Investigation of Zoonotic Cryptosporidium and 
Giardia intestinalis Species and Genotypes in Cats 
(Felis catus)

ONDER, Zuhal; Yetismis, Gamze; Inci, Abdullah; DUZLU, Onder; Yıldırım, Alparslan; CILOGLU, ARIF; DELİBAŞI, Nesrin; Pekmezci, Gokmen Zafer; PEKMEZCİ, Didem

doi:10.4274/tpd.galenos.2021.46320

Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)

Zuhal ÖNDER, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Gamze YETİŞMİŞ, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Didem PEKMEZCİ, (Ondokuz Mayıs University Faculty of Veterinary Medicine, Department of Internal Medicine, Samsun, Turkey)

Nesrin DELİBAŞI KÖKÇÜ, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Gökmen Zafer PEKMEZCİ, (Ondokuz Mayıs University Faculty of Veterinary Medicine, Department of Preclinical Science, Samsun, Turkey)

Arif ÇİLOĞLU, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Önder DÜZLÜ, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Abdullah İNCİ, (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Alparslan YILDIRIM (Erciyes University Faculty of Veterinary Medicine, Department of Parasitology, Kayseri, Turkey)

Türkiye Parazitoloji Dergisi

11 2

Yıl: 2021 Cilt: 45 Sayı: 4 Sayfa Aralığı: 252 - 256 Metin Dili: İngilizce DOI: 10.4274/tpd.galenos.2021.46320 İndeks Tarihi: 25-05-2022

Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)

Öz:

Objective: Giardia intestinalis and Cryptosporidium spp. are important zoonotic protozoan parasites that infect humans and various animals. We investigated the occurrence of G. intestinalis and Cryptosporidium spp. infection in cats. To provide data on the zoonotic transmission dynamics of these parasites, genotypes of the detected isolates were investigated through DNA sequence characterization. Methods: A total of 100 fecal samples were collected from cats between June and October 2020 in Kayseri and Samsun provinces. Fecal samples were examined by nested polymerase chain reaction (PCR), targeting the β-giardin gene of G. intestinalis and small subunit (SSU) rRNA gene of Cryptosporidium spp. All PCR products were sequenced for genotyping. Results: Of the samples examined, Giardia intestinalis was determined in 8 samples (8.0%), whereas none of the samples were found positive for Cryptosporidium spp. Sequence analyses of the β-giardin PCR products indicated that all G. intestinalis isolates were classed into the zoonotic assemblage B. Conclusion: This study adds to the current data on the molecular epidemiology of cryptosporidiosis and giardiasis in cats. The findings also highlight the potential risk of cats for public health concerning the zoonotic transmission dynamics of G. intestinalis.

Anahtar Kelime:

Kedilerde (Felis catus) Zoonotik Cryptosporidium ve Giardia intestinalisTür/Genotiplerinin Araştırılması

Öz:

Amaç: Giardia intestinalis ve Cryptosporidium spp. insanları ve çeşitli hayvanları enfekte eden, önemli zoonotik protozoon parazitlerdendir. Bu çalışmanın amacı, kedilerde G. intestinalis ve Cryptosporidium spp. varlığını belirlemek ve zoonotik bulaşma dinamikleri açısından izolatların moleküler karakterizasyonunu yaparak genotiplerini ortaya çıkarmaktır. Yöntemler: Kayseri ve Samsun illerinde, Haziran-Ekim 2020 tarihleri arasında toplam 100 kediden dışkı örneği toplanmıştır. Dışkı örnekleri, G. intestinalis’in β-giardin genini ve Cryptosporidium spp.’nin small subunit ribosomal RNA (SSU) rRNA genini hedefleyen nested polimeraz zincir reaksiyon (PZR) analizleri ile incelenmiştir. Tüm PCR ürünleri genotipleme için sekanslanmıştır. Bulgular: İncelemesi yapılan örneklerin 8’inde (%8,0) G. intestinalis pozitifliği belirlenirken, Cryptosporidium spp. enfeksiyonuna rastlanmamıştır. G. intestinalis izolatlarının sekans analizleri sonucu zoonotik assemblage B içerisinde olduğu tespit edilmiştir. Sonuç: Bu çalışma, kedilerde Cryptosporidiosis ve Giardiasis’in moleküler epidemiyolojisi üzerine mevcut bilgi birikimine katkı sağlamıştır. Ayrıca, elde edilen çıktılar G. intestinalis’in zoonotik bulaşma dinamikleri çerçevesinde kedilerin halk sağlığı açısından risk potansiyelini vurgulamıştır.

Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. de Aquino MCC, Inácio SV, Rodrigues FS, de Barros LD, Garcia JL, Headley SA, et al. Cryptosporidiosis and giardiasis in buffaloes (Bubalus bubalis). Front Vet Sci 2020; 7: 557967.
2. Li W, Liu X, Gu Y, Liu J, Luo J. Prevalence of Cryptosporidium, Giardia, Blastocystis, and trichomonads in domestic cats in East China. J Vet Med Sci 2019; 81: 890-6.
3. Yoshiuchi R, Matsubayashi M, Kimata I, Furuya M, Tani H, Sasai K. Survey and molecular characterization of Cryptosporidium and Giardia spp. in owned companion animal, dogs and cats, in Japan. Vet Parasitol 2010; 174: 313-6.
4. Surl CG, Jung BD, Park BK, Kim HC. Resistance of Cryptosporidium parvum oocysts following commercial bleach treatment. Korean J Vet Res 2011; 51: 101-5.
5. Yang R, Ying JL, Monis P, Ryan U. Molecular characterisation of Cryptosporidium and Giardia in cats (Felis catus) in Western Australia. Exp Parasitol 2015; 155: 13-8.
6. Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res 2011; 45: 6603-14.
7. Ježková J, Prediger J, Holubová N, Sak B, Konečný R, Feng Y, et al. Cryptosporidium ratti n. sp. (Apicomplexa: Cryptosporidiidae) and genetic diversity of Cryptosporidium spp. in brown rats (Rattus norvegicus) in the Czech Republic. Parasitology 2021; 148: 84-97.
8. Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 2010; 124: 80-9.
9. Xu H, Jin Y, Wu W, Li P, Wang L, Li N, et al. Genotypes of Cryptosporidium spp., Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai, China. Parasit Vectors 2016; 9: 121.
10. Tangtrongsup S, Scorza AV, Reif JS, Ballweber LR, Lappin MR, Salman MD. Seasonal distributions and other risk factors for Giardia duodenalis and Cryptosporidium spp. infections in dogs and cats in Chiang Mai, Thailand. Prev Vet Med 2020; 174: 104820.
11. Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol 2013; 43: 943-56.
12. Enemark HL, Starostka TP, Larsen B, Takeuchi-Storm N, Thamsborg SM. Giardia and Cryptosporidium infections in Danish cats: risk factors and zoonotic potential. Parasitol Res 2020; 119: 2275-86.
13. Hoopes JH, Polley L, Wagner B, Jenkins EJ. A retrospective investigation of feline gastrointestinal parasites in western Canada. Can Vet J 2013; 54: 359-62.
14. Scorza V, Willmott A, Gunn-Moore D, Lappin MR. Cryptosporidium felis in faeces from cats in the UK. Vet Rec 2014; 174: 609.
15. Bouzid M, Halai K, Jeffreys D, Hunter PR. The prevalence of Giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samples. Vet Parasitol 2015; 207: 181-202.
16. Ito Y, Itoh N, Kimura Y, Kanai K. Molecular detection and characterization of Cryptosporidium spp. among breeding cattery cats in Japan. Parasitol Res 2016; 115: 2121-3.
17. Kostopoulou D, Claerebout E, Arvanitis D, Ligda P, Voutzourakis N, Casaert S, et al. Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: The scenario of Crete, Greece. Parasit Vectors 2017; 10: 43.
18. Sursal N, Simsek E, Yildiz K. Occurrence and first molecular characterization of Cryptosporidium felis in a cat in Turkey. Kafkas Univ Vet Fak Derg 2020; 26: 833-7.
19. Sursal N, Simsek E, Yildiz K. Feline giardiasis in turkey: prevalence and genetic and haplotype diversity of Giardia duodenalis based on the β-giardin gene sequence in symptomatic cats. J Parasitol 2020; 106: 699- 706.
20. Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, et al. Phylogenetic analysis of Cryptosporidium parasites based on the smallsubunit rRNA gene locus. Appl Environ Microbiol 1999; 65: 1578-83.
21. Sulaiman IM, Jiang J, Singh A, Xiao L. Distribution of Giardia duodenalis genotypes and subgenotypes in raw urban wastewater in Milwaukee, Wisconsin. Appl Environ Microbiol 2004; 70: 3776-80.
22. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33: 1870-4.
23. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9: 772.
24. Koloren Z, Ayaz E. Genotyping of Cryptosporidium spp. in environmental water in Turkey. Acta Parasitol 2016; 61: 671-9.
25. Taylan-Ozkan A, Yasa-Duru S, Usluca S, Lysen C, Ye J, Roellig DM, et al. Cryptosporidium species and Cryptosporidium parvum subtypes in dairy calves and goat kids reared under traditional farming systems in Turkey. Exp Parasitol 2016; 170: 16-20.
26. Koloren Z, Seferoğlu O, Karanis P. Occurency of Giardia duodenalis assemblages in river water sources of Black Sea, Turkey. Acta Trop 2016; 164: 337-44.
27. Demircan K, Onder Z, Duzlu O, Yildirim A, Okur M, Ciloglu A, et al. First molecular detection and phylogenetic analyses of zoonotic Giardia intestinalis in horses in Turkey. J Equine Vet Sci 2019; 80: 56-60.
28. Kabir MHB, Ceylan O, Ceylan C, Shehata AA, Bando H, Essa MI, et al. Molecular detection of genotypes and subtypes of Cryptosporidium infection in diarrheic calves, lambs, and goat kids from Turkey. Parasitol Int 2020; 79: 102163.
29. Yildirim A, Adanir R, Inci A, Yukari BA, Duzlu O, Onder Z, et al. Prevalence and genotyping of bovine Cryptosporidium species in the Mediterranean and Central Anatolia Region of Turkey. Comp Immunol Microbiol Infect Dis 2020; 69: 101425.
30. Onder Z, Simsek E, Duzlu O, Yetismis G, Ciloglu A, Okur M, et al. Molecular prevalence and genotyping of Giardia duodenalis in cattle in Central Anatolia Region of Turkey. Parasitol Res 2020; 119: 2927-34.
31. Orunc Kilinc O, Yilmaz AB, Goz Y, Ozkan C, Denizhan V. Determination of Cryptosporidium spp. in Van cats by nested PCR. Med Weter 2018; 74: 456-9.
32. Korkmaz UF, Gökpınar S, Yıldız K. Prevalence of intestinal parasites in cats and their importance in terms of public health. Turkiye Parazitol Derg 2016; 40: 194-8.
33. Goz Y, Yuksek N, Altug N, Ceylan E, Deger S. Prevalence of Cryptosporidium infection in Van cats. Indian Vet J 2005; 82: 995-6.
34. Paoletti B, Otranto D, Weigl S, Giangaspero A, Di Cesare A, Traversa D. Prevalence and genetic characterization of Giardia and Cryptosporidium in cats from Italy. Res Vet Sci 2011; 91: 397-9.
35. Gow AG, Gow DJ, Hall EJ, Langton D, Clarke C, Papasouliotis K. Prevalence of potentially pathogenic enteric organisms in clinically healthy kittens in the UK. J Feline Med Surg. 2009; 11: 655-62.
36. Sotiriadou I, Pantchev N, Gassmann D, Karanis P. Molecular identification of Giardia and Cryptosporidium from dogs and cats. Parasite 2013; 20: 8.
37. Moreira ADS, Baptista CT, Brasil CL, Valente JSS, Bruhn FRP, Pereira DIB. Risk factors and infection due to Cryptosporidium spp. in dogs and cats in southern Rio Grande do Sul. Rev Bras Parasitol Vet 2018; 27: 113-8.
38. Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Cacciò SM. Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardiaduodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 2005; 35: 207-13.
39. Marangi M, Berrilli F, Otranto D, Giangaspero A. Genotyping of Giardia duodenalis among children and dogs in a closed socially deprived community from Italy. Zoonoses Public Health 2010; 57: e54-8.
40. van Keulen H, Macechko PT, Wade S, Schaaf S, Wallis PM, Erlandsen SL. Presence of human Giardia in domestic, farm and wild animals, and environmental samples suggests a zoonotic potential for giardiasis. Vet Parasitol 2002; 108: 97-107.
41. Read CM, Monis PT, Thompson RC. Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol 2004; 4: 125-30.
42. Jaros D, Zygner W, Jaros S, Wedrychowicz H. Detection of Giardia intestinalis assemblages A, B and D in domestic cats from Warsaw, Poland. Pol J Microbiol 2011; 60: 259-63.
43. McDowall RM, Peregrine AS, Leonard EK, Lacombe C, Lake M, Rebelo AR, et al. Evaluation of the zoonotic potential of Giardia duodenalis in fecal samples from dogs and cats in Ontario. Can Vet J 2011; 52: 1329-33.
44. Iijima Y, Itoh N, Ito Y, Kimura Y. Multilocus genotyping of Giardia duodenalis isolates from household cats and pet shop kittens. Vet Parasitol 2018; 259: 44-8.
45. Değerli S, Değerli N, Çeliksöz A, Özçelik S. Genotyping of Giardia intestinalis isolated from people living in Sivas, Turkey. Turk J Med Sci 2012; 42(Suppl 1): 1268-72.
46. Aydin AF, Besirbellioglu BA, Avci IY, Tanyuksel M, Araz E, Pahsa A. Classification of Giardia duodenalis parasites in Turkey into groups A and B using restriction fragment length polymorphism. Diagn Microbiol Infect Dis 2004; 50: 147-51.
47. Balcıoğlu C, Kurt Ö, Sevil N, Dağcı H, Tetik A, Ergunay K, et al. Genotyping of Giardia lamblia in a cohort of Turkish patients: A search for a relationship between symptoms and genotypes. Kafkas Univ Vet Fak Derg 2012; 18(Suppl-A): A125-A131.
48. Gelanew T, Lalle M, Hailu A, Pozio E, Cacciò SM. Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Trop 2007; 102: 92-9.
49. Sprong H, Cacciò SM, van der Giessen JW; ZOOPNET network and partners. Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 2009; 3: e558

APA	ONDER Z, Yetismis G, PEKMEZCİ D, DELİBAŞI N, Pekmezci G, CILOGLU A, DUZLU O, Inci A, Yıldırım A (2021). Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). , 252 - 256. 10.4274/tpd.galenos.2021.46320
Chicago	ONDER Zuhal,Yetismis Gamze,PEKMEZCİ Didem,DELİBAŞI Nesrin,Pekmezci Gokmen Zafer,CILOGLU ARIF,DUZLU Onder,Inci Abdullah,Yıldırım Alparslan Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). (2021): 252 - 256. 10.4274/tpd.galenos.2021.46320
MLA	ONDER Zuhal,Yetismis Gamze,PEKMEZCİ Didem,DELİBAŞI Nesrin,Pekmezci Gokmen Zafer,CILOGLU ARIF,DUZLU Onder,Inci Abdullah,Yıldırım Alparslan Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). , 2021, ss.252 - 256. 10.4274/tpd.galenos.2021.46320
AMA	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). . 2021; 252 - 256. 10.4274/tpd.galenos.2021.46320
Vancouver	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). . 2021; 252 - 256. 10.4274/tpd.galenos.2021.46320
IEEE	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A "Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)." , ss.252 - 256, 2021. 10.4274/tpd.galenos.2021.46320
ISNAD	ONDER, Zuhal vd. "Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)". (2021), 252-256. https://doi.org/10.4274/tpd.galenos.2021.46320

APA	ONDER Z, Yetismis G, PEKMEZCİ D, DELİBAŞI N, Pekmezci G, CILOGLU A, DUZLU O, Inci A, Yıldırım A (2021). Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). Türkiye Parazitoloji Dergisi, 45(4), 252 - 256. 10.4274/tpd.galenos.2021.46320
Chicago	ONDER Zuhal,Yetismis Gamze,PEKMEZCİ Didem,DELİBAŞI Nesrin,Pekmezci Gokmen Zafer,CILOGLU ARIF,DUZLU Onder,Inci Abdullah,Yıldırım Alparslan Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). Türkiye Parazitoloji Dergisi 45, no.4 (2021): 252 - 256. 10.4274/tpd.galenos.2021.46320
MLA	ONDER Zuhal,Yetismis Gamze,PEKMEZCİ Didem,DELİBAŞI Nesrin,Pekmezci Gokmen Zafer,CILOGLU ARIF,DUZLU Onder,Inci Abdullah,Yıldırım Alparslan Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). Türkiye Parazitoloji Dergisi, vol.45, no.4, 2021, ss.252 - 256. 10.4274/tpd.galenos.2021.46320
AMA	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). Türkiye Parazitoloji Dergisi. 2021; 45(4): 252 - 256. 10.4274/tpd.galenos.2021.46320
Vancouver	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus). Türkiye Parazitoloji Dergisi. 2021; 45(4): 252 - 256. 10.4274/tpd.galenos.2021.46320
IEEE	ONDER Z,Yetismis G,PEKMEZCİ D,DELİBAŞI N,Pekmezci G,CILOGLU A,DUZLU O,Inci A,Yıldırım A "Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)." Türkiye Parazitoloji Dergisi, 45, ss.252 - 256, 2021. 10.4274/tpd.galenos.2021.46320
ISNAD	ONDER, Zuhal vd. "Investigation of Zoonotic Cryptosporidium and Giardia intestinalis Species and Genotypes in Cats (Felis catus)". Türkiye Parazitoloji Dergisi 45/4 (2021), 252-256. https://doi.org/10.4274/tpd.galenos.2021.46320