Research article Open Access
Like 0


Salmonellosis, campylobacteriosis and listeriosis are food-borne diseases. We estimated and forecasted the number of cases of these three diseases in Belgium from 2012 to 2020, and calculated the corresponding number of disability-adjusted life years (DALYs). The salmonellosis time series was fitted with a Bai and Perron two-breakpoint model, while a dynamic linear model was used for campylobacteriosis and a Poisson autoregressive model for listeriosis. The average monthly number of cases of salmonellosis was 264 (standard deviation (SD): 86) in 2012 and predicted to be 212 (SD: 87) in 2020; campylobacteriosis case numbers were 633 (SD: 81) and 1,081 (SD: 311); listeriosis case numbers were 5 (SD: 2) in 2012 and 6 (SD: 3) in 2014. After applying correction factors, the estimated DALYs for salmonellosis were 102 (95% uncertainty interval (UI): 8–376) in 2012 and predicted to be 82 (95% UI: 6–310) in 2020; campylobacteriosis DALYs were 1,019 (95% UI: 137–3,181) and 1,736 (95% UI: 178–5,874); listeriosis DALYs were 208 (95% UI: 192–226) in 2012 and 252 (95% UI: 200–307) in 2014. New actions are needed to reduce the risk of food-borne infection with spp. because campylobacteriosis incidence may almost double through 2020.


Article metrics loading...

Loading full text...

Full text loading...



  1. Esan OB, Pearce M, van Hecke O, Roberts N, Collins DR, Violato M, et al. Factors Associated with Sequelae of Campylobacter and Non-typhoidal Salmonella Infections: A Systematic Review. EBioMedicine. 2017;15:100-11.  https://doi.org/10.1016/j.ebiom.2016.12.006  PMID: 27965105 
  2. Mastroeni P, Maskell D, editors. Salmonella infections: clinical, immunological and molecular aspects. Cambridge: Cambridge University Press; 2006.
  3. World Health Organization (WHO). WHO estimates of the global burden of foodborne diseases: Foodborne disease burden epidemiology reference group 2007-2015. Geneva: WHO; 2015. Available from: http://www.who.int/foodsafety/publications/foodborne_disease/fergreport/en/
  4. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. World Health Organization Foodborne Disease Burden Epidemiology Reference Group. World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Med. 2015;12(12):e1001923.  https://doi.org/10.1371/journal.pmed.1001923  PMID: 26633896 
  5. Domingues AR, Pires SM, Halasa T, Hald T. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Epidemiol Infect. 2012;140(6):970-81.  https://doi.org/10.1017/S0950268811002676  PMID: 22214729 
  6. Humphrey T, O’Brien S, Madsen M. Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol. 2007;117(3):237-57.  https://doi.org/10.1016/j.ijfoodmicro.2007.01.006  PMID: 17368847 
  7. Sejvar JJ, Baughman AL, Wise M, Morgan OW. Population incidence of Guillain-Barré syndrome: a systematic review and meta-analysis. Neuroepidemiology. 2011;36(2):123-33.  https://doi.org/10.1159/000324710  PMID: 21422765 
  8. Schlech WF 3rd, Lavigne PM, Bortolussi RA, Allen AC, Haldane EV, Wort AJ, et al. Epidemic listeriosis--evidence for transmission by food. N Engl J Med. 1983;308(4):203-6.  https://doi.org/10.1056/NEJM198301273080407  PMID: 6401354 
  9. Maertens De Noordhout C, Devleesschauwer B, Maertens De Noordhout A, Blocher J, Haagsma JA, Havelaar AH, et al. Comorbidities and factors associated with central nervous system infections and death in non-perinatal listeriosis: a clinical case series. BMC Infect Dis. 2016;16(1):256.  https://doi.org/10.1186/s12879-016-1602-3  PMID: 27267465 
  10. Lamont RF, Sobel J, Mazaki-Tovi S, Kusanovic JP, Vaisbuch E, Kim SK, et al. Listeriosis in human pregnancy: a systematic review. J Perinat Med. 2011;39(3):227-36.  https://doi.org/10.1515/jpm.2011.035  PMID: 21517700 
  11. de Noordhout CM, Devleesschauwer B, Angulo FJ, Verbeke G, Haagsma J, Kirk M, et al. The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(11):1073-82.  https://doi.org/10.1016/S1473-3099(14)70870-9  PMID: 25241232 
  12. Devleesschauwer B, Havelaar AH, Maertens de Noordhout C, Haagsma JA, Praet N, Dorny P, et al. Calculating disability-adjusted life years to quantify burden of disease. Int J Public Health. 2014;59(3):565-9.  https://doi.org/10.1007/s00038-014-0552-z  PMID: 24752429 
  13. Murray CJ, Acharya AK. Understanding DALYs (disability-adjusted life years). J Health Econ. 1997;16(6):703-30.  https://doi.org/10.1016/S0167-6296(97)00004-0  PMID: 10176780 
  14. Tromme I, Legrand C, Devleesschauwer B, Leiter U, Suciu S, Eggermont A, et al. Melanoma burden by melanoma stage: Assessment through a disease transition model. Eur J Cancer. 2016;53:33-41.  https://doi.org/10.1016/j.ejca.2015.09.016  PMID: 26693897 
  15. Henrard S, Devleesschauwer B, Beutels P, Callens M, De Smet F, Hermans C, et al. The health and economic burden of haemophilia in Belgium: a rare, expensive and challenging disease. Orphanet J Rare Dis. 2014;9(1):39.  https://doi.org/10.1186/1750-1172-9-39  PMID: 24655371 
  16. Dhondt S, Macharis C, Terryn N, Van Malderen F, Putman K. Health burden of road traffic accidents, an analysis of clinical data on disability and mortality exposure rates in Flanders and Brussels. Accid Anal Prev. 2013;50:659-66.  https://doi.org/10.1016/j.aap.2012.06.019  PMID: 22771286 
  17. Havelaar AH, Haagsma JA, Mangen MJ, Kemmeren JM, Verhoef LP, Vijgen SM, et al. Disease burden of foodborne pathogens in the Netherlands, 2009. Int J Food Microbiol. 2012;156(3):231-8.  https://doi.org/10.1016/j.ijfoodmicro.2012.03.029  PMID: 22541392 
  18. Gkogka E, Reij MW, Havelaar AH, Zwietering MH, Gorris LG. Risk-based estimate of effect of foodborne diseases on public health, Greece. Emerg Infect Dis. 2011;17(9):1581-90.  https://doi.org/10.3201/eid1709.101766  PMID: 21888782 
  19. Pires SM. Burden of Disease of Foodborne Pathogens in Denmark. Søborg: National Food Institute, Technical University of Denmark; 2014. Available from: http://www.dtu.dk/-/media/Institutter/Foedevareinstituttet/Publikationer/Pub-2014/Burden-of-Disease-of-Foodborne-Pathogens-in-Denmark.ashx?la=da
  20. Muyldermans G, Litzroth A, Ducoffre G, Quoilin SMedical-Technical Advisory Board. Establishment and reinforcement of the national reference centers for human microbiology in Belgium. Arch Public Health. 2012;70(1):16.  https://doi.org/10.1186/0778-7367-70-16  PMID: 22958353 
  21. Berger N, Muyldermans G, Dupont Y, Quoilin S. Assessing the sensitivity and representativeness of the Belgian Sentinel Network of Laboratories using test reimbursement data. Arch Public Health. 2016;74(1):29.  https://doi.org/10.1186/s13690-016-0145-9  PMID: 27504181 
  22. Hald T, Aspinall W, Devleesschauwer B, Cooke R, Corrigan T, Havelaar AH, et al. World Health Organization estimates of the relative contributions of food to the burden of disease due to selected foodborne hazards: a structured expert elicitation. PLoS One. 2016;11(1):e0145839.  https://doi.org/10.1371/journal.pone.0145839  PMID: 26784029 
  23. Center for Burden and Risk Assessment. Index of /fbd-burden-appendix. Brussels: Center for Burden and Risk Assessment; 16 Mar 2017. Available from: http://projects.cbra.be/fbd-burden-appendix/
  24. Collard JM, Bertrand S, Dierick K, Godard C, Wildemauwe C, Vermeersch K, et al. Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect. 2008;136(6):771-81.  https://doi.org/10.1017/S095026880700920X  PMID: 17645812 
  25. Maddala GS, Kim I-M. Unit Roots, Cointegration, and Structural Change. Cambridge: Cambridge University Press; 1998.
  26. Bai J, Perron P. Estimating and testing linear models with multiple structural changes. Econometrica. 1998;66(1):47-78.  https://doi.org/10.2307/2998540 
  27. Bai J, Perron P. Critical values for multiple structural change tests. Econom J. 2003;6(1):72-8.  https://doi.org/10.1111/1368-423X.00102 
  28. Brandt PT, Williams JT. A Linear Poisson Autoregressive Model: The Poisson AR(p) Model. Polit Anal. 2001;9(2):164-84.  https://doi.org/10.1093/oxfordjournals.pan.a004869 
  29. Devleesschauwer B, Havelaar AH, Maertens de Noordhout C, Haagsma JA, Praet N, Dorny P, et al. DALY calculation in practice: a stepwise approach. Int J Public Health. 2014;59(3):571-4.  https://doi.org/10.1007/s00038-014-0553-y  PMID: 24748107 
  30. Murray CJ, Ezzati M, Flaxman AD, Lim S, Lozano R, Michaud C, et al. GBD 2010: design, definitions, and metrics. Lancet. 2012;380(9859):2063-6.  https://doi.org/10.1016/S0140-6736(12)61899-6  PMID: 23245602 
  31. United Nations Department of Economic and Social Affairs. World Population Prospects: The 2012 Revision. File MORT/16-1: Life expectancy at exact age, e(x), for both sexes combined, by major area, region and country, 1950-2100. Medium fertility, 2010-2100. POP/DB/WPP/Rev.2012/MORT/F16-1. New York: United Nations; June 2013. Available from: https://esa.un.org/unpd/wpp/Download/Standard/Population/
  32. United Nations Department of Economic and Social Affairs. File POP/7-1: Total population (both sexes combined) by five-year age group, major area, region and country, 1950-2100 (thousands). Medium fertility, 2010-2100. POP/DB/WPP/Rev.2012/POP/F07-1. New York: United Nations; June 2013. Available from: http://esa.un.org/unpd/wpp/Download/Standard/Population/
  33. Havelaar AH, Ivarsson S, Löfdahl M, Nauta MJ. Estimating the true incidence of campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol Infect. 2013;141(2):293-302.  https://doi.org/10.1017/S0950268812000568  PMID: 22717051 
  34. Devleesschauwer B, Haagsma JA, Angulo FJ, Bellinger DC, Cole D, Döpfer D, et al. Methodological Framework for World Health Organization Estimates of the Global Burden of Foodborne Disease. PLoS One. 2015;10(12):e0142498.  https://doi.org/10.1371/journal.pone.0142498  PMID: 26633883 
  35. European Centre for Disease Prevention and Control (ECDC). Toolkit - Application to calculate DALYs. BCoDE toolkit v1.2. Stockholm: ECDC; 2015. [Accessed 9 Oct 2015]. Available from: http://ecdc.europa.eu/en/healthtopics/burden_of_communicable_diseases/Pages/Tool.aspx
  36. Mangen M-J, Havelaar A, Bernsen R, Van Koningsveld R, De Wit G. The costs of human Campylobacter infections and sequelae in the Netherlands: A DALY and cost-of-illness approach. Anta Agriculturae Scandinavica, Section C – Food Economics. 2005;2(1):35-51.  https://doi.org/10.1080/16507540510033451 
  37. Hannu T, Mattila L, Rautelin H, Pelkonen P, Lahdenne P, Siitonen A, et al. Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology (Oxford). 2002;41(3):312-8.  https://doi.org/10.1093/rheumatology/41.3.312  PMID: 11934969 
  38. Havelaar AH, de Wit MA, van Koningsveld R, van Kempen E. Health burden in the Netherlands due to infection with thermophilic Campylobacter spp. Epidemiol Infect. 2000;125(3):505-22.  https://doi.org/10.1017/S0950268800004933  PMID: 11218201 
  39. Haagsma JA, Siersema PD, De Wit NJ, Havelaar AH. Disease burden of post-infectious irritable bowel syndrome in The Netherlands. Epidemiol Infect. 2010;138(11):1650-6.  https://doi.org/10.1017/S0950268810000531  PMID: 20223049 
  40. Tokars JI, Burkom H, Xing J, English R, Bloom S, Cox K, et al. Enhancing time-series detection algorithms for automated biosurveillance. Emerg Infect Dis. 2009;15(4):533-9.  https://doi.org/10.3201/1504.080616  PMID: 19331728 
  41. Burkom HS, Murphy SP, Shmueli G. Automated time series forecasting for biosurveillance. Stat Med. 2007;26(22):4202-18.  https://doi.org/10.1002/sim.2835  PMID: 17335120 
  42. Cardinal M, Roy R, Lambert J. On the application of integer-valued time series models for the analysis of disease incidence. Stat Med. 1999;18(15):2025-39.  https://doi.org/10.1002/(SICI)1097-0258(19990815)18:15<2025::AID-SIM163>3.0.CO;2-D  PMID: 10440884 
  43. Myers MF, Rogers DJ, Cox J, Flahault A, Hay SI. Forecasting disease risk for increased epidemic preparedness in public health. Adv Parasitol. 2000;47:309-30.  https://doi.org/10.1016/S0065-308X(00)47013-2  PMID: 10997211 
  44. Benschop J, Stevenson MA, Dahl J, Morris RS, French NP. Temporal and longitudinal analysis of Danish Swine Salmonellosis Control Programme data: implications for surveillance. Epidemiol Infect. 2008;136(11):1511-20.  https://doi.org/10.1017/S0950268807000234  PMID: 18198001 
  45. McDonald SA, van Lier A, Plass D, Kretzschmar ME. The impact of demographic change on the estimated future burden of infectious diseases: examples from hepatitis B and seasonal influenza in the Netherlands. BMC Public Health. 2012;12(1):1046.  https://doi.org/10.1186/1471-2458-12-1046  PMID: 23217094 
  46. Zhang Y, Bi P, Hiller JE. Projected burden of disease for Salmonella infection due to increased temperature in Australian temperate and subtropical regions. Environ Int. 2012;44:26-30.  https://doi.org/10.1016/j.envint.2012.01.007  PMID: 22321536 
  47. Valcour JE, Charron DF, Berke O, Wilson JB, Edge T, Waltner-Toews D. A descriptive analysis of the spatio-temporal distribution of enteric diseases in New Brunswick, Canada. BMC Public Health. 2016;16(1):204.  https://doi.org/10.1186/s12889-016-2779-5  PMID: 26932766 
  48. Plass D, Mangen MJ, Kraemer A, Pinheiro P, Gilsdorf A, Krause G, et al. The disease burden of hepatitis B, influenza, measles and salmonellosis in Germany: first results of the burden of communicable diseases in Europe study. Epidemiol Infect. 2014;142(10):2024-35.  https://doi.org/10.1017/S0950268813003312  PMID: 24480146 
  49. van Lier A, McDonald SA, Bouwknegt M, Kretzschmar ME, Havelaar AH, Mangen MJ, et al. EPI group. Disease Burden of 32 Infectious Diseases in the Netherlands, 2007-2011. PLoS One. 2016;11(4):e0153106.  https://doi.org/10.1371/journal.pone.0153106  PMID: 27097024 
  50. Weisent J, Seaver W, Odoi A, Rohrbach B. Comparison of three time-series models for predicting campylobacteriosis risk. Epidemiol Infect. 2010;138(6):898-906.  https://doi.org/10.1017/S0950268810000154  PMID: 20092672 
  51. Nobre FF, Monteiro AB, Telles PR, Williamson GD. Dynamic linear model and SARIMA: a comparison of their forecasting performance in epidemiology. Stat Med. 2001;20(20):3051-69.  https://doi.org/10.1002/sim.963  PMID: 11590632 
  52. Bertrand S, Mattheus W, Vanhoof R. Centre National de références des listeria: rapport d'activités 2014. [National Reference Center for Listeria: report of activities 2014]. Brussels: Maladies bactériennes; 2015. French. Available from: http://bacterio.wiv-isp.be/reporting/reportspdf/Centre%20Listeria%20rapport%20annuel%202014-versfinal.pdf
  53. Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis. 2013;10(7):639-48.  https://doi.org/10.1089/fpd.2012.1389  PMID: 23659355 
  54. Schmutz C, Mäusezahl D, Jost M, Baumgartner A, Mäusezahl-Feuz M. Inverse trends of Campylobacter and Salmonella in Swiss surveillance data, 1988-2013. Euro Surveill. 2016;21(6):30130.  https://doi.org/10.2807/1560-7917.ES.2016.21.6.30130  PMID: 26898102 
  55. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). The European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J. 2014;12(2):3547.  https://doi.org/10.2903/j.efsa.2014.3547 
  56. Weisent J, Seaver W, Odoi A, Rohrbach B. The importance of climatic factors and outliers in predicting regional monthly campylobacteriosis risk in Georgia, USA. Int J Biometeorol. 2014;58(9):1865-78.  https://doi.org/10.1007/s00484-014-0788-6  PMID: 24458769 
  57. Bavishi C, Dupont HL. Systematic review: the use of proton pump inhibitors and increased susceptibility to enteric infection. Aliment Pharmacol Ther. 2011;34(11-12):1269-81.  https://doi.org/10.1111/j.1365-2036.2011.04874.x  PMID: 21999643 
  58. Cobb CA, Curtis GD, Bansi DS, Slade E, Mehal W, Mitchell RG, et al. Increased prevalence of Listeria monocytogenes in the faeces of patients receiving long-term H2-antagonists. Eur J Gastroenterol Hepatol. 1996;8(11):1071-4.  https://doi.org/10.1097/00042737-199611000-00008  PMID: 8944368 

Data & Media loading...

Comment has been disabled for this content
Submit comment
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error