The DOI matches its Crossref record; 53 of the 54 references it cites were found in a registry or an index.
Disease burden of foodborne pathogens in the Netherlands, 2009
Open accessAbstract
To inform risk management decisions on control, prevention and surveillance of foodborne disease, the disease burden of foodborne pathogens is estimated using Disability Adjusted Life Years as a summary metric of public health. Fourteen pathogens that can be transmitted by food are included in the study (four infectious bacteria, three toxin-producing bacteria, four viruses and three protozoa). Data represent the burden in the Netherlands in 2009. The incidence of community-acquired non-consulting cases, patients consulting their general practitioner, those admitted to hospital, as well as the incidence of sequelae and fatal cases is estimated using surveillance data, cohort studies and published data. Disease burden includes estimates of duration and disability weights for non-fatal cases and loss of statistical life expectancy for fatal cases. Results at pathogen level are combined with data from an expert survey to assess the fraction of cases attributable to food, and the main food groups contributing to transmission. Among 1.8 million cases of disease (approx. 10,600 per 100,000) and 233 deaths (1.4 per 100,000) by these fourteen pathogens, approximately one-third (680,000 cases; 4100 per 100,000) and 78 deaths (0.5 per 100,000) are attributable to foodborne transmission. The total burden is 13,500 DALY (82 DALY per 100,000). On a population level, Toxoplasma gondii, thermophilic Campylobacter spp., rotaviruses, noroviruses and Salmonella spp. cause the highest disease burden. The burden per case is highest for perinatal listeriosis and congenital toxoplasmosis. Approximately 45% of the total burden is attributed to food. T. gondii and Campylobacter spp. appear to be key targets for additional intervention efforts, with a focus on food and environmental pathways. The ranking of foodborne pathogens based on burden is very different compared to when only incidence is considered. The burden of acute disease is a relatively small part of the total burden. In the Netherlands, the burden of foodborne pathogens is similar to the burden of upper respiratory and urinary tract infections.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Foodborne illness acquired in the United States—Major pathogens
Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M.-A., Roy, S. L., Jones, J. L., & Griffin, P. M. (2011) · Emerging Infectious Diseases · doi:10.3201/eid1701.p11101 · Cited by 7,657
(1996) · Cited by 6,884
Encyclopedia of food sciences and nutrition
Caballero, B. H., Trugo, L. C., & Finglas, P. M. (2003) · Academic eBooks · Cited by 1,639
Quantifying the burden of disease: the technical basis for disability-adjusted life years.
Murray, C. J. (1994) · PubMed · Cited by 1,556
Foodborne Illness Acquired in the United States—Unspecified Agents
Scallan, E., Griffin, P. M., Angulo, F. J., Tauxe, R. V., & Hoekstra, R. M. (2010) · Emerging infectious diseases · doi:10.3201/eid1701.p21101 · Cited by 1,048
Wheeler, J. G., Sethi, D., Cowden, J. M., Wall, P. G., Rodrigues, L. C., Tompkins, D. S., Hudson, M. J., & Roderick, P. J. (1999) · BMJ · doi:10.1136/bmj.318.7190.1046 · Cited by 794
Summary Measures of Population Health: Concepts, Ethics, Measurement and Applications
Murray, C. J. L., Salomon, J. A., Mathers, C. D., & López, A. D. (2002) · Cited by 655
Murray, C., & Acharya, A. K. (1997) · Journal of Health Economics · doi:10.1016/s0167-6296(97)00004-0 · Cited by 634
de Wit, M. A. S., Koopmans, M. P. G., Kortbeek, L. M., Wannet, W. J. B., Vinjé, J., van Leusden, F., Bartelds, A. I. M., & van Duynhoven, Y. T. H. P. (2001) · American Journal of Epidemiology · doi:10.1093/aje/154.7.666 · Cited by 583
Self-citationTam, C. C., Rodrigues, L. C., Viviani, L., Dodds, J. P., Evans, M. R., Hunter, P. R., Gray, J. J., Letley, L. H., Rait, G., Tompkins, D. S., et al. (2011) · Gut · doi:10.1136/gut.2011.238386 · Cited by 565
Research works printed but not linked: 4
- European Food Safety Authority; European Centre for Disease Prevention and Control, 2011, Trends and sources of zoonoses and zoonotic agents in the European Union in 2009, The EFSA Journal, 9, 2090
- Friesema, 2011, Intensieve surveillance van Shiga toxine producerende Escherichia coli in Nederland, 2009, Infectieziekten Bulletin, 22, 22
- Kortbeek, 2009, 104, 370
- Van de Laar, 2000, Vaccineren tegen hepatitis A: een verkenning van kosten, Infectieziekten Bulletin, 11, 262
Cited by
Sorted by citations
Items 301–379 of 379
Ma, J.-X., An, D.-Z., Cui, B., Liu, M., Zhu, H., Li, M., Ai, X.-J., Ali, W., & Cheng, Y. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-21447-9 · Cited by 3
A systematic review of the methodological considerations in Campylobacter burden of disease studies
Tumulty, M., Bari, C. D., Devleesschauwer, B., Pires, S. M., & Kabir, Z. (2025) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0012681 · Cited by 4
Kosola, M., Markkula, A., Rimhanen‐Finne, R., & Lundén, J. M. (2025) · Food Control · doi:10.1016/j.foodcont.2025.111404 · Cited by 2
van der Vossen-Wijmenga, W. P., Zwietering, M. H., & den Besten, H. M. W. (2026) · LWT · doi:10.1016/j.lwt.2026.119216 · Cited by 2
Audiat‐Perrin, F., Guillier, L., Augustin, J.-C., Bornert, G., Fédérighi, M., Gautier, M., Silva, N. J., Pouillot, R., Mérad, M., on behalf of the Anses Working Group on Prioritization of food risks, et al. (2024) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2023.0105 · Cited by 2
Hu, Y.-N., Wan, W.-D., Wu, J.-T., Lai, T.-N., Ali, W., He, S., Liu, S., Li, X., Tang, Z., Wang, C., et al. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.124611 · Cited by 2
Manipis, K., Cronin, P., Street, D. J., Church, J., Viney, R. C., & Goodall, S. (2025) · PharmacoEconomics · doi:10.1007/s40273-024-01458-9 · Cited by 3
In-vitro Antibacterial Evaluation of Some Fluoroquinolone Derivatives Against Food Borne Bacteria
Shariatifar, N., Rezaei, M., Sayadi, M., Moshafi, M. H., Saeedi, M., Mohammadhosseini, N., Moghimi, S., & Foroumadi, A. (2016) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 2
Genomics and Foodborne Viral Infections
Smits, S., & Koopmans, M. (2017) · Applied Genomics of Foodborne Pathogens · doi:10.1007/978-3-319-43751-4_9 · Cited by 2
Niazi, S., ایران, گ. م. ب. م. د. ب. د. ع. پ. ت. ت., Mazloomi, S., ایران, گ. م. ب. م. د. ب. د. ع. پ. ت. ت. ا. و. گ. م. ب. م. د. ب. د. ع. پ. ا. ک., Shirzad, M. R., ایران, م. H. پ. م. آ. پ. ج. ع. ب., Mokamelkande, A., ایران, گ. م. ب. م. د. ب. د. ع. پ. ت. ت., Ahmadi, F., & ایران, گ. م. ب. م. د. ب. د. ع. پ. ت. ت. (2013) · Journal of Environmental Health Engineering · doi:10.18869/acadpub.jehe.1.1.37 · Cited by 2
Wang, J., Zhou, C., & Wang, Y. (2023) · Risk Analysis · doi:10.1111/risa.14233 · Cited by 2
Estimation of the occurrence of foodborne salmonellosis in Hungary
Vajda, Á., Kasza, G., & Mohácsi-Farkas, C. (2019) · Acta Alimentaria · doi:10.1556/066.2019.48.1.11 · Cited by 2
Wild and domestic animals as hosts of Toxoplasma gondii in Finland
Jokelainen, P. (2013) · Työväentutkimus Vuosikirja · Cited by 2
Public Health Measures: Health Education, Information, and Risk Communication
Motarjemi, Y. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-378612-8.00334-6 · Cited by 2
Quantitative and ecological aspects of Listeria monocytogenes population heterogeneity
Metselaar, K. I. (2016) · doi:10.18174/376546 · Cited by 2
Food safety management strategies based on acceptable risk and risk acceptance
Gkogka, E. (2019) · doi:10.18174/496132 · Cited by 3
A systematic review of the methodological considerations in Campylobacter burden of disease studiesPreprint
Tumulty, M., Bari, C. D., Devleesschauwer, B., Pires, S. M., & Kabir, Z. (2024) · medRxiv · doi:10.1101/2024.11.08.24316954 · Cited by 2
He, W., Zhang, S., Qi, Y., Wang, Y., Bai, L., Xu, J., Liu, Z., Wu, J., & Wang, Y. (2026) · Food Research International · doi:10.1016/j.foodres.2026.118933 · Cited by 1
Ali, M., Liang, X., Raza, A., Xu, C., Sun, T., He, Q., Zhu, Z., Li, K., & Peng, L. (2026) · Food and Waterborne Parasitology · doi:10.1016/j.fawpar.2026.e00341 · Cited by 1
Zai, M. J. Y., & Cock, I. E. (2026) · Molecules · doi:10.3390/molecules31132265 · Cited by 1
Plaß, D., Pinheiro, P. G., & Mange, M.-J. (2012) · InTech eBooks · doi:10.5772/38269 · Cited by 1
Developments in food disease surveillance: using source attribution to inform risk management
Pires, S. M. (2015) · Elsevier eBooks · doi:10.1533/9781782421153.2.197 · Cited by 1
Systematischer Review zur Krankheitslast durch Campylobacter spp.
Lackner, J., Schlichting, D., Müller‐Graf, C., & Greiner, M. (2017) · Das Gesundheitswesen · doi:10.1055/s-0043-121885 · Cited by 1
Hovdey, R., Sargeant, J. M., Fisman, D. N., & Greer, A. L. (2022) · BMC Research Notes · doi:10.1186/s13104-022-06075-3 · Cited by 1
Campylobacter: Animal Reservoirs, Human Infections, and Options for Control
Wagenaar, J. A., Newell, D. G., Kalupahana, R. S., & Mughini‐Gras, L. (2023) · Springer eBooks · doi:10.1007/978-3-030-85877-3_6-1 · Cited by 1
A decision analysis of cancer patients and the consumption of ready‐to‐eat salad
Gomez, C. B., Mitchell, J., & Marks, B. P. (2024) · Risk Analysis · doi:10.1111/risa.17658 · Cited by 1
Bokken, G. C. A. M., Portengen, L., Cornelissen, J. B. W. J., Bergwerff, A. A., & Knapen, F. V. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.11.020 · Cited by 1
Das Internet der Dinge und neue digitale Geschäftsmodelle in der Lebensmittelindustrie
Brink, G., & Chaves, F. (2021) · Schwerpunkt Business Model Innovation · doi:10.1007/978-3-658-31980-9_20 · Cited by 1
Towards microbial safety of fresh vegetables in Rwanda
Ssemanda, J. N. (2018) · doi:10.18174/452828
Genomic variation of Salmonella Typhimurium and dynamics of epidemics
Castillo, S., & Fabiola, C. (2017) · The Sydney eScholarship Repository (The University of Sydney) · Cited by 1
Schlundt, J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803678-5.00161-2 · Cited by 1
Dynamique spatio-temporelle de la contamination environnementale par Toxoplasma gondii
Gotteland, C. (2013) · theses.fr (ABES) · doi:10.70675/41962744ze623z47bbzb445zdc2c38a1af3d · Cited by 1
Assessing the risk of irritable bowel syndrome one year post-acute gastroenteritis
Kowalcyk, B. B. (2011)
Economic evaluation studies of obstetric interventions in high risk pregnancies
Vijgen, S. M. C. (2013) · UvA-DARE (University of Amsterdam)
Self-citationDas Internet der Dinge und neue digitale Geschäftsmodelle in der Lebensmittelindustrie
Brink, G., & Chaves, F. (2016) · Springer eBooks · doi:10.1007/978-3-658-12388-8_20
The limits of testing for microbiological food safety
Joosten, H. M. L. J. (2014) · Socio-Environmental Systems Modeling
Impact of microbial variability on food safety and quality
Aryani, D. C. (2016) · doi:10.18174/371102
van Kaam, F. (2017) · Utrecht University Repository (Utrecht University)
Burden and Risk Assessment of Foodborne Parasites
Devleesschauwer, B., Dorny, P., Faes, C., Havelaar, A. H., Torgerson, P. R., & Speybroeck, N. (2018) · Springer eBooks · doi:10.1007/978-3-319-67664-7_15
Self-citationMonophasic Salmonella Typhimurium in Australian pigs
Weaver, T. J. (2017) · Minerva Access (University of Melbourne)
ACUTE GASTROENTERITIS IN CHILDREN. CURRENT EPIDEMIO-LOGICAL AND ETIOLOGICAL CONSIDERATIONS
Mihai, M., Manole, A., Rugină, A., Manole, M., Ștreangă, V., & Mîndru, D. E. (2018) · The Medical-Surgical Journal
Katzer, F., Burrells, A., & Opsteegh, M. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-415846-7.00021-4
Low, A., Kadir, A. J., & Iqbal, T. (2020) · Infectious Diseases in Clinical Practice · doi:10.1097/ipc.0000000000000932
Source attribution of human toxoplasmosis
Deng, H. (2020) · doi:10.33540/278
Thelberg, S. E., Etsch, A. F., Orsgaard, H. K., Pitznagel, H. S., & Centrum, E. M. (2013)
Food Borne Pathogens and Their Impact on Health
Bell, S. (2021)
Ma, J.-X., Cui, B., Liu, M.-L., Yuan, J., & Yan, C. (2021) · Research Square · doi:10.21203/rs.3.rs-1070258/v1
de Wit, N. J., Schierenberg, A., & Witteman, B. J. M. (2016) · Kernboek · doi:10.1007/978-90-368-1274-0_34
Muris, J. W. M., & Keszthelyi, D. (2021) · Bohn Stafleu van Loghum eBooks · doi:10.1007/978-90-368-2620-4_36
Membré, J. (2022) · doi:10.1002/9781119986980.app
Élelmiszer eredetű szalmonellózisok társadalmi költsége Magyarországon
Gortva-Vajda, Á. (2021) · doi:10.54598/000690
Health Education, Information, and Risk Communication
Flint, S., & Bremer, P. J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-822521-9.00163-5
Malik, K., Shoukani, H. I., Hassan, S., Bibi, S., & Bano, S. A. (2023) · Pakistan BioMedical Journal · doi:10.54393/pbmj.v6i08.911
Alobaidi, D. A. (2024) · University of Thi-Qar Journal of agricultural research · doi:10.54174/utjagr.v13i1.314
Kömeç, S., Gülmez, A., & Tuna, G. (2024) · Türk Mikrobiyoloji Cemiyeti Dergisi · doi:10.54453/tmcd.2024.65902
Nanotherapeutics for Bacterial Livestock Diseases
Kumar, R., Banerjee, S., Akshita, A., Maurya, K., Kumari, K., Prasad, M., & Ghosh, M. (2024) · Livestock diseases and management · doi:10.1007/978-981-16-1610-5_19
Schlundt, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-323-99967-0.00394-x
Middel, K., Strydhorst, H., McKenzie, H., Mainali, C., & Visscher, D. R. (2025) · PLoS ONE · doi:10.1371/journal.pone.0324617
Yan, X., Kooh, P., Fédérighi, M., Jury, V., Cappelier, J.-M., & Boué, G. (2025) · Food Research International · doi:10.1016/j.foodres.2025.117150
Filho, G., & Pereira, J. B. (2014) · Aleph UCLA Undergraduate Research Journal for the Humanities and Social Sciences
Hovdey, R., Sargeant, J. M., Fisman, D. N., & Greer, A. L. (2022) · Figshare · doi:10.6084/m9.figshare.19808985
Hovdey, R., Sargeant, J. M., Fisman, D. N., & Greer, A. L. (2022) · Figshare · doi:10.6084/m9.figshare.19808991
Additional file 1 of Dutch DALYs, current and future burden of disease in the Netherlands
Hilderink, H. B. M., Plasmans, M. H. D., Poos, M. J. J. C., Eysink, P. E. D., & Gijsen, R. (2020) · Figshare · doi:10.6084/m9.figshare.12992072
Hovdey, R., Sargeant, J. M., Fisman, D. N., & Greer, A. L. (2022) · Figshare · doi:10.6084/m9.figshare.19808994
Hovdey, R., Sargeant, J. M., Fisman, D. N., & Greer, A. L. (2022) · Figshare · doi:10.6084/m9.figshare.19808988
Epidemiological patterns of salmonellosis incidence among the population of Armenia in 2009–2024
Palozyan, G. H., Hovhannisyan, A. S., Grigoryan, N. A., Abovyan, R. A., Tsakanyan, A. V., Margaryan, A. V., Khachatryan, T. S., Melik-Andreasyan, G., & Atoyan, S. A. (2025) · Russian Journal of Infection and Immunity · doi:10.15789/2220-7619-epo-17963
Cancino‐Faure, B., Piñeiro-González, A., D’Afonseca, V., Moraga, F., Segovia, C., Moraga, J. C., Valenzuela, M. F., & Hernandez, D. (2026) · Acta Tropica · doi:10.1016/j.actatropica.2026.108049
Détection des virus entériques dans les matrices alimentaires
Hennechart-Collette, C. (2017) · doi:10.70675/342af4f4z04ccz4c76zaae2z4493f3d9de64
Evaluation du microbiote du lait maternel
Togo, A. H. (2019) · theses.fr (ABES) · doi:10.70675/303974f2za181z42e1z9480zdf8e9d35cea2
Mota, J. D. O. (2020) · theses.fr (ABES) · doi:10.70675/83d60308z5af5z4077zb799ze79efe7dfdc7
Toxoplasma gondii in pork production : a stable to table approach
Dámek, F. (2023) · theses.fr (ABES) · doi:10.70675/a083df93z3f88z493fzb10aze88e07562fef
Ali, W., Yan, Q., Chen, K., Yang, Z.-Q., Cheng, S.-B., Wang, R., Hu, Z., & Yan, C. (2026) · Risk Analysis · doi:10.1111/risa.70253
Chang, T., Shin, H., Hong, S., Chai, J.-Y., Min, K., & Jung, B.-K. (2026) · Food Microbiology · doi:10.1016/j.fm.2026.105246
Risk Ranking of Microbiological Hazards in Food (2015–2019)
Glennon, C., O’Connor, L. M., Burke, K., Russell, L., Smith, S., Bolton, D., de Waal, T., Garvey, P., Gutiérrez, M., McCarthy, N., et al. (2026) · Food Risk Assess Europe · doi:10.2903/fr.efsa.2026.fr-00110
Shrestha, K., & Shrestha, R. (2026) · Food Control · doi:10.1016/j.foodcont.2026.112513
Pîrvulescu, A.-M., Schaik, G. V., Mughini‐Gras, L., & Steeneveld, W. (2026) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2026.107018
Metadata
- Authors
- Havelaar, A. H., Haagsma, J. A., Mangen, M.-J. J., Kemmeren, J. M., Verhoef, L. P. B., Vijgen, S. M. C., Wilson, M., Friesema, I. H. M., Kortbeek, L. M., van Duynhoven, Y. T. H. P., & van Pelt, W.
- Affiliations
- Utrecht University (NL)
- Erasmus MC (NL)
- University Medical Center Utrecht (NL)
- National Institute for Public Health and the Environment (NL)
- Corresponding author
- Havelaar, Arie H.
- ORCID
- Venue
- International Journal of Food Microbiology
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 156
- Issue
- 3
- Pages
- 231-238
- ISSN
- 0168-1605 (ISSN-L)
- OpenAlex
- W2040888966
- Cited by
- 380
- References
- 54
- Citations by year
- 2026: 10 · 2025: 11 · 2024: 16 · 2023: 11 · 2022: 23 · 2021: 18 · 2020: 34 · 2019: 24 · 2018: 31 · 2017: 30 · 2016: 39 · 2015: 30 · 2014: 50 · 2013: 42 · 2012: 10
- FWCI
- 64.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- International Journal of Food Microbiology (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Rivm Repository (Netherlands National Institute for Public Health and the Environment) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Agricultural and Biological Sciences › Food Science › Food Safety and Hygiene
- Life Sciences › Agricultural and Biological Sciences › Food Science › Listeria monocytogenes in Food Safety
- Keywords
- foodborne pathogens, disease burden, disability-adjusted life years, foodborne transmission, Toxoplasma gondii, Campylobacter, Salmonella, norovirus, rotavirus, listeriosis, congenital toxoplasmosis, attributable fraction, foodborne illness prevention, Netherlands
- MeSH terms
- Adolescent, Adult, Aged, Bacterial Infections, Cause of Death, Child, Child, Preschool, Foodborne Diseases, Persons with Disabilities, Humans, Infant, Listeriosis, Male, Middle Aged, Netherlands, Population Surveillance, Public Health, Salmonella, Salmonella Infections, Cohort Studies, Incidence, Cost of Illness, Risk Assessment, Quality-Adjusted Life Years, Norovirus
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review