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Toxoplasma gondii in water buffaloes (Bubalus bubalis) from Romania: what is the importance for public health?

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Abstract

The purpose of our study was to evaluate the prevalence of Toxoplasma gondii infection in autochthonous Carpathian buffaloes from northwestern Romania by serology, PCR techniques, and mouse bioassay. Agreement between MAT and ELISA, correlation between indirect and direct detection methods, and risk factors were evaluated. The apparent overall seroprevalence of T. gondii was 8.1% by MAT and 6.6% by ELISA. The agreement between ELISA and MAT was fair. The apparent seroprevalence was significantly higher in adult buffaloes (12.5%) compared to calves (0.0%) and juveniles (1.9%) by MAT. Most of the positive adult buffaloes detected by MAT had antibodies at a low sera dilution and the highest dilution was 1:768 in a juvenile female (30 months). No viable T. gondii was detected by mouse bioassay, as no T. gondii cyst or DNA was found in the brain of mice and they did not seroconvert. However, T. gondii DNA was detected in two buffaloes: in a 30-month-old male buffalo by qPCR on the diaphragm digest and in a 252-month-old female buffalo by RE nPCR on the mesenteric lymph node. Both animals were negative in MAT and ELISA. The total prevalence of T. gondii by direct detection methods was 2.7%. There was no correlation between indirect and direct detection methods. Since no viable T. gondii was detected in buffaloes, the risk of human infection from buffalo meat is minimal. Buffaloes’ biological response to a T. gondii infection appears to be very similar to the response of cattle.

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References

  • Ahmad N, Qayyum M (2014) Seroprevalence and risk factors for toxoplasmosis in large ruminants in northern Punjab, Pakistan. J Infect Dev Ctries 8:1022–1028

    Article  Google Scholar 

  • Belluco S, Mancin M, Conficoni D, Simonato G, Pietrobelli M, Ricci A (2016) Investigating the determinants of Toxoplasma gondii prevalence in meat: a systematic review and meta-regression. PLoS One 11(4):0153856

    Article  Google Scholar 

  • Belluco S, Simonato G, Mancin M, Pietrobelli M, Ricci A (2017) Toxoplasma gondii infection and food consumption: a systematic review and meta-analysis of case-controlled studies. CRIT REV FOOD SCI NUTR 58:3085–3096. https://doi.org/10.1080/10408398.2017.1352563

    Article  PubMed  Google Scholar 

  • Borghese A (2005) Buffalo production and research, Food and Agriculture Organization of the United Nations, Rome. Buffalo production and research. In: FAO (ed) REU Technical Series 67:1–315

  • Borghese A (2013) Buffalo livestock and products. CRA – Council for Research in Agriculture, pp 511 ISBN 978-88-97081-27

  • Bouwknegt M, Devleesschauwer B, Graham H, Robertson LJ, van der Giessen JW, The Euro-FBP workshop participants (2018) Prioritisation of food-borne parasites in Europe, 2016. Euro Surveill 23(9):17–00161

    Article  Google Scholar 

  • Brasil AW, Parentoni RN, Feitosa TF, Bezerra S, Vilela VL, Pena HF, de Azevedo SS (2015) Risk factors for Toxoplasma gondii and Neospora caninum seropositivity in buffaloes in Paraiba state, Brazil. Rev Bras Parasitol Vet 24:459–463

    Article  CAS  Google Scholar 

  • Burrells A, Taroda A, Opsteegh M, Schares G, Benavides J, Dam-Deisz C, Bartley PM, Chianini F, Villena I, van der Giessen J, Innes EA, Katzer F (2018) Detection and dissemination of Toxoplasma gondii in experimentally infected calves, a single test does not tell the whole story. Parasit Vectors 11(1):45

    Article  Google Scholar 

  • Chaudhary ZI, Ahmed RS, Hussain SMI, Shakoori AR (2006) Detection of Toxoplasma gondii infection in butchers and buffaloes by polymerase chain reaction and latex agglutination test. Pak J Zool 38:333–336

    CAS  Google Scholar 

  • Dehkordi FS, Borujeni MR, Rahimi E, Abdizadeh R (2013) Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine, and camel milk using cell cultivation, cat bioassay, capture ELISA, and PCR methods in Iran. Foodborne Pathog Dis 10(2):120–125

    Article  CAS  Google Scholar 

  • Dubey JP (2010) Toxoplasmosis of animals and humans, 2nd edn. CRC Press Taylor, Francis Group, Boca Raton

    Google Scholar 

  • Dubey JP, Desmonts G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet J 19(4):337–339

    Article  CAS  Google Scholar 

  • Dubey JP, Thulliez P (1993) Persistence of tissue cysts in edible tissues of cattle fed Toxoplasma gondii oocysts. Am J Vet Res 54:270–273

    CAS  PubMed  Google Scholar 

  • Dubey JP, Desmonts G, McDonald C, Walls KW (1985) Serologic evaluation of cattle inoculated with Toxoplasma gondii: comparison of Sabin-Feldman dye test and other agglutination tests. Am J Vet Res 46(5):1085–1088

    CAS  PubMed  Google Scholar 

  • Dubey JP, Verma SK, Ferreira LR, Oliveira S, Cassinelli AB, Ying Y, Kwok OCH, Tuo W, Chiesa OA, Jones JL (2014) Detection and survival of Toxoplasma gondii in milk and cheese from experimentally infected goats. J Food Prot 77:1747–1753

    Article  CAS  Google Scholar 

  • Fallahi S, Kazemi B, Seyyed Tabaei SJ, Bandehpour M, Lasjerdi Z, Taghipour N, Zebardast N, Nikmanesh B, Omrani VF, Ebrahimzadeh F (2014) Comparison of the RE and B1 gene for detection of Toxoplasma gondii infection in children with cancer. Parasitol Int 63:37–41

    Article  CAS  Google Scholar 

  • FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization] (2014) Multicriteria-based ranking for risk management of food-borne parasites. Microbiological risk assessment Series 23, Rome, pp 302

  • Gautam OP, Chhabra MB, Gupta SL, Mahajan SK (1982) Experimental toxoplasmosis in buffalo calves. Vet Parasitol 11(4):293–299

    Article  CAS  Google Scholar 

  • Giordano G, Guarini P, Ferrari P, Biondi-Zoccai G, Schiavone B, Giordano A (2010) Beneficial impact on cardiovascular risk profile of water buffalo meat consumption. Eur J Clin Nutr 64:1000–1006

    Article  CAS  Google Scholar 

  • Hamidinejat H, Ghorbanpour M, Nabavi L, Hajikolaie MRH, Jalali MHR (2010) Seroprevalence of Toxoplasma gondii in water buffaloes (Bubalus bubalis) in south-west of Iran. Trop Biomed 27:275–279

    PubMed  Google Scholar 

  • Hassanain MA, El-Fadal HA, Hassanain NA, Shaapan RM, Barakat AM, El-Razik KAA (2013) Serological and molecular diagnosis of toxoplasmosis in human and animals. World J Med Sci 9(4):243–247

    CAS  Google Scholar 

  • 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 30:69–75

    Article  CAS  Google Scholar 

  • Hosein S, Limon G, Dadios N, Guitian J, Blake DP (2016) Toxoplasma gondii detection in cattle: a slaughterhouse survey. Vet Parasitol 228:126–129

    Article  Google Scholar 

  • Jones CD, Okhravi N, Adamson P, Tasker S, Lightman S (2000) Comparison of PCR detection methods for B1, P30, and 18S rDNA genes of T. gondii in aqueous humor. Invest Ophthalmol Vis Sci 41:634–644

    CAS  PubMed  Google Scholar 

  • Kondaiah N, Anjaneyulu ASR (2003) Potential of buffalo meat to processing different products. Proc. of Fourth Asian Buffalo Congress, New Delhi, India 28:200–204

  • Kos K (1975) Contribuții la cercetarea etnografică a creșterii bivolilor, Anuarul Muzeului Etnografic al Transilvaniei, VII, seria 1974-1975, pp 121–136

  • Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  Google Scholar 

  • National Institute of Statistics (2017) Livestock and animal production in 2016. http://www.insse.ro/cms/sites/default/files/field/publicatii/efective_de_animale_si_productia_animala_in_anul_2016.pdf

  • Naveena BM, Kiran M (2014) Buffalo meat quality, composition, and processing characteristics: contribution to the global economy and nutritional security. Anim Front 4:18–24

    Article  Google Scholar 

  • Opsteegh M, Langelaar M, Sprong H, Den Hartog L, De Craeye S, Bokken G, Ajzenberg D, Kijlstra A, Van Der Giessen J (2010) Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. Int J Food Microbiol 139:193–201

    Article  CAS  Google Scholar 

  • Opsteegh M, Prickaerts S, Frankena K, Evers EG (2011) A quantitative microbial risk assessment for meatborne Toxoplasma gondii infection in the Netherlands. Int J Food Microbiol 150:103–114

    Article  Google Scholar 

  • Opsteegh M, Schares G, Blaga R, Van der Giessen J, on behalf of the consortium (2016a) Experimental studies on Toxoplasma gondii in the main livestock species (GP/EFSA/BIOHAZ/2013/01) Final report. EFSA supporting publication, EFSA

  • Opsteegh M, Maas M, Schares G, Van der Giessen J, on behalf of the consortium (2016b) Relationship between seroprevalence in the main livestock species and presence of Toxoplasma gondii in meat (GP/EFSA/BIOHAZ/2013/01) An extensive literature review. Final report. EFSA supporting publication, EFSA

  • Persad A, Charles R, Adesiyun AA (2011) Frequency of toxoplasmosis in water Buffalo (Bubalus bubalis) in Trinidad. Vet Med Int 705358

  • Santos LM, Damé MC, Cademartori BG, da Cunha Filho NA, Farias NA, Ruas JL (2013) Occurrence of antibodies to Toxoplasma gondii in water buffaloes and meat cattle in Rio Grande do Sul state, southern Brazil. Acta Parasitol 58:334–336

    CAS  PubMed  Google Scholar 

  • Sergeant ESG (2017) Epitools epidemiological calculators. Ausvet Pty Ltd. http://epitools.ausvet.com.au

  • Villena I, Durand B, Aubert D, Blaga R, Geers R, Thomas M, Perret C, Alliot A, Escotte-Binet S, Thebault A, Boireau P, Halos L (2012) New strategy for the survey of Toxoplasma gondii in meat for human consumption. Vet Parasitol 183:203–208

    Article  Google Scholar 

  • Vitale M, Galluzzo P, Currò V, Gozdzik K, Schillaci D, Di Marco Lo Presti V (2013) A high sensitive nested PCR for Toxoplasma gondii detection in animal and food samples. J Microb Biochem Technol 5:39–41

    Article  CAS  Google Scholar 

  • Watson PF, Petrie A (2010) Method agreement analysis: a review of correct methodology. Theriogenology 73:1167–1179

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Marieke Opsteegh for the helpful suggestions.

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Correspondence to Diana Bărburaș or Adriana Gyӧrke.

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Bărburaș, D., Gyӧrke, A., Blaga, R. et al. Toxoplasma gondii in water buffaloes (Bubalus bubalis) from Romania: what is the importance for public health?. Parasitol Res 118, 2695–2703 (2019). https://doi.org/10.1007/s00436-019-06396-6

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