The Prevalence of Intestinal Helminths in Free-Ranging Canids of Mazandaran, Northern Iran
-
Abolghasem SIYADATPANAH
,
Shirzad GHOLAMI
,
Ahmad DARYANI
,
Shahabeddin SARVI
,
Mehdi SHARIF
,
Mauricio SEGUEL
,
Larson BOUNDENGA
,
Afsaneh AMOUEI
,
Abdol Sattar PAGHEH
,
Mohammad Taghi RAHIMI
,
Seyed Abdollah HOSSEINI
,
Davood ANVARI
Abstract
Background: The purpose of this study was to investigate the current knowledge on the epidemiology of importance zoonotic parasitic diseases in free-ranging canids of Mazandaran, north of Iran.
Methods: Overall, 63 small intestinal samples of animals (20 stray dogs and 43 golden jackals) were collected from April 2017 to May 2018. The intestine contents were studied to detect and identify helminth infections. Additionally, 274 fecal samples (130 dogs, 35 fox, 90 golden jackal and 19 wolf) were examined by Sheather's flotation method for detection of Taenia eggs.
Results: Sixty (95.2%) animals were infected with at least one species of intestinal helminth. the intestinal helminths were found in dogs and golden jackals included: Dipylidium caninum (25.3%), Uncinaria stenocephala (52.3%), Ancylostoma caninum (41.2%), Mesocestoides spp. (33.3%) and Toxocara canis (14.2%). In fecal examination, 2.5% of samples contained Taenia eggs, and through a species-specific PCR, 1.09% of these samples were confirmed positive for Echinococcus granulosus.
Conclusion: There is a high prevalence and clear risks of zoonotic helminths in free-ranging carnivores in Mazandaran province, north of Iran. Therefore, understanding the epidemiology of zoonotic parasite infection is useful for health care access both domestic animals and humans health.
1. Chidumayo NN. Epidemiology of canine gastrointestinal helminths in sub-Saharan Africa. Parasit Vectors. 2018;11(1):100.
2. Zare-Bidaki M, Mobedi I, Ahari SS et al. Prevalence of zoonotic intestinal helminths of canids in moghan plain, northwestern iran. Iran J Parasitol. 2010;5(2):42-51.
3. Thompson RC, Kutz SJ, Smith A. Parasite zoonoses and wildlife: emerging issues. Int J Environ Res Public Health. 2009;6(2):678-93.
4. Massei G, Miller LA. Nonsurgical fertility control for managing free-roaming dog populations: a review of products and cri-teria for field applications. Theriogenology. 2013;80(8):829-38.
5. Lembo T, Craig PS, Miles MA et al. Zo-onoses Prevention, Control, and Elimina-tion in Dogs. In: Macpherson, C.N.L., Meslin, F.X. and Wandeler, A.I. (eds.) Dogs, Zoonoses and Public Health. CABI: Oxford, UK, pp. 205-258.
6. Little SE, Johnson EM, Lewis D et al. Prevalence of intestinal parasites in pet dogs in the United States. Vet Parasitol. 2009;166(1-2):144-52.
7. Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop. 2001;78(2):103-16.
8. Dalimi A, Motamedi G, Hosseini M et al. Echinococcosis/hydatidosis in western Iran. Vet Parasitol. 2002;105(2):161-71.
9. Tun S, Ithoi I, Mahmud R et al. Detection of Helminth Eggs and Identification of Hookworm Species in Stray Cats, Dogs and Soil from Klang Valley, Malaysia. PLoS One. 2015;10(12):e0142231.
10. Stacey A. Elmore, Laura F. Lalonde, Gus-taf Samelius et al. Endoparasites in the fe-ces of arctic foxes in a terrestrial ecosystem in Canada. Int J Parasitol Parasites Wildl. 2013;2: 90–96.
11. Anvari D, Saadati D, Nabavi R, Alipour eskandani M. Epidemiology and Molecular Prevalence of Toxoplasma gondii in Cattle Slaughtered in Zahedan and Zabol Dis-tricts, South East of Iran. Iran J Parasitol. 2018;13(1):114–119.
12. Vergles Rataj A, Posedi J, Zele D, Vengušt G. Intestinal parasites of the red fox (Vul-pes vulpes) in Slovenia. Acta Vet Hung. 2013;61(4):454-62.
13. Al-Jassim KBN, Mahmmod YS, Salem ZM, Al-Jubury A. Epidemiological investi-gation of gastrointestinal parasites in dog populations in Basra province, Southern Iraq. J Parasit Dis. 2017;41(4):1006-1013.
14. Savilla TM, Joy JE, May JD, Somerville CC. Prevalence of dog intestinal nematode parasites in south central West Virginia, USA. Vet Parasitol. 2011;178(1-2):115-20.
15. Nabavi R, Manouchehri Naeini K, Zebar-dast N, Hashemi H. Epidemiological study of gastrointestinal helminthes of canids in chaharmahal and bakhtiari province of iran. Iran J Parasitol. 2014;9(2):276-81.
16. Adinezadeh A, Kia EB, Mohebali M et al. Endoparasites of stray dogs in mashhad, khorasan razavi province, northeast iran with special reference to zoonotic para-sites. Iran J Parasitol. 2013;8(3):459-66.
17. Gholami I, Daryani A, Sharif M et al. Seroepidemiological survey of helminthic parasites of stray dogs in Sari City, north-ern Iran. Pak J Biol Sci. 2011;14(2):133-7.
18. Moshfe A, Mowlavi G, Mobedi I et al. Fauna of Zoontic Parasites of Stray Dogs in Yasouj Suburbs in 2008. Armaghane Danesh Bimonthly Journal. 2011;16(1):80-9.
19. Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Int J Parasitol Parasites Wildl. 2017;6(3):177-194.
20. Rojas CAA, Mathis A, Deplazes P. As-sessing the Contamination of Food and the Environment With Taenia and Echino-coccus Eggs and Their Zoonotic Transmis-sion. Curr Clin Microbiol Rep. 2018;5(2):154-63.
21. Raoul F, Deplazes P, Nonaka N et al. As-sessment of the epidemiological status of Echinococcus multilocularis in foxes in France using ELISA coprotests on fox faeces col-lected in the field. Int J Parasitol. 2001;31(14):1579-88.
22. Weischer B. Nematode parasites of verte-brates: their development and transmis-sion: Cabi; 2000. ISBN-10: 0851994210.
23. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals: Bailliere Tindall; 1982.
24. Dryden MW, Payne PA, Ridley R, Smith V. Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts. Vet Ther. 2005;6(1):15-28.
25. Bowles J, McManus DP. Genetic charac-terization of the Asian Taenia, a newly de-scribed taeniid cestode of humans. Am J Trop Med Hyg. 1994;50(1):33-44.
26. Dalimi A, Mobedi I. Helminth parasites of carnivores in northern Iran. Ann Trop Med Parasitol. 1992;86(4):395-7.
27. Kimura A, Morishima Y, Nagahama S et al. A coprological survey of intestinal hel-minthes in stray dogs captured in osaka prefecture, Japan. J Vet Med Sci. 2013;75(10):1409-11.
28. Emamapour SR, Borji H, Nagibi A. An epidemiological survey on intestinal hel-minths of stray dogs in Mashhad, North-east of Iran. J Parasit Dis. 2015;39(2):266-71.
29. Fiocchi A, Gustinelli A, Gelmini L et al. Helminth parasites of the red fox Vulpes vulpes (L., 1758) and the wolf Canis lupus ital-icus Altobello, 1921 in Emilia-Romagna, Italy. Ital J Zool. 2016;83(4):503-13.
30. Takács A, Szabó L, Juhász L et al. Data on the parasitological status of golden jackal (Canis aureus L., 1758) in Hungary. Acta Vet Hung. 2014;62(1):33-41.
31. Croese J, Loukas A, Opdebeeck J, Prociv P. Occult enteric infection by Ancylostoma caninum: a previously unrecognized zoono-sis. Gastroenterology. 1994;106(1):3-12.
32. Loukas A, Croese J, Opdebeeck J, Prociv P. Detection of antibodies to secretions of Ancylostoma caninum in human eosinophilic enteritis. Trans R Soc Trop Med Hyg. 1992;86(6):650-3.
33. Mahdy MA, Lim YA, Ngui R et al. Preva-lence and zoonotic potential of canine hookworms in Malaysia. Parasit Vectors. 2012;5:88.
34. Cantó GJ, García MP, García A et al. The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico. J Helminthol. 2011;85(3):263-9.
35. Eira C, Vingada J, Torres J, Miquel J. The helminth community of the red fox, Vulpes vulpes, in Dunas de Mira (Portugal) and its effect on host condition. Wildl Biol Pract. 2006.
36. Papdopoulos H, Himonas C, Papazahari-adou M, Antoniadou-Sotiriadou K. Hel-minths of foxes and other wild carnivores from rural areas in Greece. J Helminthol. 1997;71(3):227-31.
37. Ramírez-Barrios RA, Barboza-Mena G, Muñoz J et al. Prevalence of intestinal par-asites in dogs under veterinary care in Maracaibo, Venezuela. Vet Parasitol. 2004;121(1-2):11-20.
38. Martínez-Moreno FJ, Hernández S, López-Cobos E et al. Estimation of ca-nine intestinal parasites in Cordoba (Spain) and their risk to public health. Vet Parasi-tol. 2007;143(1):7-13.
39. Garedaghi Y. Prevalence of gastrointestinal helminthic infestation in pet and stray dogs in Tabriz (East-Azerbaijan Province), Iran. Advances in Environmental Biology. 2011:735-9.
40. Umar Y. Intestinal helminthoses in dogs in Kaduna metropolis, Kaduna state, Nige-ria. Iran J Parasitol. 2009;4(1):34-9.
41. Jiang P, Zhang X1, Liu RD et al. A Hu-man Case of Zoonotic Dog Tapeworm, Dipylidium caninum (Eucestoda: Dilepidiidae), in China. Korean J Parasitol. 2017;55(1):61-64.
42. Dalimi A, Sattari A, Motamedi G. A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet Parasitol. 2006;142(1-2):129-33.
43. El-Tras WF, Holt HR, Tayel AA. Risk of Toxocara canis eggs in stray and domestic dog hair in Egypt. Vet Parasitol. 2011;178(3-4):319-23.
44. Oudni-M'rad M, Chaâbane-Banaoues R, M'rad S et al. Gastrointestinal parasites of canids, a latent risk to human health in Tunisia. Parasit Vectors. 2017;10(1):280.
45. Macpherson CN. The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. Int J Para-sitol. 2013;43(12-13):999-1008.
46. Magnaval JF, Glickman LT, Dorchies P, Morassin B. Highlights of human toxoca-riasis. Korean J Parasitol. 2001;39(1):1-11.
47. Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev. 1981;3:230-50.
48. WHO. Echinococcosis 2016 [Available from: http://www.who.int/mediacentre/factsheets/fs377/en/
49. Shariatzadeh SA, Spotin A, Gholami S et al. The first morphometric and phyloge-netic perspective on molecular epidemiol-ogy of Echinococcus granulosus sensu lato in stray dogs in a hyperendemic Middle East focus, northwestern Iran. Parasit Vectors. 20156;8:409.
50. Rahmati K, Maghsoud AH, Matini M et al. Study of Intestinal Helminthes of Stray Dogs and Thir Public Heath Importance in Hamadan City. Scientific Journal of Hamadan University of Medical Sciences. 2016;23(3):214-20.
51. Sardarian K, Maghsood AH, Ghiasian SA, Zahirnia AH. Prevalence of zoonotic intes-tinal parasites in household and stray dogs in rural areas of Hamadan, Western Iran. Trop Biomed. 2015;32(2):240-6.
2. Zare-Bidaki M, Mobedi I, Ahari SS et al. Prevalence of zoonotic intestinal helminths of canids in moghan plain, northwestern iran. Iran J Parasitol. 2010;5(2):42-51.
3. Thompson RC, Kutz SJ, Smith A. Parasite zoonoses and wildlife: emerging issues. Int J Environ Res Public Health. 2009;6(2):678-93.
4. Massei G, Miller LA. Nonsurgical fertility control for managing free-roaming dog populations: a review of products and cri-teria for field applications. Theriogenology. 2013;80(8):829-38.
5. Lembo T, Craig PS, Miles MA et al. Zo-onoses Prevention, Control, and Elimina-tion in Dogs. In: Macpherson, C.N.L., Meslin, F.X. and Wandeler, A.I. (eds.) Dogs, Zoonoses and Public Health. CABI: Oxford, UK, pp. 205-258.
6. Little SE, Johnson EM, Lewis D et al. Prevalence of intestinal parasites in pet dogs in the United States. Vet Parasitol. 2009;166(1-2):144-52.
7. Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop. 2001;78(2):103-16.
8. Dalimi A, Motamedi G, Hosseini M et al. Echinococcosis/hydatidosis in western Iran. Vet Parasitol. 2002;105(2):161-71.
9. Tun S, Ithoi I, Mahmud R et al. Detection of Helminth Eggs and Identification of Hookworm Species in Stray Cats, Dogs and Soil from Klang Valley, Malaysia. PLoS One. 2015;10(12):e0142231.
10. Stacey A. Elmore, Laura F. Lalonde, Gus-taf Samelius et al. Endoparasites in the fe-ces of arctic foxes in a terrestrial ecosystem in Canada. Int J Parasitol Parasites Wildl. 2013;2: 90–96.
11. Anvari D, Saadati D, Nabavi R, Alipour eskandani M. Epidemiology and Molecular Prevalence of Toxoplasma gondii in Cattle Slaughtered in Zahedan and Zabol Dis-tricts, South East of Iran. Iran J Parasitol. 2018;13(1):114–119.
12. Vergles Rataj A, Posedi J, Zele D, Vengušt G. Intestinal parasites of the red fox (Vul-pes vulpes) in Slovenia. Acta Vet Hung. 2013;61(4):454-62.
13. Al-Jassim KBN, Mahmmod YS, Salem ZM, Al-Jubury A. Epidemiological investi-gation of gastrointestinal parasites in dog populations in Basra province, Southern Iraq. J Parasit Dis. 2017;41(4):1006-1013.
14. Savilla TM, Joy JE, May JD, Somerville CC. Prevalence of dog intestinal nematode parasites in south central West Virginia, USA. Vet Parasitol. 2011;178(1-2):115-20.
15. Nabavi R, Manouchehri Naeini K, Zebar-dast N, Hashemi H. Epidemiological study of gastrointestinal helminthes of canids in chaharmahal and bakhtiari province of iran. Iran J Parasitol. 2014;9(2):276-81.
16. Adinezadeh A, Kia EB, Mohebali M et al. Endoparasites of stray dogs in mashhad, khorasan razavi province, northeast iran with special reference to zoonotic para-sites. Iran J Parasitol. 2013;8(3):459-66.
17. Gholami I, Daryani A, Sharif M et al. Seroepidemiological survey of helminthic parasites of stray dogs in Sari City, north-ern Iran. Pak J Biol Sci. 2011;14(2):133-7.
18. Moshfe A, Mowlavi G, Mobedi I et al. Fauna of Zoontic Parasites of Stray Dogs in Yasouj Suburbs in 2008. Armaghane Danesh Bimonthly Journal. 2011;16(1):80-9.
19. Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Int J Parasitol Parasites Wildl. 2017;6(3):177-194.
20. Rojas CAA, Mathis A, Deplazes P. As-sessing the Contamination of Food and the Environment With Taenia and Echino-coccus Eggs and Their Zoonotic Transmis-sion. Curr Clin Microbiol Rep. 2018;5(2):154-63.
21. Raoul F, Deplazes P, Nonaka N et al. As-sessment of the epidemiological status of Echinococcus multilocularis in foxes in France using ELISA coprotests on fox faeces col-lected in the field. Int J Parasitol. 2001;31(14):1579-88.
22. Weischer B. Nematode parasites of verte-brates: their development and transmis-sion: Cabi; 2000. ISBN-10: 0851994210.
23. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals: Bailliere Tindall; 1982.
24. Dryden MW, Payne PA, Ridley R, Smith V. Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts. Vet Ther. 2005;6(1):15-28.
25. Bowles J, McManus DP. Genetic charac-terization of the Asian Taenia, a newly de-scribed taeniid cestode of humans. Am J Trop Med Hyg. 1994;50(1):33-44.
26. Dalimi A, Mobedi I. Helminth parasites of carnivores in northern Iran. Ann Trop Med Parasitol. 1992;86(4):395-7.
27. Kimura A, Morishima Y, Nagahama S et al. A coprological survey of intestinal hel-minthes in stray dogs captured in osaka prefecture, Japan. J Vet Med Sci. 2013;75(10):1409-11.
28. Emamapour SR, Borji H, Nagibi A. An epidemiological survey on intestinal hel-minths of stray dogs in Mashhad, North-east of Iran. J Parasit Dis. 2015;39(2):266-71.
29. Fiocchi A, Gustinelli A, Gelmini L et al. Helminth parasites of the red fox Vulpes vulpes (L., 1758) and the wolf Canis lupus ital-icus Altobello, 1921 in Emilia-Romagna, Italy. Ital J Zool. 2016;83(4):503-13.
30. Takács A, Szabó L, Juhász L et al. Data on the parasitological status of golden jackal (Canis aureus L., 1758) in Hungary. Acta Vet Hung. 2014;62(1):33-41.
31. Croese J, Loukas A, Opdebeeck J, Prociv P. Occult enteric infection by Ancylostoma caninum: a previously unrecognized zoono-sis. Gastroenterology. 1994;106(1):3-12.
32. Loukas A, Croese J, Opdebeeck J, Prociv P. Detection of antibodies to secretions of Ancylostoma caninum in human eosinophilic enteritis. Trans R Soc Trop Med Hyg. 1992;86(6):650-3.
33. Mahdy MA, Lim YA, Ngui R et al. Preva-lence and zoonotic potential of canine hookworms in Malaysia. Parasit Vectors. 2012;5:88.
34. Cantó GJ, García MP, García A et al. The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico. J Helminthol. 2011;85(3):263-9.
35. Eira C, Vingada J, Torres J, Miquel J. The helminth community of the red fox, Vulpes vulpes, in Dunas de Mira (Portugal) and its effect on host condition. Wildl Biol Pract. 2006.
36. Papdopoulos H, Himonas C, Papazahari-adou M, Antoniadou-Sotiriadou K. Hel-minths of foxes and other wild carnivores from rural areas in Greece. J Helminthol. 1997;71(3):227-31.
37. Ramírez-Barrios RA, Barboza-Mena G, Muñoz J et al. Prevalence of intestinal par-asites in dogs under veterinary care in Maracaibo, Venezuela. Vet Parasitol. 2004;121(1-2):11-20.
38. Martínez-Moreno FJ, Hernández S, López-Cobos E et al. Estimation of ca-nine intestinal parasites in Cordoba (Spain) and their risk to public health. Vet Parasi-tol. 2007;143(1):7-13.
39. Garedaghi Y. Prevalence of gastrointestinal helminthic infestation in pet and stray dogs in Tabriz (East-Azerbaijan Province), Iran. Advances in Environmental Biology. 2011:735-9.
40. Umar Y. Intestinal helminthoses in dogs in Kaduna metropolis, Kaduna state, Nige-ria. Iran J Parasitol. 2009;4(1):34-9.
41. Jiang P, Zhang X1, Liu RD et al. A Hu-man Case of Zoonotic Dog Tapeworm, Dipylidium caninum (Eucestoda: Dilepidiidae), in China. Korean J Parasitol. 2017;55(1):61-64.
42. Dalimi A, Sattari A, Motamedi G. A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet Parasitol. 2006;142(1-2):129-33.
43. El-Tras WF, Holt HR, Tayel AA. Risk of Toxocara canis eggs in stray and domestic dog hair in Egypt. Vet Parasitol. 2011;178(3-4):319-23.
44. Oudni-M'rad M, Chaâbane-Banaoues R, M'rad S et al. Gastrointestinal parasites of canids, a latent risk to human health in Tunisia. Parasit Vectors. 2017;10(1):280.
45. Macpherson CN. The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. Int J Para-sitol. 2013;43(12-13):999-1008.
46. Magnaval JF, Glickman LT, Dorchies P, Morassin B. Highlights of human toxoca-riasis. Korean J Parasitol. 2001;39(1):1-11.
47. Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev. 1981;3:230-50.
48. WHO. Echinococcosis 2016 [Available from: http://www.who.int/mediacentre/factsheets/fs377/en/
49. Shariatzadeh SA, Spotin A, Gholami S et al. The first morphometric and phyloge-netic perspective on molecular epidemiol-ogy of Echinococcus granulosus sensu lato in stray dogs in a hyperendemic Middle East focus, northwestern Iran. Parasit Vectors. 20156;8:409.
50. Rahmati K, Maghsoud AH, Matini M et al. Study of Intestinal Helminthes of Stray Dogs and Thir Public Heath Importance in Hamadan City. Scientific Journal of Hamadan University of Medical Sciences. 2016;23(3):214-20.
51. Sardarian K, Maghsood AH, Ghiasian SA, Zahirnia AH. Prevalence of zoonotic intes-tinal parasites in household and stray dogs in rural areas of Hamadan, Western Iran. Trop Biomed. 2015;32(2):240-6.
| Files | ||
| Issue | Vol 14 No 4 (2019) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v14i4.2098 | |
| Keywords | ||
| Canids Intestinal helminth Iran | ||
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How to Cite
1.
SIYADATPANAH A, GHOLAMI S, DARYANI A, SARVI S, SHARIF M, SEGUEL M, BOUNDENGA L, AMOUEI A, PAGHEH AS, RAHIMI MT, HOSSEINI SA, ANVARI D. The Prevalence of Intestinal Helminths in Free-Ranging Canids of Mazandaran, Northern Iran. Iran J Parasitol. 2019;14(4):563-571.
