Cited by 133Salmonella and Campylobacter epidemiologyColorectal Cancer Screening and DetectionBacterial Cancer Therapy

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Increased colon cancer risk after severe Salmonella infection

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Mughini-Gras, Lapo, Schaapveld, Michael, Kramers, Jolanda, Mooij, Sofie, Neefjes-Borst, E. Andra, Pelt, Wilfrid van, Neefjes, Jacques·2018·PLoS ONE

DOI 10.1371/journal.pone.0189721PMC PMC5771566

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Abstract

BACKGROUND: Colon cancer constitutes one of the most frequent malignancies. Previous studies showed that Salmonella manipulates host cell signaling pathways and that Salmonella Typhimurium infection facilitates colon cancer development in genetically predisposed mice. This epidemiological study examined whether severe Salmonella infection, usually acquired from contaminated food, is associated with increased colon cancer risk in humans. METHODS AND FINDINGS: We performed a nationwide registry-based study to assess colon cancer risk after diagnosed Salmonella infection. National infectious disease surveillance records (1999-2015) for Dutch residents aged ≥20 years when diagnosed with salmonellosis (n = 14,264) were linked to the Netherlands Cancer Registry. Salmonella-infected patients were laboratory-confirmed under medical consultation after 1-2 weeks of illness. These datasets also contained information on Salmonella serovar and type of infection. Colon cancer risk (overall and per colon subsite) among patients with a diagnosed Salmonella infection was compared with expected colon cancer risk in the general population. Data from the nationwide registry of histo- and cytopathology (PALGA) and Statistics Netherlands (CBS) allowed assessing potential effects of age, gender, latency, socioeconomic status, genetic predisposition, inflammatory bowel disease (IBD), and tumor features. We found that compared to the general population, colon cancer risk was significantly increased (standardized incidence ratio [SIR] 1.54; 95%CI 1.09-2.10) among patients with Salmonella infection diagnosed <60 years of age. Such increased risk concerned specifically the ascending/transverse colon (SIR 2.12; 95%CI 1.38-3.09) after S. Enteritidis infection (SIR 2.97; 95%CI 1.73-4.76). Salmonellosis occurred more frequently among colon cancer patients with pre-infectious IBD, a known risk factor for colon cancer. Colon tumors of patients with a history of Salmonella infection were mostly of low grade. CONCLUSIONS: Patients diagnosed with severe salmonellosis have an increased risk of developing cancer in the ascending/transverse parts of the colon. This risk concerns particularly S. Enteritidis infection, suggesting a contribution of this major foodborne pathogen to colon cancer development.

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Fig 1 Schematic representation of the data management process. Number of patients in the two linked databases, as well as the number of patients excluded from further analyses according to each inclusion criterion.CC BY · PubMed Central

Fig 2 Cumulative incidence of colon cancer in patients with Salmonella infection and in the general population. Cumulative incidence of colon cancer over attained age in patients with a reported history of Salmonella infection and in the general population. Inset: cumulative incidence of colon cancer in patients with any Salmonella serovar infection and in the general population. Main graph: cumulative incidence of colon cancer in patients infected with the two major Salmonella serovars (Enteritidis and Typhimurium), the other less often diagnosed Salmonella serovars combined, and in the general population.CC BY · PubMed Central

Fig 3 Cumulative incidence of cancer in the ascending and transverse parts of the colon. Cumulative incidence of cancer in the ascending/transverse colon over attained age in patients with a reported history of Salmonella infection and in the general population. Inset: cumulative incidence of cancer in the ascending/transverse colon in patients with any Salmonella serovar infection and in the general population. Main graph: cumulative incidence of cancer in the ascending/transverse colon in patients infected with the two major Salmonella serovars (Enteritidis and Typhimurium), the other less often diagnosed Salmonella serovars combined, and in the general population.CC BY · PubMed Central

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Authors: Mughini-Gras, L., Schaapveld, M., Kramers, J., Mooij, S., Neefjes-Borst, E. A., Pelt, W. V., & Neefjes, J.
Affiliations: The Netherlands Cancer Institute (NL)
National Institute for Public Health and the Environment (NL)
Leiden University Medical Center (NL)
Corresponding author: Neefjes, Jacques
ORCID: Schaapveld, Michael
Neefjes, Jacques
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2018-01-17
Volume: 13
Issue: 1
Pages: e0189721
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0189721
PMC: PMC5771566
OpenAlex: W2783067021
Cited by: 133
References: 47
Citations by year: 2026: 7 · 2025: 12 · 2024: 15 · 2023: 29 · 2022: 14 · 2021: 21 · 2020: 17 · 2019: 13 · 2018: 5
FWCI: 13.13
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
Pure Amsterdam UMC (acceptedVersion, cc-by)
Leiden Repository (Leiden University) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Figshare (submittedVersion, cc-by)
Rivm Repository (Netherlands National Institute for Public Health and the Environment) (submittedVersion)
Rivm (National Institute for Public Health and the Environment) (submittedVersion)
Funders: KWF Kankerbestrijding (NKI 2013-5969)
European Research Council
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
Keywords: salmonellosis, colon cancer risk, Salmonella Enteritidis, ascending colon, transverse colon, inflammatory bowel disease, foodborne pathogens, tumor latency, tumor grade, host-pathogen interaction
MeSH terms: Adult, Aged, Animals, Colonic Neoplasms, Female, Humans, Male, Middle Aged, Registries, Retrospective Studies, Risk Factors, Salmonella Infections, Mice, Young Adult

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Increased colon cancer risk after severe Salmonella infection

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