Is contamination of bovine-sourced material with bovine viral diarrhea virus still a problem in countries with ongoing eradication campaigns?

Antos, Aleksandra; Rola, Jerzy; Bednarski, Michał; Krzysiak, Michał Konrad; Kęsik-Maliszewska, Julia; Larska, Magdalena

doi:10.2478/aoas-2020-0056

Abstract

In this report, we describe the detection of bovine viral diarrhea virus (BVDV) contamination in commercial animal-derived sera and vaccines against animal viral pathogens on the market in Poland. Antibodies against BVDV were detected in 4/45 sera samples (8.9%) using an ELISA test. The presence of BVDV antigen was found using ELISA in 3/45 serum samples (6.6%) and 18/172 vaccine samples (10.5%). An RT -PCR was conducted using primers targeting two genome regions, the five prime untranslated region (5’UTR) and N-terminal protease (N^pro). BVDV RNA was detected in 33/45 (73.3%) of sera, and 11/172 samples (6.4%) of collected vaccines, of which one vaccine did not declare BVDV strain in its composition. A single serum showed the presence of an infectious virus and only one was contaminated with all 3 species of BVDV. The most frequent species in sera was BVDV-3 (75.5%), whereas in vaccines only BVDV-1 was identified. Sequence analysis showed that the tested commercial sera and one vaccine were contaminated by six genotypes of BVDV: -1a, -1b, -1c, -1d, -2a, and -3. Identification of BVDV and its genetic material in animal-derived products is important due to the possibility of pestivirus transmission as well as the chance of falsifying the results of a diagnostic test. It also demonstrates the necessity of rigorous monitoring of the bioproducts used at the laboratory and industry level.

References

Audet S.A., Crim R.L., Beeler J. (2000). Evaluation of vaccines, interferons and cell substrates for pestivirus contamination. Biologicals, 28: 41–46.
Search in Google Scholar Back to article
Barkema H.W., Bartels C.J., van Wuijckhuise L., Hesselink J.W., Holzhauer M., Weber M.F., Franken P., Kock P.A., Bruschke C.J., Zimmer G.M. (2001). Outbreak of bovine virus diarrhea on Dutch dairy farms induced by a bovine herpesvirus 1 marker vaccine contaminated with bovine virus diarrhea virus type 2. Tijdschr. Diergeneeskd., 126: 158–165.
Search in Google Scholar Back to article
Bauermann F.V., Flores E.F., Ridpath J.F. (2012). Antigenic relationships between Bovine viral diarrhea virus 1 and 2 and HoBi virus: possible impacts on diagnosis and control. J. Vet. Diagn. Invest., 24: 253–261.
Search in Google Scholar Back to article
Bauermann F.V., Flores E.F., Falkenberg S.M., Weiblen R., Ridpath J.F. (2014). Lack of evidence for the presence of emerging HoBi-like viruses in North American fetal bovine serum lots. J. Vet. Diagn. Invest., 26: 10–17.
Search in Google Scholar Back to article
Baxi M., Mc Rae D., Baxi S., Greiser-Wilke I., Vilcek S., Amoako K., Deregt D. (2006). A one-step multiplex real-time RT-PCR for detection and typing of bovine viral diarrhea viruses. Vet. Microbiol., 116: 37–44.
Search in Google Scholar Back to article
Cortez A., Heinemann M.B., de Castro A.M.M.G., Soares R.M., Pinto A.M.V., Al-fieri A.A., Flores E.F., Leite R.C., Richtzenhain L.J. (2006). Genetic characterization of Brazilian bovine viral diarrhea virus isolates by partial nucleotide sequencing of the 5’-UTR region. Pesq. Vet. Bras., 26: 211–216.
Search in Google Scholar Back to article
Decaro N., Lucente M.S., Mari V., Cirone F., Cordioli P., Camero M., Sciarret-ta R., Losurdo M., Lorusso E., Buonavaglia C. (2011). Atypical pestivirus and severe respiratory disease in calves, Europe. Emerg. Infect. Dis., 17: 1549–1552.
Search in Google Scholar Back to article
Deregt D., Loewen K.G. (1995). Bovine viral diarrhea virus: biotypes and disease. Can. Vet. J., 36: 371–378.
Search in Google Scholar Back to article
Falcone E., Cordioli P., Tarantino M., Muscillo M., Sala G., La Rosa G., Archetti I.L., Marianelli C., Lombardi G., Tollis M. (2003). Experimental infection of calves with bovine viral diarrhoea virus type-2 (BVDV-2) isolated from a contaminated vaccine. Vet. Res. Commun., 27: 577–589.
Search in Google Scholar Back to article
Giammarioli M., Ridpath J.F., Rossi E., Bazzucchi M., Casciari C., De Mia G.M. (2015). Genetic detection and characterization of emerging HoBi-like viruses in archival foetal bovine serum batches. Biologicals, 43: 220–224.
Search in Google Scholar Back to article
Giangaspero M., Harasawa R., Verhulst A. (1997). Genotypic analysis of the 5’-untranslated region of a pestivirus strain isolated from human leukocytes. Microbiol. Immunol., 41: 829–834.
Search in Google Scholar Back to article
Giangaspero M., Vacirca G., Harasawa R., Büttner M., Panuccio A., De Giuli Morghen C., Zanetti A., Belloli A., Verhulst A. (2001). Genotypes of pestivirus RNA detected in live virus vaccines for human use. J. Vet. Med. Sci., 63: 723–733.
Search in Google Scholar Back to article
Hawkes P.W. (2015). Fetal bovine serum: geographic origin and regulatory relevance of viral contamination. Bioresour. Bioprocess, 2: 34.
Search in Google Scholar Back to article
Hawkes P.W. (2016). Fetal Bovine Serum (FBS). Irradiation Working Group. Paper was written with input from: GE Life Sciences (HyClone Laboratories), SAFC (Sigma Aldrich), and Biowest, https://www.biowest.net/media/biowest_topics_for_discussion__analysis_chapter_8__066350600_0934_20052016.pdf, Access date: 20 May 2016.
Search in Google Scholar Back to article
IDEXXLaboratories. (2005). Bovine Viral Diarrhea Virus Antigen Serum/Plus Test Kit Validation Data Report. Westbrook, Maine. On file at IDEXX Laboratories, Inc.
Search in Google Scholar Back to article
Kuta A., Polak M.P., Larska M., Żmudziński J.F. (2013 a). Monitoring of Bovine Viral Diarrhoea Virus (BVDV) infection in Polish dairy herds using bulk tank milk samples. Bull. Vet. Inst. Pulawy, 57: 149–156.10.2478/bvip-2013-0028
Search in Google Scholar Back to article
Kuta A., Polak M.P., Larska M., Żmudziński J.F. (2013 b). Predominance of bovine viral diarrhea virus 1b and 1d subtypes during eight years of survey in Poland. Vet. Microb., 166: 639–644.10.1016/j.vetmic.2013.07.00223890673
Search in Google Scholar Back to article
Laassri M., Mee E.T., Connaughton S.M., Manukyan H., Gruber M., Rodriguez-Hernandez C., Minor P.D., Schepelmann S., Chumakov K., Wood D.J. (2018). Detection of bovine viral diarrhoea virus nucleic acid, but not infectious virus, in bovine serum used for human vaccine manufacture. Biologicals, 55: 63–70.
Search in Google Scholar Back to article
Lanyon S.R., Anderson M.L., Bergman E., Reichel M.P. (2013). Validation and evaluation of a commercially available ELISA for the detection of antibodies specific to bovine viral diarrhoea virus (bovine pestivirus). Aust. Vet. J., 91: 52–56.
Search in Google Scholar Back to article
Liu L., Xia H., Belák S., Baule C. (2008). A TaqMan real-time RT-PCR assay for selective detection of atypical bovine pestiviruses in clinical samples and biological products. J. Virol. Methods, 154: 82–85.
Search in Google Scholar Back to article
Liu L., Xia H., Baule C., Belak S. (2009). Maximum likelihood and Bayesian analyses of a combined nucleotide sequence dataset for genetic characterization of a novel pestivirus, SVA/cont-08. Arch. Virol., 154: 1111–1116.
Search in Google Scholar Back to article
Mirosław P., Polak M. (2019). Increased genetic variation of bovine viral diarrhea virus in dairy cattle in Poland. BMC Vet. Res., 15: 278.
Search in Google Scholar Back to article
Monteiro F.L., Cargnelutti J.F., Braunig P., Folgueras-Flatschart A.V., Santos N.C., Pituco E.M., Weiblen R., Flores E.F. (2018). Detection and genetic identification of pestiviruses in Brazilian lots of fetal bovine serum collected from 2006 to 2014. Pesq. Vet. Bras., 38: 387–392.
Search in Google Scholar Back to article
Nogueira F.C.S., Velasquez E., Melo A.S.O., Domont G.B. (2016). Zika virus may not be alone: proteomics associates a bovine-like viral diarrhea virus to microcephaly. Biorxiv, doi: http://dx.doi.org/10.1101/062596.10.1101/062596
Search in Google Scholar Back to article
Pecora A., Perez Aquirreburualde M.S., Ridpath J.F., Dus Santos M.J. (2019). Molecular characterization of pestiviruses in fetal bovine sera originating from Argentina: evidence of circulation of HoBi-like viruses. Front. Vet. Sci., 6: 359.
Search in Google Scholar Back to article
Peletto S., Zuccon F., Pitti M., Gobbi E., Marco L.D., Caramelli M., Masoero L., Acutis P.L. (2012). Detection and phylognetic analysis of an atypical pestivirus, strain IZSPLV_ To. Res. Vet. Sci., 92: 147–150.
Search in Google Scholar Back to article
Polak M.P., Rola J., Żmudziński J.F. (2008). Contamination of foetal bovine serum with bovine viral diarrhoea virus (BVDV). Bull. Vet. Inst. Pulawy, 52: 501–505.
Search in Google Scholar Back to article
Polak M.P., Kuta A., Rybałtowski W., Rola J., Larska M., Żmudziński J.F. (2014). First report of bovine viral diarrhoea virus-2 infection in cattle in Poland. Vet. J., 202: 643–645.
Search in Google Scholar Back to article
Rypuła K., Kumala A., Kaba J., Płoneczko-Janeczko K., Wojewoda-Kotwi-ca B., Mazurkiewicz M. (2010). Epidemiological aspects of BVDV infections in dairy cattle herds in Poland. Med. Weter., 66: 684–687.
Search in Google Scholar Back to article
Sasaki T., Harasawa R., Shintani M., Fujiwara H., Sasaki Y., Horino A., Kenri T., Asada K., Kato I., Chino F. (1996). Application of PCR for detection of mycoplasma DNA and pestivirus RNA in human live viral vaccines. Biologicals, 24: 371–375.
Search in Google Scholar Back to article
Schirrmeier H., Strebelow G., Depner K., Hoffmann B., Beer M. (2004). Genetic and antigenic characterization of an atypical pestivirus isolate, a putative member of a novel pestivirus species. J. Gen. Virol., 85: 1647–3652.
Search in Google Scholar Back to article
Smith D.B., Meyers G., Bukh J., Gould E.A., Monath T., Muerhoff A.S., Pletnev A., Rico-Hesse R., Stapleton J.T., Simmonds P., Becher P. (2017). Proposed revision to the taxonomy to the genus Pestivirus, family Flaviviridae. J. Gen. Virol., 98: 2106–2112.
Search in Google Scholar Back to article
Stahl K., Kampa J., Alenius S., Persson Wasman A., Baule C., Aiumlamai S., Belak S. (2007). Natural infection of cattle with an atypical ‘HoBi’-like pestivirus – implications for BVD control and for the safety of biological products. Vet. Res., 38: 517–523.
Search in Google Scholar Back to article
Stahl K., Beer M., Schirrmeier H., Hoffmann B., Belak S., Alenius S. (2010). Atypical ‘HoBi’-like pestiviruses – recent findings and implications thereof. Vet. Microbiol., 142: 90–93.
Search in Google Scholar Back to article
Studer E., Bertoni G., Candrian U. (2002). Detection and characterization of pestivirus contaminations in human live viral vaccines. Biologicals, 30: 289–296.
Search in Google Scholar Back to article
Toplak I., Sandvik T., Barlic-Maganja D., Grom J., Paton D.J. (2004). Genetic typing of bovine viral diarrhoea virus: most Slovenian isolates are of genotypes 1d and 1f. Vet. Microbiol., 99: 175–185.
Search in Google Scholar Back to article
Van Maanen C. (2001). Deventer validation report – Bovine Viral Diarrhea Virus (BVDV) antigen detecting ELISAs. Deventer, The Netherlands: Animal Health Service.
Search in Google Scholar Back to article
Vilcek S., Herring A.J., Herring J.A., Nettleton P.F., Lowings J.P., Paton D.J. (1994). Pestivirus isolated from pigs cattle and sheep can be allocated into at least three genogroups using polymerase chain reaction and restriction endonuclease analysis. Arch. Virol., 136: 309–323.
Search in Google Scholar Back to article
Vilcek S., Durkovic B., Kolesarova M., Paton D.J. (2005). Genetic diversity of BVDV: Consequences for classification and molecular epidemiology. Prev. Vet. Med., 72: 31–35.
Search in Google Scholar Back to article
Weber M.N., Silveira S., Machado G., Groff F.H.S., Mosena A.C.S., Budaszewski R.F., Dupont P.M., Corbellini L.G., Canal C.W. (2014). High frequency of bovine viral diarrhea virus type 2 in Southern Brazil. Virus Res., 191: 117–124.
Search in Google Scholar Back to article
Wernicki A., Urban-Chmiel R., Stęgierska D., Adaszek Ł., Kalinowski M., Puchalski A., Dec M. (2015). Detection of the bovine viral diarrhoea virus (BVDV) in young beef cattle in eastern and south-eastern regions of Poland. Pol. J. Vet., 18: 141–146.
Search in Google Scholar Back to article
Wernike K., Gethmann J., Schirrmeier H., Schröder R., Conraths F.J., Beer M. (2017). Six years (2011–2016) of mandatory nationwide bovine viral diarrhea control in Germany – a success story. Pathogens, 6: 50.
Search in Google Scholar Back to article
Wolf G. (2007). The perfect BVDV diagnosis? Proc. Symposium on Diagnosis of BVDV in Ear Notch Samples. Stendal, Germany.
Search in Google Scholar Back to article
Yolken R., Dubovi E., Leister F., Reid R., Almeido-Hill J., Santosham M. (1989). Infantile gastroenteritis associated with excretion of pestivirus antigens. Lancet, 1: 517–520.
Search in Google Scholar Back to article

Is contamination of bovine-sourced material with bovine viral diarrhea virus still a problem in countries with ongoing eradication campaigns?

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