Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 5, 2017

Intestinal coccidian parasites as an underestimated cause of travellers’ diarrhoea in Polish immunocompetent patients

Matylda Kłudkowska, Łukasz Pielok, Krystyna Frąckowiak and Małgorzata Paul
From the journal Acta Parasitologica


Intestinal coccidian parasites are intracellular protozoa most frequently transmitted during food-borne and water-borne infections. This group of parasites is responsible for acute diarrhoeal illnesses especially among immunocompromised patients. However, they are more frequently detected in immunocompetent individuals including travellers, and they should also be considered as important etiologic factors of travellers’ diarrhoea. We examined 221 immunocompetent patients hospitalized due to acute or chronic diarrhoea and other gastrointestinal symptoms after returning from international journeys to hot climates. A basic microscopical examination and acid – fast staining of stool samples was performed. Each patient was also a part of the epidemiological investigation to define potential risk factors of tropical gastrointestinal infections. Intestinal coccidiosis was confirmed in 12 out of 221 successively hospitalized patients (5.4%). The most common coccidian parasite was Cryptosporidium spp., detected in nine Polish travellers (4.1%). Cyclospora spp. was diagnosed in three cases (1.4%), including two mixed infections with Cryptosporidium spp., and Cystoisospora spp. in two other cases (0.9%). The study has revealed that intestinal coccidian parasites are a significant threat to immunocompetent travellers and should be always considered in the differential diagnosis of gastrointestinal disorders. Therefore, it is necessary to perform specialized diagnostic methods for the detection of Cryptosporidium spp., Cystoisospora spp., and Cyclospora spp. oocysts in reference parasitology laboratories. Clinical observations demonstrated simultaneously an insufficient level of knowledge in Polish tourists concerning the main risk factors of intestinal parasitic diseases during international travels, particularly to developing countries with lower economic and sanitary conditions.


Agnamey P., Djeddi D., Oukachbi Z., Totet A., Raccurt C.P. 2010. Cryptosporidium hominis and Isospora belli diarrhea in travelers returning from West Africa. Journal of Travel Medicine, 17, 141–142. 10.1111/j.1708-8305.2010.00393.xSearch in Google Scholar

Ashford R.W. 1979. Occurrence of an undescribed coccidian in man in Papua New Guinea. Annals of Tropical Medicine and Parasitology, 73, 497–500. 10.1080/00034983.1979.11687291Search in Google Scholar

Bednarska M., Bajer A., Welc-Falęciak R., Pawełas A. 2015. Cyclospora cayetanensis infection in transplant traveller: a case report of outbreak. Parasites & Vectors, 8, 411. 10.1186/s13071-015-1026-8Search in Google Scholar

Betancourt W.Q., Duarte D.C., Vásquez R.C., Gurian P.L. 2014. Cryptosporidium and Giardia in tropical recreational marine waters contaminated with domestic sewage: estimation of bathing-associated disease risks. Marine Pollution Bulletin, 85, 268–273. 10.1016/j.marpolbul.2014.05.059Search in Google Scholar

Bohaychuk V.M., Bradbury R.W., Dimock R., Fehr M., Gensler G.E., King R.K., et al. 2009. A microbiological survey of selected Alberta-grown fresh produce from farmers’ markets in Alberta, Canada. Journal of Food Protection, 72, 415–420. in Google Scholar

Briggs A.D., Boxall N.S., Van Santen D., Chalmers R.M., McCarthy N.D. 2014. Approaches to the detection of very small, common, and easily missed outbreaks that together contribute substantially to human Cryptosporidium infection. Epidemiology & Infection, 142, 1869–1876. 10.1017/S0950268814000673Search in Google Scholar

Certad G., Arenas-Pinto A., Pocaterra L., Ferrara G., Castro J., Bello A., Núñez L. 2003. Isosporiasis in Venezuelan adults infected with human immunodeficiency virus: clinical characterization. American Journal of Tropical Medicine and Hygiene, 69, 217–222. in Google Scholar

Chandra V., Torres M., Y.R. Ortega. 2014. Efficacy of wash solutions in recovering Cyclospora cayetanensis, Cryptosporidium parvum, and Toxoplasma gondii from basil. Journal of Food Protection, 77, 1348–1354. 10.4315/0362-028X.JFP-13-381Search in Google Scholar

Checkley W., White Jr. A.C., Jaganath D., Arrowood M.J., Chalmers R.M., Chen X.M., et al. 2015. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infectious Diseases, 15, 85–94. 10.1016/S1473-3099(14)70772-8Search in Google Scholar

Dash M., Padhi S., Panda P., Parida B. 2013. Intestinal Protozoans in Adults with Diarrhea. North American Journal of Medical Sciences, 5, 707–712. 10.4103/1947-2714.123261Search in Google Scholar PubMed PubMed Central

Din N.U., Torka P., Hutchison R.E., Riddell S.W., Wright J., Gajra A. 2012. Severe Isospora (Cystoisospora) belli Diarrhea Preceding the Diagnosis of Human T-Cell-Leukemia-Virus-1-Associated T-Cell Lymphoma. Case Reports in Infectious Diseases, vol. 2012, Article ID 640104. 10.1155/2012/640104Search in Google Scholar PubMed PubMed Central

DuPont HL. 2009. Systematic review: the epidemiology and clinical features of travellers’ diarrhoea. Alimentary Pharmacology & Therapeutics, 30, 187–196. 10.1111/j.1365-2036.2009.04028.xSearch in Google Scholar PubMed

Eraky M.A., El-Hamshary A.M.-S., Hamadto H.H., Abdallah K.F., Abdel-Hafed W.M., Abdel-Had S. 2014. Predominance of Cryptosporidium parvum genotype among diarrheic children from Egypt as an indicator for zoonotic transmission. Acta Parasitologica, 60, 26–34. 10.1515/ap-2015-0004Search in Google Scholar PubMed

Godiwala T., Yaeger R. 1987. Isospora and traveler’s diarrhea. Annals of Internal Medicine, 106, 908–909. 10.7326/0003-4819-106-6-908_2Search in Google Scholar PubMed

Gupta A.K. 2011. Intestinal coccidian parasitic infections in rural community in and around Loni, Maharashtra. Journal of Parasitic Diseases, 35, 54–56. 10.1007/s12639-011-0030-y.Search in Google Scholar PubMed PubMed Central

Herwaldt B.L. 2000. Cyclospora cayetanensis: a review, focusing on the outbreaks of cyclosporiasis in the 1990s. Clinical Infectious Diseases, 31, 1040–1057. 10.1086/314051Search in Google Scholar PubMed

Karanis P., Kourenti C., Smith H. 2007. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. Journal of Water and Health, 5, 1–38. in Google Scholar

Kasper M.R., Lescano A.G., Lucas C., Gilles D., Biese B.J., Stolovitz G., Reaves E.J.. 2012. Diarrhea Outbreak during U.S. Military Training in El Salvador. PLoS One, 7, e40404. 10.1371/journal.pone.0040404Search in Google Scholar PubMed PubMed Central

Kendall M.E., Crim S., Fullerton K., Han P.V., Cronquist A.B., Shiferaw B., et al. 2012. Travel-associated enteric infections diagnosed after return to the United States, Foodborne Diseases Active Surveillance Network (FoodNet), 2004-2009. Clinical Infectious Diseases, 54, 480–487. 10.1093/cid/cis052Search in Google Scholar PubMed

Kim M.J., Kim W.H., Jung H.C., Chai J.W., Chai J.Y. 2013. Isospora belli Infection with Chronic Diarrhea in an Alcoholic Patient. Korean Journal of Parasitology, 51, 207–212. 10.3347/kjp.2013.51.2.207Search in Google Scholar PubMed PubMed Central

Koru O., Araz E., Inci A., Tanyuksel M. 2006. Co-infection of Giardia intestinalis and Cyclospora cayetanensis in an immunocompetent patient with prolonged diarrhea: case report. Journal of Microbiology, 44, 360–362Search in Google Scholar

Legua P., Seas C. 2013. Cystoisospora and cyclospora. Current Opinion in Infectious Diseases, 26, 479–483. 10.1097/01.qco.0000433320.90241.60Search in Google Scholar PubMed

Malik A., Kulaar J., Shukla R., Dutta V. 2013. Triple protozoal enteropathy of the small intestine in an immunocompromised male: A rare histopathology report. Indian Journal of Sexually Transmitted Diseases, 34, 119–122. 10.4103/0253-7184.120548Search in Google Scholar PubMed PubMed Central

Mallet V. 2015. The Ganges: holy, deadly river. Financial Times, in Google Scholar

Masucci L., Graffeo R., Siciliano M., Franceschelli A., Bugli F., Fadda G. 2008. First Italian case of cyclosporiasis in an immunocompetent woman: local acquired infection. New Microbiologica, 31, 281–284Search in Google Scholar

McHardy I.H., Wu M., Shimizu-Cohen R., Couturier M.R., Humphries R.M.. 2014. Detection of intestinal protozoa in the clinical laboratory. Journal of Clinical Microbiology, 52, 712–720. 10.1128/JCM.02877-13Search in Google Scholar PubMed PubMed Central

Milord F., Lampron-Goulet E., St-Amour M., Levac E., Ramsay D. 2012. Cyclospora cayetanensis: a description of clinical aspects of an outbreak in Quebec, Canada. Epidemiology & Infection, 140, 626-632. 10.1017/S095026881100121XSearch in Google Scholar PubMed

Miró J.M., Buira E., Mallolas J., Gallart T., Moreno A., Zamora L., et al. 1994. CD4+ lymphocytes and opportunistic infections and neoplasms in patients with human immunodeficiency virus infection (in Spanish). Medicina Clinica (Barc), 102, 566–570Search in Google Scholar

Nair P., Mohamed J.A., DuPont H.L., Flores Figueroa J., Carlin L.G., Jiang Z.D., et al. 2008. Epidemiology of cryptosporidiosis in North American travelers to Mexico. American Journal of Tropical Medicine and Hygiene, 79, 210–214. in Google Scholar

Navaneethan U., Venkatesh P.G., Downs-Kelly E., Shen B. 2012. Isospora belli superinfection in a patient with eosinophilic gastroenteritis – a diagnostic challenge. Journal of Crohn’s and Colitis, 6, 236–239. 10.1016/j.crohns.2011.08.010Search in Google Scholar PubMed

Omoruyi B.E., Nwodo U.U., Udem C.S., Okonkwo F.O. 2014. Comparative diagnostic techniques for Cryptosporidium infection. Molecules, 19, 2674–2683. 10.3390/molecules19022674Search in Google Scholar PubMed PubMed Central

Ortega Y.R., Sanchez R. 2010. Update on Cyclospora cayetanensis, a Food-Borne and Waterborne Parasite. Clinical Microbiology Reviews, 23, 218–234. 10.1128/CMR.00026-09Search in Google Scholar PubMed PubMed Central

Pandey P., Bodhidatta L., Lewis M., Murphy H., Shlim D.R., Cave W., et al. 2011. Travelers’ diarrhea in Nepal: an update on the pathogens and antibiotic resistance. Journal of Travel Medicine, 18, 102–108. 10.1111/j.1708-8305.2010.00475.xSearch in Google Scholar PubMed

Paschke C., Apelt N., Fleischmann E., Perona P., Walentiny C., Löscher T., Herbinger K.H. 2011. Controlled study on enteropathogens in travellers returning from the tropics with and without diarrhoea. Clinical Microbiology & Infection, 17, 1194–1200. 10.1111/j.1469-0691.2010.03414.xSearch in Google Scholar PubMed

Pérez-Ayala A., Monge-Maíllo B., Díaz-Menéndez M., Norman F., Pérez-Molina J.A., López-Vélez R. 2011. Self-limited travelers’ diarrhea by Isospora belli in a patient with dengue infection. Journal of Travel Medicine, 18, 212–213. 10.1111/j.1708-8305.2010.00494.xSearch in Google Scholar

Porter C.K., Riddle M.S., Tribble D.R., Putnam S.D., Rockabrand D.M., Frenck R.W., et al. 2010. The epidemiology of travelers’ diarrhea in Incirlik, Turkey: a region with a predominance of heat-stabile toxin producing enterotoxigenic Escherichia coli. Diagnostic Microbiology and Infectious Diseases, 66, 241–247. 10.1016/j.diagmicrobio.2009.10.002Search in Google Scholar

Putignani L., Menichella D. 2010. Global Distribution, Public Health and Clinical Impact of the Protozoan Pathogen Cryptosporidium. Interdisciplinary Perspectives on Infectious Diseases, vol. 2010, Article ID 753512. 10.1155/2010/753512Search in Google Scholar

Quintero-Betancourt W., Peele E.R., Rose J.B. 2002. Cryptosporidium parvum and Cyclospora cayetanensis: a review of laboratory methods for detection of these waterborne parasites. Journal of Microbiology Methods, 49, 209–224. 10.1016/S0167-7012(02)00007-6Search in Google Scholar

Rao A.C.K., Geetha V., Kudva R., Vidhyalakshmi S., Rupashree S. 2014. Histology as a diagnostic tool for intestinal isosporiasis in immunocompromised patients. Asian Pacific Journal of Tropical Disease, 2, 251–252. 10.1016/S2222-1808(12)60055-3Search in Google Scholar

Ribes J.A., Seabolt J.P., Overman S.B. 2004. Point prevalence of Cryptosporidium, Cyclospora, and Isospora infections in patients being evaluated for diarrhea. American Journal of Clinical Pathology, 122, 28–32. 10.1309/AUJ5-WKE0-497X-KRUUSearch in Google Scholar PubMed

Riddle M.S., Rockabrand D.M., Schlett C., Monteville M.R., Frenck R.W, Romine M., et al. 2011. A prospective study of acute diarrhea in a cohort of United States military personnel on deployment to the Multinational Force and Observers, Sinai, Egypt. American Journal of Tropical Medicine and Hygiene, 84, 59–64. 10.4269/ajtmh.2011.10-0093Search in Google Scholar PubMed PubMed Central

Romeu J., Miró J.M., Sirera G., Mallolas J., Arnal J., Valls M.E., et al. 1991. Efficacy of octreotide in the management of chronic diarrhoea in AIDS. AIDS, 5, 1495–149910.1097/00002030-199112000-00012Search in Google Scholar PubMed

Rzezutka A., Nichols R.A., Connelly L., Kaupke A., Kozyra I., Cook N., et al. 2010. Cryptosporidium oocysts on fresh produce from areas of high livestock production in Poland. International Journal of Food Microbiology, 139, 96–101. 10.1016/j.ijfoodmicro.2010.01.027Search in Google Scholar PubMed

Sancak B, Akyon Y., Ergüven S. 2006. Cyclospora infection in five immunocompetent patients in a Turkish university hospital. Journal of Medical Microbiology, 55, 459–462. 10.1099/jmm.0.46279-0Search in Google Scholar PubMed

Vignesh R., Balakrishnan P., Shankar E.M., Murugavel K.G., Hanas S., Cecelia A.J., et al. 2007. High Proportion of Isosporiasis among HIV-Infected Patients with Diarrhea in Southern India. American Journal of Tropical Medicine and Hygiene, 77, 823–824. in Google Scholar

Vuong T.A., Nguyen T.T., Klank L.T., Phung D.C., Dalsgaard A. 2007. Faecal and protozoan parasite contamination of water spinach (Ipomoea aquatica) cultivated in urban wastewater in Phnom Penh, Cambodia. Tropical Medicine and International Health, 12, 73–81. 10.1111/j.1365-3156.2007.01944.xSearch in Google Scholar PubMed

Widerström M., Schönning C., Lilja M., Lebbad M., Ljung T., Allestam G., et al. 2014. Large outbreak of Cryptosporidium hominis infection transmitted through the public water supply, Sweden. Emerging Infectious Diseases, 20, 581–589. 10.3201/eid2004.121415Search in Google Scholar PubMed PubMed Central

Wilhelm C.L., Yarovinsky F. Apicomplexan infections in the gut. 2014. Parasite Immunology, 36, 409–420. 10.1111/pim.12115Search in Google Scholar PubMed

Received: 2017-2-9
Revised: 2017-4-26
Accepted: 2017-5-9
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS