Folia Parasitologica, vol. 64 (2017)

Folia Parasitologica 64:018 (2017) | DOI: 10.14411/fp.2017.018

Cryptosporidium meleagridis and C. baileyi (Apicomplexa) in domestic and wild birds in Algeria

Abd Elkarim Laatamna1, Nikola Holubová2,3, Bohumil Sak2, Martin Kváč2,3
1 Faculty of Natural Sciences and Life, University of Djelfa, Moudjbara, Djelfa, Algeria;
2 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic;
3 Faculty of Agriculture, University of South Bohemia, České Budějovice, Czech Republic

A total of 345 faecal samples were collected from domestic, captive and wild birds in rural areas, urban areas and a Zoo in Algeria. Samples were screened for the presence of parasites belonging to the genus Cryptosporidium Tyzzer, 1910 by microscopy and PCR analysis of the small-subunit rRNA (SSU), actin and 60-kDa glycoprotein (gp60) genes. Cryptosporidium spp. were detected in 31 samples. Sequence analysis of SSU and actin genes revealed the presence of C. baileyi Current, Upton et Haynes, 1986 in domestic chicken broilers (n = 12), captive ostriches (n = 4) and a wild mallard (n = 1), and C. meleagridis Slavin, 1955 in a graylag goose (n = 1), chickens (n = 11) and turkeys (n = 2). Twenty-three chicken and two turkey broilers from five farms were positive for cryptosporidia, with an overall prevalence of 2% and 6%, respectively. Both C. meleagridis and C. baileyi were detected in farmed chicken broilers, with a prevalence ranging from 9% to 69%. Farmed turkeys broilers were positive only for C. meleagridis, with a 13% prevalence at the animal level. Subtyping of C. meleagridis isolates at the gp60 locus showed the presence of subtype IIIgA22G3R1 in graylag goose and chicken broilers and IIIgA23G2R1 in chicken and turkey broilers. Infection with cryptosporidia was not associated with any clinical diseases. The results of the present study, which provides the first data on the prevalence of Cryptosporidium spp. in wild birds in Africa, demonstrate the presence of human pathogenic C. meleagridis in both domestic and wild birds in Algeria.

Keywords: avian cryptosporidia, PCR, epidemiology, Northern Africa

Received: February 23, 2017; Accepted: June 6, 2017; Published online: June 13, 2017


References

  1. Abal-Fabeiro J.L., Maside X., Bello X., Llovo J., Bartolome C. 2013: Multilocus patterns of genetic variation across Cryptosporidium species suggest balancing selection at the gp60 locus. Mol. Ecol. 22: 4723-4732. Go to original source... Go to PubMed...
  2. Alves M., Xiao L.H., Sulaiman I., Lal A.A., Matos O., Antunes F. 2003: Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J. Clin. Microbiol. 41: 2744-2747. Go to original source... Go to PubMed...
  3. Baroudi D., Khelef D., Goucem R., Adjou K.T., Adamu H., Zhang H., Xiao L. 2013: Common occurrence of zoonotic pathogen Cryptosporidium meleagridis in broiler chickens and turkeys in Algeria. Vet. Parasitol. 196: 334-340. Go to original source... Go to PubMed...
  4. Berrilli F., D'Alfonso R., Giangaspero A., Marangi M., Brandonisio O., Kabore Y., Gle C., Cianfanelli C., Lauro R., Di Cave D. 2012: Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Cote d'Ivoire: occurrence and evidence for environmental contamination. Trans. R. Soc. Trop. Med. Hyg. 106: 191-195. Go to original source... Go to PubMed...
  5. Bezuidenhout A.J., Penrith M.L., Burger W.P. 1993: Prolapse of the phallus and cloaca in the ostrich (Struthio camelus). J. S. Afr. Vet. Assoc. 64: 156-158. Go to PubMed...
  6. Cama V.A., Bern C., Roberts J., Cabrera L., Sterling C.R., Ortega Y., Gilman R.H., Xiao L. 2008: Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerg. Infect. Dis. 14: 1567-1574. Go to original source... Go to PubMed...
  7. Cama V.A., Bern C., Sulaiman I.M., Gilman R.H., Ticona E., Vivar A., Kawai V., Vargas D., Zhou L., Xiao L.H. 2003: Cryptosporidium species and genotypes in HIV-positive patients in Lima, Peru. J. Eukaryot. Microbiol. 50: 531-533. Go to original source... Go to PubMed...
  8. Chelladurai J.J., Clark M.E., Kváč M., Holubová N., Khan E., Stenger B.L., Giddings C.W., McEvoy J. 2016: Cryptosporidium galli and novel Cryptosporidium avian genotype VI in North American red-winged blackbirds (Agelaius phoeniceus). Parasitol. Res. 115: 1901-1906. Go to original source... Go to PubMed...
  9. Chvala S., Fragner K., Hackl R., Hess M., Weissenbock H. 2006: Cryptosporidium infection in domestic geese (Anser anser f. domestica) detected by in-situ hybridization. J. Comp. Pathol. 134: 211-218. Go to original source... Go to PubMed...
  10. Current W.L., Upton S.J., Haynes T.B. 1986: The life cycle of Cryptosporidium baileyi n. sp. (Apicomplexa, Cryptosporidiidae) infecting chickens. J. Protozool. 33: 289-296. Go to original source... Go to PubMed...
  11. Essid R., Mousli M., Aoun K., Abdelmalek R., Mellouli F., Kanoun F., Derouin F., Bouratbine A. 2008: Identification of Cryptosporidium species infecting humans in Tunisia. Am. J. Trop. Med. Hyg. 79: 702-705. Go to PubMed...
  12. Gharagozlou M.J., Dezfoulian O., Rahbari S., Bokaie S., Jahanzad I., Razavi A.N.E. 2006: Intestinal cryptosporidiosis in turkeys in Iran. J. Vet. Med. A 53: 282-285. Go to original source...
  13. Goodwin M.A. 1988: Small-intestinal cryptosporidiosis in a chicken. Avian Dis. 32: 844-848. Go to original source... Go to PubMed...
  14. Goodwin M.A., Brown J., Resurreccion R.S., Smith J.A. 1996: Respiratory coccidiosis (Cryptosporidium baileyi) among northern Georgia broilers in one company. Avian Dis. 40: 572-575. Go to original source... Go to PubMed...
  15. Goodwin M.A., Steffens W.L., Russell I.D., Brown J. 1988: Diarrhea associated with intestinal cryptosporidiosis in turkeys. Avian Dis. 32: 63-67. Go to original source... Go to PubMed...
  16. Gordo F.P., Herrera S., Castro A.T., Duran B.G., Diaz R.A.M. 2002: Parasites from farmed ostriches (Struthio camelus) and rheas (Rhea americana) in Europe. Vet. Parasitol. 107: 137-160. Go to original source... Go to PubMed...
  17. Graczyk T.K., Fayer R., Trout J.M., Lewis E.J., Farley C.A., Sulaiman I., Lal A.A. 1998: Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese (Branta canadensis). Appl. Environ. Microbiol. 64: 2736-2738. Go to PubMed...
  18. Graczyk T.K., Majewska A.C., Schwab K.J. 2008: The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol. 24: 55-59. Go to original source... Go to PubMed...
  19. Guo Y., Cebelinski E., Matusevich C., Alderisio K.A., Lebbad M., McEvoy J., Roellig D.M., Yang C., Feng Y., Xiao L. 2015: Subtyping novel zoonotic pathogen Cryptosporidium chipmunk genotype I. J. Clin. Microbiol. 53: 1648-1654. Go to original source... Go to PubMed...
  20. Holubová N., Sak B., Horčičková M., Hlásková L., Květoňová D., Menchaca S., McEvoy J., Kváč M. 2016: Cryptosporidium avium n. sp. (Apicomplexa: Cryptosporidiidae) in birds. Parasitol. Res. 115: 2243-2251. Go to original source... Go to PubMed...
  21. Huber F., da Silva S., Bomfim T.C., Teixeira K.R., Bello A.R. 2007: Genotypic characterization and phylogenetic analysis of Cryptosporidium sp. from domestic animals in Brazil. Vet. Parasitol. 150: 65-74. Go to original source... Go to PubMed...
  22. Jiang J., Alderisio K.A., Xiao L. 2005: Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Appl. Environ. Microbiol. 71: 4446-4454. Go to original source... Go to PubMed...
  23. Kichou F., Saghir F., El Hamidi M. 1996: Infection naturelle à Cryptosporidium sp. chez le poulet de chair au Maroc. Avian. Pathol. 25: 103-111. Go to original source... Go to PubMed...
  24. Kváč M., McEvoy J., Stenger B., Clark M. 2014: Cryptosporidiosis in other vertebrates. In: S.M. Cacciò and G. Widmer (Eds.), Cryptosporidium: Parasite and Disease. Springer, Wien, pp. 237-326.
  25. Kváč M., Ondráčková Z., Květoňová D., Sak B., Vítovec J. 2007: Infectivity and pathogenicity of Cryptosporidium andersoni to a novel host, southern multimammate mouse (Mastomys coucha). Vet. Parasitol. 143: 229-233. Go to original source... Go to PubMed...
  26. Li N., Xiao L., Alderisio K., Elwin K., Cebelinski E., Chalmers R., Santin M., Fayer R., Kváč M., Ryan U., Sak B., Stanko M., Guo Y., Wang L., Zhang L., Cai J., Roellig D., Feng Y. 2014: Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerg. Infect. Dis. 20: 217-224. Go to original source... Go to PubMed...
  27. McEvoy J.M., Giddings C.W. 2009: Cryptosporidium in commercially produced turkeys on-farm and postslaughter. Lett. Appl. Microbiol. 48: 302-306. Go to original source... Go to PubMed...
  28. McLauchlin J., Amar C., Pedraza-Diaz S., Nichols G.L. 2000: Molecular epidemiological analysis of Cryptosporidium spp. in the United Kingdom: results of genotyping Cryptosporidium spp. in 1,705 fecal samples from humans and 105 fecal samples from livestock animals. J. Clin. Microbiol. 38: 3984-3990. Go to PubMed...
  29. Miláček P., Vítovec J. 1985: Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitol. 32: 50. Go to PubMed...
  30. Morgan U.M., Monis P.T., Xiao L., Limor J., Sulaiman I., Raidal S., O'Donoghue P., Gasser R., Murray A., Fayer R., Blagburn B.L., Lal A.A., Thompson R.C. 2001: Molecular and phylogenetic characterisation of Cryptosporidium from birds. Int. J. Parasitol. 31: 289-296. Go to original source... Go to PubMed...
  31. Nakamura A.A., Meireles M.V. 2015: Cryptosporidium infections in birds - a review. Rev. Bras. Parasitol. Vet. 24: 253-267. Go to original source... Go to PubMed...
  32. Ng J., Pavlásek I., Ryan U. 2006: Identification of novel Cryptosporidium genotypes from avian hosts. Appl. Environ. Microbiol. 72: 7548-7553. Go to original source... Go to PubMed...
  33. O'Donoghue P.J. 1995: Cryptosporidium and cryptosporidiosis in man and animals. Int. J. Parasitol. 25: 139-195. Go to original source... Go to PubMed...
  34. Pavlásek I. 1994: [Localization of endogenous developmental stages of Cryptosporidium meleagridis Slavin, 1955 (Apicomplexa: Cryptosporidiidae) in birds]. Vet. Med. (Praha) 39: 733-742. (In Czech.) Go to PubMed...
  35. Penrith M.L., Bezuidenhout A.J., Burger W.P., Putterill J.F. 1994: Evidence for cryptosporidial infection as a cause of prolapse of the phallus and cloaca in ostrich chicks (Struthio camelus). Onderstepoort J. Vet. 61: 283-289. Go to PubMed...
  36. Qi M., Huang L., Wang R., Xiao L., Xu L., Li J., Zhang L. 2014: Natural infection of Cryptosporidium muris in ostriches (Struthio camelus). Vet. Parasitol. 205: 518-522. Go to original source... Go to PubMed...
  37. Rahmouni I., Essid R., Aoun K., Bouratbine A. 2014: Glycoprotein 60 diversity in Cryptosporidium parvum causing human and cattle cryptosporidiosis in the rural region of Northern Tunisia. Am. J. Trop. Med. Hyg. 90: 346-350. Go to original source... Go to PubMed...
  38. Reed K.D., Meece J.K., Henkel J.S., Shukla S.K. 2003: Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin. Med. Res. 1: 5-12. Go to original source... Go to PubMed...
  39. Robertson L.J., Björkman C., Axén C., Fayer R. 2014: Cryptosporidiosis in farmed Animals. In: S.M. Cacciò and G. Widmer (Eds.), Cryptosporidium: Parasite and Disease. Springer, Wien, pp. 149-236.
  40. Ryan U., Xiao L., Read C., Zhou L., Lal A.A., Pavlásek I. 2003b: Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl. Environ. Microbiol. 69: 4302-4307. Go to original source... Go to PubMed...
  41. Ryan U.M., Xiao L., Read C., Sulaiman I.M., Monis P., Lal A.A., Fayer R., Pavlásek I. 2003a: A redescription of Cryptosporidium galli Pavlásek, 1999 (Apicomplexa: Cryptosporidiidae) from birds. J. Parasitol. 89: 809-813. Go to original source... Go to PubMed...
  42. Slavin D. 1955: Cryptosporidium meleagridis (sp. nov.). J. Comp. Pathol. 65: 262-266. Go to original source... Go to PubMed...
  43. Soltane R., Guyot K., Dei-Cas E., Ayadi A. 2007: Prevalence of Cryptosporidium spp. (Eucoccidiorida: Cryptosporiidae) in seven species of farm animals in Tunisia. Parasite 14: 335-338. Go to original source... Go to PubMed...
  44. Stensvold C.R., Beser J., Axen C., Lebbad M. 2014: High applicability of a novel method for gp60-based subtyping of Cryptosporidium meleagridis. J. Clin. Microbiol. 52: 2311-2319. Go to original source... Go to PubMed...
  45. Sulaiman I.M., Lal A.A., Xiao L. 2002: Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. J. Parasitol. 88: 388-394. Go to original source... Go to PubMed...
  46. 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. Go to original source... Go to PubMed...
  47. Wang L., Xue X., Li J., Zhou Q., Yu Y., Du A. 2014: Cryptosporidiosis in broiler chickens in Zhejiang Province, China: molecular characterization of oocysts detected in fecal samples. Parasite 21: 36. Go to original source... Go to PubMed...
  48. Wang R.J., Qi M., Zhu J.J., Sun D., Ning C.S., Zhao J.F., Zhang L.X., Xiao L.H. 2011: Prevalence of Cryptosporidium baileyi in ostriches (Struthio camelus) in Zhengzhou, China. Vet. Parasitol. 175: 151-154. Go to original source... Go to PubMed...
  49. Xiao L., Escalante L., Yang C., Sulaiman I., Escalante A.A., Montali R.J., Fayer R., Lal A.A. 1999: Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl. Environ. Microbiol. 65: 1578-1583. Go to PubMed...
  50. Zhou L., Kassa H., Tischler M.L., Xiao L. 2004: Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl. Environ. Microbiol. 70: 4211-4215. Go to original source... Go to PubMed...