Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt

Veterinary Parasitology

Volumn 193, Issue 1-3, 2013, Pages 15-24

  Helmy, Yosra A ^a,b   Krücken, Jürgen ^b   Nöckler, Karsten ^c   von Samson Himmelstjerna, Georg ^b   Zessin, Karl H ^b  

^a Suez Canal University   (Egypt)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

Author keywords

Copro antigen RIDA QUICK test; Cryptosporidium; Egypt; Gp60; Molecular epidemiology; PCR RFLP; Zoonosis

Indexed keywords

DNA 18S; DRINKING WATER; PARASITE ANTIGEN;

ANTIGEN DETECTION; ARTICLE; BUFFALO; CHILD; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM ANDERSONI; CRYPTOSPORIDIUM BOVIS; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; EGYPT; FECES ANALYSIS; FEMALE; GENE; GENE TARGETING; GENETIC VARIABILITY; GENOTYPE; GP60 GENE; HUMAN; INFECTION RISK; MALE; MOLECULAR EPIDEMIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE EXAMINATION; PARASITE IDENTIFICATION; PARASITE PREVALENCE; PARASITE TRANSMISSION; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RISK FACTOR; WATER CONTAMINATION;

ANIMALS; BUFFALOES; CATTLE; CATTLE DISEASES; CHILD; CHILD, PRESCHOOL; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; EGYPT; FECES; HUMANS; INFANT; INFANT, NEWBORN; MOLECULAR EPIDEMIOLOGY; POLYMERASE CHAIN REACTION; ZOONOSES;

ANIMALIA; BOS; BUBALUS; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM ANDERSONI; CRYPTOSPORIDIUM BOVIS; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM;

EID: 84873745644     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2012.12.015     Document Type: Article

References (75)

1. Abd el-Wahed M.M., Salem G.H., el-Assaly T.M. The role of wild rats as a reservoir of some internal parasites in Qalyobia governorate. J. Egypt. Soc. Parasitol. 1999, 29:495-503.
2. Abd El Kader N.M., Blanco M.A., Ali-Tammam M., Abd El Ghaffar Ael R., Osman A., El Sheikh N., Rubio J.M., de Fuentes I. Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo, Egypt. Parasitol. Res. 2012, 110:161-166.
3. Abdel-Hafeez E.H., Ahmed A.K., Ali B.A., Fadia A., Moslam F.A. Opportunistic parasites among immunosuppressed children in Minia district, Egypt. Korean J. Parasitol. 2012, 50:57-62.
4. Abdel-Messih I.A., Wierzba T.F., Abu-Elyazeed R., Ibrahim A.F., Ahmed S.F., Kamal K., Sanders J., Frenck R. Diarrhea associated with Cryptosporidium parvum among young children of the Nile River Delta in Egypt. J. Trop. Pediatr. 2005, 51:154-159.
5. Abdel Hameed D.M., Elwakil H.S., Ahmed M.A. A single-step immunochromatographic lateral-flow assay for detection of Giardia lamblia and Cryptosporidium parvum antigens in human fecal samples. J. Egypt. Soc. Parasitol. 2008, 38:797-804.
6. Abou-Eisha A.M. Cryptosporidial infection in man and farm animals in Ismailia governorate. Vet. Med. J. 1994, 42:107-111.
7. Abou-Eisha A.M., Hussein M.M., Abdel-Aal A.A., Saleh R.E. Cryptosporidium in drinking water sources and its zoonotic importance. Minufiya Vet. J. 2000, 1:101-116.
8. Agnamey P., Sarfati C., Pinel C., Rabodoniriina M., Kapel N., Dutoit E., Garnaud C., Diouf M., Garin J.F., Totet A., Derouin F. Evaluation of four commercial rapid immunochromatographic assays for detection of Cryptosporidium antigens in stool samples: a blind multicenter trial. J. Clin. Microbiol. 2011, 49:1605-1607.
9. Ahs J., Tao W., Löfgren J., Forsberg B. Diarrheal diseases in low- and middle-income countries: incidence, prevention and management. Open Inf. Dis. J. 2010, 4:113-124.
10. Amer S., Fayed M., Honma H., Fukuda Y., Tada C., Nakai Y. Multilocus genetic analysis of Cryptosporidium parvum from Egypt. Parasitol. Res. 2010, 107:1043-1047.
11. Amer S., Harfoush M., He H. Molecular and phylogenetic analyses of Cryptosporidium spp. from dairy cattle in Egypt. J. Egypt. Soc. Parasitol. 2010, 40:349-366.
12. Amer S., Honma H., Ikarashi M., Tada C., Fukuda Y., Suyama Y., Nakai Y. Cryptosporidium genotypes and subtypes in dairy calves in Egypt. Vet. parasitol. 2010, 169:382-386.
13. Antonios S.N., Salem S.A., Khalifa E.A. Water pollution is a risk factor for Cryptosporidium infection in Gharbia governorate. J. Egypt. Soc. Parasitol. 2001, 31:963-964.
14. Antonios S.N., Tolba O.A., Othman A.A., Saad M.A. A preliminary study on the prevalence of parasitic infections in immunocompromised children. J. Egypt. Soc. Parasitol. 2010, 40:617-630.
15. Bern C., Hernandez B., Lopez M.B., Arrowood M.J., De Merida A.M., Klein R.E. The contrasting epidemiology of Cyclospora and Cryptosporidium among outpatients in Guatemala. Am. J. Trop. Med. Hyg. 2000, 63:231-235.
16. Bhattacharya M.K., Teka T., Faruque A.S., Fuchs G.J. Cryptosporidium infection in children in urban Bangladesh. J. Trop. Pediatr. 1997, 43:282-286.
17. Boghdadi A.M. Comparison between the prospect Cryptosporidium microtiter assay and the immunofluorescent test in the diagnosis of cryptosporidiosis. J. Egypt. Soc. Parasitol. 1996, 26(April):243-247.
18. Bushen O.Y., Kohli A., Pinkerton R.C., Dupnik K., Newman R.D., Sears C.L., Fayer R., Lima A.A., Guerrant R.L. Heavy cryptosporidial infections in children in northeast Brazil: comparison of Cryptosporidium hominis and Cryptosporidium parvum. Trans. R. Soc. Trop. Med. Hyg. 2007, 101:378-384.
19. Cama V.A., Bern C., Roberts J., Cabrera L., Sterling C.R., Ortega Y., Gilman R.H., Xiao L. Cryptosporidium species and subtypes and clinical manifestations in children. Peru. Emerg. Infect. Dis. 2008, 14:1567-1574.
20. Cama V.A., Ross J.M., Crawford S., Kawai V., Chavez-Valdez R., Vargas D., Vivar A., Ticona E., Navincopa M., Williamson J., Ortega Y., Gilman R.H., Bern C., Xiao L. Differences in clinical manifestations among Cryptosporidium species and subtypes in HIV-infected persons. J. Inf. Dis. 2007, 196:684-691.
21. Certad G., Benamrouz S., Guyot K., Mouray A., Chassat T., Flament N., Delhaes L., Coiteux V., Delaire B., Praet M., Cuvelier C., Gosset P., Dei-Cas E., Creusy C. Fulminant cryptosporidiosis after near-drowning: a human Cryptosporidium parvum strain implicated in invasive gastrointestinal adenocarcinoma and cholangiocarcinoma in an experimental model. Appl. Environ. Microbiol. 2012, 78:1746-1751.
22. Chen X.M., Keithly J.S., Paya C.V., LaRusso N.F. Cryptosporidiosis. N. Engl. J. Med 2002, 346:1723-1731.
23. Current W.L., Garcia L.S. Cryptosporidiosis. Clin. Microbiol. Rev 1991, 4:325-358.
24. Dillingham R.A., Lima A.A., Guerrant R.L. Cryptosporidiosis: epidemiology and impact. Microbes Infect. 2002, 4:1059-1066.
25. Eida A.M., Eida M.M., El-Desoky A. Pathological studies of different genotypes of human Cryptosporidium Egyptian isolates in experimentally mice. J. Egypt. Soc. Parasitol. 2009, 39:975-990.
26. El-Hamshary E.M., El-Sayed H.F., Hussein E.M., Rayan H.Z., Soliman R.H. Comparison of polymerase chain reaction, immunochromatographic assay and staining techniques in diagnosis of cryptosporidiosis. Parasitologists Uni. J. 2008, 1:77-86.
27. El-Kadi M.A., Dorrah A.O., Shoukry N.M. Patients with gastrointestinal complains due to enteric parasites, with reference to Entamoeba histolytica/dispar as detected by ELISA E. histolytica adhesion in stool. J. Egypt. Soc. Parasitol. 2006, 36(April):53-64.
28. El-Khodery S.A., Osman S.A. Cryptosporidiosis in buffalo calves (Bubalus bubalis): prevalence and potential risk factors. Trop. Anim. Health. Prod. 2008, 40:419-426.
29. El-Moamly A.A., El-Sweify M.A. ImmunoCard STAT! cartridge antigen detection assay compared to microplate enzyme immunoassay and modified Kinyoun's acid-fast staining technique for detection of Cryptosporidium in fecal specimens. Parasitol. Res. 2012, 110:1037-1041.
30. El-Shazly A.M., Gabr A., Mahmoud M.S., Aziz S.S., Saleh W.A. The use of Ziehl-Neelsen stain, enzyme-linked immunosorbent assay and nested polymerase chain reaction in diagnosis of cryptosporidiosis in immuno-competent, - compromised patients. J. Egypt. Soc. Parasitol. 2002, 32(April):155-166.
31. El-Sherbini G.T., Mohammad K.A. Zoonotic cryptosporidiosis in man and animal in farms, Giza governorate, Egypt. J. Egypt. Soc. Parasitol. 2006, 36:49-58.
32. El-Sibaei M.M., Rifaat M.M., Hameed D.M., el-Din H.M. Nosocomial sources of cryptosporidial infection in newly admitted patients in Ain Shams University Pediatric hospital. J. Egypt. Soc. Parasitol. 2003, 33:177-188.
33. El Naggar H.H., Handousa A.E., El Hamshary E.M., El Shazly A.M. Evaluation of five stains in diagnosing human intestinal coccidiosis. J. Egypt. Soc. Parasitol. 1999, 29:883-891.
34. Elshazly A.M., Elsheikha H.M., Soltan D.M., Mohammad K.A., Morsy T.A. Protozoal pollution of surface water sources in Dakahlia governorate, Egypt. J. Egypt. Soc. Parasitol. 2007, 37:51-64.
35. Fayer R., Santin M., Trout J.M., Greiner E. Prevalence of species and genotypes of Cryptosporidium found in 1-2-year-old dairy cattle in the eastern United States. Vet. Parasitol. 2006, 135:105-112.
36. Feng Y., Ortega Y., He G., Das P., Xu M., Zhang X., Fayer R., Gatei W., Cama V., Xiao L. Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Vet. Parasitol. 2007, 144:1-9.
37. Gatei W., Wamae C.N., Mbae C., Waruru A., Mulinge E., Waithera T., Gatika S.M., Kamwati S.K., Revathi G., Hart C.A. Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya. Am. J. Trop. Med. Hyg. 2006, 75:78-82.
38. Geurden T., Berkvens D., Martens C., Casaert S., Vercruysse J., Claerebout E. Molecular epidemiology with subtype analysis of Cryptosporidium in calves in Belgium. Parasitology 2007, 134:1981-1987.
39. Goni P., Martin B., Villacampa M., Garcia A., Seral C., Castillo F.J., Clavel A. Evaluation of an immunochromatographic dip strip test for simultaneous detection of Cryptosporidium spp., Giardia duodenalis, and Entamoeba histolytica antigens in human faecal samples. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31(August (8)):2077-2082.
40. Hassanein S.M., Abd-El-Latif M.M., Hassanin O.M., Abd-El-Latif L.M., Ramadan N.I. Cryptosporidium gastroenteritis in Egyptian children with acute lymphoblastic leukemia: magnitude of the problem. Infection 2012, 40:279-284.
41. Helmy M.M., Rashed L.A., Abdel-Fattah H.S. Co-infection with Cryptosporidium parvum and Cyclospora cayetanensis in immunocompromised patients. J. Egypt. Soc. Parasitol. 2006, 36:613-627.
42. Helmy M.M., Rashed L.A., el-Garhy M.F. Molecular characterization of Cryptosporidium parvum isolates obtained from humans. J. Egypt. Soc. Parasitol. 2004, 34(August):447-458.
43. Hijjawi N., Ng J., Yang R., Atoum M.F., Ryan U. Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Exp. Parasitol. 2010, 125:161-164.
44. Iqbal A., Lim Y.A., Surin J., Sim B.L. High diversity of Cryptosporidium subgenotypes identified in Malaysian HIV/AIDS individuals targeting gp60 gene. PLoS ONE 2012, 7:e31139.
45. Jex A.R., Gasser R.B. Genetic richness and diversity in Cryptosporidium hominis and C. parvum reveals major knowledge gaps and a need for the application of "next generation" technologies-research review. Biotechnol. Adv. 2010, 28:17-26.
46. Khan S.M., Debnath C., Pramanik A.K., Xiao L., Nozaki T., Ganguly S. Molecular characterization and assessment of zoonotic transmission of Cryptosporidium from dairy cattle in West Bengal, India. Vet. Parasitol. 2010, 171:41-47.
47. Khashba A., Hilali M., el-Hennawi S., Marei M. Cryptosporidiosis among children suffering from diarrhea in Benha, Egypt. J. Egypt. Soc. Parasitol. 1989, 19:701-705.
48. Konkle D.M., Nelson K.M., Lunn D.P. Nosocomial transmission of Cryptosporidium in a veterinary hospital. J. Vet. Int. Med. 1997, 11:340-343.
49. Kvac M., Hromadova N., Kvetonova D., Rost M., Sak B. Molecular characterization of Cryptosporidium spp. in pre-weaned dairy calves in the Czech Republic: absence of C. ryanae and management-associated distribution of C. andersoni, C. bovis and C. parvum subtypes. Vet. Parasitol. 2011, 177:378-382.
50. Levine J.F., Levy M.G., Walker R.L., Crittenden S. Cryptosporidiosis in veterinary students. J. Am. Vet. Med. Assess. 1988, 193:1413-1414.
51. Meamar A.R., Guyot K., Certad G., Dei-Cas E., Mohraz M., Mohebali M., Mohammad K., Mehbod A.A., Rezaie S., Rezaian M. Molecular characterization of Cryptosporidium isolates from humans and animals in Iran. Appl. Environ. Microbiol. 2007, 73:1033-1035.
52. Morgan U.M., Pallant L., Dwyer B.W., Forbes D.A., Rich G., Thompson R.C. Comparison of PCR and microscopy for detection of Cryptosporidium parvum in human fecal specimens: clinical trial. J. Clin. Microbiol. 1998, 36:995-998.
53. Nasir A., Avais M., Khan M.S., Ahmed N. Prevalence of Cryptosporidium parvum infection in Lahore (Pakistan) and its association with diarrhea in dairy calves. Int. J. Agric. Biol. 2009, 11:221-224.
54. Neira-Otero P., Munoz-Saldias N., Sanchez-Moreno M., Rosales-Lombardo M.J. Molecular characterization of Cryptosporidium species and genotypes in Chile. Parasitol. Res. 2005, 97:63-67.
55. Newman R.D., Sears C.L., Moore S.R., Nataro J.P., Wuhib T., Agnew D.A., Guerrant R.L., Lima A.A. Longitudinal study of Cryptosporidium infection in children in northeastern Brazil. J. Infect. Dis. 1999, 180:167-175.
56. Ng J.S., Eastwood K., Walker B., Durrheim D.N., Massey P.D., Porigneaux P., Kemp R., McKinnon B., Laurie K., Miller D., Bramley E., Ryan U. Evidence of Cryptosporidium transmission between cattle and humans in northern New South Wales. Exp. Parasitol. 2012, 130:437-441.
57. Nora L.E., Hala A.E., Doaa M.S. Diagnosis of Giardia and Cryptosporidium infection in children with diarrheal illness using rapid immunochromatographic assay. Arch. Clinic. Microbiol. 2012, 3(1).
58. Peng M.M., Matos O., Gatei W., Das P., Stantic-Pavlinic M., Bern C., Sulaiman I.M., Glaberman S., Lal A.A., Xiao L. A comparison of Cryptosporidium subgenotypes from several geographic regions. J. Eukaryot. Microbiol. Suppl. 2001, 28S-31S.
59. Plutzer J., Karanis P. Genetic polymorphism in Cryptosporidium species: an update. Vet. Parasitol. 2009, 165:187-199.
60. Regnath T., Klemm T., Ignatius R. Rapid and accurate detection of Giardia lamblia and Cryptosporidium spp. antigens in human fecal specimens by new commercially available qualitative immunochromatographic assays. Eur. J. Clin. Microbiol. Infect. Dis. 2006, 25:807-809.
61. Ridley R.K., Olsen R.M. Rapid diagnosis of bovine cryptosporidiosis with a modified commercial acid-fast staining procedure. J. Vet. Diagn. Invest. 1991, 3:182-183.
62. Robinson G., Elwin K., Chalmers R.M. Unusual Cryptosporidium genotypes in human cases of diarrhea. Emerg. Infect. Dis. 2008, 14:1800-1802.
63. Safar E.H., Shady O.M., el Adawi A.J., Khattab H.M., Gawdat S.S. Intestinal parasitic infections in immunosuppressed patients. J. Egypt. Soc. Parasitol. 1996, 26:639-643.
64. Samn K.A.M., Samn A.A.M., Abou El-Nour M.F. A survey of Giardia and Cryptosporidium spp. in rural and urban community in North Delta, Egypt. New York Sci. J. 2012, 5:49-54.
65. Shoukry N.M., Dawoud H.A., Haridy F.M. Studies on zoonotic cryptosporidiosis parvum in Ismailia governorate, Egypt. J. Egypt. Soc. Parasitol. 2009, 39:479-488.
66. Singh B.B., Sharma R., Kumar H., Banga H.S., Aulakh R.S., Gill J.P., Sharma J.K. Prevalence of Cryptosporidium parvum infection in Punjab (India) and its association with diarrhea in neonatal dairy calves. Vet. Parasitol. 2006, 140:162-165.
67. Smith H.V., Caccio S.M., Cook N., Nichols R.A., Tait A. Cryptosporidium and Giardia as foodborne zoonoses. Vet. Parasitol. 2007, 149:29-40.
68. Soba B., Logar J. Genetic classification of Cryptosporidium isolates from humans and calves in Slovenia. Parasitology 2008, 135:1263-1270.
69. Soliman N. Cryptosporidium infection among primary school children in a rural area in Alexandria. J. Egypt. Public Health Assoc. 1992, 67:501-519.
70. Sulaiman I.M., Hira P.R., Zhou L., Al-Ali F.M., Al-Shelahi F.A., Shweiki H.M., Iqbal J., Khalid N., Xiao L. Unique endemicity of cryptosporidiosis in children in Kuwait. J. Clin. Microbiol. 2005, 43:2805-2809.
71. Webster K.A., Smith H.V., Giles M., Dawson L., Robertson L.J. Detection of Cryptosporidium parvum oocysts in faeces: comparison of conventional coproscopical methods and the polymerase chain reaction. Vet. Parasitol. 1996, 61:5-13.
72. Weitzel T., Dittrich S., Mohl I., Adusu E., Jelinek T. Evaluation of seven commercial antigen detection tests for Giardia and Cryptosporidium in stool samples. Clin. Microbiol. Infect. Dis. 2006, 12:656-659.
73. Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp. Parasitol. 2010, 124:80-89.
74. Xiao L., Escalante L., Yang C., Sulaiman I., Escalante A.A., Montali R.J., Fayer R., Lal A.A. Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl. Environ. Microbiol. 1999, 65:1578-1583.
75. Xiao L., Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int. J. Parasitol. 2008, 38:1239-1255.