Prevalence and Molecular Characterization of Toxocara cati Infection in Feral Cats in Alexandria City, Northern Egypt
-
Mahmoud Abdelnaby El-Seify
,
Naema Mohammed Marey
,
Neveen Salah Satour
,
Nagwa Mohammed Elhawary
,
Khaled Sultan
Abstract
Background: This study was performed to determine the prevalence and to identify precisely Toxocara spp., which infects feral cats in Alexandria, Egypt based on morphological and molecular approaches.
Methods: This cross-sectional study was carried out on 100 feral cats trapped from different areas of Alexandria during 2018. Adult male and female worms were recovered from small intestinal contents after euthanasia and dissection of cats. Distinct morphological features were initially determined using available keys, and then after amplification and sequencing of the mitochondrial NADH dehydrogenase subunit 1 (nad1) gene was carried out and phylogenetic trees were constructed.
Results: Forty out of 100 cats were infected with Toxocara spp. Intensity of infection ranged from 1 to 9 worms/cat, with a mean of 2.27±1.6. All isolates were confirmed as T. cati based on morphological features and the sequence of nad1 gene. Results of the current study clearly show that Egyptian T. cati isolate examined herein is genetically similar to those recorded in other countries.
Conclusion: The current work revealed high prevalence of T. cati in feral cats in the study area. This is the first genetic study that confirms T. cati from feral cats in Egypt. In addition, it demonstrated the suitability and need of genetic markers such as nad1 for identification of Toxocara spp. Furthermore highlights the public health importance of T. cati in Egypt.
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3. Fisher M. Toxocara cati: an underestimated zoonotic agent. Trends Parasitol. 2003; 19(4):167-170.
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7. Sharghi N, Schantz PM, Caramico L, et al. Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case-control study. Clin Infect Dis. 2001; 32(7):E111-6.
8. Mircean V, Titilincu A, Vasile C. Prevalence of endoparasites in household cat (Felis ca-tus) populations from Transylvania (Ro-mania) and association with risk factors. Vet Parasitol. 2010; 171(1-2):163-166.
9. Nareaho A, Puomio J, Saarinen K, et al. Feline intestinal parasites in Finland: preva-lence, risk factors and anthelmintic treat-ment practices. J Feline Med Surg. 2012; 14(6):378-383.
10. Khalafalla RE. A survey study on gastroin-testinal parasites of stray cats in northern region of Nile delta, Egypt. PLoS One. 2011; 6(7):e20283.
11. El-Seify MA, Aggour MG, Sultan K, Marey NM. Gastrointestinal helminthes of stray cats in Alexandria, Egypt: A fecal ex-amination survey study. Vet Parasitol Reg Stud Reports. 2017; 8:104-106.
12. Rostami S, Salavati R, Beech RN, et al. Ge-netic variability of Taenia saginata inferred from mitochondrial DNA sequences. Par-asitol Res. 2015; 114:1365-1376.
13. Gibbons LM. Keys to the nematode para-sites of vertebrates, Supplementary vol-ume. 10th Vol. CABI: London; 2017.
14. Li K, Luo H, Zhang H, et al. First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Vet Parasitol. 2016; 223:91-95.
15. Oguz B, Ozdal N, Serdae Deger M. Ge-netic analysis of Toxocara sp. in stray cats and dogs in Van province, Esatern Tur-key. J Vet Res. 2018; 62(3):291-295.
16. Mikaeili F, Mirhendi H, Mohebali M, et al. Sequence variation in mitochondrial cox1 and nad1 genes of ascaridoid nematodes in cats and dogs from Iran. J Helminthol. 2015; 89(4):496-501.
17. Sultan K, Omar M, Desouky AY, El-Seify MA. Molecular and phylogenetic study on Toxocara vitulorum from cattle in the mid-Delta of Egypt. J Parasit Dis. 2015; 39(3):584-587.
18. Oguz B. Genetic characterization of Toxo-cara vitulorum in Turkey by mitochondrial gene marker (cox1). Acta Sci Vet. 2018; 46(1):1-6.
19. He XI, Lv Mn, Liu GH, Lin RQ. Genetic analysis of Toxocara cati (Nema-toda:Ascarididae) from Guangdong prov-ince, subtropical China. Mitochondrial DNA A DNA Mapp Seq Anal. 2018; 29(1):132-135.
20. Frihy OE, Dewidar KM, El Raey MM. Evaluation of coastal problems at Alexan-dria, Egypt. Ocean & Coastal Manage-ment. 1996; 30(2-3):281-95.
21. Liu GH, Wang Y, Song HQ, et al. Charac-terization of the complete mitochondrial genome of Spirocerca lupi: sequence, gene organization and phylogenetic implica-tions. Parasit Vectors. 2013; 6:45.
22. Yamaguti S. Systema Helminthum: Nema-todes of vertebrates. (in 2 pts.), 1961. In-terscience publishers; 1958.
23. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. ELBS and Bailliere Tindall: London, UK; 1982.
24. Li K, Lan Y, Luo H, et al. Prevalence, as-sociated risk factors, and phylogenetic analysis of Toxocara vitulorum infection in yaks on the Qinghai Tibetan plateau, Chi-na. Korean J Parasitol. 2016; 54(5):645-652.
25. Altschul SF, Gish W, Miller W, et al. Basic Local Alignment Search Tool. J Mol Biol. 1990; 215(3):403-410.
26. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple se-quence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-4680.
27. Tamura K, Stecher G, Peterson D, et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725–9.
28. Chen J, Liu Q, Liu GH, et al. Toxocariasis: a silent threat with a progressive public health importance. Infect Dis Poverty. 2018; 7(1):59.
29. Sadjjadi SM, Oryan A, Jalali AR, Mehrabani D. Prevalence and intensity of infestation with Toxocara cati stray cats in Shiraz, Iran. Veterinarski Arhiv. 2001; 71(3):149-157.
30. Zibaei M, Sadjjadi SM, Sarkari B. Preva-lence of Toxocara cati and other intestinal helminths in stray cats in Shiraz, Iran. Trop Biomed. 2007; 24(2):39-43.
31. Bahrami AM, Shamsi M. Zoonotic Parasit-ic infections of cats in human community: A histopathological Study. J Bas Res Med Sci. 2015; 2(3):49-56.
32. Capári B, Hamelc D, Visserc M, et al. Par-asitic infections of domestic cats “Felis ca-tus” in western Hungary. Vet Parasitol. 2013; 192(1-3):33-42.
33. Lefkaditis MA, Pastiu AI, Rodi-Buriel A, et al. Helminth burden in stray cats from Thessaloniki, Greece. Helminthologia. 2014; 51(1):73–76.
34. Gürler At, Bölükbaş Cs, Pekmezci Gz, et al. Nematode and cestode eggs scattered with cats-dogs feces and significance of public health in Samsun, Turkey. Ankara Üniv Vet Fak Derg. 2015; 62:23-26
35. Mohsen A, Hooshyar H. Gastrointestinal parasites of stray cats in Kashan, Iran. Trop Biomed. 2009; 26(1):16-22.
36. Changizi E, Mobedi I, Salimi-Bejestani MR, Rezaei-Doust A. Gastrointestinal Helminthic Parasites in stray cats (Felis ca-tus) from North of Iran. Iran J Parasitol. 2007; 2(4):25-29.
37. Prichard R, Tait A. The role of molecular biology in Veterinary Parasitology. Vet Par-asitol. 2001; 98(1-3):169–194.
38. Wickramasinghe S, Yatawara L, Rajapakse RPVJ, Agatsuma T. Toxocara vitulorum (As-caridida: Nematoda): mitochondrial gene content, arrangement and composition compared with other Toxocara spp. Mol Biochem Parasitol. 2009; 166:89–92.
39. Wickramasinghe S, Yatawara L, Rajapakse RPVJ, Agatsuma T. Toxocara canis and Tox-ocara vitulorum: molecular characterization, discrimination, and phylogenetic analysis based on mitochondrial (ATP synthase subunit 6 and 12S) and nuclear ribosomal (ITS-2 and 28S) genes. Parasitol Res. 2009; 104(6):1425–1430.
40. Fava NM, Cury MC, Santos HA, et al. Phylogenetic relationships among Toxocara spp. and Toxascaris sp. from different re-gions of the world. Vet Parasitol. 2020; 282:109133.
41. El-Shazly AMY, Abdel Baset SM, Kamal A, et al. Seroprevalence of human toxoca-riasis (visceral larval migrans). J Egypt Soc Parasitol. 2009; 39:731-744.
42. Awadallah MA, Salem LMA. Zoonotic enteric parasites transmitted from dogs in Egypt with special concern to Toxocara ca-nis infection. Vet World. 2015; 8(8):946-957.
43. Aidaros H. Global Perspectives-the Middle East: Egypt. Rev Sci Tech. 2005; 24(2):589-596.
44. Seimenis A, Tabbaa D. Stray animal popu-lations and public health in the South Mediterranean and Middle East regions. Vet Ital. 2014; 50(2):131-136.
45. Aidaros, H. Control of Rabies in the Mid-dle East Region with Emphasis of stray dog control. Middle East-OIE Regional Commission; 2015.
46. Robertson SA. A review of feral cat con-trol. J Feline Med Surg. 2008; 10(4):366-375.
47. Rostami A, Sepidarkish M, Ma G, et al. Global prevalence of Toxocara infection in cats. Adv Parasitol. 2020; 109:615-639.
2. Li MW, Zhu XQ, Gasser RB, et al. The occurrence of Toxocara malaysiensis in cats in China, confirmed by sequence-based anal-yses of ribosomal DNA. Parasitol Res. 2006; 99(5):554–557.
3. Fisher M. Toxocara cati: an underestimated zoonotic agent. Trends Parasitol. 2003; 19(4):167-170.
4. Smith H, Holland C, Taylor M, et al. How common is human toxocariasis? Towards standardizing our knowledge. Trend Para-sitol. 2009; 25(4):182–188.
5. Akao N, Ohta N. Toxocariasis in Japan. Parasitol Int. 2007; 56(2):87-93.
6. Uga S, Hoa N, Noda S, Moji K, Cong L. Parasite eggs contamination of vegetables from a suburban market in Hanoi, Vi-etnam. Nepal Med Coll J. 2009; 11(2):75-78.
7. Sharghi N, Schantz PM, Caramico L, et al. Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case-control study. Clin Infect Dis. 2001; 32(7):E111-6.
8. Mircean V, Titilincu A, Vasile C. Prevalence of endoparasites in household cat (Felis ca-tus) populations from Transylvania (Ro-mania) and association with risk factors. Vet Parasitol. 2010; 171(1-2):163-166.
9. Nareaho A, Puomio J, Saarinen K, et al. Feline intestinal parasites in Finland: preva-lence, risk factors and anthelmintic treat-ment practices. J Feline Med Surg. 2012; 14(6):378-383.
10. Khalafalla RE. A survey study on gastroin-testinal parasites of stray cats in northern region of Nile delta, Egypt. PLoS One. 2011; 6(7):e20283.
11. El-Seify MA, Aggour MG, Sultan K, Marey NM. Gastrointestinal helminthes of stray cats in Alexandria, Egypt: A fecal ex-amination survey study. Vet Parasitol Reg Stud Reports. 2017; 8:104-106.
12. Rostami S, Salavati R, Beech RN, et al. Ge-netic variability of Taenia saginata inferred from mitochondrial DNA sequences. Par-asitol Res. 2015; 114:1365-1376.
13. Gibbons LM. Keys to the nematode para-sites of vertebrates, Supplementary vol-ume. 10th Vol. CABI: London; 2017.
14. Li K, Luo H, Zhang H, et al. First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Vet Parasitol. 2016; 223:91-95.
15. Oguz B, Ozdal N, Serdae Deger M. Ge-netic analysis of Toxocara sp. in stray cats and dogs in Van province, Esatern Tur-key. J Vet Res. 2018; 62(3):291-295.
16. Mikaeili F, Mirhendi H, Mohebali M, et al. Sequence variation in mitochondrial cox1 and nad1 genes of ascaridoid nematodes in cats and dogs from Iran. J Helminthol. 2015; 89(4):496-501.
17. Sultan K, Omar M, Desouky AY, El-Seify MA. Molecular and phylogenetic study on Toxocara vitulorum from cattle in the mid-Delta of Egypt. J Parasit Dis. 2015; 39(3):584-587.
18. Oguz B. Genetic characterization of Toxo-cara vitulorum in Turkey by mitochondrial gene marker (cox1). Acta Sci Vet. 2018; 46(1):1-6.
19. He XI, Lv Mn, Liu GH, Lin RQ. Genetic analysis of Toxocara cati (Nema-toda:Ascarididae) from Guangdong prov-ince, subtropical China. Mitochondrial DNA A DNA Mapp Seq Anal. 2018; 29(1):132-135.
20. Frihy OE, Dewidar KM, El Raey MM. Evaluation of coastal problems at Alexan-dria, Egypt. Ocean & Coastal Manage-ment. 1996; 30(2-3):281-95.
21. Liu GH, Wang Y, Song HQ, et al. Charac-terization of the complete mitochondrial genome of Spirocerca lupi: sequence, gene organization and phylogenetic implica-tions. Parasit Vectors. 2013; 6:45.
22. Yamaguti S. Systema Helminthum: Nema-todes of vertebrates. (in 2 pts.), 1961. In-terscience publishers; 1958.
23. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. ELBS and Bailliere Tindall: London, UK; 1982.
24. Li K, Lan Y, Luo H, et al. Prevalence, as-sociated risk factors, and phylogenetic analysis of Toxocara vitulorum infection in yaks on the Qinghai Tibetan plateau, Chi-na. Korean J Parasitol. 2016; 54(5):645-652.
25. Altschul SF, Gish W, Miller W, et al. Basic Local Alignment Search Tool. J Mol Biol. 1990; 215(3):403-410.
26. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple se-quence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-4680.
27. Tamura K, Stecher G, Peterson D, et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725–9.
28. Chen J, Liu Q, Liu GH, et al. Toxocariasis: a silent threat with a progressive public health importance. Infect Dis Poverty. 2018; 7(1):59.
29. Sadjjadi SM, Oryan A, Jalali AR, Mehrabani D. Prevalence and intensity of infestation with Toxocara cati stray cats in Shiraz, Iran. Veterinarski Arhiv. 2001; 71(3):149-157.
30. Zibaei M, Sadjjadi SM, Sarkari B. Preva-lence of Toxocara cati and other intestinal helminths in stray cats in Shiraz, Iran. Trop Biomed. 2007; 24(2):39-43.
31. Bahrami AM, Shamsi M. Zoonotic Parasit-ic infections of cats in human community: A histopathological Study. J Bas Res Med Sci. 2015; 2(3):49-56.
32. Capári B, Hamelc D, Visserc M, et al. Par-asitic infections of domestic cats “Felis ca-tus” in western Hungary. Vet Parasitol. 2013; 192(1-3):33-42.
33. Lefkaditis MA, Pastiu AI, Rodi-Buriel A, et al. Helminth burden in stray cats from Thessaloniki, Greece. Helminthologia. 2014; 51(1):73–76.
34. Gürler At, Bölükbaş Cs, Pekmezci Gz, et al. Nematode and cestode eggs scattered with cats-dogs feces and significance of public health in Samsun, Turkey. Ankara Üniv Vet Fak Derg. 2015; 62:23-26
35. Mohsen A, Hooshyar H. Gastrointestinal parasites of stray cats in Kashan, Iran. Trop Biomed. 2009; 26(1):16-22.
36. Changizi E, Mobedi I, Salimi-Bejestani MR, Rezaei-Doust A. Gastrointestinal Helminthic Parasites in stray cats (Felis ca-tus) from North of Iran. Iran J Parasitol. 2007; 2(4):25-29.
37. Prichard R, Tait A. The role of molecular biology in Veterinary Parasitology. Vet Par-asitol. 2001; 98(1-3):169–194.
38. Wickramasinghe S, Yatawara L, Rajapakse RPVJ, Agatsuma T. Toxocara vitulorum (As-caridida: Nematoda): mitochondrial gene content, arrangement and composition compared with other Toxocara spp. Mol Biochem Parasitol. 2009; 166:89–92.
39. Wickramasinghe S, Yatawara L, Rajapakse RPVJ, Agatsuma T. Toxocara canis and Tox-ocara vitulorum: molecular characterization, discrimination, and phylogenetic analysis based on mitochondrial (ATP synthase subunit 6 and 12S) and nuclear ribosomal (ITS-2 and 28S) genes. Parasitol Res. 2009; 104(6):1425–1430.
40. Fava NM, Cury MC, Santos HA, et al. Phylogenetic relationships among Toxocara spp. and Toxascaris sp. from different re-gions of the world. Vet Parasitol. 2020; 282:109133.
41. El-Shazly AMY, Abdel Baset SM, Kamal A, et al. Seroprevalence of human toxoca-riasis (visceral larval migrans). J Egypt Soc Parasitol. 2009; 39:731-744.
42. Awadallah MA, Salem LMA. Zoonotic enteric parasites transmitted from dogs in Egypt with special concern to Toxocara ca-nis infection. Vet World. 2015; 8(8):946-957.
43. Aidaros H. Global Perspectives-the Middle East: Egypt. Rev Sci Tech. 2005; 24(2):589-596.
44. Seimenis A, Tabbaa D. Stray animal popu-lations and public health in the South Mediterranean and Middle East regions. Vet Ital. 2014; 50(2):131-136.
45. Aidaros, H. Control of Rabies in the Mid-dle East Region with Emphasis of stray dog control. Middle East-OIE Regional Commission; 2015.
46. Robertson SA. A review of feral cat con-trol. J Feline Med Surg. 2008; 10(4):366-375.
47. Rostami A, Sepidarkish M, Ma G, et al. Global prevalence of Toxocara infection in cats. Adv Parasitol. 2020; 109:615-639.
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| Issue | Vol 16 No 2 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i2.6319 | |
| Keywords | ||
| Cat Toxocara cati Prevalence Molecular Egypt | ||
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How to Cite
1.
Abdelnaby El-Seify M, Marey N, Salah Satour N, Mohammed Elhawary N, Sultan K. Prevalence and Molecular Characterization of Toxocara cati Infection in Feral Cats in Alexandria City, Northern Egypt. Iran J Parasitol. 2021;16(2):270-278.
