Parasitology 101, 341–350.CrossRefGoogle ScholarPubMed
Herwaldt, BL (2000) Cyclospora cayetanensis: a review, focusing on the outbreaks of cyclosporiasis in the 1990s. Clinical Infectious Diseases 31, 1040–1057.CrossRefGoogle ScholarPubMed
Herwaldt, BL and Ackers, ML (1997) An outbreak in 1996 of cyclosporiasis associated with imported raspberries. The Cyclospora Working Group. The New England Journal of Medicine 336, 1548–1556.CrossRefGoogle ScholarPubMed
Hoge, CW, Shlim, DR, Ghimire, M, Rabold, JG, Pandey, P, Walch, A, Rajah, R, Gaudio, P and Echeverria, P (1995) Placebo-controlled trial of co-trimoxazole for Cyclospora infections among travellers and foreign residents in Nepal. The Lancet 345, 691–693.CrossRefGoogle ScholarPubMed
Huang, P, Weber, JT, Sosin, DM, Griffin, PM, Long, EG, Murphy, JJ, Kocka, F, Peters, C and Kallick, C (1995) The first reported outbreak of diarrheal illness associated with Cyclospora in the United States. Annals of Internal Medicine 123, 409–414.CrossRefGoogle ScholarPubMed
Hussein, EM (2007) Molecular identification of Cycospora spp. using multiplex PCR from diarrheic children compared to others conventional methods. Journal of the Egyptian Society of Parasitology 37, 585–598.Google ScholarPubMed
Hussein, EM, Abdul-Manaem, AH and El-Attary, SL (2005) Cyclospora cayetanensis oocysts in sputum of a patient with active pulmonary tuberculosis, case report in Ismailia, Egypt. Journal of the Egyptian Society of Parasitology 35, 787–793.Google ScholarPubMed
Jeevitha, D, Pushparaj, SP and Kanchana, M (2014) Comparative study of the prevalence of intestinal parasites in low socioeconomic areas from South Chennai, India. Journal of Parasitology Research 2014, 630968.Google Scholar
Jiang, Y, Yuan, Z, Zang, G, Li, D, Wang, Y, Zhang, Y, Liu, H, Cao, J and Shen, Y (2018) Cyclospora cayetanensis infections among diarrheal outpatients in Shanghai: a retrospective case study. Frontiers of Medicine 12, 98–103.CrossRefGoogle ScholarPubMed
Jiménez-González, GB, Martínez-Gordillo, MN, Caballero-Salazar, S, Peralta-Abarca, GE, Cárdenas-Cardoz, R, Arzate-Barbosa, P and Ponce-Macotela, M (2012) Microsporidia in pediatric patients with leukemia or lymphoma. Revista de Investigacio Clinica 64, 25–31.Google ScholarPubMed
Kaminsky, RG, Lagos, J, Raudales Santos, G and Urrutia, S (2016) Marked seasonality of Cyclospora cayetanensis infections: ten-year observation of hospital cases, Honduras. BMC Infectious Diseases 16, 66.CrossRefGoogle ScholarPubMed
Karaman, U, Daldal, N, Ozer, A, Enginyurt, O and Erturk, O (2015) Epidemiology of Cyclospora species in humans in Malatya Province in Turkey. Jundishapur Journal of Microbiology 8, e18661.CrossRefGoogle ScholarPubMed
Kimura, K, Rai, SK, Rai, G, Insisiengmay, S, Kawabata, M, Karanis, P and Uga, S (2005) Study on Cyclospora cayetanensis associated with diarrheal disease in Nepal and Loa PDR. Southeast Asian Journal of Tropical Medicine and Public Health 36, 1371–1376.Google Scholar
Kłudkowska, M, Pielok, Ł, Frąckowiak, K and Paul, M (2017) Intestinal coccidian parasites as an underestimated cause of travellers' diarrhoea in Polish immunocompetent patients. Acta Parasitologica 62, 630–638.CrossRefGoogle ScholarPubMed
Lainson, R (2005) The genus Cyclospora (apicomplexa: Eimeriidae), with a description of Cyclospora schneideri n. sp. in the snake Anilius scytale scytale (Aniliidae) from Amazonian Brazil – a review. Memórias do Instituto Oswaldo Cruz 100, 103–110.CrossRefGoogle ScholarPubMed
Lalonde, LF and Gajadhar, AA (2008) Highly sensitive and specific PCR assay for reliable detection of Cyclospora cayetanensis oocysts. Applied and Environmental Microbiology 74, 4354–4358.CrossRefGoogle ScholarPubMed
Lalonde, LF and Gajadhar, AA (2011) Detection and differentiation of coccidian oocysts by real-time PCR and melting curve analysis. Journal of Parasitology 97, 725–730.CrossRefGoogle ScholarPubMed
Li, G, Xiao, S, Zhou, R, Li, W and Wadeh, H (2007) Molecular characterization of Cyclospora-like organism from dairy cattle. Parasitology Research 100, 955–961.CrossRefGoogle ScholarPubMed
Li, N, Ye, J, Arrowood, MJ, Ma, J, Wang, L, Xu, H, Feng, Y and Xiao, L (2015) Identification and morphologic and molecular characterization of Cyclospora macacae n. sp. from rhesus monkeys in China. Parasitology Research 114, 1811–1816.CrossRefGoogle Scholar
Li, J, Chang, Y, Shi, KE, Wang, R, Fu, K, Li, S, Xu, J, Jia, L, Guo, Z and Zhang, L (2017) Multilocus sequence typing and clonal population genetic structure of Cyclospora cayetanensis in humans. Parasitology 144, 1890–1897.CrossRefGoogle ScholarPubMed
Liu, S, Wang, L, Zheng, H, Xu, Z, Roellig, DM, Li, N, Frace, MA, Tang, K, Arrowood, MJ, Moss, DM, Zhang, L, Feng, Y and Xiao, L (2016) Comparative genomics reveals Cyclospora cayetanensis possesses coccidia-like metabolism and invasion components but unique surface antigens. BMC Genomics 17, 316.CrossRefGoogle ScholarPubMed
Madico, G, McDonald, J, Gilman, RH, Cabrera, L and Sterling, CR (1997) Epidemiology and treatment of Cyclospora cayetanensis infection in Peruvian children. Clinical Infectious Diseases 24, 977–981.CrossRefGoogle ScholarPubMed
Mansfield, LS and Gajadhar, AA (2004) Cyclospora cayetanensis, a food- and waterborne coccidian parasite. Veterinary Parasitology 126, 73–90.CrossRefGoogle ScholarPubMed
McAllister, CT, Motriuk-Smith, D and Kerr, CM (2018) Three new coccidians (Cyclospora, Eimeria) from eastern moles, Scalopus aquaticus (Linnaeus) (Mammalia: Soricomorpha: Talpidae) from Arkansas, USA. Systematic Parasitology 95, 271–279.CrossRefGoogle ScholarPubMed
Murphy, HR, Cinar, HN, Gopinath, G, Noe, KE, Chatman, LD, Miranda, NE, Wetherington, JH, Neal-McKinney, J, Pires, GS, Sachs, E, Stanya, KJ, Johnson, CL, Nascimento, FS, Santin, M, Molokin, A, Samadpour, M, Janagama, H, Kahler, A, Miller, C and da Silva, AJ (2018) Interlaboratory validation of an improved method for detection of Cyclospora cayetanensis in produce using a real-time PCR assay. Food Microbiology 69, 170–178.CrossRefGoogle ScholarPubMed
Nascimento, FS, Barta, JR, Whale, J, Hofstetter, JN, Casillas, S, Barratt, J, Talundzic, E, Arrowood, MJ and Qvarnstrom, Y (2019) Mitochondrial junction region as genotyping marker for Cyclospora cayetanensis. Emerging Infectious Diseases 25, 1314–1319.CrossRefGoogle ScholarPubMed
Nundy, S, Gilman, RH, Xiao, L, Cabrera, L, Cama, R, Ortega, YR, Kahn, G and Cama, VA (2011) Wealth and its associations with enteric parasitic infections in a low-income community in Peru: use of principal component analysis. American Journal of Tropical Medicine and Hygiene 84, 38–42.CrossRefGoogle Scholar
Ogedengbe, ME, Qvarnstrom, Y, da Silva, AJ, Arrowood, MJ and Barta, JR (2015) A linear mitochondrial genome of Cyclospora cayetanensis (Eimeriidae, Eucoccidiorida, Coccidiasina, Apicomplexa) suggests the ancestral start position within mitochondrial genomes of eimeriid coccidia. International Journal for Parasitology 45, 361–365.CrossRefGoogle ScholarPubMed
Olivier, C, van de Pas, S, Lepp, PW, Yoder, K and Relman, DA (2001) Sequence variability in the first internal transcribed spacer region within and among Cyclospora species is consistent with polyparasitism. International Journal for Parasitology 31, 1475–1487.CrossRefGoogle ScholarPubMed
Orozco-Mosqueda, GE, Martínez-Loya, OA and Ortega, YR (2014) Cyclospora cayetanensis in a pediatric hospital in Morelia, México. American Journal of Tropical Medicine and Hygiene 91, 537–540.CrossRefGoogle Scholar
Ortega, YR and Sanchez, R (2010) Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clinical Microbiology Reviews 23, 218–234.CrossRefGoogle ScholarPubMed
Ortega, YR, Nagle, R, Gilman, RH, Watanabe, J, Miyagui, J, Quispe, H, Kanagusuku, P, Roxas, C and Sterling, CR (1997) Pathologic and clinical findings in patients with cyclosporiasis and a description of intracellular parasite life-cycle stages. The Journal of Infectious Diseases 176, 1584–1589.CrossRefGoogle Scholar
Ozdamar, M, Hakko, E and Turkoglu, S (2010) High occurrence of cyclosporiasis in Istanbul, Turkey, during a dry and warm summer. Parasites & Vectors 3, 39.CrossRefGoogle ScholarPubMed
Pandey, P, Bodhidatta, L, Lewis, M, Murphy, H, Shlim, DR, Cave, W, Rajah, R, Springer, M, Batchelor, T, Sornsakrin, S and Mason, CJ (2011) Travelers' diarrhea in Nepal: an update on the pathogens and antibiotic resistance. Journal of Travel Medicine 18, 102–108.CrossRefGoogle ScholarPubMed
Pape, JW, Verdier, RI, Boncy, M, Boncy, J and Johnson, WD Jr (1994) Cyclospora infection in adults infected with HIV. Clinical manifestations, treatment and prophylaxis. Annals of Internal Medicine 121, 654–657.CrossRefGoogle ScholarPubMed
Parija, SC, Shivaprakash, MR and Jayakeerthi, SR (2003) Evaluation of lacto-phenol cotton blue (LPCB) for detection of Cryptosporidium, Cyclospora and Isospora in the wet mount preparation of stool. Acta Tropica 85, 349–354.CrossRefGoogle ScholarPubMed
Quintero-Betancourt, W, Peele, ER and Rose, JB (2002) Cryptosporidium parvum and Cyclospora cayetanensis: a review of laboratory methods for detection of these waterborne parasites. Journal of Microbiological Methods 49, 209–224.CrossRefGoogle ScholarPubMed
Relman, DA, Schmidt, TM, Gajadhar, A, Sogin, M, Cross, J, Yoder, K, Sethabutr, O and Echeverria, P (1996) Molecular phylogenetic analysis of Cyclospora, the human intestinal pathogen, suggests that it is closely related to Eimeria species. The Journal of Infectious Diseases 173, 440–445.Google ScholarPubMed
Riner, DK, Nichols, T, Lucas, SY, Mullin, AS, Cross, JH and Lindquist, HD (2010) Intragenomic sequence variation of the ITS-1 region within a single flow-cytometry-counted Cyclospora cayetanensis oocysts. Journal of Parasitology 96, 914–919.CrossRefGoogle ScholarPubMed
Robertson, LJ, Gjerde, B and Campbell, AT (2000) Isolation of Cyclospora oocysts from fruits and vegetables using lectin-coated paramagnetic beads. Journal of Food Protection 63, 1410–1414.CrossRefGoogle ScholarPubMed
Rose, JB and Slifko, TR (1999) Giardia, Cryptosporidium, and Cyclospora and their impact on foods: a review. Journal of Food Protection 62, 1059–1070.CrossRefGoogle ScholarPubMed
Ryan, U, Paparini, A and Oskam, C (2017) New technologies for detection of enteric parasites. Trends in Parasitology 33, 532–546.CrossRefGoogle ScholarPubMed
Sherchand, JB and Cross, JH (2001) Emerging pathogen Cyclospora cayetanensis infection in Nepal. Southeast Asian Journal of Tropical Medicine And Public Health 32(suppl. 2), 143–150.Google ScholarPubMed
Shields, JM and Olson, BH (2003) Cyclospora cayetanensis: a review of an emerging parasitic coccidian. International Journal for Parasitology 33, 371–391.CrossRefGoogle ScholarPubMed
Shields, JM, Lee, MM and Murphy, HR (2012) Use of a common laboratory glassware detergent improves recovery of Cryptosporidium parvum and Cyclospora cayetanensis from lettuce, herbs and raspberries. International Journal of Food Microbiology 153, 123–128.CrossRefGoogle ScholarPubMed
Shlim, DR, Cohen, MT, Eaton, M, Rajah, R, Long, EG and Ungar, BL (1991) An alga-like organism associated with an outbreak of prolonged diarrhea among foreigners in Nepal. American Journal of Tropical Medicine and Hygiene 45, 383–389.CrossRefGoogle ScholarPubMed
Sifuentes-Osornio, J, Porras-Cortés, G, Bendall, RP, Morales-Villarreal, F, Reyes-Terán, G and Ruiz-Palacios, GM (1995) Cyclospora cayetanensis infection in patients with and without AIDS: biliary disease as another clinical manifestation. Clinical Infectious Diseases 21, 1092–1097.CrossRefGoogle ScholarPubMed
Smith, HV, Paton, CA, Mitambo, MM and Girdwood, RW (1997) Sporulation of Cyclospora sp. oocysts. Applied and Environmental Microbiology 63, 1631–1632.CrossRefGoogle ScholarPubMed
Steele, M, Unger, S and Odumeru, J (2003) Sensitivity of PCR detection of Cyclospora cayetanensis in raspberries, basil, and mesclun lettuce. Journal of Microbiological Methods 54, 277–280.CrossRefGoogle ScholarPubMed
Sturbaum, GD, Ortega, YR, Gilman, RH, Sterling, CR, Cabrera, L and Klein, DA (1998) Detection of Cyclospora cayetanensis in wastewater. Applied and Environmental Microbiology 64, 2284–2286.CrossRefGoogle ScholarPubMed
Sulaiman, IM, Torres, P, Simpson, S, Kerdahi, K and Ortega, Y (2013) Sequence characterization of heat shock protein gene of Cyclospora cayetanensis isolates from Nepal, Mexico, and Peru. Journal of Parasitology 99, 379–382.CrossRefGoogle ScholarPubMed
Sulaiman, IM, Ortega, Y, Simpson, S and Kerdahi, K (2014) Genetic characterization of human-pathogenic Cyclospora cayetanensis parasites from three endemic regions at the 18S ribosomal RNA locus. Infection Genetics and Evolution 22, 229–234.CrossRefGoogle ScholarPubMed
Sun, T, Ilardi, CF, Asnis, D, Bresciani, AR, Goldenberg, S, Roberts, B and Teichberg, S (1996) Light and electron microscopic identification of Cyclospora species in the small intestine. Evidence of the presence of asexual life cycle in human host. American Journal of Clinical Pathology 105, 216–220.CrossRefGoogle ScholarPubMed
Tang, K, Guo, Y, Zhang, L, Rowe, LA, Roellig, DM, Frace, MA, Li, N, Liu, S, Feng, Y and Xiao, L (2015) Genetic similarities between Cyclospora cayetanensis and cecum-infecting avian Eimeria spp. in apicoplast and mitochondrial genomes. Parasites & Vectors 8, 358.CrossRefGoogle ScholarPubMed
Tram, NT, Hoang, LM, Cam, PD, Chung, PT, Fyfe, MW, Isaac-Renton, JL and Ong, CS (2008) Cyclospora spp. in herbs and water samples collected from markets and farms in Hanoi, Vietnam. Tropical Medicine & International Health 13, 1415–1420.CrossRefGoogle ScholarPubMed
Turgay, N, Yolasigmaz, A, Erdogan, DD, Zeyrek, FY and Uner, A (2007) Incidence of cyclosporiasis in patients with gastrointestinal symptoms in western Turkey. Medical Science Monitor 13, CR34–CR39.Google ScholarPubMed
Varma, M, Hester, JD, Schaefer, FW III, Ware, MW and Lindquist, HD (2003) Detection of Cyclospora cayetanensis using a quantitative real-time PCR assay. Journal of Microbiological Methods 53, 27–36.CrossRefGoogle ScholarPubMed
Verdier, RI, Fitzgerald, DW, Johnson, WD Jr and Pape, JW (2000) Trimethoprim-sulfamethoxazole compared with ciprofloxacin for treatment and prophylaxis of Isospora belli and Cyclospora cayetanensis infection in HIV-infected patients. A randomized, controlled trial. Annals of Internal Medicine 132, 885–888.CrossRefGoogle ScholarPubMed
Verweij, JJ, Laeijendecker, D, Brienen, EA, van Lieshout, L and Polderman, AM (2003) Detection of Cyclospora cayetanensis in travellers returning from the tropics and subtropics using microscopy and real-time PCR. International Journal of Medical Microbiology 293, 199–202.CrossRefGoogle ScholarPubMed
Visvesvara, GS, Moura, H, Kovacs-Nace, E, Wallace, S and Eberhard, ML (1997) Uniform staining of Cyclospora oocysts in fecal smears by a modified safranin technique with microwave heating. Journal of Clinical Microbiology 35, 730–733.CrossRefGoogle ScholarPubMed
Wiwanitkit, V (2006) Intestinal parasite infestation in HIV infected patients. Current HIV Research 4, 87–96.CrossRefGoogle ScholarPubMed
Zar, FA, El-Bayoumi, E and Yungbluth, MM (2001) Histologic proof of acalculous cholecystitis due to Cyclospora cayetanensis. Clinical Infectious Diseases 33, E140–E141.CrossRefGoogle ScholarPubMed
Zhou, Y, Lv, B, Wang, Q, Wang, R, Jian, F, Zhang, L, Ning, C, Fu, K, Wang, Y, Qi, M, Yao, H, Zhao, J, Zhang, X, Sun, Y, Shi, K, Arrowood, MJ and Xiao, L (2011) Prevalence and molecular characterization of Cyclospora cayetanensis, Henan, China. Emerging Infectious Diseases 17, 1887–1890.CrossRefGoogle ScholarPubMed
Zimmer, SM, Schuetz, AN and Franco-Paredes, C (2007) Efficacy of nitazoxanide for cyclosporiasis in patients with sulfa allergy. Clinical Infectious Diseases 44, 466–467.CrossRefGoogle ScholarPubMed
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material

Download Li et al. supplementary material(File)
File 1.3 MB