#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Seroprevalence of anti-Toxoplasma gondii antibodies in wild boars (Sus scrofa), hunting dogs, and hunters of Brazil


Autoři: Fernanda Pistori Machado aff001;  Louise Bach Kmetiuk aff002;  Pedro Irineu Teider-Junior aff001;  Maysa Pellizzaro aff003;  Ana Carolina Yamakawa aff004;  Camila Marinelli Martins aff005;  Renato van Wilpe Bach aff006;  Vívien Midori Morikawa aff007;  Ivan Roque de Barros-Filho aff001;  Hélio Langoni aff004;  Andrea Pires dos Santos aff008;  Alexander Welker Biondo aff001
Působiště autorů: Graduate College of Veterinary Science, Federal University of Paraná (UFPR), Curitiba, Paraná, Brazil aff001;  Graduate College of Cellular and Molecular Biology, Federal University of Paraná (UFPR), Curitiba, Paraná, Brazil aff002;  Public Health Institute (PHI), Federal University of Bahia (UFBA), Salvador, Bahia, Brazil aff003;  Department of Veterinary Hygiene and Public Health, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil aff004;  Department of Nursing and Public Health, State University of Ponta Grossa, Ponta Grossa, Paraná, Brazil aff005;  Department of Medicine, State University of Ponta Grossa, Ponta Grossa, Paraná, Brazil aff006;  Department of Collective Health, Federal University of Parana, Curitiba, Paraná, Brazil aff007;  Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, United States of America aff008
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223474

Souhrn

Seroprevalence of Toxoplasma gondii has been extensively studied in wild boars worldwide due to the emerging risk for human infection through meat consumption. However, this is the first study that reports toxoplasmosis seroprevalence in wild boars, wild boar hunters and their hunting dogs. The aim of the present study was to evaluate the seroprevalence of anti-T. gondii antibodies in the complex wild boars, hunting dogs and hunters, and to determine the risk factors associated with seropositivity in southern and central-western Brazil. Overall, anti-T. gondii seropositivity was observed in 15/71 (21.1%) wild boars by modified agglutination test (MAT); and 49/157 (31.2%) hunting dogs and 15/49 (32.7%) hunters by indirect immunofluorescent antibody test (IFAT). Seroprevalence of toxoplasmosis in Brazilian wild boars was within the national and international range, posting wild boars as potential environmental sentinels for T. gondii presence. In addition, the findings have comparatively shown that wild boars have been less exposed to infection than hunting dogs or hunters in both Brazilian regions. Seropositivity for T. gondii was statistically higher in 12/14 (85.7%) captured wild boars when compared to 5/57 (7.0%) free-range wild boars (p = 0.000001). Similarly, captured wild boars from anthropized areas were more likely to be seropositive than of natural regions (p = 0.000255). When in multiple regression model, dogs with the habit of wild boar hunting had significant more chance to be positive (adjusted-OR 4.62 CI 95% 1.16–18.42). Despite potential as sentinels of environmental toxoplasmosis, seroprevalence in wild boars alone may provide a biased basis for public health concerns; thus, hunters and hunting dogs should be always be included in such studies. Although hunters should be aware of potential T. gondii infection, wild boars from natural and agricultural areas may present lower protozoa load when compared to wild boars from anthropized areas, likely by the higher presence of domestic cats as definitive hosts.

Klíčová slova:

Brazil – Cats – Dogs – Domestic animals – Meat – Pets and companion animals – Swine – Toxoplasma gondii


Zdroje

1. Dubey JP. Toxoplasmosis of Animals and Humans. 2 nd ed. Florida: CRC Press; 2010.

2. Hill DE, Dubey JP. Toxoplasma gondii. Biology of Foodborne Parasites. CRC Press; 2015. pp. 209–222.

3. Hill DE, Dubey JP. Toxoplasma gondii as a parasite in food: analysis and control. Microbiol Spectr. 2016;4(4). doi: 10.1128/microbiolspec.PFS-0011-2015 27726776

4. Pedrosa F, Salerno R, Padilhac FVB, Galetti M. Current distribution of invasive feral pigs in Brazil: economic impacts and ecological uncertainty. Nat Conserv. 2015;13(1): 84–87. doi: 10.1016/j.ncon.2015.04.005

5. Brazilian Institute of Environment and Natural Renewable Resources–IBAMA. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis. Instrução Normativa nº 3, 31 Jan 2013. 2013. Available from: http://www.ibama.gov.br/legislacao/javali. Cited 20 April 2019.

6. Rosa CA, Wallau MO, Pedrosa F. Hunting as the Main Technique Used to Control Wild boars in Brazil. Wildl Soc Bull. 2018;42(1): 111–118. doi: 10.1002/wsb.851

7. Rostami A, Riahi SM, Fakhri Y, Saber V, Hanifehpour H, Valizadeh S, et al. The global seroprevalence of Toxoplasma gondii among wild boars: A systematic review and meta-analysis. Vet Parasitol. 2017;244: 12–20. doi: 10.1016/j.vetpar.2017.07.013 28917302

8. Winter M, Abate SD, Pasqualetti MI, Fariña FA, Ercole ME, Pardini L, et al. Toxoplasma gondii and Trichinella infections in wild boars (Sus scrofa) from Northeastern Patagonia, Argentina. Prev Vet Med. 2019;1(168): 75–80. doi: 10.1016/j.prevetmed.2019.04.014

9. Fornazari F, Langoni H, Silva RC, Guazzelli A, Ribeiro MG, Chiacchio SB. Toxoplasma gondii infection in wild boars (Sus scrofa) bred in Brazil. Vet Parasitol. 2009;164(2–4): 333–334. doi: 10.1016/j.vetpar.2009.05.005 19515494

10. Santos LMJF Farias NAR, Oliveira PA Cademartori BG, Ramos TS, Oliveira FC, et al. Presence of Toxoplasma gondii infection in wild boar in southern Brazil. Sch J Agric Vet Sci. 2016;3(3): 238–241.

11. Brandão LNS, Rosa JMA, Kramer B, Sousa ATHI, Trevisol IM, Nakazato L, et al. Detection of Toxoplasma gondii infection in feral wild boars (Sus scrofa) through indirect hemagglutination and PCR. Cienc. Rural. 2019;49(3): e20180640.

12. Berger‐Schoch AE, Bernet D, Doherr MG, Gottstein B, Frey CF. Toxoplasma gondii in Switzerland: A Serosurvey Based on Meat Juice Analysis of Slaughtered Pigs, Wild Boar, Sheep and Cattle. Zoonoses and Public Health. 2011;58(7): 472–478. doi: 10.1111/j.1863-2378.2011.01395.x 21824348

13. Lopes AP, Sargo R, Rodrigues M, Cardoso L. High seroprevalence of antibodies to Toxoplasma gondii in wild animals from Portugal. Parasitol Res. 2011;108(5): 1163–1169. doi: 10.1007/s00436-010-2158-6 21104273

14. Shiibashi T., Narasaki K., Yoshida M., Nogami S. Prevalence of anti-Toxoplasma gondii antibody in hunter-killed wild boars, Sus scrofa leucomystax, on Amakusa Island, Kumamoto Prefecture, Japan. J Vet Med Sci. 2004;66: 327–328. doi: 10.1292/jvms.66.327 15107568

15. Jeong W, Yoon H, Kim YK, Moon OK, Kim DS, An DJ. Prevalence of antibodies to Toxoplasma gondii in South Korean wild boar (Sus scrofa coreanus). J. Wildlife. Dis. 2014; 50, 902–905. doi: 10.7589/2013-03-077 25014905

16. Pedersen K, Bauer NE, Rodgers S, Bazan LR, Mesenbrink BT, Gidlewski T. Antibodies to Various Zoonotic Pathogens Detected in Feral Swine (Sus scrofa) at Abattoirs in Texas, USA. J Food Prot. 2017;80(8): 1239–1242. doi: 10.4315/0362-028X.JFP-17-016 28686494

17. Gresham CS, Gresham CA, Duffy MJ, Faulkner CT, Patton S. Increased prevalence of Brucella suis and pseudorabies virus antibodies in adults of an isolated feral swine population in coastal South Carolina. J Wildl Dis. 2002;38(3): 653–6. doi: 10.7589/0090-3558-38.3.653 12238392

18. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30(12–13): 1217–1258. doi: 10.1016/s0020-7519(00)00124-7 11113252

19. Carlos RSA, Albuquerque GR, Bezerra RA, Sicupira PML, Munhoz AD, Lopes CWG. Ocorrência de anticorpos anti-Toxoplasma gondii e principais fatores de risco associados à infecção canina na região de Ilhéus-Itabuna, estado da Bahia. Rev. Bras. Med. Vet. 2010;32(2): 115–121.

20. Benitez ADN, Martins FDC, Mareze M, Santos NJR, Ferreira FP, Martins CM. Spatial and simultaneous representative seroprevalence of anti-Toxoplasma gondii antibodies in owners and their domiciled dogs in a major city of southern Brazil. PLoS One. 2017;12(7): e0180906. doi: 10.1371/journal.pone.0180906 28732033

21. De Almeida JC, Frehse MS, Navarro IT, Garcia JL, Biondo AW, Freire RL. 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 Parasitol. 2016;61(4): 694–696. doi: 10.1515/ap-2016-0097 27787201

22. Witkowski L, Czopowicz M, Nagy DA, Potarniche AV, Aoanei MA, Imomov N, Mickiewicz M, Welz M, Szaluś-Jordanow O, Kaba J. Seroprevalence of Toxoplasma gondii in wild boars, red deer and roe deer in Poland. Parasite. 2015;22: 17. doi: 10.1051/parasite/2015017 25993468

23. Ullmann LS, Gravinatti ML, Yamatogi RS, Santos LCD, Moraes W, Cubas ZS, et al. Serosurvey of anti- Leptospira sp. and anti- Toxoplasma gondii antibodies in capybaras and collared and white-lipped peccaries. Rev Soc Bras Med Trop. 2017;50(2): 248–250. doi: 10.1590/0037-8682-0315-2016 28562764

24. Carmo EL, Morais RAPB, Oliveira AS, Figueredo JE, Figueredo MC, Silva AV, et al. Soroepidemiologia da infecção pelo Toxoplasma gondii no Município de Novo Repartimento, Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2016;7(4): 79–87. doi: 10.5123/S2176-62232016000400010

25. Carmo EL, Póvoa MM, Monteiro NS, Marinho RR, Nascimento JM, Freitas SN, et al. Surto de toxoplasmose humana no Distrito de Monte Dourado, Município de Almeirim, Pará, Brasil. Rev Pan-Amaz Saude. 2010;1(1): 61–66. doi: 10.5123/S2176-62232010000100009

26. Garcia JL, Navarro IT, Ogawa L, Oliveira RC. Soroepidemiologia da toxoplasmose em gatos e cães de propriedades rurais do município de Jaguapitã, estado do Paraná, Brasil. Cienc Rural. 1999;29(1): 99–104. http://dx.doi.org/10.1590/S0103-84781999000100018.

27. IBGE. Ponta Grossa- Panorama geral [Internet]. 2010. Available: https://cidades.ibge.gov.br/brasil/pr/ponta-grossa/panorama.

28. IBGE. Aporé- Panorama Geral [Internet]. 2010. https://cidades.ibge.gov.br/brasil/go/apore/panorama

29. Desmonts G, Remington JS. Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. J Clin Microbiol. 1980;11(6): 562–568. 7000807

30. Camargo ME. Introdução às técnicas de imunofluorescência. Rev Bras. Patol Clín. 1974;10(30): 43–169.

31. Djokic V, Blaga R, Aubert D, Durand B, Perret C, Geers R, et al. Toxoplasma gondii infection in pork produced in France. Parasitology. 2016;143(5): 557–567. doi: 10.1017/S0031182015001870 26928081

32. Opsteegh M, Swart A, Fonville M, Dekkers L, van der Giessen J. Age-related Toxoplasma gondii seroprevalence in Dutch wild boar inconsistent with lifelong persistence of antibodies. PLoS One. 2011;6(1): e16240. doi: 10.1371/journal.pone.0016240 21283764

33. Costa DG, Marvulo MF, Silva JS, Santana SC, Magalhães FJ, Filho CD, et al. Seroprevalence of Toxoplasma gondii in domestic and wild animals from the Fernando de Noronha, Brazil. J Parasitol. 2012;98(3): 679–680. doi: 10.1645/GE-2910.1 22150091

34. Liu Q, Wang ZD, Huang SY, Zhu XQ. Diagnosis of toxoplasmosis and typing of Toxoplasma gondii. Parasit Vectors. 2015;8: 292. doi: 10.1186/s13071-015-0902-6 26017718

35. IBM Corp. Released in 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.

36. Environmental Systems Research Institute (ESRI), (2014). ArcGIS Desktop Help 10.2 Geostatistical Analyst.

37. Minho AP, Freire RL, Vidotto O, Gennari SM, Marana EM, Garcia JL, et al. Evaluation of the indirect fluorescent antibody test and modified agglutination test for detection of antibodies against Toxoplasma gondii in experimentally infected pigs. Pesq. Vet. Bras. 2004;24(4): 199–202 http://dx.doi.org/10.1590/S0100-736X2004000400005.

38. Beral M, Rossi M, Aubert D, Gasqui P, Terrier ME, Klein F, et al. Environmental factors associated with the seroprevalence of Toxoplasma gondii in Wild Boars (Sus scrofa), France. Ecohealth. 2012;9(3): 303–309. doi: 10.1007/s10393-012-0786-2 22820902

39. Ranucci D, Veronesi F, Moretti A, Branciari R, Miraglia D, Manfredi MT, et al. Seroprevalence of Toxoplasma gondii in wild boars (Sus scrofa) from Central Italy. Parasite. 2013;20: 48. doi: 10.1051/parasite/2013048 24280567

40. Paştiu AI, Györke A, Blaga R, Mircean V, Rosenthal BM, Cozma V. In Romania, exposure to Toxoplasma gondii occurs twice as often in swine raised for familial consumption as in hunted wild boar, but occurs rarely, if ever, among fattening pigs raised in confinement. Parasitol Res. 2013;112(6): 2403–2407. doi: 10.1007/s00436-013-3353-z 23455939

41. Gaston W, Armstrong JB, Arjo W, Stribling HL. Home range and habitat use of feral hogs (Sus scrofa) on Lowndes County WMA, Alabama. In: National Conference on feral hogs. 2008: 6. Available from: https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1003&context=feralhog

42. Allwin B, Swaminathan R, Mohanraj A, Suhas GN, Vedaminckam S, Gopal S, et al., The Wild Pig (Sus scrofa) Behavior- A Retrospective Study Veterinar Sci Techno. 2016;7: 4. doi: 10.4172/2157-7579.1000333

43. De Souza SLP, Gennari SM, Yai LEO, D´Auria SRN, Cardoso SMS, Guimarães Junior JS, et al. Occurrence of Toxoplasma gondii antibodies in sera from dogs of the urban and rural areas from brazil. Rev. Bras. Parasitol. Vet. 2003;12(1): 1–3.

44. Ali CN, Harris JA, Watkins JD, Adesiyun AA. Seroepidemiology of Toxoplasma gondii in dogs in Trinidad and Tobago. Vet Parasitol. 2003;113(3–4): 179–187. doi: 10.1016/s0304-4017(03)00075-x 12719132

45. Machacova T, Bartova E, Sedlak K, Slezakova R, Budikova M, Piantedosi D, et al. Seroprevalence and risk factors of infections with Neospora caninum and Toxoplasma gondii in hunting dogs from Campania region, southern Italy. Folia Parasitol (Praha). 2016;63. doi: 10.14411/fp.2016.012 27189127

46. Cano-Terriza D, Puig-Ribas M, Jiménez-Ruiz S, Cabezón Ó, Almería S, Galán-Relaño Á, et al. Risk factors of Toxoplasma gondii infection in hunting, pet and watchdogs from southern Spain and northern Africa. Parasitol Int. 2016;65(5 Pt A): 363–366. doi: 10.1016/j.parint.2016.05.001 27155133

47. Belluco S, Mancin M, Conficoni D, Simonato G, Pietrobelli M, Ricci A. Investigating the Determinants of Toxoplasma gondii Prevalence in Meat: A Systematic Review and Meta-Regression. PLoS One. 2016;11(4): e0153856. doi: 10.1371/journal.pone.0153856 27082633

48. Giménez-Anaya A, Herrero J, Rosell C, Couto S, García-Serrano A. Food habits of wild boars (Sus Scrofa) in a Mediterranean coastal wetland. Wetlands. 2008;28(1): 197–203. doi: 10.1672/07-18.1

49. Schley L, Roper TJ. Diet of Wild Boar (Sus scrofa) in Western Europe, with particular reference to consumption of agricultural crops. Mammal Review. 2003;33(1): 43–56.

50. Ferroglio E, Bosio F, Trisciuoglio A, Zanet S. Toxoplasma gondii in sympatric wild herbivores and carnivores: epidemiology of infection in the Western Alps. Parasites & Vectors. 2014;7(1): 196. doi: 10.1186/1756-3305-7-196 24766665

51. Alves BF, Oliveira S, Soares HS, Pena HFJ, Conte-Junior CA, Gennari SM. Isolation of viable Toxoplasma gondii from organs and Brazilian commercial meat cuts of experimentally infected pigs. Parasitol Res. 2019;118(4): 1331–1335. doi: 10.1007/s00436-019-06229-6 30783860

52. Foroutan M, Fakhri Y, Riahi SM, Ebrahimpour S, Namroodi S, Taghipour A, et al. The global seroprevalence of Toxoplasma gondii in pigs: A systematic review and meta-analysis. Vet Parasitol. 2019;269: 42–52. doi: 10.1016/j.vetpar.2019.04.012 31079827

53. Czaplewski RL, Crowe DM, Mcdonald LL. Sample sizes and confidence intervals for wildlife population ratios. Wildl Soc Bull. 1983;11(2): 121–128.


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#