Contribution of Foods and Poor Food-Handling Practices to the Burden of Foodborne Infectious Diseases in France
Abstract
:1. Introduction
2. Materials and Methods
2.1. Working Group
2.2. Estimating the Burden of Foodborne Diseases
2.3. Attribution of Foodborne Disease Burden to Foods and Practices
3. Results
3.1. Estimation of the Foodborne Disease Burden in France
3.2. Attribution of Disease Burden to Foods and Practices
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A. Source Attribution (Foods and Practices) for Foodborne Hazards in France
References
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Hazards | Incidence | Incidence Rate | References | Scores | |
---|---|---|---|---|---|
Bacteria, toxins and metabolites | Bacillus cereus | 69,000 | 110 | Van Cauteren et al. [1] | 5 |
Brucella spp. | 24 | 0.04 | Mailles et al. [22] | 1 | |
Campylobacter spp. | 390,000 | 600 | Van Cauteren et al. [1] | 5 | |
Clostridium botulinum | 21 | 0.03 | Van Cauteren et al. [1] | 1 | |
Clostridium perfringens | 120,000 | 180 | Van Cauteren et al. [1] | 5 | |
Histamine | 167 | 0.3 | Santé Publique France [23] | 2 | |
Listeria monocytogenes | 400 | 0.6 | Van Cauteren et al. [1] | 2 | |
Salmonella non-typhoidal | 180,000 | 280 | Van Cauteren et al. [1] | 5 | |
Shiga toxin-producing E. coli (STEC) | 18,000 | 28 | Van Cauteren et al. [1] | 4 | |
Shigella spp. | 3400 | 5.2 | Van Cauteren et al. [1] | 3 | |
Staphylococcus aureus | 73,000 | 110 | Van Cauteren et al. [1] | 5 | |
Vibrio parahaemolyticus | 5 | 0.008 | NRC Vibrio [24] | 0 | |
Yersinia enterocolitica | 21,000 | 32 | Van Cauteren et al. [1] | 4 | |
Viruses | Hepatitis A virus | 2600 | 4.0 | Van Cauteren et al. [1] | 3 |
Hepatitis E virus | 2300 | 3.5 | NRC HEV [25] | 3 | |
Norovirus | 520,000 | 800 | Van Cauteren et al. [1] | 5 | |
Parasites | Anisakis spp. | 8 | 0.01 | Van Cauteren et al. [15] | 1 |
Cryptosporidium spp. | 101 | 0.2 | NRC Cryptosporidium [26] | 2 | |
Cyclospora cayetanensis | 8 | 0.01 | Medical network Anofel [26] | 1 | |
Echinococcus multilocularis | 29 | 0.04 | Van Cauteren et al. [15] | 1 | |
Fasciola hepatica | 5 | 0.008 | Van Cauteren et al. [15] | 0 | |
Giardia spp. | 482 | 0.7 | Medical network Anofel [26] | 2 | |
Taenia saginata | 33,000 | 51 | Van Cauteren et al. [1] | 4 | |
Toxoplasma gondii, acquired | 11,500 | 18 | Van Cauteren et al. [1] | 4 | |
Toxoplasma gondii, congenital | 300 | 0.5 | Van Cauteren et al. [1] | 2 | |
Trichinella spp. | 11 | 0.02 | Van Cauteren [27] | 1 |
Hazards | Severity | Incidence | Foodborne Disease Burden (FBDB) | ||||
---|---|---|---|---|---|---|---|
The Netherlands, 2009 [17] | EUR A, 2010 [18,19] | This Study | |||||
DALYs | DALYs | Score | Score | Score | % of Total FBDB | ||
Bacteria, toxins and metabolites | Bacillus cereus | 2.3 | - | 1 | 5 | 6 | 3% |
Brucella spp. | - | 300 | 3 | 1 | 4 | 0.03% | |
Campylobacter spp. | 41 | 20 | 2 | 5 | 7 | 32% | |
Clostridium botulinum | - | - | 3 | 1 | 4 | 0.03% | |
Clostridium perfringens | 3.2 | - | 1 | 5 | 6 | 3% | |
Histamine | - | - | 1 | 2 | 3 | 0.003% | |
Listeria monocytogenes | 1450 | 8000 | 4 | 2 | 6 | 3% | |
Salmonella, non-typhoidal | 49 | 70 | 2 | 5 | 7 | 32% | |
Shiga toxin-producing E. coli | 143 1 | 20 | 2 | 4 | 6 | 3% | |
Shigella spp. | - | 70 | 2 | 3 | 5 | 0.3% | |
Staphylococcus aureus | 2.6 | - | 1 | 5 | 6 | 3% | |
Vibrio parahaemolyticus | - | - | 1 | 0 | 1 | 0.00003% | |
Yersinia enterocolitica | - | - | 2 | 4 | 6 | 3% | |
Virus | Hepatitis A virus | 167 | 100 | 3 | 3 | 6 | 3% |
Hepatitis E virus | 460 | - | 3 | 3 | 6 | 3% | |
Norovirus | 2.4 | 2 | 1 | 5 | 6 | 3% | |
Parasites | Anisakis spp. | - | - | 1 | 1 | 2 | 0.0003% |
Cryptosporidium spp. | 2.9 | 8 | 1 | 2 | 3 | 0.003% | |
Cyclospora cayentanensis | - | - | 1 | 1 | 2 | 0.0003% | |
Echinococcus multilocularis | - | 2000 | 4 | 1 | 5 | 0.3% | |
Fasciola hepatica | - | 9000 | 2 | 0 | 2 | 0.0003% | |
Giardia spp. | 2.1 | 1 | 1 | 2 | 3 | 0.003% | |
Taenia saginata | - | - | 1 | 4 | 5 | 0.3% | |
Toxoplasma gondii, acquired | 3170 | 60 | 2 | 4 | 6 | 3% | |
Toxoplasma gondii, congenital | 6360 | 6300 | 4 | 2 | 6 | 3% | |
Trichinella spp. | - | 100 | 2 | 1 | 3 | 0.003% |
Food Categories | Sub-Categories | Specific Foods | Hazards | Default in Handling Practices Contributing to the Onset of Foodborne Illnesses | No Contribution from Food Handlers at the Final Preparation | |||||
---|---|---|---|---|---|---|---|---|---|---|
Cross Contamination | Inadequate Washing and Disinfection of Produce | Inadequate Processing or Cooling | Inadequate Freezing | Inadequate Cooking (Including Reheating) | Inadequate Storage (Temperature and/or Shelf-Life) | |||||
Meats | Beef | Cooked ground beef | STEC | - | - | - | - | (0.2–1.8) | - | - |
Salmonella | - | - | - | - | (0.2–6.6) | (0.2–6.6) | - | |||
Raw ground beef | STEC | - | - | - | - | - | (0.2–1.8) | |||
Salmonella | - | - | - | - | - | (0.2–6.6) | (0.2–6.6) | |||
Beef meat | T. saginata | - | - | (0.0–0.3) | (0.0–0.3) | - | - | |||
Poultry | Poultry meat | Campylobacter spp. | (3–29) | - | - | - | (3–29) | - | - | |
Salmonella | (0.1–4.7) | - | - | - | (0.1–4.7) | (0.1–4.7) | - | |||
Pork | Pork meat | Salmonella | (0.1–4.7) | - | - | - | (0.1–4.7) | (0.1–4.7) | - | |
Y. enterocolitica | (0.2–2.5) | - | - | - | (0.2–2.5) | (0.2–2.5) | - | |||
Raw pig liver products, boar offal | Hepatitis E virus | - | - | - | - | 3.2 | - | - | ||
Open-air pig, boar, game | Trichinella spp. | - | - | - | (0.000–0.003) | (0.000–0.003) | - | - | ||
Cooked pork meats | L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | ||
S. aureus | - | - | - | - | - | (0.2–2.5) | - | |||
Home-made cooked and salt pork meat | C. botulinum | - | - | (0.00–0.02) | - | - | (0.00–0.02) | - | ||
Other meats | Lamb, open-air pigs, imported horses | T. gondii, congenital | - | - | - | (0.2–2.1) | (0.2–2.1) | - | - | |
T. gondii, acquired | - | - | - | (0.2–2.1) | (0.2–2.1) | - | - | |||
Dairy | Unpasteurised milk | Heated milk | Brucella spp. | - | - | - | - | (0.00–0.03) | - | - |
STEC | - | - | - | - | (0.2–1.8) | - | - | |||
Raw milk | Brucella spp. | - | - | - | - | - | - | (0.00–0.03) | ||
STEC | - | - | - | - | - | - | (0.2–1.8) | |||
Raw milk cheeses | Fresh non-ripened cheeses | Brucella spp. | - | - | - | - | - | - | (0.00–0.03) | |
Hard non-cooked cheeses | Salmonella | - | - | - | - | - | - | (1.6–12.5) | ||
Soft cheeses | STEC | - | - | - | - | - | - | (0.2–1.8) | ||
Salmonella | - | - | - | - | - | - | (1.6–12.5) | |||
S. aureus | - | - | - | - | - | - | (0.2–2.5) | |||
L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | |||
Pasteurized milk cheeses | Soft cheeses | L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | |
Eggs | - | Eggs | Salmonella | - | - | - | - | (1.6–12.5) | - | - |
Raw eggs products | Salmonella | - | - | - | - | - | (0.2–6.8) | (0.2–6.8) | ||
Seafood | Fish | Cooked fish | Anisakis spp. | - | - | (0–0.0002) | (0–0.0002) | (0–0.0002) | - | - |
Raw fish | Anisakis spp. | - | - | (0–0.0002) | (0–0.0002) | - | - | - | ||
Cold smoked fish | L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | ||
Fish species with a high amount of histidine (particularly tuna) | Histamine | - | - | - | - | - | - | 0.03 | ||
Shellfish | Crustaceans | V. parahaemolyticus | - | - | - | - | (0–0.00003) | - | - | |
L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | |||
Cooked bivalve mollusks | V. parahaemolyticus | - | - | - | - | (0–0.00003) | - | - | ||
Norovirus | - | - | - | - | (0.2–2.0) | - | - | |||
Hepatitis A virus | - | - | - | - | (0.2–2.0) | - | - | |||
Raw bivalve mollusks | V. parahaemolyticus | - | - | - | - | - | (0–0.00003) | (0–0.00003) | ||
Norovirus | - | - | - | - | - | - | (0.2–2.0) | |||
Hepatitis A virus | - | - | - | - | - | - | (0.2–2.0) | |||
Raw produce | - | Frozen raw produce (red fruits, vegetables) | Norovirus | - | - | - | - | - | - | (0.2–2.0) |
Hepatitis A virus | - | - | - | - | - | - | (0.2–2.0) | |||
Not frozen raw produce | STEC | - | (0.2–1.8) | - | - | - | - | |||
L. monocytogenes | - | (0.0–0.6) | - | - | - | (0.0–0.6) | (0.0–0.6) | |||
Salmonella | - | (1.6–12.5) | - | - | - | - | ||||
Norovirus | - | - | - | - | - | - | (0.2–2.0) | |||
Hepatitis A virus | - | - | - | - | - | - | (0.2–2.0) | |||
Cryptosporidium spp. | - | 0.003 | - | - | - | - | ||||
C. cayetanensis | - | - | - | - | - | - | 0.0003 | |||
Giardia spp. | - | 0.003 | - | - | - | - | ||||
T. gondii, congenital | - | - | - | - | - | - | (0.3–2.9) | |||
T. gondii, acquired | - | - | - | - | - | - | (0.3–2.9) | |||
Wild raw produce (watercress, dandelion) | F. hepatica | - | - | - | - | - | - | 0.0003 | ||
Red fruits and berries | E. multilocularis | - | - | - | - | (0.0–0.3) | - | (0.0–0.3) | ||
Ready-made meals and complex foods | Refrigerated and processed foods of extended durability (REPFED) | All kinds of packaging | B. cereus | - | - | - | - | - | (0.3–2.9) | - |
Vacuum-packed | C. botulinum | - | - | - | - | (0.00–0.02) | (0.00–0.02) | - | ||
Home-made meal | Particularly those containing grain (pasta, rice, semolina) or dehydrated ingredients | B. cereus | - | - | (0.0–1.6) | - | (0.0–1.6) | (0.0–1.6) | - | |
Particularly meat cooked in a sauce | C. perfringens | - | - | (0.2–2.5) | - | (0.2–2.5) | (0.2–2.5) | - | ||
Composite foods | Ready-made meals, cakes, extensively manipulated foods (sandwiches) | L. monocytogenes | - | - | - | - | - | (0.0–0.9) | (0.0–0.9) | |
S. aureus | - | - | (0.1–1.6) | - | - | (0.1–1.6) | - | |||
Shigella spp. | 0.2 (0.0–0.3) | - | - | - | - | - | (0.0–0.3) | |||
Norovirus | 0.6 (0.2–2.0) | - | - | - | - | - | - | |||
Hepatitis A virus | 0.6 (0.2–2.0) | - | - | - | - | - | - | |||
Home-made canned food | C. botulinum | - | - | (0.00–0.02) | - | (0.00–0.02) | - | - |
Food Categories | CI90 1 (%) | Sub-Categories | CI90 (%) | Specific Foods | CI90 (%) |
---|---|---|---|---|---|
Meats | (50–69) | Beef | (4–20) | Cooked ground beef | (2–13) |
Raw ground beef | (2–13) | ||||
Beef meat | 0.3 | ||||
Poultry | (34–44) | Poultry meat | (34–44) | ||
Pork | (9–21) | Pork meat | (5–16) | ||
Raw pig liver products, boar offal | 3 | ||||
Open-air pig, boar, game | 0.003 | ||||
Cooked pork meats | (0–3) | ||||
Home-made cooked and salt pork meat | (0–0.03) | ||||
Other meats | (1–5) | Lamb, open-air pigs, imported horses | (1–5) | ||
Dairy | (5–22) | Unpasteurised milk | (0–2) | Heated milk | (0–2) |
Raw milk | (0–2) | ||||
Raw milk cheeses | (4–21) | Fresh non-ripened cheeses | (0–0.03) | ||
Hard non-cooked cheeses | (2–12) | ||||
Soft cheeses | (2–15) | ||||
Pasteurized milk cheeses | (0.2–1.6) | Soft cheeses | (0.2–1.6) | ||
Eggs | (3–19) | - | - | Eggs | (2–13) |
Raw eggs products | (2–13) | ||||
Seafood | (1–6) | Fish | (0.2–1.6) | Cooked fish | (0–0.0003) |
Raw fish | (0–0.0003) | ||||
Cold smoked fish | (0.2–1.6) | ||||
Fish species with a high amount of histidine (particularly tuna) | 0.003 | ||||
Shellfish | (1–5) | Crustaceans | (0.2–1.6) | ||
Cooked bivalve mollusks | (0–3) | ||||
Raw bivalve mollusks | (0–3) | ||||
Raw produce | (6–20) | - | - | Frozen raw produce (red fruits, vegetables) | (0–3) |
Not frozen raw produce | (5–18) | ||||
Wild raw produce (watercress, dandelion) | 0.0003 | ||||
Red fruits and berries | 0.3 | ||||
Ready-made meals and complex foods | (8–12) | Refrigerated and processed foods of extended durability (REPFED) | (0–3) | All kinds of packaging | (0–3) |
Vacuum-packed | (0–0.02) | ||||
Home-made meal | (3–6) | Particularly those containing grain (pasta, rice, semolina) or dehydrated ingredients | (0–3) | ||
Particularly meat cooked in a sauce | 3 | ||||
Composite foods | (1–5) | Ready-made meals, cakes, extensively manipulated foods (sandwiches) | (1–5) | ||
Home-made canned food | (0–0.03) |
Food Categories | CI90 1 (%) | Poor Handling Practices Contributing to the Onset of Foodborne Illnesses | No Contribution from Food Handlers at the Final Preparation | |||||
---|---|---|---|---|---|---|---|---|
Cross-Contamination | Inadequate Washing and Disinfection of Produce | Inadequate Processing or Cooling | Inadequate Freezing | Inadequate Cooking (Including Reheating) | Inadequate Storage (Temperature and/or Shelf-Life) | |||
Meats | (50–69) | (6–33) | 0 | (0.00–0.02) | (1–3) | (13–41) | (3–15) | (1–7) |
Dairy | (5–22) | 0 | 0 | 0 | 0 | (0–2) | (0.1–1.4) | (5–21) |
Eggs | (3–19) | 0 | 0 | 0 | 0 | (2–13) | (0–7) | (0–7) |
Seafoods | (1–6) | 0 | 0 | (0–0.0002) | (0–0.0002) | (0–3) | (0.1–1.4) | (1–3) |
Raw produce | (6–20) | 0 | (2–13) | 0 | 0 | 0 | (0.0–0.6) | (3–9) |
Ready-made meals and complex foods | (8–12) | (0–3) | 0 | (1–4) | 0 | (0–3) | (2–6) | (0.1–1.0) |
Total | - | (7–34) | (2–13) | (1–4) | (1–3) | (19–49) | (9–23) | (15–33) |
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Augustin, J.-C.; Kooh, P.; Bayeux, T.; Guillier, L.; Meyer, T.; Jourdan-Da Silva, N.; Villena, I.; Sanaa, M.; Cerf, O.; on Behalf of the Anses Working Group on Consumer Information on Foodborne Biological Risks. Contribution of Foods and Poor Food-Handling Practices to the Burden of Foodborne Infectious Diseases in France. Foods 2020, 9, 1644. https://doi.org/10.3390/foods9111644
Augustin J-C, Kooh P, Bayeux T, Guillier L, Meyer T, Jourdan-Da Silva N, Villena I, Sanaa M, Cerf O, on Behalf of the Anses Working Group on Consumer Information on Foodborne Biological Risks. Contribution of Foods and Poor Food-Handling Practices to the Burden of Foodborne Infectious Diseases in France. Foods. 2020; 9(11):1644. https://doi.org/10.3390/foods9111644
Chicago/Turabian StyleAugustin, Jean-Christophe, Pauline Kooh, Thomas Bayeux, Laurent Guillier, Thierry Meyer, Nathalie Jourdan-Da Silva, Isabelle Villena, Moez Sanaa, Olivier Cerf, and on Behalf of the Anses Working Group on Consumer Information on Foodborne Biological Risks. 2020. "Contribution of Foods and Poor Food-Handling Practices to the Burden of Foodborne Infectious Diseases in France" Foods 9, no. 11: 1644. https://doi.org/10.3390/foods9111644
APA StyleAugustin, J.-C., Kooh, P., Bayeux, T., Guillier, L., Meyer, T., Jourdan-Da Silva, N., Villena, I., Sanaa, M., Cerf, O., & on Behalf of the Anses Working Group on Consumer Information on Foodborne Biological Risks. (2020). Contribution of Foods and Poor Food-Handling Practices to the Burden of Foodborne Infectious Diseases in France. Foods, 9(11), 1644. https://doi.org/10.3390/foods9111644