Livestock-associated spatial risk factors for human salmonellosis and campylobacteriosis

Annemieke Christine Mulder; Lapo Mughini-Gras; Jan van de Kassteele; Sara Lynn Blanken; Roan Pijnacker; Eelco Franz

doi:10.1111/zph.13170

Livestock-associated spatial risk factors for human salmonellosis and campylobacteriosis

Annemieke Christine Mulder
, Lapo Mughini-Gras
, Jan van de Kassteele
, Sara Lynn Blanken
, Roan Pijnacker
, Eelco Franz^*

^*Corresponding author for this work

National Institute of Public Health and the Environment
Institute for Public Health and the Environment (RIVM)

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Aims: Most human infections with non-typhoid Salmonella (NTS) or Campylobacter are zoonotic in nature and acquired though consumption of contaminated food of mainly animal origin. However, individuals may also acquire salmonellosis or campylobacteriosis through non-foodborne transmission pathways, such as those mediated by the environment. This emphasizes the need to consider both direct and indirect exposure to livestock sources as a possible transmission route for NTS and Campylobacter. Therefore, this study aimed at assessing whether salmonellosis and campylobacteriosis incidence is spatially associated with exposure to livestock (i.e. small ruminants, dairy cows, veal calves, laying hens, broiler chickens and pigs) in the Netherlands for the years 2007–2019 and 2014–2019 respectively. Methods and Results: Risk factors (population-weighted number of animals) and their population attributable fractions were determined using a Poisson regression model with a log-link function fitted using integrated nested Laplace approximation. The analyses were performed for different hexagonal sizes (90, 50, 25 and 10 km²) and accounted for geographical coverage of the diagnostic laboratory catchment areas. Moreover, serological data were used to look into the possible effects of acquired immunity due to repeated exposure to the pathogen through the environment that would potentially hinder the analyses based on the incidence of reported cases. A linear mixed-effects model was then fitted where the postal code areas were included as a random effect. Livestock was not consistently significantly associated with acquiring salmonellosis or campylobacteriosis in the Netherlands. Conclusions: Results showed that living in livestock-rich areas in the Netherlands is not a consistently significant, spatially restricted risk factor for acquiring salmonellosis or campylobacteriosis, thereby supporting current knowledge that human infections with Salmonella and Campylobacter are mainly foodborne.

Original language	English
Pages (from-to)	876-899
Number of pages	24
Journal	Zoonoses and Public Health
Volume	71
Issue number	8
Early online date	24 Jul 2024
DOIs	https://doi.org/10.1111/zph.13170
Publication status	Published - Dec 2024

Bibliographical note

Publisher Copyright:
© 2024 The Author(s). Zoonoses and Public Health published by Wiley-VCH GmbH.

Funding

The authors would like to thank Ben Bom for his valuable input about the PIENTER II study and for providing data on the total number of farm animals per species reared in each farm in the Netherlands and Maarten Schipper for his help with the creation of the figures. We also want to thank ISIS-AR, the ISIS-AR study group and participating medical microbiological laboratories, as well as Wieke Altorf-van der Kuil for her role in data extraction. This study was supported by the Netherlands' Organization for Health Research and Development (ZonMw) with grant number 50-52200-98-316 (project name: 'DEPiCT - Discerning Environmental Pathways of Campylobacter Transmission').

Funders	Funder number
Netherlands' Organization for Health Research and Development
ZonMw	50‐52200‐98‐316
ZonMw

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

Campylobacter
environmental exposure
livestock
Salmonella
spatial risk factors

Access to Document

10.1111/zph.13170Licence: CC BY-NC-ND

Zoonoses and Public Health - 2024 - Mulder - Livestock‐associated spatial risk factors for human salmonellosis andFinal published version, 2.79 MBLicence: CC BY-NC-ND

Cite this

@article{6d4e1b1fbded4fceb211e1013cb7c739,

title = "Livestock-associated spatial risk factors for human salmonellosis and campylobacteriosis",

abstract = "Aims: Most human infections with non-typhoid Salmonella (NTS) or Campylobacter are zoonotic in nature and acquired though consumption of contaminated food of mainly animal origin. However, individuals may also acquire salmonellosis or campylobacteriosis through non-foodborne transmission pathways, such as those mediated by the environment. This emphasizes the need to consider both direct and indirect exposure to livestock sources as a possible transmission route for NTS and Campylobacter. Therefore, this study aimed at assessing whether salmonellosis and campylobacteriosis incidence is spatially associated with exposure to livestock (i.e. small ruminants, dairy cows, veal calves, laying hens, broiler chickens and pigs) in the Netherlands for the years 2007{\textendash}2019 and 2014{\textendash}2019 respectively. Methods and Results: Risk factors (population-weighted number of animals) and their population attributable fractions were determined using a Poisson regression model with a log-link function fitted using integrated nested Laplace approximation. The analyses were performed for different hexagonal sizes (90, 50, 25 and 10 km2) and accounted for geographical coverage of the diagnostic laboratory catchment areas. Moreover, serological data were used to look into the possible effects of acquired immunity due to repeated exposure to the pathogen through the environment that would potentially hinder the analyses based on the incidence of reported cases. A linear mixed-effects model was then fitted where the postal code areas were included as a random effect. Livestock was not consistently significantly associated with acquiring salmonellosis or campylobacteriosis in the Netherlands. Conclusions: Results showed that living in livestock-rich areas in the Netherlands is not a consistently significant, spatially restricted risk factor for acquiring salmonellosis or campylobacteriosis, thereby supporting current knowledge that human infections with Salmonella and Campylobacter are mainly foodborne.",

keywords = "Campylobacter, environmental exposure, livestock, Salmonella, spatial risk factors",

author = "Mulder, \{Annemieke Christine\} and Lapo Mughini-Gras and \{van de Kassteele\}, Jan and Blanken, \{Sara Lynn\} and Roan Pijnacker and Eelco Franz",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). Zoonoses and Public Health published by Wiley-VCH GmbH.",

year = "2024",

month = dec,

doi = "10.1111/zph.13170",

language = "English",

volume = "71",

pages = "876--899",

journal = "Zoonoses and Public Health",

issn = "1863-1959",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "8",

}

TY - JOUR

T1 - Livestock-associated spatial risk factors for human salmonellosis and campylobacteriosis

AU - Mulder, Annemieke Christine

AU - Mughini-Gras, Lapo

AU - van de Kassteele, Jan

AU - Blanken, Sara Lynn

AU - Pijnacker, Roan

AU - Franz, Eelco

PY - 2024/12

Y1 - 2024/12

N2 - Aims: Most human infections with non-typhoid Salmonella (NTS) or Campylobacter are zoonotic in nature and acquired though consumption of contaminated food of mainly animal origin. However, individuals may also acquire salmonellosis or campylobacteriosis through non-foodborne transmission pathways, such as those mediated by the environment. This emphasizes the need to consider both direct and indirect exposure to livestock sources as a possible transmission route for NTS and Campylobacter. Therefore, this study aimed at assessing whether salmonellosis and campylobacteriosis incidence is spatially associated with exposure to livestock (i.e. small ruminants, dairy cows, veal calves, laying hens, broiler chickens and pigs) in the Netherlands for the years 2007–2019 and 2014–2019 respectively. Methods and Results: Risk factors (population-weighted number of animals) and their population attributable fractions were determined using a Poisson regression model with a log-link function fitted using integrated nested Laplace approximation. The analyses were performed for different hexagonal sizes (90, 50, 25 and 10 km2) and accounted for geographical coverage of the diagnostic laboratory catchment areas. Moreover, serological data were used to look into the possible effects of acquired immunity due to repeated exposure to the pathogen through the environment that would potentially hinder the analyses based on the incidence of reported cases. A linear mixed-effects model was then fitted where the postal code areas were included as a random effect. Livestock was not consistently significantly associated with acquiring salmonellosis or campylobacteriosis in the Netherlands. Conclusions: Results showed that living in livestock-rich areas in the Netherlands is not a consistently significant, spatially restricted risk factor for acquiring salmonellosis or campylobacteriosis, thereby supporting current knowledge that human infections with Salmonella and Campylobacter are mainly foodborne.

AB - Aims: Most human infections with non-typhoid Salmonella (NTS) or Campylobacter are zoonotic in nature and acquired though consumption of contaminated food of mainly animal origin. However, individuals may also acquire salmonellosis or campylobacteriosis through non-foodborne transmission pathways, such as those mediated by the environment. This emphasizes the need to consider both direct and indirect exposure to livestock sources as a possible transmission route for NTS and Campylobacter. Therefore, this study aimed at assessing whether salmonellosis and campylobacteriosis incidence is spatially associated with exposure to livestock (i.e. small ruminants, dairy cows, veal calves, laying hens, broiler chickens and pigs) in the Netherlands for the years 2007–2019 and 2014–2019 respectively. Methods and Results: Risk factors (population-weighted number of animals) and their population attributable fractions were determined using a Poisson regression model with a log-link function fitted using integrated nested Laplace approximation. The analyses were performed for different hexagonal sizes (90, 50, 25 and 10 km2) and accounted for geographical coverage of the diagnostic laboratory catchment areas. Moreover, serological data were used to look into the possible effects of acquired immunity due to repeated exposure to the pathogen through the environment that would potentially hinder the analyses based on the incidence of reported cases. A linear mixed-effects model was then fitted where the postal code areas were included as a random effect. Livestock was not consistently significantly associated with acquiring salmonellosis or campylobacteriosis in the Netherlands. Conclusions: Results showed that living in livestock-rich areas in the Netherlands is not a consistently significant, spatially restricted risk factor for acquiring salmonellosis or campylobacteriosis, thereby supporting current knowledge that human infections with Salmonella and Campylobacter are mainly foodborne.

KW - Campylobacter

KW - environmental exposure

KW - livestock

KW - Salmonella

KW - spatial risk factors

UR - https://www.scopus.com/pages/publications/85199419462

U2 - 10.1111/zph.13170

DO - 10.1111/zph.13170

M3 - Article

AN - SCOPUS:85199419462

SN - 1863-1959

VL - 71

SP - 876

EP - 899

JO - Zoonoses and Public Health

JF - Zoonoses and Public Health

IS - 8

ER -

Livestock-associated spatial risk factors for human salmonellosis and campylobacteriosis

Abstract

Bibliographical note

Funding

UN SDGs

Keywords

Access to Document

Other files and links

Fingerprint

Cite this