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Acta Parasitologica

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Volume 62, Issue 3


The Prevalence of Cyclospora cayetanensis and Cryptosporidium spp. in Turkish patients infected with HIV-1

Hayriye Kirkoyun Uysal
  • Istanbul University İstanbul Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Gokhan Tolga Adas / Kevser Atalik
  • Istanbul University İstanbul Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Semih Altiparmak
  • Istanbul University İstanbul Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Ozer Akgul / Suat Saribas
  • Istanbul University Cerrahpasa Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Mert Gurcan / Pelin Yuksel
  • Istanbul University Cerrahpasa Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Taner Yildirmak
  • Okmeydanı Training and Research Hospital, Department of Microbiology and Clinical Microbiology, Istanbul, Turkey
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/ Bekir Kocazeybek
  • Corresponding author
  • Istanbul University Cerrahpasa Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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/ Tevhide Ziver / Yasar Ali Oner
  • Istanbul University İstanbul Medical Faculty Department of Medical Microbiology, Istanbul, Turkey
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Published Online: 2017-07-05 | DOI: https://doi.org/10.1515/ap-2017-0067


Opportunistic infections such as cryptosporidiosis and cyclosporiasis are commonly encountered in patients with acquired immunodeficiency syndrome (AIDS). We investigated the existence of opportunistic protozoans that significantly affect the quality of life in HIV-1 infected patients using conventional and molecular methods. The study group comprised 115 HIV-1 positive patients. In the identification of Cyclospora cayetanensis and Cryptosporidium, the formol-ether precipitation method was used and smears were evaluated in optical microscope by staining modified Ziehl–Neelsen (ZN). The primers and probes used for PCR were Heat shock protein 70 for C. cayetanensis and the oocysts wall protein for Cryptosporidium spp.. Cyclospora and Cryptosporidium spp. oocysts were detected in one and two patients, respectively, by staining, whereas we detected C. cayetanensis in three patients out of 115 (2.6%) by PCR, and Cryptosporidium spp. in a further three patients (2.6%). C. cayetensis was detected in patients with CD4 counts of 64 cells/μm, 182 cells/μm and 287 cells/μm, respectively. Cryptosporidium spp. was detected in patients with CD4 counts of 176 cells/μm, 241 cells/μm and 669 cells/μm. As conclusion, PCR method is faster and more sensitive than microscopic methods and to screen intestinal pathogens routinely in patients infected with HIV should not be neglected in developing countries like Turkey.

Keywords: Cyclospora cayetanensis; Cryptosporidium spp; HIV-1


  • Agholi M., Hatam G.R., Motazedian M.H. 2013. HIV/AIDS associated opportunistic protozoal diarrhea. AIDS Research and Human Retroviruses, 29, 35–441. CrossrefGoogle Scholar

  • Adjei A., Lartey M., Adiku T.K., Rodrigues O., Renner L., Sifah E., et al. 2003. Cryptosporidium oocysts in Ghanaian AIDS patients with diarrhoea. East African Medical Journal, 80, 369–372. CrossrefGoogle Scholar

  • Akin H., Boluk G., Akalin H., Oguz A., Kazak E., Aslan E., et al. 2012: HIV/AIDS: retrospective analysis of 78 cases. Klimik Journal, 25, 111–116. . (In Turkish)CrossrefGoogle Scholar

  • Alakpa G., Fagbenro-Beyioku A.F., Clarke S.C. 2002. Cyclospora cayetanensis in stools submitted to hospitals in Lagos, Nigeria. International Journal of Infectious Diseases, 6, 314–318. CrossrefGoogle Scholar

  • Assefa S., Erko B., Medhin G., Assefa Z., Shimelis T. 2009. Intestinal parasitic infections in relation to HIV/AIDS status, diarrhea and CD4 T-cell count. BMC Infectious Diseases, 9, 155. CrossrefWeb of ScienceGoogle Scholar

  • Asma I., Johari S., Sim B.L., Lim Y.A. 2011. How common is intestinal parasitism in HIV-infected patients in Malaysia? Tropical Biomedicine, 28, 400–410Google Scholar

  • Atambay M., Daldal N., Celik T. 2003. Investigation of Cryptosporidium spp. in diarrhea in Malatya. Turkish Journal of Parasitology, 27: 12–14. (In Turkish)Google Scholar

  • Blans M.C., Ridwan B.U., Verweij J.J., Rozenberg-Arska M., Verhoef J. 2005. Cyclosporiasis outbreak Indonesia. Emerging Infectious Diseases, 11, 1453–1455. CrossrefGoogle Scholar

  • Bouzid M., Hunter P.R., Chalmers R.M., Tyler K.M. 2013. Cryptosporidium pathogenicity and virulence. Clinical Microbiology Reviews, 26, 115–134. CrossrefWeb of ScienceGoogle Scholar

  • Chacin-Bonilla L., Estevez J., Monsalve F., Quijada L. 2001. Cyclospora cayetenensis infections among diarrhea patients from Venezuela. The American Journal of Tropical Medicine and Hygiene, 65, 351–354CrossrefGoogle Scholar

  • Chacin-Bonilla L. 2010. Epidemiology of Cyclospora cayetenensis: a review focusing in endemic areas. Acta Tropica, 115, 181–193. CrossrefGoogle Scholar

  • Chalmers R.M., Katzer F. 2013. Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends in Parasitology, 29, 237–251. CrossrefGoogle Scholar

  • Chawla R, Ichhpujani R.L. 2011. Enteric spore-forming opportunistic parasites in HIV/ IDS. Tropical Parasitology, 1, 15–19. CrossrefGoogle Scholar

  • Cranendonk R.J., Kodde C.J., Chipeta, D. Zijlstra E.E., Sluiters J.F. 2003. Cryptosporidium parvum and Isospora belli infections among patients with and without diarrhoea. East African Medical Journal, 80, 398–401Google Scholar

  • Eberhard M.L., Pieniazek N.J., Arrowood M.J. 1997. Laboratory diagnosis of Cyclospora infections. Archives of Pathology & Laboratory Medicine, 121, 792–797Google Scholar

  • Farthing M.J.G., Kelly M.P., Veitch A.M. 1996. Recently recognized microbial enteropathies and HIV infection. Journal of Antimicrobial Chemotherapy, 37, 61–70CrossrefGoogle Scholar

  • Findik D., Karabayraktar A. 1994. Investigation of Cryptosporidium oocysts in Gaita specimens. Turkish Journal of Parasitology, 18, 415–419. (In Turkish)Google Scholar

  • Goodgame R. 1996. Understanding intestinal spore-froming protozoa: cryptosporidia, microsporidia, isospora and cyclospora. Annals of Internal Medicine, 124, 429–441CrossrefGoogle Scholar

  • Gupta S., Narang S., Nunavath V., Singh S. 2008. Chronic diarrhoea in HIV patients: Prevalence of coccidian parasites. Indian Journal of Medical Microbiology, 26, 172–175. CrossrefGoogle Scholar

  • Helmy M.M., Rashed L.A., Abdel-Fattah H.S. 2006. Co-infection with Cryptosporidium parvum and Cyclospora cayetanensis in immunocompromised patients. Journal of the Egyptian Society of Parasitology, 36, 613–627Google Scholar

  • Hunter P., Nichols G. 2002. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clinical Microbiology Reviews, 15, 145–154. CrossrefGoogle Scholar

  • Koc A.N., Aygen B., Sahin I., Kayabas U. 1998. Cyclospora sp. associated with diarrhea in a patient with AIDS in Turkey. Turkish Journal of Medical Sciences, 28, 577–578Google Scholar

  • Kulkarni S.V., Kairon R., Sane S.S., Padmawar P.S., Kale V.A., Thakar M.R., et al. 2009. Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunesuppression. Indian Journal of Medical Research, 130, 63–66Google Scholar

  • 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. Transactions of The Royal Society of Tropical Medicine and Hygiene, 103, 892–898. CrossrefWeb of ScienceGoogle Scholar

  • Lalonde L.F., Gajadhar A.A. 2008. Highly sensitive and specific PCR assay for reliable detection of Cyclospora cayetanensis oocysts. Applied and Environmental Microbiology, 74, 4354–4358. CrossrefGoogle Scholar

  • Lim Y.A., Rohela M., Sim B.L., Jamaiah I., Nurbayah M. 2005. Prevalence of cryptosporidiosis in HIV-infected patients in Kajang Hospital, Selangor. The Southeast Asian Journal of Tropical Medicine and Public Health, 36, 30–33Google Scholar

  • Mathur M.K., Verma A.K., Makwana G.E., Sinha M. 2013. Study of opportunictic intestinal parasitic infections in human immunodeficiency virus/ecquired immunodeficiency syndrome patients. Journal of Global Infectious Diseases, 5, 164–167. CrossrefGoogle Scholar

  • Mtapuri-Zinyowera S., Ruhanya V., Midzi N., Berejena C., Chin’ombe N., Nziramasanga P., et al. 2014. Human parasitic protozoa in drinking water sources in rural Zimbabwe and their link to HIV infection. Germs, 4, 86–91. CrossrefGoogle Scholar

  • Mundaca C.C., Torres-Slimming P.A., Araujo-Castillo R.V., Moran M., Bacon D.J., Ortega Y., et al. 2008. Use of PCR to improve diagnostic yield in an outbreak of cyclosporiasis in Lima, Peru. Transactions of the Royal Society of Tropical Medicine and Hygiene, 102, 712–717. CrossrefWeb of ScienceGoogle Scholar

  • Otag F., Aslan G., Emekdas G., Aydin E., Ozkan A.T, Ceber K. 2007. The investigation of Cryptosporidium oocysts in elementary school students in Mersin. Turkish Journal of Parasitology, 31, 17–19. (In Turkish)Google Scholar

  • Ozdamar M., Hakki E., Turkoglu S. 2010. High occurrence of cyclosporiasis in Istanbul, Turkey, during a dry and warm summer. Parasites & Vectors, 3, 39–41. CrossrefWeb of ScienceGoogle Scholar

  • Rivero-Rodríguez Z., Hernández A., Bracho Á., Salazar S., Villalobos R. 2013. Prevalence of intestinal microsporidia and other intestinal parasites in HIV positive patients from Maracaibo, Venezuela. Biomedica, 33, 538–545. . (In Spanish)CrossrefGoogle Scholar

  • Ryan U, Hijjawi N. 2015. New developments in Cryptosporidium research. International Journal for Parasitology, 45, 367–373. CrossrefWeb of ScienceGoogle Scholar

  • Saksirisampant W., Eampokalap B., Rattanasrithong M., Likanonsakul S., Wiwanitkit V., Nasingkarn A., Denmasae N. 2002. A prevalence of Cryptosporidium infections among Thai HIV-infected patients. Journal of the Medical Association of Thailand, 85, S424–S428Google Scholar

  • Sherchan J.B, Ohara H., Sakurada S., Basnet A., Tandukar S., Sherchand J.B., Bam D.S. 2012. Enteric opportunistic parasitic infections among HIV-seropositive patients in Kathmandu, Nepal. Kathmandu University Medical Journal, 10, 14–17Google Scholar

  • Silva C.V., Ferreira M.S., Goncalves-Pires Mdo R., Costa-Cruz J.M. 2003. Detection of Cryptosporidium- specific coproantigen in human immunodeficiency virus/acquired immunodeficiency syndrome patients by using a commercially available immune enzymatic assay. Memórias do Instituto Oswaldo Cruz, 98, 1097–1099CrossrefGoogle Scholar

  • Swindells S, Evans S, Zackin R, Goldman M, Haubrich R, Filler SG, Balfour H.H. 2002. Predictive value of HIV-1 viral load on risk for opportunistic infection. Journal of Acquired Immune Deficiency Syndromes, 30, 154–158. CrossrefGoogle Scholar

  • ten Hove R.J., van Esbroeck M., Vervoort T., van den Ende J., van Lieshout L., Verweij J.J. 2009. Molecular diagnostics of intestinal parasites in returning travellers. European Journal of Clinical Microbiology & Infectious Diseases, 28, 1045–1053. CrossrefGoogle Scholar

  • Tumwine J.K., Kekitiinwa A., Bakeera-Kitaka S., Ndeezi G., Downing R., Freng X., et al. 2005. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. American Society of Tropical Medicine and Hygiene, 73, 921–925Google Scholar

  • Uppal B., Singh O., Chadha S., Jha A.K. 2014. A comparison of nested PCR assay with conventional techniques for diagnosis of intestinal cryptosporidiosis in AIDS cases from northern India. Journal of Parasitology Research, 2014, 706105. CrossrefGoogle Scholar

  • van Hal S.J., Muthiah K., Matthews G., Harkness J., Stark D., Cooper D., Marriott D. 2007. Declining incidence of intestinal microsporidiosis and reduction in AIDS-related mortality following introduction of HAART in Sydney, Australia. Transactions of the Royal Society of Tropical Medicine and Hygiene, 101, 1096–1100. CrossrefWeb of ScienceGoogle Scholar

  • Varma M., Hester J.D., Schaefer F.W., Ware M.W., Lindquist H.D. 2003. Detection of Cyclospora cayetanensis using a quantitative real-time PCR assayGoogle Scholar

  • Velásquez J.N., Carnevale S., Cabrera M., Kuo L., Chertcoff A., Mariano M., et al. 2004. Cyclospora cayetanensis in patients with AIDS and chronic diarrhea. Acta Gastroenterológica Latinoamericana, 34, 133–137Google Scholar

  • Yadav P., Khalil S., Mirdha B.R., Makharia G.K., Bhatnagar S. 2015. Molecular characterization of clinical isolates of Cyclospora cayetanensis from patients with diarrhea in India. Indian Journal of Medical Microbiology, 33,351–356. CrossrefGoogle Scholar

  • Yazar S., Yalcin S., Sahin I. 2004. Human cyclosporiosis in Turkey. World Journal of Gastroenterology, 10, 1844–1847. CrossrefGoogle Scholar

About the article

Received: 2016-07-17

Revised: 2017-02-23

Accepted: 2017-04-12

Published Online: 2017-07-05

Published in Print: 2017-09-26

Conflict of interests None declared.

Citation Information: Acta Parasitologica, Volume 62, Issue 3, Pages 557–564, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0067.

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