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Seroprevalence of Toxoplasma gondii in outdoor dogs and cats in Bangkok, Thailand

Published online by Cambridge University Press:  10 March 2021

Ana Huertas-López Open the ORCID record for Ana Huertas-López [Opens in a new window] ,
Woraporn Sukhumavasi ,
Gema Álvarez-García Open the ORCID record for Gema Álvarez-García [Opens in a new window] ,
Silvia Martínez-Subiela ,
David Cano-Terriza Open the ORCID record for David Cano-Terriza [Opens in a new window] ,
Sonia Almería ,
Jitender P. Dubey Open the ORCID record for Jitender P. Dubey [Opens in a new window] ,
Ignacio García-Bocanegra Open the ORCID record for Ignacio García-Bocanegra [Opens in a new window] ,
José Joaquín Cerón  and
Carlos Martínez-Carrasco
Ana Huertas-López
Affiliation:
Interdisciplinary Laboratory of Clinical Analysis, Interlab-UMU, University of Murcia, 30100Espinardo, Murcia, Spain
Woraporn Sukhumavasi
Affiliation:
Parasitology Unit, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, 10330Bangkok, Thailand Feline Infectious Disease and Health for Excellence Research Unit, Microbial Food Safety and Antimicrobial Resistance Research Unit, Animal Vector-Borne Disease Research Unit, Chulalongkorn University, 10330Bangkok, Thailand
Gema Álvarez-García
Affiliation:
Department of Animal Health, Complutense University of Madrid, Ciudad Universitaria s/n, 28040Madrid, Spain
Silvia Martínez-Subiela
Affiliation:
Interdisciplinary Laboratory of Clinical Analysis, Interlab-UMU, University of Murcia, 30100Espinardo, Murcia, Spain
David Cano-Terriza
Affiliation:
Animal Health and Zoonosis Research Group (GISAZ), Department of Animal Health, University of Córdoba, 14014Córdoba, Spain
Sonia Almería
Affiliation:
Department of Health and Human Services, Food and Drug Administration, Center for Food Safety and Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), Division of Virulence Assessment, Laurel, USA
Jitender P. Dubey
Affiliation:
U. S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland20705-2350, USA
Ignacio García-Bocanegra*
Affiliation:
Animal Health and Zoonosis Research Group (GISAZ), Department of Animal Health, University of Córdoba, 14014Córdoba, Spain
José Joaquín Cerón
Affiliation:
Interdisciplinary Laboratory of Clinical Analysis, Interlab-UMU, University of Murcia, 30100Espinardo, Murcia, Spain
Carlos Martínez-Carrasco
Affiliation:
Department of Animal Health, University of Murcia, 30100Espinardo, Murcia, Spain
*
Author for correspondence: Ignacio García-Bocanegra, Email: v62garbo@uco.es
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Abstract

The aim of this study was to estimate the seroprevalence and risk factors associated with Toxoplasma gondii exposure in dogs and cats from Bangkok, Thailand. Blood samples from 318 dogs and 321 cats were tested for T. gondii antibodies by modified agglutination test (cut-off 1:25). Additionally, 18 dogs and 20 cats were longitudinally sampled for T. gondii antibodies during the same study period, between June and July 2019. The overall seroprevalence in dogs and cats was 7.9% (25/318; 95% CI 4.9–10.8%) and 18.7% (95% CI 14.4–23.0%), respectively. For dogs, risk factors identified were being a mixed-breed animal and living totally outdoors, while increasing age was shown to be a risk factor for cats. Seroconversion was not detected and titres from positive animals remained constant over longitudinal study. The present study indicates that there is a prominent presence of T. gondii in urban and peri-urban areas of Bangkok, suggesting that outdoor dogs and cats should be considered as a possible risk factor for humans.

Keywords

BangkokcatdogMATseroprevalenceToxoplasma gondii
Type
Research Article
Information
Parasitology , Volume 148 , Issue 7 , June 2021 , pp. 843 - 849
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Afonso, E, Thulliez, P and Gilot-Fromont, E (2006) Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). International Journal for Parasitology 36, 1373–1382.CrossRefGoogle Scholar
Andiappan, H, Nissapatorn, V, Sawangjaroen, N, Chemoh, W, Lau, YL, Kumar, T, i Onichandran, S, Suwanrath, C and Chandeying, V (2014) Toxoplasma infection in pregnant women: a current status in Songklanagarind hospital, southern Thailand. Parasites and Vectors 7, 1–7.CrossRefGoogle Scholar
Arunvipas, P, Jittapalapong, S, Inpankaew, T and Pinyopanuwat, N (2013) Seroprevalence and risk factors influenced transmission of Toxoplasma gondii in dogs and cats in dairy farms in Western Thailand. African Journal of Agricultural Research 8, 591–595.Google Scholar
Cano-Terriza, D, Puig-Ribas, M, Jiménez-Ruiz, S, Cabezón, Ó, Almería, S, Galán-Relaño, Á, Dubey, JP and García-Bocanegra, I (2016) Risk factors of Toxoplasma gondii infection in hunting, pet and watchdogs from southern Spain and Northern Africa. Parasitology International 65, 363–366.CrossRefGoogle ScholarPubMed
Cong, W, Elsheikha, HM, Zhou, N, Peng, P, Qin, SY, Meng, QF and Qian, AD (2018) Prevalence of antibodies against Toxoplasma gondii in pets and their owners in Shandong province, Eastern China. BMC Infectious Diseases 18, 1.CrossRefGoogle ScholarPubMed
Dabritz, HA and Conrad, PA (2010) Cats and toxoplasma: implications for public health. Zoonoses and Public Health 57, 34–52.CrossRefGoogle ScholarPubMed
Dantas, SBA, Da Fonsêca Fernandes, AR, De Souza Neto, OL, Mota, RA, Alves, CJ and de Azevedo, SS (2014) Fatores de risco para a ocorrência de anticorpos contra Toxoplasma gondii e Neospora caninum em cães domiciliados no Nordeste do Brasil. Semina:Ciencias Agrarias 35, 875–881.Google Scholar
de Almeida, JC, Frehse, MS, Navarro, IT, Garcia, JL, Biondo, AW and Freire, RL (2016) Comparison of indirect fluorescent antibody test and the modified agglutination test for the detection of Toxoplasma gondii antibodies in stray dogs from Southern Brazil. Acta Parasitologica 61, 694–696.CrossRefGoogle ScholarPubMed
de Moura, AB, de Souza, AP, Sartor, AA, Bellato, V, Teixeira, EB, Pisetta, GM and Junior, AH (2009) Ocorrência de anticorpos e fatores de risco para infecção por Toxoplasma gondii em cães, nas cidades de Lages e Balneário Camboriú, Santa Catarina, Brasil. Revista Brasileira de Parasitologia Veterinaria 18, 52–56.CrossRefGoogle Scholar
de Oliveira, GMS, Simões, JM, Schaer, RE, Freire, SM, Nascimento, RJM, de Pinheiro, AMCM, Carvalho, SMS, Mariano, APM, de Carvalho, RC and Munhoz, AD (2019) Frequency and factors associated with Toxoplasma gondii infection in pregnant women and their pets in Ilhéus, Bahia, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 52, 2–7. doi: 10.1590/0037-8682-0250-2019CrossRefGoogle Scholar
de Wit, LA, Kilpatrick, AM, VanWormer, E, Croll, DA, Tershy, BR, Kim, M and Saphiro, K (2020) Seasonal and spatial variation in Toxoplasma gondii contamination in soil in urban public spaces in California, United States. Zoonoses and Public Health 67, 70–78.CrossRefGoogle ScholarPubMed
Ding, H, Gao, YM, Deng, Y, Lamberton, PHL and Lu, DB (2017) A systematic review and meta-analysis of the seroprevalence of Toxoplasma gondii in cats in mainland China. Parasites and Vectors 10, 2–9. doi: 10.1186/s13071-017-1970-6CrossRefGoogle ScholarPubMed
Dubey, JP (2010) Toxoplasmosis of Animals and Humans, 2nd Edn. Boca Raton, FL, USA: C. Press.Google Scholar
Dubey, JP and Desmonts, G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337–339.CrossRefGoogle ScholarPubMed
Dubey, JP, Tiwari, K, Chikweto, A, Deallie, C, Sharma, R, Thomas, D, Choudhary, S, Ferreira, LR, Oliveira, S, Verma, SK, Kwok, OCH and Su, C (2013 a) Isolation and RFLP genotyping of Toxoplasma gondii from the domestic dogs (Canis familiaris) from Grenada, West Indies revealed high genetic variability. Veterinary Parasitology 197, 623–626.10.1016/j.vetpar.2013.07.029CrossRefGoogle ScholarPubMed
Dubey, JP, Darrington, C, Tiao, N, Ferreira, LR, Choudhary, S, Molla, B, Saville, WJA, Tilahun, G, Kwok, OCH and Gebreyes, WA (2013 b) Isolation of viable Toxoplasma gondii from tissues and feces of cats from Addis Ababa, Ethiopia. Journal of Parasitology 99, 56–58.CrossRefGoogle ScholarPubMed
Dubey, JP, Cerqueira-Cézar, CK, Murata, FHA, Kwok, OCH, Yang, YR and Su, C (2020 a) All about toxoplasmosis in cats: the last decade. Veterinary Parasitology 283, 109145.CrossRefGoogle ScholarPubMed
Dubey, JP, Murata, FHA, Cerqueira-Cézar, CK, Kwok, OCH, Yang, YR and Su, C (2020 b) Toxoplasma gondii infections in dogs: 2009-2020. Veterinary Parasitology 287, 109223.CrossRefGoogle ScholarPubMed
El Behairy, AM, Choudhary, S, Ferreira, LR, Kwok, OCH, Hilali, M, Su, C and Dubey, JP (2013) Genetic characterization of viable Toxoplasma gondii isolates from stray dogs from Giza, Egypt. Veterinary Parasitology 193, 25–29.10.1016/j.vetpar.2012.12.007CrossRefGoogle ScholarPubMed
Fábrega, L, Restrepo, CM, Torres, A, Smith, D, Chan, P, Pérez, D, Cumbrera, A and Caballero, Z (2020) Frequency of Toxoplasma gondii and risk factors associated with the infection in stray dogs and cats of Panama. Microorganisms 8, 927.10.3390/microorganisms8060927CrossRefGoogle ScholarPubMed
Frenkel, JK, Lindsay, DS, Parker, BB and Dobesh, M (2003) Dogs as possible mechanical carriers of Toxoplasma, and their fur as a source of infection of young children. International Journal of Infectious Diseases 7, 292–293.CrossRefGoogle ScholarPubMed
Hosmer, DW and Lemeshow, S (2000) Applied Logistic Regression. Hoboken, NJ, USA: John Wiley & Sons, Inc. doi: 10.1002/0471722146.CrossRefGoogle Scholar
Jittapalapong, S, Nimsupan, B, Pinyopanuwat, N, Chimnoi, W, Kabeya, H and Maruyama, S (2007) Seroprevalence of Toxoplasma gondii antibodies in stray cats and dogs in the Bangkok metropolitan area, Thailand. Veterinary Parasitology 145, 138–141.CrossRefGoogle ScholarPubMed
Jittapalapong, S, Sittisan, P, Sakpuaram, T, Kabeya, H, Maruyama, S and Inpankaew, T (2009) Coinfection of Leptospira spp and Toxoplasma gondii among stray dogs in Bangkok, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 40, 247–252.Google ScholarPubMed
Jittapalapong, S, Inpankaew, T, Pinyopanuwat, N, Chimnoi, W, Kengradomkij, C, Wongnarkpet, S, Maruyama, S, Lekkla, A and Sukthana, Y (2010) Epidemiology of Toxoplasma gondii infection of stray cats in Bangkok, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 41, 13–18.Google ScholarPubMed
Kasempimolporn, S, Jitapunkul, S and Sitprija, V (2008) Moving towards the elimination of rabies in Thailand. Journal of the Medical Association of Thailand 91, 433–437.Google ScholarPubMed
Lindsay, DS, Dubey, JP, Butler, JM and Blagburn, BL (1997) Mechanical transmission of Toxoplasma gondii oocysts by dogs. Veterinary Parasitology 73, 27–33.CrossRefGoogle ScholarPubMed
Lopes, AP, Santos, H, Neto, F, Rodrigues, M, Kwok, OCH, Dubey, JP and Cardoso, L (2011) Prevalence of antibodies to Toxoplasma gondii in dogs from Northeastern Portugal. Journal of Parasitology 97, 418–420.CrossRefGoogle ScholarPubMed
Oi, M, Yoshikawa, S, Maruyama, S and Nogami, S (2015) Comparison of Toxoplasma gondii seroprevalence in shelter cats and dogs during 1999–2001 and 2009–2011 in Tokyo, Japan. PLoS ONE 10, 8.CrossRefGoogle ScholarPubMed
Olbera, AVG, Fornazari, F, Babboni, SD, Rossi, RS, Sevá, AP, Latosinski, GS, da Silva, MAR, Modolo, JR and Langoni, H (2020) Cumulative incidence and spatial distribution of dogs exposed to Toxoplasma gondii. Revista Brasileira de Parasitologia Veterinária 29, 2–9.CrossRefGoogle ScholarPubMed
Park, Y, Noh, J, Seo, HJ, Kim, KH, Min, S, Yoo, MS, Yun, BR, Kim, JH, Choi, EJ, Cheon, DS, Hong, SJ, Yoon, SS and Cho, YS (2020) Seroprevalence and B1 gene phylogeny of Toxoplasma gondii of dogs and cats in Republic of Korea. Korean Journal of Parasitology 58, 257–265.CrossRefGoogle ScholarPubMed
Pereira, PF, da Barbosa, AS, Santos, ALC, Bolais, PF, Dardé, ML and Amendoeira, MRR (2018) Toxoplasma gondii: infection among shelter and stray cats in Rio de Janeiro. Brazil. Revista Brasileira de Parasitologia Veterinaria 27, 401–408.Google ScholarPubMed
Rengifo-Herrera, C, Pile, E, García, A, Pérez, A, Pérez, D, Nguyen, FK, de la Guardia, V, Mcleod, R and Caballero, Z (2017) Seroprevalence of Toxoplasma gondii in domestic pets from metropolitan regions of Panama. Parasite 24, 2–4. doi: 10.1051/parasite/2017009CrossRefGoogle ScholarPubMed
Rostami, A, Riahi, SM, Contopoulos-Ioannidis, DG, Gamble, HR, Fakhri, Y, Shiadeh, MN, Foroutan, M, Behniafar, H, Taghipour, A, Maldonado, YA, Mokdad, AH and Gasser, RB (2019) Acute Toxoplasma infection in pregnant women worldwide: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 13, 1–20.CrossRefGoogle ScholarPubMed
Rostami, A, Riahi, SM, Gamble, HR, Fakhri, Y, Nourollahpour Shiadeh, M, Danesh, M, Behniafar, H, Paktinat, S, Foroutan, M, Mokdad, AH, Hotez, PJ and Gasser, RB (2020) Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clinical Microbiology and Infection 26, 673–683.CrossRefGoogle ScholarPubMed
Savvides, N (2013) Living with dogs : alternative animal practices in Bangkok, Thailand. Animal Studies Journal 2, 28–50.Google Scholar
Schares, G, Pantchev, N, Barutzki, D, Heydorn, AO, Bauer, C and Conraths, FJ (2005) Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. International Journal for Parasitology 35, 1525–1537.CrossRefGoogle ScholarPubMed
Schreiber, N, Basso, W, Riond, B, Willi, B, Torgerson, PR and Deplazes, P (2020) Antibody kinetics and exposure to Toxoplasma gondii in cats: a seroepidemiological study. International Journal for Parasitology 51, 291–299. doi: 10.1016/j.ijpara.2020.09.011.CrossRefGoogle ScholarPubMed
Simon, JA, Pradel, R, Aubert, D, Geers, R, Villena, I and Poulle, ML (2018) A multi-event capture-recapture analysis of Toxoplasma gondii seroconversion dynamics in farm cats. Parasites & Vectors 11, 1–13. doi: 10.1186/s13071-018-2834-4CrossRefGoogle ScholarPubMed
Sukhumavasi, W, Bellosa, ML, Lucio-Forster, A, Liotta, JL, Lee, ACY, Pornmingmas, P, Chungpivat, S, Mohammed, HO, Lorentzen, L, Dubey, JP and Bowman, DD (2012) Serological survey of Toxoplasma gondii, Dirofilaria immitis, Feline Immunodeficiency Virus (FIV) and Feline Leukemia Virus (FeLV) infections in pet cats in Bangkok and vicinities, Thailand. Veterinary Parasitology 188, 25–30.CrossRefGoogle ScholarPubMed
Sukthana, Y, Kaewkungwal, J, Jantanavivat, C, Lekkla, A, Chiabchalard, R and Aumarm, W (2003) Toxoplasma gondii antibody in Thai cats and their owners. Southeast Asian Journal of Tropical Medicine and Public Health 34, 733–738.Google ScholarPubMed
Torrey, EF and Yolken, RH (2013) Toxoplasma oocysts as a public health problem. Trends in Parasitology 29, 380–384. doi: 10.1016/j.pt.2013.06.001CrossRefGoogle ScholarPubMed
Toukhsati, SR, Phillips, CJC, Podberscek, AL and Coleman, GJ (2015) Companion animals in Thailand: human factors that predict sterilization of cats and dogs. Society and Animals 23, 569–593.10.1163/15685306-12341381CrossRefGoogle Scholar
Wang, S, Zhou, YH, Xie, Q, Zheng, B, Zhang, HZ, Yao, ZJ, Wang, D, Liu, SG and Zhang, ZC (2017) Prevalence of Toxoplasma gondii antibodies in dogs in central China. Israel Journal of Veterinary Medicine 72, 11–15.Google Scholar
World Organisation for Animal Health (OIE) (2019) Animal population. Retrieved from World Animal Health Information Database (WAHIS Interface) website: https://www.oie.int/wahis_2/public/wahid.php/Countryinformation/Animalpopulation (Accessed 6 March 2020).Google Scholar
Zarra-Nezhad, F, Borujeni, MP, Mosallanejad, B and Hamidinejat, H (2017) A seroepidemiological survey of Toxoplasma gondii infection in referred dogs to Veterinary Hospital of Ahvaz, Iran. International Journal of Veterinary Science and Medicine 5, 148–151.10.1016/j.ijvsm.2017.08.006CrossRefGoogle ScholarPubMed
Zulpo, DL, Sammi, AS, dos Santos, JR, Sasse, JP, Martins, TA, Minutti, AF, Cardim, ST, de Barros, LD, Navarro, IT and Garcia, JL (2018) Toxoplasma gondii: a study of oocyst re-shedding in domestic cats. Veterinary Parasitology 249, 17–20.CrossRefGoogle ScholarPubMed