Migratory Wild Birds as Potential Long-Distance Transmitters of Toxoplasma gondii Infection

Filippo Maria Dini; Giulia Graziosi; Caterina Lupini; Elena Catelli; Roberta Galuppi

doi:10.3390/pathogens12030478

journal article Open Access Mar 18, 2023

Migratory Wild Birds as Potential Long-Distance Transmitters of Toxoplasma gondii Infection

Filippo Maria Dini

Giulia Graziosi

Caterina Lupini

Elena Catelli

Roberta Galuppi

Pathogens Vol. 12 No. 3 pp. 478 · MDPI AG

View at Publisher Save 10.3390/pathogens12030478

Abstract

Toxoplasma gondii is a worldwide distributed zoonotic protozoan capable of infecting a wide range of mammals (including humans) and birds as intermediate hosts. Migratory wild birds, through interconnecting countries along their flyways, can play a role in the spatial spread of T. gondii and could contribute to its sylvatic cycle. Additionally, hunted wild birds used for meat consumption could represent a further source of human infection. To determine the presence of T. gondii in wild birds, a total of 50 individuals belonging to the Anseriformes and Charadriiformes orders were sampled during the 2021–2022 hunting season in Northern Italy. Cardiac muscle samples of three Northern shovelers (Anas clypeata), two wild mallards (A. platyrhynchos), one Eurasian teal (A. crecca), and one Northern lapwing (Vanellus vanellus) were positive for the molecular detection of T. gondii based on a targeted amplification of the B1 gene. A 14% (7/50) overall positivity was observed in the sampled population. Results from this study suggest a moderate exposure of wild aquatic birds to T. gondii, highlighting the importance of a further characterization of T. gondii in its wildlife hosts.

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References

50

[1]

Dubey, J.P. (2020). Toxoplasma gondii, Elsevier.

[2]

Dubey, J.P. (2022). Toxoplasmosis of Animals and Humans, CRC Press. [3rd ed.]. 10.1201/9781003199373

[3]

Environmental transmission of Toxoplasma gondii: Oocysts in water, soil and food

Karen Shapiro, Lillian Bahia-Oliveira, Brent Dixon et al.

Food and Waterborne Parasitology 2019 10.1016/j.fawpar.2019.e00049

[4]

Dubey "Long term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork" Am. J. Vet. Res. (1988)

[5]

Akerstedt "Serosurvey for canine distemper virus, canine adenovirus, Leptospira interrogans, and Toxoplasma gondii in free-ranging canids in Scandinavia and Svalbard" J. Wildl. Dis. (2010) 10.7589/0090-3558-46.2.474

[6]

Zanet "Epidemiology of Leishmania infantum, Toxoplasma gondii, and Neospora caninum in Rattus rattus in absence of domestic reservoir and definitive hosts" Vet. Parasitol. (2014) 10.1016/j.vetpar.2013.10.023

[7]

Yan "Impact of environmental factors on the emergence, transmission and distribution of Toxoplasma gondii" Parasit Vectors (2016) 10.1186/s13071-016-1432-6

[8]

Frenkel "Transmission of Toxoplasma gondii in Panama City, Panama: A Five-Year Prospective Cohort Study of Children, Cats, Rodents, Birds, and Soil" Am. J. Trop. Med. (1995) 10.4269/ajtmh.1995.53.458

[9]

Dubey "A review of toxoplasmosis in wild birds" Vet. Parasitol. (2002) 10.1016/s0304-4017(02)00034-1

[10]

Wendte "Population genetics of Toxoplasma gondii: New perspectives from parasite genotypes in wildlife" Vet. Parasitol. (2011) 10.1016/j.vetpar.2011.07.018

[11]

Shapiro "Surface properties of Toxoplasma gondii oocysts and surrogate microspheres" Appl. Environ. Microbiol. (2009) 10.1128/aem.02109-08

[12]

Wilson "Interaction of diet and habitat predicts Toxoplasma gondii infection rates in wild birds at a global scale" Glob. Ecol. Biogeogr. (2020) 10.1111/geb.13096

[13]

Graziosi "Infectious bursal disease virus in free-living wild birds: A systematic review and meta-analysis of its sero-viroprevalence on a global scale" Transbound. Emerg. Dis. (2021) 10.1111/tbed.14433

[14]

Graziosi "Disentangling the role of wild birds in avian metapneumovirus (aMPV) epidemiology: A systematic review and meta-analysis" Transbound. Emerg. Dis. (2022) 10.1111/tbed.14680

[15]

De Marco, M.A., Delogu, M., Facchini, M., Di Trani, L., Boni, A., Cotti, C., Graziosi, G., Venturini, D., Regazzi, D., and Ravaioli, V. (2021). Serologic Evidence of Occupational Exposure to Avian Influenza Viruses at the Wildfowl/Poultry/Human Interface. Microorganisms, 9. 10.3390/microorganisms9102153

[16]

Benskin "Bacterial pathogens in wild birds: A review of the frequency and effects of infection" Biol. Rev. Camb. Philos. Soc. (2009) 10.1111/j.1469-185x.2008.00076.x

[17]

Ayala "A Review of Pathogen Transmission at the Backyard Chicken-Wild Bird Interface" Front. Vet. Sci. (2020) 10.3389/fvets.2020.539925

[18]

Zhang "Molecular detection and genotypic characterization of Toxoplasma gondii in wild waterfowls in Jilin Province, Northeastern China" Parasitol. Int. (2015) 10.1016/j.parint.2015.08.008

[19]

Murao "Serological Survey of Toxoplasma gondii in Wild Waterfowl in Chukotka, Kamchatka, Russia and Hokkaido, Japan" J. Parasitol. (2008) 10.1645/ge-1434.1

[20]

Guo "Prevalence and Risk Factors for Toxoplasma gondii Infection in Meat Animals and Meat Products Destined for Human Consumption" J. Food Prot. (2015) 10.4315/0362-028x.jfp-14-328

[21]

Jones "Comparison of PCR Detection Methods for B1, P30, and 18S rDNA Genes of T. gondii in Aqueous Humor" Investig. Ophtalmol. Vis. Sci. (2000)

[22]

Team, Q.D., and QGIS Geographic Information System (2022, December 10). Open Source Geospatial Foundation. Available online: http://qgis.org/.

[23]

Adamska "Molecular detection of Toxoplasma gondii in natural surface water bodies in Poland" J. Water Health (2018) 10.2166/wh.2018.236

[24]

Aramini "Potential contamination of drinking water with Toxoplasma gondii oocysts" Epidemiol. Infect. (1999) 10.1017/s0950268899002113

[25]

Mancianti "Toxoplasma gondii in waterfowl: The first detection of this parasite in Anas crecca and Anas clypeata from Italy" J. Parasitol. (2013) 10.1645/12-34.1

[26]

Nardoni, S., Rocchigiani, G., Varvaro, I., Altomonte, I., Ceccherelli, R., and Mancianti, F. (2019). Serological and Molecular Investigation on Toxoplasma gondii Infection in Wild Birds. Pathogens, 8. 10.3390/pathogens8020058

[27]

Puvanesuaran "Isolation and genotyping of Toxoplasma gondii from free-range ducks in Malaysia" Avian Dis. (2013) 10.1637/10304-071212-resnote.1

[28]

Aubert "Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France" Vet. Parasitol. (2010) 10.1016/j.vetpar.2010.03.033

[29]

Lewis "Active wild bird surveillance of avian influenza viruses, a report" EFSA Support. Publ. (2022)

[30]

Fanelli "A systematic review and meta-analysis of Toxoplasma gondii in roe deer (Capreolus capreolus) and red deer (Cervus elaphus) in Europe" Zoonoses Public Health (2021) 10.1111/zph.12780

[31]

Damek, F., Swart, A., Waap, H., Jokelainen, P., Le Roux, D., Deksne, G., Deng, H., Schares, G., Lunden, A., and Alvarez-Garcia, G. (2023). Systematic Review and Modelling of Age-Dependent Prevalence of Toxoplasma gondii in Livestock, Wildlife and Felids in Europe. Pathogens. 10.3390/pathogens12010097

[32]

Schüz, E., Berthold, P., Gwinner, E., and Oelke, H. (1971). Grundriss der Vogelzugskunde, Verlag.

[33]

Dubey "Recent epidemiologic and clinical importance of Toxoplasma gondii infections in marine mammals: 2009–2020" Vet. Parasitol. (2020) 10.1016/j.vetpar.2020.109296

[34]

Spina, F., and Volponi, S. (2008). Atlante Della Migrazione Degli Uccelli in Italia: Non-Passeriformi, Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA).

[35]

Biancifiori "Avian toxoplasmosis: Experimental infection of chicken and pigeon" Comp. Immunol. Microbiol. Infect. Dis. (1986) 10.1016/0147-9571(86)90046-9

[36]

Epidemiologic significance of Toxoplasma gondii infections in turkeys, ducks, ratites and other wild birds: 2009–2020

J. P. Dubey, F. H. A. Murata, C. K. Cerqueira-Cézar et al.

Parasitology 2021 10.1017/s0031182020001961

[37]

Opsteegh "Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR" Int. J. Food Microbiol. (2010) 10.1016/j.ijfoodmicro.2010.02.027

[38]

Koethe "Quantitative detection of Toxoplasma gondii in tissues of experimentally infected turkeys and in retail turkey products by magnetic-capture PCR" Food Microbiol. (2015) 10.1016/j.fm.2015.06.005

[39]

Bachand "Serological and molecular detection of Toxoplasma gondii in terrestrial and marine wildlife harvested for food in Nunavik, Canada" Parasites Vectors (2019) 10.1186/s13071-019-3408-9

[40]

Zou "First genetic characterization of Toxoplasma gondii infection in poultry meat intended for human consumption in eastern China" Infect. Genet. Evol. (2017) 10.1016/j.meegid.2017.08.022

[41]

Work, T.M., Verma, S.K., Su, C., Medeiros, J., Kaiakapu, T., Kwok, O.C., and Dubey, J.P. (2016). Toxoplasma gondii antibody prevalence and two new genotypes of the parasite in endangered hawaiian geese (Nene: Branta sandvicensis). J. Wildl. Dis., 52. 10.7589/2015-09-235

[42]

Skorpikova "Molecular detection of Toxoplasma gondii in feathered game intended for human consumption in the Czech Republic" Int. J. Food Microbiol. (2018) 10.1016/j.ijfoodmicro.2018.07.019

[43]

Karakavuk, M., Aldemir, D., Mercier, A., Atalay Şahar, E., Can, H., Murat, J.B., Döndüren, Ö., Can, Ş., Özdemir, H.G., and Değirmenci Döşkaya, A. (2018). Prevalence of toxoplasmosis and genetic characterization of Toxoplasma gondii strains isolated in wild birds of prey and their relation with previously isolated strains from Turkey. PLoS ONE, 13. 10.1371/journal.pone.0196159

[44]

Opsteegh "Low predictive value of seroprevalence of Toxoplasma gondii in cattle for detection of parasite DNA" Int. J. Parasitol. (2011) 10.1016/j.ijpara.2010.10.006

[45]

Latitudinal variability in the seroprevalence of antibodies against Toxoplasma gondii in non-migrant and Arctic migratory geese

Cecilia A.M. Sandström, Anita G.J. Buma, Bethany J. Hoye et al.

Veterinary Parasitology 2013 10.1016/j.vetpar.2012.12.027

[46]

Vitaliano "Experimental infection of Crested Caracara (Caracara plancus) with Toxoplasma gondii simulating natural conditions" Vet. Parasitol. (2010) 10.1016/j.vetpar.2010.04.010

[47]

Ross "Presumed acquired ocular toxoplasmosis in deer hunters" Retina (2001) 10.1097/00006982-200106000-00005

[48]

Conrady "Ocular Toxoplasmosis after Exposure to Wild Game" Ocul. Immunol. Inflamm. (2022) 10.1080/09273948.2020.1854316

[49]

Toxoplasma gondii: from animals to humans

Astrid M Tenter, Anja R Heckeroth, Louis M Weiss

International Journal for Parasitology 2000 10.1016/s0020-7519(00)00124-7

[50]

Smith "Documented Outbreaks of Toxoplasmosis: Transmission of Toxoplasma gondii to Humans" J. Food Prot. (1993) 10.4315/0362-028x-56.7.630

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Published: Mar 18, 2023
Vol/Issue: 12(3)
Pages: 478
License: View

Authors

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Filippo Maria Dini