Abstract
Toxoplasmosis is a disease with a worldwide distribution that affects a wide variety of animal species, though with rare descriptions in chickens. We describe the clinical, epidemiological, pathological, and molecular aspects of a toxoplasmosis outbreak in domestic chickens and guinea fowl in southern Brazil. The flock was composed of 47 domestic chickens and 29 guinea fowl. Of these, 22 birds showed clinical signs of lethargy, anorexia, and neurological signs over a clinical course of 24–72 h, and 15 died. Epidemiological data were obtained through fieldwork performed at the chicken farm and necropsies of six birds. Gross lesions were absent at necropsy, and histopathological findings included inflammatory infiltrate of macrophages, lymphocytes, and plasma cells and necrosis in several tissues associated with intralesional Toxoplasma gondii. Immunohistochemistry for T. gondii was positive. Additionally, restriction fragment length polymorphism (RFLP) analysis with 11 markers (SAG1, SAG2 (5′3′SAG2 and alt. SAG2), SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, Apico, and CS3) and microsatellite (MS) analysis with 15 markers (TUB2, W35, TgMA, B18, B17, M33, IV.1, XI.1, N60, N82, AA, N61, N83, M48, and M102) were performed. PCR-RFLP revealed T. gondii genotype ToxoDB-PCR-RFLP #280, and MS analysis also showed a unique genotype. This is the first description of this genotype in chickens and adds to the evidence suggesting considerable genotypic diversity of T. gondii in Brazil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ajzenberg D, Collinet F, Mercier A, Vignoles P, Darde´ ML (2010) Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. J Clin Microbiol 48(12):4641–4645. https://doi.org/10.1128/JCM.01152-10
Beltrame MA, Pena HF, Ton NC, Lino AJ, Gennari SM, Dubey JP, Pereira FE (2012) Seroprevalence and isolation of Toxoplasma gondii from free-range chickens from Espirito Santo state, southeastern Brazil. Vet Parasitol 188(3–4):225–230. https://doi.org/10.1016/j.vetpar.2012.03.053
Biancifiori F, Rondini C, Grelloni V, Frescura T (1986) Avian toxoplasmosis: experimental infection of chicken and pigeon. Comp Immunol Microbiol Infect Dis 9(4):337–346. https://doi.org/10.1016/0147-9571(86)90046-9
Casagrande RA, Pena HFJ, Cabral AD, Rolim VM, De Oliveira LGS, Boabaid FM, Wouters ATB, Wouters F, Cruz CEF, Driemeier D (2015) Fatal systemic toxoplasmosis in valley quail (Callipepla californica). Int J Parasitol Parasites Wildl 4(2):264–267. https://doi.org/10.1016/j.ijppaw.2015.04.003
do Nascimento LC, Pena HF, Leite Filho RV, Argenta FF, Alves BF, Oliveira S, Gennari SM, Driemeier D (2017) Rare case of acute toxoplasmosis in a domestic rabbit (Oryctolaguscuniculus) in Brazil associated with the type BrIII Brazilian clonal lineage of Toxoplasma gondii. Parasitol Res 116(10):2873–2876. https://doi.org/10.1007/s00436-017-5600-1
Dubey JP (1998) Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Vet Parasitol 74:75–77. https://doi.org/10.1016/S0304-4017(97)00135-0
Dubey JP (2009) History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol 39:877–882. https://doi.org/10.1016/j.ijpara.2009.01.005
Dubey JP (2010) Toxoplasmosis of animals and humans, 2nd edn. CRC Press, Boca Raton, FL, 313p
Dubey JP, Desmonds G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet J 19(4):337–339. https://doi.org/10.1111/j.2042-3306.1987.tb01426.x
Dubey JP, Graham DH, Blackston CR, Lehmann T, Gennari SM, Ragozo AM, Nishi SM. Shen SK, Kwok OC, Hill DE, Thulliez P (2002) Biological and genetic characterization of Toxoplasma gondii isolates from chickens (Gallus domesticus) from Sao Paulo, Brazil: unexpected findings. Int J Parasitol 32(1):99–105. https://doi.org/10.1016/S0020-7519(01)00364-2
Dubey JP, Ruff MD, Camargo ME, Shen SK, Wilkins GL, Kwok OC, Thulliez P (1993) Serologic and parasitologic responses of domestic chickens after oral inoculation with Toxoplasma gondii oocysts. Am J Vet Res 54(10):1668–1672
Dubey JP, Sundar N, Gennari SM, Minervino AH, Farias NA, Ruas JL, dos Santos TR, Cavalcante GT, Kwok OC, Su C (2007a) Biologic and genetic comparison of Toxoplasma gondii isolates in free-range chickens from the northern Pará state and the southern state Rio Grande do Sul, Brazil revealed highly diverse and distinct parasite populations. Vet Parasitol 143(2):182–188. https://doi.org/10.1016/j.vetpar.2006.08.024
Dubey JP, Webb DM, Sundar N, Velmurugan GV, Bandini LA, Kowk OC, Su C (2007b) Endemic avian toxoplasmosis on a farm in Illinois: clinical disease, diagnosis, biologic and genetic characteristic of Toxoplasma gondii isolates from chickens (Gallus domesticus), and a goose (Anser anser). Vet Parasitol 148(3–4):207–212. https://doi.org/10.1016/j.vetpar.2007.06.033
Dubey JP (2008) Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health significance. Zoonoses Public Health 57(1):60–73. https://doi.org/10.1111/j.1863-2378.2009.01274.x
Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 38(11):1257–1278. https://doi.org/10.1016/j.ijpara.2008.03.007
Dubey JP, Lappin MR (2015) Toxoplasmosis e neosporosis. In: Greene CE (ed) Infectious diseases of the dog and cat, 4th edn. Elsevier Saunder, St. Louis, Missouri, pp 806–821
Dubey JP, Velmurugan GV, Chockalingam A, Pena HF, de Oliveira LN, Leifer CA, Gennari SM, Bahia Oliveira LM, Su C (2008) Genetic diversity of Toxoplasma gondii isolates from chickens from Brazil. Vet Parasitol 157(3–4):299–305. https://doi.org/10.1016/j.vetpar.2008.07.036
Feitosa TF, Vilela VLR, de Almeida-Neto JL, de Melo LRB, de Morais DF, Alves BF, Nakashima F, Gennari SM, Athayde ACR, de Jesus Pena HF (2017) First report of typical Brazilian Toxoplasma gondii genotypes from isolates of free-range chickens (Gallus gallus domesticus) circulating in the state of Paraiba, Northeast Brazil. Parasitol Res 116(8):2265–2270. https://doi.org/10.1007/s00436-017-5531-x
Gilbert RE, Freeman K, Lago EG, Bahia-Oliveira LM, Tan HK, Wallon M, Buffolano W, Stanford MR, Petersen E (2008) Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Negl Trop Dis 2(8):e277. https://doi.org/10.1371/journal.pntd.0000277
Homan WL, Vercammen M, De Braekeleer J, Verschueren H (2000) Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol 30(1):69–75. https://doi.org/10.1016/S0020-7519(99)00170-8
Howerth EW, Rodenroth N (1985) Fatal systemic toxoplasmosis in a wild turkey. J Wildl Dis 21:446–449
Jones KH, Wilson FD, Fitzgerald SD, Kiupel M (2012) A natural outbreak of clinical toxoplasmosis in a backyard flock of a guinea fowl in Mississippi. Avian Dis 56(4):750–753. https://doi.org/10.1637/10226-043012-Case.1
Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, Belfort R Jr, Vitor RW, Silveira C, Sibley LD (2006) Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg Infect Dis 12(6):942–949. https://doi.org/10.3201/eid1206.060025
Meireles MV, Paulillo AC, Da Costa AJ, Moraes FR, De Ávila FA, Da Silva GS (1995) Correlação entre Toxoplasma gondii e Cryptosporidium baileyi em frangos de corte experimentalmente infectados. Brazil J Vet Parasitol 4(2):105–112
Millar PM, Alves FMX, Teixeira VQ, Vicente RT, Menezes EM, Sobreiro LGO, Pereira VLA, Amendoeira MRR (2012) Occurrence of infection with Toxoplasma gondii and factors associated with transmission in broiler chickens and laying hens in different raising systems. Pesq Vet Bras 32(3):231–236. https://doi.org/10.1590/S0100-736X2012000300009
Pena HF, Gennari SM, Dubey JP, Su C (2008) Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int J Parasitol 38(5):561–569. https://doi.org/10.1016/j.ijpara.2007.09.004
Quist CF, Dubey JP, Luttrell MP, Davidson WR (1995) Toxoplasmosis in wild turkeys: a case report and serologic survey. J Wildl Dis 31(2):255–258 https://doi.org/10.7589/0090-3558-31.2.255
Ruiz A, Frenkel JK (1980) Intermediate and transport hosts of Toxoplama gondii in Costa Rica. Am J Trop Med Hyg 29(6):1161–1166. https://doi.org/10.4269/ajtmh.1980.29.1161
Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP (2010) Moving towards an integrated approach to molecular detection and identification of Toxoplama gondii. Parasitology 137(1):1–11. https://doi.org/10.1017/S0031182009991065
Santos SV, Pena HFJ, Talebi MG, Teixeira RHF, Kanamura CT, Diaz-Delgado J, Gennari SM, Catão-Dias JL (2017) Fatal toxoplasmosis in a southern muriqui (Brachyteles arachnoides) from São Paulo state, Brazil: pathological, immunohistochemical and molecular characterization. J Med Primatol 47(2):124–127. https://doi.org/10.1111/jmp.12326
Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, Su C (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141(4):453–461. https://doi.org/10.1017/S0031182013001844
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30(12–13):1217–1258. https://doi.org/10.1016/S0020-7519(00)00124-7
Vesco G, Buffolano W, La Chiusa S, Mancuso G, Caracappa S, Chianca A, Villari S, Currò V, Liga F, Petersen E (2007) Toxoplasma gondii infections in sheep in Sicily, southern Italy. Vet Parasitol 146(1–2):3–8. https://doi.org/10.1016/j.vetpar.2007.02.019
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Larissa Howe
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vielmo, A., Pena, H.F.J., Panziera, W. et al. Outbreak of toxoplasmosis in a flock of domestic chickens (Gallus gallus domesticus) and guinea fowl (Numida meleagris). Parasitol Res 118, 991–997 (2019). https://doi.org/10.1007/s00436-019-06233-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06233-w