Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk
Autor(a) principal: | |
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Data de Publicação: | 2019 |
Outros Autores: | , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/10400.18/6631 |
Resumo: | Shiga toxin-producing Escherichia coli (STEC) and Campylobacter jejuni are notable health hazards associated with the consumption of raw milk. These bacteria may colonize the intestines of asymptomatic cattle and enter bulk tank milk via fecal contamination during milking. We studied the frequency of STEC O157:H7 and C. jejuni contamination in tank milk (n = 785) and the in-line milk filters of milking machines (n = 631) versus the frequency of isolation from cattle feces (n = 257) on three Finnish dairy farms for 1 year. Despite simultaneous isolation of STEC O157:H7 (17%) or C. jejuni (53%) from cattle, these bacteria were rarely isolated from milk filters (2% or <1%, respectively) and milk (0%). As revealed by phylogenomics, one STEC O157:H7 strain at a time was detected on each farm and persisted for ≤12 months despite rigorous hygienic measures. C. jejuni strains of a generalist sequence type (ST-883 and ST-1080) persisted in the herds for ≥11 months, and several other C. jejuni types were detected sporadically. The stx gene carried by STEC was detected more frequently from milk filters (37%) than from milk (7%), suggesting that milk filters are more suitable sampling targets for monitoring than milk. A questionnaire of on-farm practices suggested lower stx contamination of milk when major cleansing in the barn, culling, or pasturing of dairy cows was applied, while a higher average outdoor temperature was associated with higher stx contamination. Because pathogen contamination occurred despite good hygiene and because pathogen detection from milk and milk filters proved challenging, we recommend heat treatment for raw milk before consumption.IMPORTANCE The increased popularity of raw milk consumption has created demand for relaxing legislation, despite the risk of contamination by pathogenic bacteria, notably STEC and C. jejuni However, the epidemiology of these milk-borne pathogens on the herd level is still poorly understood, and data are lacking on the frequency of milk contamination on farms with cattle shedding these bacteria in their feces. This study suggests (i) that STEC contamination in milk can be reduced, but not prevented, by on-farm hygienic measures while fecal shedding is observable, (ii) that milk filters are more suitable sampling targets for monitoring than milk although pathogen detection from both sample matrices may be challenging, and (iii) that STEC and C. jejuni genotypes may persist in cattle herds for several months. The results can be utilized in developing and targeting pathogen monitoring and risk management on the farm level and contributed to the revision of Finnish legislation in 2017. |
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Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw MilkAnimalsCampylobacter jejuniCattleDairyingEscherichia coli O157FarmsFecesFemaleFinlandGenomicsGenotypeLongitudinal StudiesMilkMultilocus Sequence TypingPhylogenyRisk FactorsShiga ToxinShiga-Toxigenic Escherichia coliWhole Genome SequencingFood MicrobiologyInfecções GastrointestinaisShiga toxin-producing Escherichia coli (STEC) and Campylobacter jejuni are notable health hazards associated with the consumption of raw milk. These bacteria may colonize the intestines of asymptomatic cattle and enter bulk tank milk via fecal contamination during milking. We studied the frequency of STEC O157:H7 and C. jejuni contamination in tank milk (n = 785) and the in-line milk filters of milking machines (n = 631) versus the frequency of isolation from cattle feces (n = 257) on three Finnish dairy farms for 1 year. Despite simultaneous isolation of STEC O157:H7 (17%) or C. jejuni (53%) from cattle, these bacteria were rarely isolated from milk filters (2% or <1%, respectively) and milk (0%). As revealed by phylogenomics, one STEC O157:H7 strain at a time was detected on each farm and persisted for ≤12 months despite rigorous hygienic measures. C. jejuni strains of a generalist sequence type (ST-883 and ST-1080) persisted in the herds for ≥11 months, and several other C. jejuni types were detected sporadically. The stx gene carried by STEC was detected more frequently from milk filters (37%) than from milk (7%), suggesting that milk filters are more suitable sampling targets for monitoring than milk. A questionnaire of on-farm practices suggested lower stx contamination of milk when major cleansing in the barn, culling, or pasturing of dairy cows was applied, while a higher average outdoor temperature was associated with higher stx contamination. Because pathogen contamination occurred despite good hygiene and because pathogen detection from milk and milk filters proved challenging, we recommend heat treatment for raw milk before consumption.IMPORTANCE The increased popularity of raw milk consumption has created demand for relaxing legislation, despite the risk of contamination by pathogenic bacteria, notably STEC and C. jejuni However, the epidemiology of these milk-borne pathogens on the herd level is still poorly understood, and data are lacking on the frequency of milk contamination on farms with cattle shedding these bacteria in their feces. This study suggests (i) that STEC contamination in milk can be reduced, but not prevented, by on-farm hygienic measures while fecal shedding is observable, (ii) that milk filters are more suitable sampling targets for monitoring than milk although pathogen detection from both sample matrices may be challenging, and (iii) that STEC and C. jejuni genotypes may persist in cattle herds for several months. The results can be utilized in developing and targeting pathogen monitoring and risk management on the farm level and contributed to the revision of Finnish legislation in 2017.Our study was funded by the Finnish Ministry of Agriculture and Forestry (grant no. 1879/312/2012), Finnish Foundation of Veterinary Research, and the Walter Ehrström Foundation. The sequencing of the strains and the salary of J.I. were supported by the INNUENDO project (https://sites .google.com/site/theinnuendoproject/), which received funding from the European Food Safety Authority (EFSA) (grant no. GP/EFSA/AFSCO/2015/01/CT2).American Society for MicrobiologyRepositório Científico do Instituto Nacional de SaúdeJaakkonen, AnniinaCastro, HannaHallanvuo, SaijaRanta, JukkaRossi, MirkoIsidro, JoanaLindström, MiiaHakkinen, Marjaana2020-05-09T12:03:31Z2019-03-222019-03-22T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.18/6631engAppl Environ Microbiol. 2019 Mar 22;85(7):e02910-18. doi: 10.1128/AEM.02910-18. Print 2019 Apr 10099-224010.1128/AEM.02910-18info:eu-repo/semantics/embargoedAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-20T15:41:46Zoai:repositorio.insa.pt:10400.18/6631Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T18:41:43.134118Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
title |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
spellingShingle |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk Jaakkonen, Anniina Animals Campylobacter jejuni Cattle Dairying Escherichia coli O157 Farms Feces Female Finland Genomics Genotype Longitudinal Studies Milk Multilocus Sequence Typing Phylogeny Risk Factors Shiga Toxin Shiga-Toxigenic Escherichia coli Whole Genome Sequencing Food Microbiology Infecções Gastrointestinais |
title_short |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
title_full |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
title_fullStr |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
title_full_unstemmed |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
title_sort |
Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk |
author |
Jaakkonen, Anniina |
author_facet |
Jaakkonen, Anniina Castro, Hanna Hallanvuo, Saija Ranta, Jukka Rossi, Mirko Isidro, Joana Lindström, Miia Hakkinen, Marjaana |
author_role |
author |
author2 |
Castro, Hanna Hallanvuo, Saija Ranta, Jukka Rossi, Mirko Isidro, Joana Lindström, Miia Hakkinen, Marjaana |
author2_role |
author author author author author author author |
dc.contributor.none.fl_str_mv |
Repositório Científico do Instituto Nacional de Saúde |
dc.contributor.author.fl_str_mv |
Jaakkonen, Anniina Castro, Hanna Hallanvuo, Saija Ranta, Jukka Rossi, Mirko Isidro, Joana Lindström, Miia Hakkinen, Marjaana |
dc.subject.por.fl_str_mv |
Animals Campylobacter jejuni Cattle Dairying Escherichia coli O157 Farms Feces Female Finland Genomics Genotype Longitudinal Studies Milk Multilocus Sequence Typing Phylogeny Risk Factors Shiga Toxin Shiga-Toxigenic Escherichia coli Whole Genome Sequencing Food Microbiology Infecções Gastrointestinais |
topic |
Animals Campylobacter jejuni Cattle Dairying Escherichia coli O157 Farms Feces Female Finland Genomics Genotype Longitudinal Studies Milk Multilocus Sequence Typing Phylogeny Risk Factors Shiga Toxin Shiga-Toxigenic Escherichia coli Whole Genome Sequencing Food Microbiology Infecções Gastrointestinais |
description |
Shiga toxin-producing Escherichia coli (STEC) and Campylobacter jejuni are notable health hazards associated with the consumption of raw milk. These bacteria may colonize the intestines of asymptomatic cattle and enter bulk tank milk via fecal contamination during milking. We studied the frequency of STEC O157:H7 and C. jejuni contamination in tank milk (n = 785) and the in-line milk filters of milking machines (n = 631) versus the frequency of isolation from cattle feces (n = 257) on three Finnish dairy farms for 1 year. Despite simultaneous isolation of STEC O157:H7 (17%) or C. jejuni (53%) from cattle, these bacteria were rarely isolated from milk filters (2% or <1%, respectively) and milk (0%). As revealed by phylogenomics, one STEC O157:H7 strain at a time was detected on each farm and persisted for ≤12 months despite rigorous hygienic measures. C. jejuni strains of a generalist sequence type (ST-883 and ST-1080) persisted in the herds for ≥11 months, and several other C. jejuni types were detected sporadically. The stx gene carried by STEC was detected more frequently from milk filters (37%) than from milk (7%), suggesting that milk filters are more suitable sampling targets for monitoring than milk. A questionnaire of on-farm practices suggested lower stx contamination of milk when major cleansing in the barn, culling, or pasturing of dairy cows was applied, while a higher average outdoor temperature was associated with higher stx contamination. Because pathogen contamination occurred despite good hygiene and because pathogen detection from milk and milk filters proved challenging, we recommend heat treatment for raw milk before consumption.IMPORTANCE The increased popularity of raw milk consumption has created demand for relaxing legislation, despite the risk of contamination by pathogenic bacteria, notably STEC and C. jejuni However, the epidemiology of these milk-borne pathogens on the herd level is still poorly understood, and data are lacking on the frequency of milk contamination on farms with cattle shedding these bacteria in their feces. This study suggests (i) that STEC contamination in milk can be reduced, but not prevented, by on-farm hygienic measures while fecal shedding is observable, (ii) that milk filters are more suitable sampling targets for monitoring than milk although pathogen detection from both sample matrices may be challenging, and (iii) that STEC and C. jejuni genotypes may persist in cattle herds for several months. The results can be utilized in developing and targeting pathogen monitoring and risk management on the farm level and contributed to the revision of Finnish legislation in 2017. |
publishDate |
2019 |
dc.date.none.fl_str_mv |
2019-03-22 2019-03-22T00:00:00Z 2020-05-09T12:03:31Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/10400.18/6631 |
url |
http://hdl.handle.net/10400.18/6631 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Appl Environ Microbiol. 2019 Mar 22;85(7):e02910-18. doi: 10.1128/AEM.02910-18. Print 2019 Apr 1 0099-2240 10.1128/AEM.02910-18 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/embargoedAccess |
eu_rights_str_mv |
embargoedAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
American Society for Microbiology |
publisher.none.fl_str_mv |
American Society for Microbiology |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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1799132161731723264 |