Abstract
The epidemiology and public health significance of Cryptosporidium species and genotypes were investigated in Beni-Suef Governorate, Egypt. A total of 610 animal fecal samples (480 from cattle and 130 from buffaloes) beside 290 stool samples from humans were collected in the period between January and December 2014. Based on the microscopic examination, the overall estimated prevalence of Cryptosporidium spp. in cattle, buffaloes, and humans was 10.2, 12.3, and 19 %, respectively. The highest detection rates were in calves less than 2 months of age (17.1 %) and diarrheic animals (13.0 %). Likewise in humans, the highest prevalence of Cryptosporidium was in infants (31.3 %) and diarrheic individuals (21.1 %). The gender distribution in humans denoted that Cryptosporidium was reported more frequently in males (21.7 %) than females (14.5 %). Based on the molecular characterization of Cryptosporidium, Cryptosporidium oocyst wall protein (COWP) and gp60 genes were successfully amplified in 36 out of 50 samples subjected to genotyping. Restriction fragment length polymorphism (RFLP) analysis of the COWP fragments revealed that Cryptosporidium parvum was the only species detected in cattle (12 isolates) and buffaloes (4 isolates), while in humans, the detected species were Cryptosporidium hominis (15 isolates) and C. parvum (5 isolates). Sequence analysis of the gp60 gene identified the subtype IIdA20G1 within C. parvum isolated from both animals and humans. The common occurrence of zoonotic subtypes of C. parvum in cattle and buffaloes highlights the potential role of these animals as significant reservoirs of infection to humans. Also, the presence of C. hominis and C. parvum in humans indicates that both anthroponotic and zoonotic pathways are expected.
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References
Abd El Kader NM, Blanco MA, Ali-Tammam M, Abd El Ghaffar R, Osman A, El Sheikh N, Rubio JM, de Fuentes I (2012) Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo, Egypt. Parasitol Res 110:161–166
Abdel-Messih IA, Wierzba TF, Abu-Elyazeed R, Ibrahim AF, Ahmed SF, Kamal K, Sanders J, Frenck R (2005) Diarrhea associated with Cryptosporidium parvum among young children of the Nile River Delta in Egypt. J Trop Pediatr 51:154–159
Abu Samra N, Jori F, Samie A, Thompson P (2011) The prevalence of Cryptosporidium spp. oocysts in wild mammals in the Kruger National Park, South Africa. Vet Parasitol 175:155–159
Al-Braiken FA, Amin A, Beeching NJ, Hommel M, Hart CA (2003) Detection of Cryptosporidium amongst diarrheic and symptomatic children in Jeddah, Saudi Arabia. Ann Trop Med Parasitol 97:505–510
Amar CF, Dear PH, McLauchlin J (2004) Detection and identification by real time PCR-RFLP analyses of Cryptosporidium species from human feces. Lett Appl Microbiol 38:217–222
Amer S, Honma H, Ikarashi M, Oishi R, Endo M, Otawa K, Nakai Y (2009) The first detection of Cryptosporidium deer-like genotype in cattle in Japan. Parasitol Res 104:745–752
Amer S, Honma H, Ikarashi M, Tada C, Fukuda Y, Suyama Y, Nakai Y (2010) Cryptosporidium genotypes and subtypes in dairy calves in Egypt. Vet Parasitol 169:382–386
Amer S, Zidan S, Feng Y, Adamua H, Li N, Xiao L (2013) Identity and public health potential of Cryptosporidium spp. in water-buffalo calves in Egypt. Vet Parasitol 191:123–127
Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks—an update 2004–2010. Water Res 20:6603–6614
Becher KA, Robertson ID, Fraser DM, Palmer DG, Thompson RCA (2004) Molecular epidemiology of Giardia and Cryptosporidium infections in dairy calves originating from three sources in Western Australia. Vet Parasitol 123:1–9
Bhat S, Juyal P, Singla L (2012) Prevalence of cryptosporidiosis in neonatal buffalo calves in Ludhiana District of Punjab, India. Asian J Anim Vet Adv 7:512–520
Blagburn BL, Butler JM (2006) Optimize intestinal parasite detection with centrifugal fecal flotation. Vet Med 101:455–464
Brook E, Hart CA, French N, Christley R (2008) Prevalence and risk factors for Cryptosporidium spp. infection in young calves. Vet Parasitol 152:46–52
Caccio SM, Rinaldi L, Cringoli G, Condoleo R, Pozio E (2007) Molecular identification of Cryptosporidium parvum and Giardia duodenalis in the Italian water buffalo (Bubalus bubalis). Vet Parasitol 150:146–149
Casemore D, Armstrong M, Sands R (1985) Laboratory diagnosis of cryptosporidiosis. J Clin Pathol 38:1337–1341
Chalmers RM, Davies AP (2010) Mini review: clinical cryptosporidiosis. Exp Parasitol 124:138–146
Chalmers R, Hadfield SJ, Jackson CJ, Elwin K, Xiao L, Hunter P (2008) Geographic linkage and variation in Cryptosporidium hominis. Emerg Infect Dis 14:496–498
Coklin T, Farber J, Parrington L, Dixon B (2007) Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario, Canada. Vet Parasitol 150:297–305
El-Khodery S, Osman S (2008) Cryptosporidiosis in buffalo calves (Bubalus bubalis): prevalence and potential risk factors. Trop Anim Health Prod 40:419–426
El-Mohamady H, Abdel Messih IA, Youssef FG, Said M (2006) Enteric pathogens associated with diarrhea in children in Fayoum Egypt. Diagn Microbial Infect 56:1–5
Elwin K, Hadfield SJ, Robinson G, Crouch ND, Chalmers RM (2012) Cryptosporidium viatorum. sp. (Apicomplexa: Cryptosporidiidae) among travelers returning to Great Britain from the Indian subcontinent, 2007–2011. Int J Parasitol 42:675–682
Fayer R (2009) Taxonomy and species delimitation in Cryptosporidium. Exp Parasitol 124:90–97
Gait R, Soutar RH, Hanson M, Fraser C, Chalmers R (2008) Outbreak of cryptosporidiosis among veterinary students. Vet Rec 162:843–845
Geurden T, Berkvens D, Martens C, Casaert S, Vercruysse J, Claerebout E (2007) Molecular epidemiology with subtype analysis of Cryptosporidium in calves in Belgium. Parasitology 134:1981–1987
Gomez-Couso H, Amar CF, McLauchlin J, Ares-Mazas E (2005) Characterization of a Cryptosporidium isolate from water buffalo (Bubalus bubalis) by sequencing of a fragment of the Cryptosporidium oocyst wall protein gene (COWP). Vet Parasitol 131:139–144
Gormley FJ, Little CL, Chalmers RM, Rawal N, Adak GK (2011) Zoonotic cryptosporidiosis from petting farms, England and Wales, 1992–2009. Emerg Infect Dis 17:151–152
Helmy AY, Krücken J, Nöckler K, Samson-Himmelstjerna G, Zessin KH (2013) Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt. Vet Parasitol 193:15–24
Hijjawi N, Ng J, Yang R, Atoum M, Ryan U (2010) Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Exp Parasitol 125:161–164
Imre K, Luca C, Costache M, Sala C, Morar A, Morariu S, Ilie MS, Dărăbuş G (2013) Zoonotic Cryptosporidium parvum in Romanian newborn lambs (Ovis aries). Vet Parasitol 191:119–122
Jex AR, Gasser RB (2010) Genetic richness and diversity in C. hominis and C. parvum reveals major knowledge gaps and a need for the application of “next generation” technologies research review. Biotechnol Adv 28:17–26
Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 1:1–38
Learmonth JJ, Ionas G, Ebbett KA, Kwan ES (2004) Genetic characterization and transmission cycles of Cryptosporidium species isolated from humans in New Zealand. Appl Environ Microbiol 70:3973–3978
Lim YA, Iqbal A, Surin J, Sim BL, Jex AR, Nolan MJ, Smith HV, Gasser RB (2011) First genetic classification of Cryptosporidium and Giardia from HIV/AIDS patients in Malaysia. Infect Genet Evol 11:968–974
Maddox-Hyttel C, Langkjar RB, Enemark HL, Vigre H (2006) Cryptosporidium and Giardia in different age groups of Danish cattle and pigs—occurrence and management associated risk factors. Vet Parasitol 141:48–59
Mahfouz ME, Mira NN, Amer S (2014) Prevalence and genotyping of Cryptosporidium spp. in farm animals in Egypt. J Vet Med Sci 76:1569–1575
Majowicz SE, Michel P, Aramini JJ, McEwen SA, Wilson JB (2001) Descriptive analysis of endemic cryptosporidiosis cases reported in Ontario, 1996–1997. Can J Public Health 92:62–66
Mathew AO, David OO, Olubunmi FI, Mosunmola OJ, Tiamiyu AR, Gbenga AO (2014) Infection rate of Cryptosporidium parvum among diarrhea children in Ibadan, Oyo State, Nigeria. Sch J App Med Sci 2:3127–3131
Mehdiazami M (2007) Prevalence of Cryptosporidium infection in cattle in Isfahan, Iran. J Eukaryot Microbiol 54:100–102
Mendoca C, Almeida A, Castro A, de Lurdes Delgado M, Soares S, da Costa JM, Canada N (2007) Molecular characterization of Cryptosporidium and Giardia isolates from cattle from Portugal. Vet Parasitol 147:47–50
Mirzaei M (2007) Prevalence of Cryptosporidium sp. infection in diarrheic and non-diarrheic humans in Iran. Korean J Parasitol 45:33–37
Morgan UM, Xiao L, Hill BD, O’Donoghue P, Limor J, Lal A, Thompson RCA (2000) Detection of the Cryptosporidium parvum “human” genotype in a dugong (Dugong dugon). J Parasitol 86:1352–1354
Muhid A, Robertson I, Ng J, Ryan U (2011) Prevalence of and management factors contributing to Cryptosporidium sp. infection in pre-weaned and post-weaned calves in Johor, Malaysia. Exp Parasitol 127:534–538
Nouri M, Toroghi R (1991) Asymptomatic cryptosporidiosis in cattle and humans in Iran. Vet Rec 128:358–359
Pedraza-Díaz S, Amar C, McLauchlin J (2000) The identification and characterization of an unusual genotype of Cryptosporidium from human feces as Cryptosporidium meleagridis. FEMS Microbiol Lett 189:189–194
Peng M, Matos M, Gatei OW, Das P, Stantic-Pavlinic M (2001) A comparison of Cryptosporidium subgenotypes from several geographic regions. J Eukaryot Microbiol 48:28S–31S
Plutzer J, Karanis P (2007) Genotype and subtype analyses of Cryptosporidium isolates from cattle in Hungary. Vet Parasitol 146:357–362
Plutzer J, Karanis P (2009) Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol 165:187–199
Preiser G, Preiser L, Madeo L (2003) An outbreak of cryptosporidiosis among veterinary science students who work with calves. J Am Coll Health 5:213–215
Ren X, Zhao J, Zhang L, Ning C, Jian F, Wang R, Lv C, Wang Q, Arrowood MJ, Xiao L (2012) Cryptosporidium tyzzeri sp. (Apicomplexa: Cryptosporidiidae) in domestic mice (Mus musculus). Exp Parasitol 130:274–281
Ryan UM, Bath C, Robertson I, Read C, Elliot A, McInnes L, Traub R, Besier B (2005) Sheep may not be an important zoonotic reservoir for Cryptosporidium and Giardia parasites. Appl Environ Microbiol 71:4992–4997
Rzezutka A, Kaupke A (2013) Occurrence and molecular identification of Cryptosporidium species isolated from cattle in Poland. Vet Parasitol 196:301–306
Santín M, Trout JM (2007) Cryptosporidiosis of livestock. In: Fayer R, Xiao L (eds) Cryptosporidium and cryptosporidiosis, 2nd edn. CRC, Boca Raton, pp 451–483
Santín M, Trout JM, Xiao L, Zhou L, Greiner E, Fayer R (2004) Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Vet Parasitol 122:103–117
Santín M, Trout JM, Fayer R (2008) A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Vet Parasitol 155:15–23
Semenza JC, Nichols G (2007) Cryptosporidiosis surveillance and water-borne outbreaks in Europe. Euro Surveill 12:E13–E14
Sharma P, Sharma A, Sehgal R, Malla N, Khurana S (2013) Genetic diversity of Cryptosporidium isolates from patients in North India. Int J Infect Dis 17:e601–e605
Silverlås C, De Verdier K, Emanuelson U, Mattsson JG, Björkman C (2010) Cryptosporidium infection in herds with and without calf diarrheal problems. Parasitol Res 107:1435–1444
Snel SJ, Baker MG, Venugopal K (2009) The epidemiology of cryptosporidiosis in New Zealand, 1997–2006. N Z Med J 122:47–61
Spano F, Putignani L, McLauchlin J (1997) PCR-RFLP analysis of the Cryptosporidium oocyst wall protein (COWP) gene discriminates between C. wrairi and C. parvum, and between C. parvum isolates of human and animal origin. FEMS Microbiol Lett 150:209–217
Sulaiman IM, Hira PR, Zhou L, Al-Ali FM, Al-Shelahi FA, Shweiki HM, Iqbal J, Khalid N, Xiao L (2005) Unique endemicity of cryptosporidiosis in children in Kuwait. J Clin Microbiol 43:2805–2809
Taghipour N, Nazemalhosseini-Mojarad E, Haghighi A, Rostami-Nejad M, Romani S, Keshavarz A, Alebouyeh M, Zali M (2011) Molecular epidemiology of cryptosporidiosis in Iranian children, Tehran, Iran. Iran J Parasitol 6:41–45
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tumwine JK, Kekittiinwa A, Nabukeera N, Akiyoshi DE (2003) Cryptosporidium parvum in children with diarrhea in Mulago Hospital, Kampala, Uganda. Am J Trop Med Hyg 68:710–715
Walana W, Tay SCK, Tetteh P, Ziem JB (2014) Prevalence of intestinal protozoan infestation among primary school children in urban and peri-urban communities in Kumasi, Ghana. Sci J Public Health 2:52–57
Wegayehu T, Adamu T, Petros B (2013) Prevalence of G. duodenalis and Cryptosporidium species infections among children and cattle in North Shew Zone, Ethiopia. BMC Infect Dis 13:419–425
Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–89
Xiao L, Escalante L, Yang C (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65:1578–1583
Xiao L, Limor J, Morgan UM, Sulaiman IM, Thompson RC, Lal AA (2000) Sequence differences in the diagnostic target region of the oocyst wall protein gene of Cryptosporidium parasites. Appl Environ Microbiol 66:5499–5502
Xiao L, Fayer R, Ryan U, Upton SJ (2004) Cryptosporidium taxonomy: recent advances and implications for public health. Clin Microbiol Rev 17:72–79
Yoder JS, Beach MJ (2010) Cryptosporidium surveillance and risk factors in the United States. Exp Parasitol 124:31–39
Acknowledgments
The authors wish to thank Dr. S. A. S. Shany, lecturer for poultry diseases, Faculty of Vet. Med., Beni-Suef University, for his valuable effort concerning molecular characterization of Cryptosporidium.
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Ibrahim, M.A., Abdel-Ghany, A.E., Abdel-Latef, G.K. et al. Epidemiology and public health significance of Cryptosporidium isolated from cattle, buffaloes, and humans in Egypt. Parasitol Res 115, 2439–2448 (2016). https://doi.org/10.1007/s00436-016-4996-3
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DOI: https://doi.org/10.1007/s00436-016-4996-3