A Risk Assessment of Campylobacteriosis and Salmonellosis Linked to Chicken Meals Prepared in Households in Dakar, Senegal

Risk Analysis

Volumn 32, Issue 10, 2012, Pages 1798-1819

  Pouillot, Régis ^a   Garin, Benoit ^b,c   Ravaonindrina, Noro ^c   Diop, Kane ^b   Ratsitorahina, Mahery ^c   Ramanantsoa, Domoina ^d   Rocourt, Jocelyne ^e  

^a Institut Pasteur de Dakar ^*  (United States)

^b INSTITUT PASTEUR DE DAKAR   (Senegal)

^c INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

^d Faculte de Medecine   (Madagascar)

^e Centre de Recherche Medicale et Sanitaire Niamey   (Niger)

Author keywords

Africa; Foodborne diseases; Risk assessment; Senegal

Indexed keywords

ANIMALS; CONTAMINATION; DIGITAL STORAGE; FOOD MICROBIOLOGY; FOOD SAFETY; FOOD STORAGE; HEATING; MEATS; RISK PERCEPTION; SALMONELLA; THERMAL PROCESSING (FOODS);

AFRICA; ANTIMICROBIAL RESISTANCES; DETECTION AND ENUMERATIONS; FOOD BORNE DISEASE; QUANTITATIVE MICROBIOLOGICAL RISK ASSESSMENTS; SALMONELLA INFECTIONS; SENEGAL; TIME-TEMPERATURE PROFILE;

RISK ASSESSMENT;

ANTIBIOTIC RESISTANCE; BACTERIAL DISEASE; DIGESTIVE SYSTEM DISORDER; EDUCATIONAL DEVELOPMENT; FOOD CONSUMPTION; FOOD PROCESSING; FOOD QUALITY; FOOD SAFETY; FOOD STORAGE; HEALTH EDUCATION; HEALTH IMPACT; HEALTH RISK; HYGIENE; MEAT; PATHOGEN; POLLUTION EXPOSURE; PUBLIC HEALTH; RISK ASSESSMENT; RISK FACTOR;

DAKAR [SENEGAL]; SENEGAL;

CAMPYLOBACTER; GALLUS GALLUS; SALMONELLA;

EID: 84866975550     PISSN: 02724332     EISSN: 15396924     Source Type: Journal    
DOI: 10.1111/j.1539-6924.2012.01796.x     Document Type: Article

References (66)

1. O'Ryan M, Prado V, Pickering LK. A millennium update on pediatric diarrheal illness in the developing world. Seminars in Pediatric Infectious Diseases, 2005; 16(2):125-136.
2. Podewils LJ, Mintz ED, Nataro JP, Parashar UD. Acute, infectious diarrhea among children in developing countries. Seminars in Pediatric Infectious Diseases, 2004; 15(3):155-168.
3. WHO. Food Safety and Foodborne Illness, fact sheet n°237, 2007 [cited 2011 July, 28th]. Available at: http://www.who.int/mediacentre/factsheets/fs237/en/index.html.
4. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States-Major pathogens. Emerging Infectious Diseases, 2011; 17(1):7-12.
5. FAO/WHO. Risk Assessment of Campylobacter spp. in broiler chickens Microbiological Risk Assessment Series 3. Technical report, Rome : Food and Agriculture Organization of the United Nations and World Health Organization, 2009.
6. Graham SM. Nontyphoidal salmonellosis in Africa. Current Opinion In Infectious Diseases, 2010; 23(5):409-414.
7. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM, Whichard JM, Bouchrif B, Fashae K, Granier SA, Jourdan-Da Silva N, Cloeckaert A, Threlfall EJ, Angulo FJ, Aarestrup FM, Wain J, Weill FX. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. Journal of Infectious Diseases, 2011; 204(5):675684.
8. Cardinale E, Perrier Gros-Claude JD, Tall F, Gueye EF, Salvat G. Risk factors for contamination of ready-to-eat street-vended poultry dishes in Dakar, Senegal. International Journal of Food Microbiology, 2005; 103(2):157-165.
9. Garin B, Aidara A, Spiegel A, Arrive P, Bastaraud A, Cartel JL, Aissa RB, Duval P, Gay M, Gherardi C, Gouali M, Karou TG, Kruy SL, Soares JL, Mouffok F, Ravaonindrina N, Rasolofonirina N, Pham MT, Wouafo M, Catteau M, Mathiot C, Mauclere P, Rocourt J. Multicenter study of street foods in 13 towns on four continents by the Food and Environmental Hygiene Study Group of the International Network of Pasteur and Associated Institutes. Journal of Food Protection, 2002; 65(1):146-152.
10. Dione MM, Leven M, Garin B, Marcotty T, Geerts S. Prevalence and antimicrobial resistance of Salmonella isolated from broiler farms, chicken carcasses, and street-vended restaurants in Casamance, Senegal. Journal of Food Protection, 2009; 72(11):2423-2427.
11. Gorman R, Bloomfield S, Adley CC. A study of cross-contamination of food-borne pathogens in the domestic kitchen in the Republic of Ireland. International Journal of Food Microbiology, 2002; 76(1-2):143-150.
12. Codex Alimentarius Commission. Principles and guidelines for the conduct of microbiological risk assessment. Roma : Codex Alimentarius Commission Report No. CAC/GL-30.
13. FAO/WHO. Risk assessment of Salmonella in eggs and broiler chickens. Microbiological Risk Assessment Series II. Technical report, Rome : Food and Agriculture Organization of the United Nations and World Health Organization, 2002.
14. Nauta M, Hill A, Rosenquist H, Brynestad S, Fetsch A, van der Logt P, Fazil A, Christensen B, Katsma E, Borck B, Havelaar A. A comparison of risk assessments on Campylobacter in broiler meat. International Journal of Food Microbiology, 2009; 129(2):107-123.
15. Garin B, Gouali M, Wouafo M, Perchec AM, Minh Thud P, Ravaonindrina N, Urbès F, Gay M, Diawaraf A, Leclercq A, Rocourt J, Pouillot R. Prevalence, quantification and antimicrobial resistance of Campylobacter spp on chickens neck-skins at points of slaughter in 5 major cities located on 4 continents. International Journal of Food Microbiology, submitted.
16. Pavic A, Groves PJ, Bailey G, Cox JM. A validated miniaturized MPN method, based on ISO 6579:2002, for the enumeration of Salmonella from poultry matrices. Journal of Applied Microbiology, 2010; 109(1):25-34.
17. Fravalo P, Hascoët Y, Fellic ML, Queguiner S, Petton J, Salvat G. Convenient method for rapid and quantitative assessment of Salmonella enterica contamination: The mini-MSRV technique. Journal of Rapid Methods & Automation in Microbiology, 2003; 11(2):81-88.
18. Lubran MB, Pouillot R, Bohm S, Calvey EM, Meng J, Dennis S. Observational study of food safety practices in retail deli departments. Journal of Food Protection, 2010; 73(10):1849-1857.
19. Clayton DA, Griffith CJ. Observation of food safety practices in catering using notational analysis. British Food Journal, 2004; 106(3):211-217.
20. Oscar TP. Development and validation of a tertiary simulation model for predicting the potential growth of Salmonella typhimurium on cooked chicken. International Journal of Food Microbiology, 2002; 76(3):177-190.
21. Hoelzer K, Pouillot R, Gallagher D, Lubran M, Akingbade D, Kause J, Dennis S. Estimation of Listeria monocytogenes transfer coefficients and efficacy of bacterial removal through cleaning and sanitation. International Journal of Food Microbiology, submitted.
22. Nauta MJ, Jacobs-Reitsma WF, Havelaar AH. A risk assessment model for Campylobacter in broiler meat. Risk Analysis, 2007; 27(4):845-861.
23. Teunis PFM, Van den Brandhof W, Nauta M, Wagenaar J, Van den Kerkhof H, Van Pelt W. A reconsideration of the Campylobacter dose-response relation. Epidemiology and Infection, 2005; 133(4):583-592.
24. Teunis PFM, Kasuga F, Fazil A, Ogden ID, Rotariu O, Strachan NJC. Dose response modeling of Salmonella using outbreak data. International Journal of Food Microbiology, 2010; 144(2):243-249.
25. Cullen AC, Frey HC. Probabilistic Techniques in Exposure Assessment. New York : Plenum Press, 1999.
26. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria : R Foundation for Statistical Computing, 2010.
27. Pouillot R, Delignette-Muller ML. Evaluating variability and uncertainty separately in microbial quantitative risk assessment using two R packages. International Journal of Food Microbiology, 2010; 142(3):330-340.
28. Nauta M. The modular process risk model (MPRM): A structured approach to food chain exposure assessment. Pp. 99-136 in DW Schaffner (ed). Microbial Risk Analysis of Foods. Washington, DC : ASM Press; 2008.
29. Gill CO, Badoni M. Recovery of bacteria from poultry carcasses by rinsing, swabbing or excision of skin. Food Microbiology, 2005; 22(1):101-107.
30. Mylius SD, Nauta MJ, Havelaar AH. Cross-contamination during food preparation: A mechanistic model applied to chicken-borne Campylobacter. Risk Analysis, 2007; 27(4):803-813.
31. Vose D. Risk Analysis: A Quantitative Guide, 2nd ed. Chichester, UK : Wiley and Sons, 1999.
32. ICMSF. Microorganisms in Food. Vol. 5: Characteristics of Microbial Pathogens. London : Blackie Academic and Professional, 1996.
33. FDA. Bad Bug Book: Foodborne Pathogenic Microorganisms and Natural Toxins Handbook- Campylobacter jejuni 2011. Available at: http://www.fda-gov/Food/FoodSafety/Foodborneillness/FoodborneillnessFoodbornepathogensNaturalTuxins/BadBugBook/ucm070024.htm, Accessed August 3, 2011.
34. Rosso L, Lobry JR, Bajard S, Flandrois JP. Convenient model to describe the combined effects of temperature and pH on microbial growth. Applied and Environmental Microbiology, 1995; 61(2):610-616.
35. Rosso L, Lobry JR, Flandrois JP. An unexpected correlation between cardinal temperatures of microbial growth highlighted by a new model. Journal of Theoretical Biology, 1993; 162(4):447-463.
36. van Gerwen SJC, Zwietering MH. Growth and inactivation models to be used in quantitative risk assessments. Journal of Food Protection, 1998; 61(11):1541-1549.
37. Haas CN. Conditional dose-response relationships for microorganisms: Development and application. Risk Analysis, 2002; 22(3):455-463.
38. Teunis PF, Havelaar AH. The Beta Poisson dose-response model is not a single-hit model. Risk Analysis, 2000; 20(4):513-520.
39. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. Experimental Campylobacter jejuni infection in humans. Journal of Infectious Diseases, 1988; 157(3):472-479.
40. Evans MR, Roberts RJ, Ribeiro CD, Gardner D, Kembrey D. A milk-borne Campylobacter outbreak following an educational farm visit. Epidemiology and Infection, 1996; 117(3):457-462.
41. Van den Brandhof W, Wagenaar J, van den Kerkhof H. An outbreak of campylobacteriosis after drinking unpasteurized milk, 2002, the Netherlands. International Journal of Medical Microbiology, 2003; 293 (Supplement 35):142.
42. Teunis PF, Nagelkerke NJ, Haas CN. Dose response models for infectious gastroenteritis. Risk Analysis, 1999; 19(6):1251-1260.
43. Murmann L, Corbellini LG, Collor AA, Cardoso M. Quantitative risk assessment for human salmonellosis through the consumption of pork sausage in Porto Alegre, Brazil. Journal of Food Protection, 2011; 74(4):553-558.
44. Howard G, Pedley S, Tibatemwa S. Quantitative microbial risk assessment to estimate health risks attributable to water supply: Can the technique be applied in developing countries with limited data Journal of Water And Health, 2006; 4(1):49-65.
45. Nzouankeu A, Ngandjio A, Ejenguele G, Njine T, Ndayo Wouafo M. Multiple contaminations of chickens with Campylobacter, Escherichia coli and Salmonella in Yaounde (Cameroon). Journal of Infection in Developing Countries, 2010; 4(9):583-586.
46. Cardinale E, Tall F, Cisse M, Gueye EF, Salvat G, Mead G. Risk factors associated with Salmonella enterica subsp. enterica contamination of chicken carcases in Senegal. British Poultry Science, 2005; 46(2):204-210.
47. Luber P. Cross-contamination versus undercooking of poultry meat or eggs-Which risks need to be managed first International Journal of Food Microbiology, 2009; 134(1-2):21-28.
48. Havelaar AH, van Pelt W, Ang CW, Wagenaar JA, van Putten JP, Gross U, Newell DG. Immunity to Campylobacter: Its role in risk assessment and epidemiology. Critical Reviews in Microbiology, 2009; 35(1):1-22.
49. Graham SM. Salmonellosis in children in developing and developed countries and populations. Current Opinion in Infectious Diseases, 2002; 15(5):507-512.
50. FAO/WHO. Risk characterization of microbiological hazards in food. Microbiological Risk Assessment Series 17. Technical report, Rome: Food and Agriculture Organization of the United Nations and World Health Organization, 2009
51. Coker AO, Isokpehi RD, Thomas BN, Amisu KO, Obi CL. Human campylobacteriosis in developing countries. Emerging Infectious Diseases, 2002; 8(3):237-244.
52. Brooks JT, Ochieng JB, Kumar L, Okoth G, Shapiro RL, Wells JG, Bird M, Bopp C, Chege W, Beatty ME, Chiller T, Vulule JM, Mintz E, Slutsker L. Surveillance for bacterial diarrhea and antimicrobial resistance in rural western Kenya, 1997-2003. Clinical Infectious Diseases, 2006; 43(4):393-401.
53. Rosenquist H, Nielsen NL, Sommer HM, Norrung B, Christensen BB. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology, 2003; 83(1):87-103.
54. Gassama-Sow A, Aidara-Kane A, Raked N, Denis F, Ploy MC. Integrons in Salmonella Keurmassar, Senegal. Emerging Infectious Diseases, 2004; 10(7):1339-1341.
55. Weill FX, Perrier-Gros-Claude JD, Demartin M, Coignard S, Grimont PA. Characterization of extended-spectrum-beta-lactamase (CTX-M-15)-producing strains of Salmonella enterica isolated in France and Senegal. FEMS Microbiology Letters, 2004; 238(2):353-358.
56. Fabre L, Delaune A, Espie E, Nygard K, Pardos M, Polomack L, Guesnier F, Galimand M, Lassen J, Weill FX. Chromosomal integration of the extended-spectrum beta-lactamase gene blaCTX-M-15 in Salmonella enterica serotype concord isolates from internationally adopted children. Antimicrobial Agents and Chemotherapy, 2009; 53(5):1808-1816.
57. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, Muyodi J, Githinji JW, Kagendo D, Munyalo A, Hart CA. Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa: Zoonotic or anthroponotic transmission? Journal of Medical Microbiology, 2006; 55(Pt 5):585-591.
58. Sire JM, Garin B, Macondo EA. Low-level resistance to ciprofloxacin in non-Typhi Salmonella enterica isolated from human gastroenteritis in Dakar, Senegal (2004-2006). International Journal of Antimicrobial Agents, 2008; 31(6):581-582.
59. Altekruse SF, Stern NJ, Fields PI, Swerdlow DL. Campylobacter jejuni-An emerging foodborne pathogen. Emerging Infectious Diseases, 1999; 5(1):28-35.
60. Chen Y, Jackson KM, Chea FP, Schaffner DW. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. Journal of Food Protection, 2001; 64(1):72-80.
61. Zhao P, Zhao T, Doyle MP, Rubino JR, Meng J. Development of a model for evaluation of microbial cross-contamination in the kitchen. Journal of Food Protection, 1998; 61(8):960-963.
62. Ellouze M, Gauchi JP, Augustin JC. Global sensitivity analysis applied to a contamination assessment model of Listeria monocytogenes in cold smoked salmon at consumption. Risk Analysis, 2010; 30(5):841-852.
63. WHO. Prevention of foodborne disease: Five keys to safer food. Available at: http://www.who.int/foodsafety/consumer/5keys/en/, Accessed August 5, 2010.
64. Busschaert P, Geeraerd AH, Uyttendaele M, Van Impe JF. Estimating distributions out of qualitative and (semi)quantitative microbiological contamination data for use in risk assessment. International Journal of Food Microbiology, 2010; 138(3):260-269.
65. Gonzales-Barron U, Kerr M, Sheridan JJ, Butler F. Count data distributions and their zero-modified equivalents as a framework for modelling microbial data with a relatively high occurrence of zero counts. International Journal of Food Microbiology, 2010; 136(3):268-277.
66. Liu C, Duan J, Su YC. Effects of electrolyzed oxidizing water on reducing Listeria monocytogenes contamination on seafood processing surfaces. International Journal of Food Microbiology, 2006; 106(3):248-253.