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Food Microbiology

Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk

Anniina Jaakkonen, Hanna Castro, Saija Hallanvuo, Jukka Ranta, Mirko Rossi, Joana Isidro, Miia Lindström, Marjaana Hakkinen
Christopher A. Elkins, Editor
Anniina Jaakkonen
aMicrobiology Research Unit, Finnish Food Safety Authority Evira, Helsinki, Finland
bDepartment of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
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  • ORCID record for Anniina Jaakkonen
Hanna Castro
bDepartment of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
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Saija Hallanvuo
aMicrobiology Research Unit, Finnish Food Safety Authority Evira, Helsinki, Finland
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Jukka Ranta
cRisk Assessment Research Unit, Finnish Food Safety Authority Evira, Helsinki, Finland
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Mirko Rossi
bDepartment of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
dBIOCONTAM Unit, European Food Safety Authority, Parma, Italy
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Joana Isidro
eNational Reference Laboratory for Gastrointestinal Infections, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal
fInnovation and Technology Unit, Department of Human Genetics, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal
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Miia Lindström
bDepartment of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
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Marjaana Hakkinen
aMicrobiology Research Unit, Finnish Food Safety Authority Evira, Helsinki, Finland
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Christopher A. Elkins
Centers for Disease Control and Prevention
Roles: Editor
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DOI: 10.1128/AEM.02910-18
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ABSTRACT

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.

FOOTNOTES

    • Received 4 December 2018.
    • Accepted 28 January 2019.
    • Accepted manuscript posted online 1 February 2019.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.02910-18.

  • Copyright © 2019 Jaakkonen et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk
Anniina Jaakkonen, Hanna Castro, Saija Hallanvuo, Jukka Ranta, Mirko Rossi, Joana Isidro, Miia Lindström, Marjaana Hakkinen
Applied and Environmental Microbiology Mar 2019, 85 (7) e02910-18; DOI: 10.1128/AEM.02910-18

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Longitudinal Study of Shiga Toxin-Producing Escherichia coli and Campylobacter jejuni on Finnish Dairy Farms and in Raw Milk
Anniina Jaakkonen, Hanna Castro, Saija Hallanvuo, Jukka Ranta, Mirko Rossi, Joana Isidro, Miia Lindström, Marjaana Hakkinen
Applied and Environmental Microbiology Mar 2019, 85 (7) e02910-18; DOI: 10.1128/AEM.02910-18
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KEYWORDS

Campylobacter jejuni
Escherichia coli
STEC
cattle
genomics
milk

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