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

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

Hayriye Kirkoyun Uysal, Gokhan Tolga Adas, Kevser Atalik, Semih Altiparmak, Ozer Akgul, Suat Saribas, Mert Gurcan, Pelin Yuksel, Taner Yildirmak, Bekir Kocazeybek, Tevhide Ziver and Yasar Ali Oner
From the journal Acta Parasitologica

Abstract

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.

  1. Conflict of interests None declared.

Ethics

This study was approved by the Non-Invasive Clinical Research Ethics Committee of Istanbul Medical Faculty (Number: 2012/54-911/, Date: 26 January 2012). All patients provided their informed consent to participate in the study.

Acknowledgements

This study was supported by the Research Fund of Istanbul University, Project No: 22451. English language edited by American Manuscript Editors.

References

Agholi M., Hatam G.R., Motazedian M.H. 2013. HIV/AIDS associated opportunistic protozoal diarrhea. AIDS Research and Human Retroviruses, 29, 35–441. 10.1089/AID.2012.0119Search in Google 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. 10.4314/eamj.v80i7.8721Search in Google 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. 10.5152/kd.2012.31. (In Turkish)Search in Google 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. 10.1016/S1201-9712(02)90167-0Search in Google 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. 10.1186/1471-2334-9-155Search in Google Scholar PubMed PubMed Central

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, 400–410Search in Google 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)Search in 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. 10.3201/eid1109.040947Search in Google Scholar PubMed PubMed Central

Bouzid M., Hunter P.R., Chalmers R.M., Tyler K.M. 2013. Cryptosporidium pathogenicity and virulence. Clinical Microbiology Reviews, 26, 115–134. 10.1128/CMR.00076-12Search in Google Scholar PubMed PubMed Central

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, 351–35410.4269/ajtmh.2001.65.351Search in Google Scholar PubMed

Chacin-Bonilla L. 2010. Epidemiology of Cyclospora cayetenensis: a review focusing in endemic areas. Acta Tropica, 115, 181–193. 10.1016/j.actatropica.2010.04.001Search in Google Scholar PubMed

Chalmers R.M., Katzer F. 2013. Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends in Parasitology, 29, 237–251. 10.1016/j.pt.2013.03.001Search in Google Scholar PubMed PubMed Central

Chawla R, Ichhpujani R.L. 2011. Enteric spore-forming opportunistic parasites in HIV/ IDS. Tropical Parasitology, 1, 15–19. 10.4103/2229-5070.72112Search in Google Scholar PubMed PubMed Central

Cranendonk R.J., Kodde C.J., ChipetaD. Zijlstra E.E., Sluiters J.F. 2003. Cryptosporidium parvum and Isospora belli infections among patients with and without diarrhoea. East African Medical Journal, 80, 398–40110.4314/eamj.v80i8.8729Search in Google Scholar

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

Farthing M.J.G., Kelly M.P., Veitch A.M. 1996. Recently recognized microbial enteropathies and HIV infection. Journal of Antimicrobial Chemotherapy, 37, 61–7010.1093/jac/37.suppl_B.61Search in Google Scholar

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

Goodgame R. 1996. Understanding intestinal spore-froming protozoa: cryptosporidia, microsporidia, isospora and cyclospora. Annals of Internal Medicine, 124, 429–44110.7326/0003-4819-124-4-199602150-00008Search in Google Scholar PubMed

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. 10.4103/0255-0857.40536Search in Google Scholar PubMed

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, 613–627Search in Google Scholar

Hunter P., Nichols G. 2002. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clinical Microbiology Reviews, 15, 145–154. 10.1128/CMR.15.1.145–154.2002Search in Google 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, 577–578Search in Google 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, 63–66Search in Google 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. 10.1016/j.trstmh.2009.02.017Search in Google Scholar PubMed

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. 10.1128/AEM.00032-08Search in Google Scholar PubMed PubMed Central

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, 30–33Search in Google 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. 10.4103/0974-777X.122012Search in Google Scholar PubMed PubMed Central

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. 10.11599/germs.2014.1061Search in Google Scholar PubMed PubMed Central

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. 10.1016/j.trstmh.2008.03.003Search in Google Scholar PubMed

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)Search in 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. 10.1186/1756-3305-3-39Search in Google Scholar PubMed PubMed Central

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. 10.7705/biomedica.v33i4.1468. (In Spanish)Search in Google Scholar PubMed

Ryan U, Hijjawi N. 2015. New developments in Cryptosporidium research. International Journal for Parasitology, 45, 367–373. 10.1016/j.ijpara.2015.01.009Search in Google Scholar PubMed

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–S428Search in Google 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, 14–1710.3126/kumj.v10i2.7336Search in Google Scholar PubMed

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, 1097–109910.1590/S0074-02762003000800022Search in Google 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. 10.1097/01.QAI.0000017998.56638.8ESearch in Google 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. 10.1007/s10096-009-0745-1Search in Google Scholar PubMed PubMed Central

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, 921–92510.4269/ajtmh.2005.73.921Search in Google 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. 10.1155/2014/706105Search in Google Scholar PubMed PubMed Central

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. 10.1016/j.trstmh.2007.06.003Search in Google 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 assay10.1016/S0167-7012(02)00209-9Search in Google 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, 133–137Search in Google 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. 10.4103/0255-0857.158547Search in Google Scholar PubMed

Yazar S., Yalcin S., Sahin I. 2004. Human cyclosporiosis in Turkey. World Journal of Gastroenterology, 10, 1844–1847. 10.3748/wjg.v10.i12.1844Search in Google Scholar PubMed PubMed Central

Received: 2016-7-17
Revised: 2017-2-23
Accepted: 2017-4-12
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS