Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 11, Number 7—July 2005
Perspective

Attributing Illness to Food

Michael B. Batz*Comments to Author , Michael S. Doyle†, J. Glenn Morris‡, John Painter§, Ruby Singh¶, Robert V. Tauxe§, Michael R. Taylor*, Danilo M.A. Lo Fo Wong#, and for the Food Attribution Working Group
Author affiliations: *Resources for the Future, Washington, DC, USA; †University of Georgia, Griffin, Georgia, USA; ‡University of Maryland School of Medicine, Baltimore, Maryland, USA; §Centers for Disease Control and Prevention, Atlanta, Georgia, USA; ¶Food and Drug Administration, Laurel, Maryland, USA; #Danish Institute for Food and Veterinary Research, Copenhagen, Denmark

Main Article

Table

Current approaches to food attribution

Approach Primary advantages Primary limitations Refs
Denmark Salmonella Accounts Microbial subtyping provides direct link between public health endpoint and animal Difficult to expand to other pathogens; requires distinctive subtypes across reservoirs 5,6
High reporting of illnesses (social health care) Focus on animals ignores nonanimal sources
National, temporal coverage for both illnesses and animal/product monitoring Focus on reservoirs, not food products at point of consumption
UK outbreak data Large dataset: national, temporal coverage May not correlate with sporadic case data 8
Results correlate with local epidemiologic findings Not all pathogens well represented
Dependence on general practitioners
US outbreak data National and temporal coverage May not correlate with sporadic case data 11,12
Large common dataset Geographic and temporal inconsistencies (local reporting) and biases towards certain foods
Straightforward, uses existing data Not all pathogens well represented
Outbreaks and outbreak cases can be aggregated into food categories
Case-control studies Population-based studies Survey format has recall bias and other limits 17,20–24
Captures risk factors not included in most surveillance data (travel, food preparation questions) Long exposure windows (problems with common exposures)
Can implicate risks missed by laboratory testing Durable immunity in population can impede associating exposures with illnesses
No laboratory verification
Microbial subtyping Subtyping of illnesses and foods can provide direct link between public health endpoint and source of infection For animal sourcing, subtypes must be distinctive across species (see Danish Salmonella Accounts) 25–28,5,6
Can be used to identify specific foods (outbreak investigations) or animal reservoirs (source tracking by species) Utility may be limited to certain pathogens
Many different techniques, growing fast Resource intensive; requires human surveillance, extensive monitoring of food and animals, plus laboratory testing, data storage, analysis
Risk assessments Can estimate cases not captured by surveillance methods (not limited by underreporting or biases in epidemiologic methods) Predictive; cannot be verified 29–33
Uses consumption and contamination data ignored by surveillance-based approaches Large uncertainties in dose-response models and exposure estimates
Resource- and time-intensive (each pathogen-food combination requires its own exhaustive study)
Food monitoring data Captures upstream contamination (avoids environmental and cross-contamination after purchase) Not usable for food attribution unless made compatible (through subtyping or other means) with public health data 34–36
Expert elicitation/judgment Useful when data are sparse or conflicting Respondents can be similarly biased 15,37–39
Formal methods increase utility Requires some level of consensus for reasonable error bounds
Based on perception, not data

Main Article

References
  1. Mead  PS, Slutsker  L, Dietz  V, McCaig  LF, Bresee  JS, Shapiro  C, Food-related illness and death in the United States. Emerg Infect Dis. 1999;5:607–25. DOIPubMedGoogle Scholar
  2. Institute of Medicine. Scientific criteria to ensure safe food. Washington: National Academy Press; 2003.
  3. US General Accounting Office. Food safety and security—fundamental changes needed to ensure safe food. GAO-02-47T. Washington: The Office; 2001.
  4. Ministry of Food, Agriculture, and Fisheries. Annual report on zoonoses in Denmark, 2002. Copenhagen: The Ministry; 2003.
  5. Wegener  HC, Hald  T, Wong  DLF, Madsen  M, Korsgaard  H, Bager  F, Salmonella control programs in Denmark. Emerg Infect Dis. 2003;9:774–80.PubMedGoogle Scholar
  6. Hald  T, Vose  D, Wegener  HC, Koupeev  T. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 2004;24:251–65. DOIPubMedGoogle Scholar
  7. Mølbak  K, Neimann  J. Risk factors for sporadic infection with Salmonella Enteritidis, Denmark, 1997–1999. Am J Epidemiol. 2002;156:654–61. DOIPubMedGoogle Scholar
  8. Department for Environment. Food and Rural Affairs. Zoonoses report—United Kingdom, 2001. London: The Department; 2003.
  9. Little  CL, Gillespie  IA, Mitchell  RT. Microbiological examination of ready-to-eat burgers sampled anonymously at the point of sale in the United Kingdom. Commun Dis Public Health. 2001;4:293–9.PubMedGoogle Scholar
  10. Gillespie  IA, Little  CL, Mitchell  RT. Microbiological examination of cold ready-to-eat sliced meats from catering establishments in the United Kingdom. J Appl Microbiol. 2000;88:467–74. DOIPubMedGoogle Scholar
  11. Olsen  SJ, MacKinnon  LC, Goulding  JS, Bean  NH, Slutsker  L. Surveillance for foodborne disease outbreaks—United States, 1993–1997. MMWR Morb Mortal Wkly Rep. 2000;49(SS01):1–51.PubMedGoogle Scholar
  12. Bean  NH, Goulding  JS, Lao  C, Angulo  FJ. Surveillance for foodborne-disease outbreaks—United States, 1988–1992. MMWR Morb Mortal Wkly Rep. 1996;45(SS-5):1–66.PubMedGoogle Scholar
  13. DeWaal  CS, Barlow  K. Outbreak alert! Closing the gaps in our federal food-safety net. Washington: Center for Science in the Public Interest; 2002.
  14. Batz  MB, Hoffmann  SA, Krupnick  AJ, Morris  JG, Sherman  DM, Taylor  MR, Identifying the most significant microbiological foodborne risks to public health: a new risk-ranking model. Discussion paper. Washington. Resources for the Future. 2005. In press.
  15. Food Safety Research Consortium. Food attribution data and methodologies in the foodborne illness risk ranking model. Washington; The Consortium; 2003.
  16. Food Safety Research Consortium. Ranking the public health impact of foodborne hazards: a conference on the FSRC risk ranking model. Washington: The Consortium; 2004. Available from http://www.rff.org/fsrc/riskrankingconference.htm
  17. Friedman  CR, Hoekstra  RM, Samuel  M, Marcus  R, Bender  J, Shiferaw  B, Emerging Infections Program FoodNet Working Group. Risk factors for sporadic Campylobacter infection in the United States: A case-control study in FoodNet sites. Clin Infect Dis. 2004;38(Suppl 3):S285–96. DOIPubMedGoogle Scholar
  18. Angulo  F, Voetsch  A, Vugia  D, Hadler  J, Farley  M, Hedberg  C, FoodNet Working Group. Determining the burden of human illness from foodborne diseases: CDC's Emerging Infectious Disease Program Foodborne Disease Active Surveillance Network (FoodNet). Vet Clin North Am Food Anim Pract. 1998;14:165–72.PubMedGoogle Scholar
  19. Centers for Disease Control and Prevention. Preliminary FoodNet data on the incidence of foodborne illnesses—selected sites, United States, 2002. MMWR Morb Mortal Wkly Rep. 2003;52:340–3.PubMedGoogle Scholar
  20. Hardnett  FP, Hoekstra  RM, Kennedy  M, Charles  L, Angulo  FJ. Epidemiologic issues in study design and data analysis related to FoodNet activities. Clin Infect Dis. 2004;38:S121–6. DOIPubMedGoogle Scholar
  21. Moore  MR, Varma  JK, Medus  C, Crume  T, Marcus  R, Zansky  SM, Risk factors for sporadic infection caused by Salmonella Enteritidis in the United States, 2002–2003. International Conference on Emerging Infectious Diseases. Feb 29–Mar 3 2004, Atlanta. [accessed 17 May 2005]. Available from http://www.cdc.gov/foodnet/publications/2004/moore_2004.pdf
  22. Kimura  A, Reddy  V, Marcus  R, Cieslak  P, Mohle-Boetani  J, Kassenborg  HD, Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case-control study in FoodNet sites. Clin Infect Dis. 2004;38:S244–52. DOIPubMedGoogle Scholar
  23. Kassenborg  H, Hedberg  C, Hoekstra  M, Evans  M, Chin  AE, Marcus  R, Farm visits and undercooked hamburgers as major risk factors for sporadic Escherichia coli O157:H7 infections: data from a case-control study in 5 FoodNet sites. Clin Infect Dis. 2004;38:S271–8. DOIPubMedGoogle Scholar
  24. Varma  JK, Samuel  MC, Marcus  R, Hoekstra  M, Medus  C, Segler  SD, Dietary and medical risk factors for sporadic Listeria monocytogenes infection: a FoodNet case-control study: United States, 2000–2003. International Conference on Emerging Infectious Diseases. Feb 29–Mar 3, 2004, Atlanta. [accessed 17 May 2005]. Available from http://www.cdc.gov/foodnet/publications/2004/varma_2004.pdf
  25. Swaminathan  B, Barrett  TJ, Hunter  SB, Tauxe  RV. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis. 2001;7:382–9.PubMedGoogle Scholar
  26. Bernstein  BB, Griffith  JF, Weisberg  SB. Microbial Source Tracking Workshop: U.S. EPA Workshop on Microbial Source Tracking. 2002 Feb 5. Irvine, CA. [cited 17 May 2005]. Available from http://www.sccwrp.org/tools/workshops/source_tracking_workshop.html
  27. Simpson  JM, Santo Domingo  JW, Reasoner  DJ. Microbial source tracking: state of the science. Environ Sci Technol. 2002;36:5279–88. DOIPubMedGoogle Scholar
  28. Singh  R, Foley  SL, White  DG, Zhao  S, Simjee  S, McDermott  PF, 2003. Microbial source tracking (MST) of foodborne Salmonella & Campylobacter. Board F-15, FDA science forum and poster session. 2003. Apr 24–25. Washington. [cited 2005 May 17]. Available from http://www.cfsan.fda.gov/~frf/forum03/F-15.htm
  29. Center for Food Safety and Applied Nutrition, Food Safety and Inspection Service, Centers for Disease Control and Prevention. Quantitative assessment of relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready-to-eat foods. Washington: US Department of Health and Human Services and US Department of Agriculture; 2003.
  30. Gallagher  DL, Ebel  ED, Kause  JR. FSIS risk assessment for Listeria monocytogenes in deli meats, draft. Washington: US Department of Agriculture, Food Safety and Inspection Service; 2003.
  31. Food Safety and Inspection Service. Draft risk assessment of the public health impact of Escherichia coli O157:H7 in ground beef. US Department of Agriculture; 2001.
  32. Food Safety and Inspection Service. Salmonella Enteritidis risk assessment: shell eggs and egg products: final report. Washington: US Department of Agriculture; 1998.
  33. Center for Food Safety and Applied Nutrition. Draft risk assessment on the public health impact of Vibrio parahaemolyticus in raw molluscan shellfish. Washington: Food and Drug Administration; 2000.
  34. Food Safety and Inspection Service. Progress report on Salmonella testing of raw meat and poultry products, 1998–2002. Washington: US Department of Agriculture; 2003.
  35. Food Safety and Inspection Service. Microbiological results of raw ground beef products analyzed for Escherichia coli O157:H7. Washington: US Department of Agriculture; 2004. Available from http://www.fsis.usda.gov/OPHS/ecoltest/
  36. Wallace  FM, Call  JE, Porto  AC, Cocoma  GJ, Luchansky  JB; ERRC Special Projects Team. Recovery rate of Listeria monocytogenes from commercially prepared frankfurters during extended refrigerated storage. J Food Prot. 2003;66:584–91.PubMedGoogle Scholar
  37. National Research Council. Estimating the public health benefits of proposed air pollution regulations. Washington: National Academies of Science; 2002.
  38. Office of Management and Budget. Circular A-4. Washington. 2003 Sep 17.
  39. U.S. Environmental Protection Agency. An examination of EPA risk assessment principles and practices. Washington; The Agency; 2004.

Main Article

1In addition to the authors, the presenters and attendees who constitute the Food Attribution Working Group are: Fred Angulo (CDC), Robert Buchanan (FDA), H. Gregg Claycamp (FDA), Caroline Smith DeWaal, Center for Science in the Public Interest (CSPI), Jorge Santo Domingo (EPA), Katherine Field (Oregon State University), David Goldman (USDA), Matthew Moore (CDC), Sarah O'Brien (Communicable Disease Surveillance Centre, England), Efrain Ribot (CDC), Stephen Sundlof (FDA), and Catherine Woteki (Iowa State University).

Page created: April 23, 2012
Page updated: April 23, 2012
Page reviewed: April 23, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external