Source attribution of human salmonellosis using a meta-analysis of case-control studies of sporadic infections

SUMMARY Salmonella is an important cause of human illness. Disease is frequently associated with foodborne transmission, but other routes of exposure are recognized. Identifying sources of disease is essential for prioritizing public health interventions. Numerous case-control studies of sporadic salmonellosis have been published, often using different methodologies and settings. Systematic reviews consist of a formal process for literature review focused on a research question. With the objective of identifying the most important risk factors for salmonellosis, we performed a systematic review of case-control studies and a meta-analysis of obtained results. Thirty-five Salmonella case-control studies were identified. In the meta-analysis, heterogeneity between studies and possible sources of bias were investigated, and pooled odds ratios estimated. Results suggested that travel, predisposing factors, eating raw eggs, and eating in restaurants were the most important risk factors for salmonellosis. Sub-analyses by serotype were performed when enough studies were available.

[1]  F. Birrell,et al.  Risk factors for sporadic Salmonella Birkenhead infection in Queensland and northern New South Wales: a case control study. , 2004, New South Wales public health bulletin.

[2]  M. S. Patel,et al.  An introduction to meta-analysis. , 1989, Health Policy.

[3]  P. Prabhakar,et al.  Emergence of Salmonella enteritidis phage type 4 in the Caribbean: case-control study in Trinidad and Tobago, West Indies. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[4]  H. Gray Systematic Reviews to Support Evidence-based Medicine , 2003 .

[5]  R. Kirby,et al.  Epidemiology and Molecular Identification of Salmonella Infections in Children , 1998 .

[6]  T. Hald,et al.  Assessing the differences in public health impact of salmonella subtypes using a bayesian microbial subtyping approach for source attribution. , 2010, Foodborne pathogens and disease.

[7]  T. Barrett,et al.  Emergence of Multidrug-Resistant Salmonella enterica Serotype Newport Infections Resistant to Expanded-Spectrum Cephalosporins in the United States , 2003 .

[8]  M. A. Wallace,et al.  Salmonellosis in a Nursing Home Patient on Enteral Feeding , 2006 .

[9]  G. T. Werner [Salmonella infections]. , 1977, Fortschritte der Medizin.

[10]  M. Osterholm,et al.  Role of egg consumption in sporadic Salmonella enteritidis and Salmonella typhimurium infections in Minnesota. , 1993, The Journal of infectious diseases.

[11]  H. Schmid,et al.  Risk factors for sporadic Salmonellosis in Switzerland , 1996, European Journal of Clinical Microbiology and Infectious Diseases.

[12]  K. Ekdahl,et al.  Travel-associated non-typhoidal salmonellosis: geographical and seasonal differences and serotype distribution. , 2005, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[13]  M. Kirk,et al.  Population-Attributable Risk Estimates for Risk Factors Associated with Campylobacter Infection, Australia , 2008, Emerging infectious diseases.

[14]  C. Hedberg,et al.  Food-related illness and death in the United States. , 1999, Emerging infectious diseases.

[15]  N. Garrett,et al.  A recurring salmonellosis epidemic in New Zealand linked to contact with sheep , 2006, Epidemiology and Infection.

[16]  T. Hald,et al.  Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections , 2012, Epidemiology and Infection.

[17]  T. Jones,et al.  A Case-Control Study of the Epidemiology of Sporadic Salmonella Infection in Infants , 2006, Pediatrics.

[18]  R. Tweedie,et al.  A Nonparametric “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis , 2000 .

[19]  T. Farley,et al.  Relationship between home food-handling practices and sporadic salmonellosis in adults in Louisiana, United States , 2002, Epidemiology and Infection.

[20]  J M Sargeant,et al.  The process of systematic review and its application in agri-food public-health. , 2006, Preventive veterinary medicine.

[21]  C. Braden,et al.  Recipes for foodborne outbreaks: a scheme for categorizing and grouping implicated foods. , 2009, Foodborne pathogens and disease.

[22]  David N. Taylor,et al.  Salmonella dublin infections in the United States, 1979-1980. , 1982, The Journal of infectious diseases.

[23]  N. Banatvala,et al.  Salmonellosis in North Thames (East), UK: associated risk factors , 1999, Epidemiology and Infection.

[24]  L R Ward,et al.  A case control study of infection with an epidemic strain of multiresistant Salmonella typhimurium DT104 in England and Wales. , 1994, Communicable disease report. CDR review.

[25]  J. D. Greig,et al.  Analysis of foodborne outbreak data reported internationally for source attribution. , 2009, International journal of food microbiology.

[26]  L. H. Cheng,et al.  Egg consumption is the principal risk factor for sporadic Salmonella serotype Heidelberg infections: a case-control study in FoodNet sites. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[27]  Y. V. van Duynhoven,et al.  Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections , 2005, Epidemiology and Infection.

[28]  T. Hald,et al.  Salmonella source attribution in different European countries , 2008 .

[29]  S. Palmer,et al.  Undercooked hens eggs remain a risk factor for sporadic Salmonella enteritidis infection. , 1999, Communicable disease and public health.

[30]  L. MacDougall,et al.  Frozen chicken nuggets and strips and eggs are leading risk factors for Salmonella Heidelberg infections in Canada , 2005, Epidemiology and Infection.

[31]  J. Engberg Contributions to the epidemiology of Campylobacter infections. A review of clinical and microbiological studies. , 2006, Danish medical bulletin.

[32]  P. Michel,et al.  Risk factors for Salmonella Typhimurium DT104 and non-DT104 infection: a Canadian multi-provincial case-control study , 2004, Epidemiology and Infection.

[33]  S. Altekruse,et al.  The pandemic of Salmonella Enteritidis phage type 4 reaches Utah: a complex investigation confirms the need for continuing rigorous control measures , 2000, Epidemiology and Infection.

[34]  Tine Hald,et al.  A Bayesian Approach to Quantify the Contribution of Animal‐Food Sources to Human Salmonellosis , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[35]  A. Arnedo-Pena,et al.  [Risk factors for the occurrence of sporadic Campylobacter, Salmonella and rotavirus diarrhea in preschool children]. , 2007, Anales de pediatria.

[36]  M. Kirk,et al.  Salmonella Mississippi infections in Tasmania: the role of native Australian animals and untreated drinking water , 2006, Epidemiology and Infection.

[37]  Roger M Cooke,et al.  Attribution of foodborne pathogens using structured expert elicitation. , 2008, Foodborne pathogens and disease.

[38]  C. Begg,et al.  Operating characteristics of a rank correlation test for publication bias. , 1994, Biometrics.

[39]  T. Halasa,et al.  Meta-analysis of dry cow management for dairy cattle. Part 1. Protection against new intramammary infections. , 2009, Journal of dairy science.

[40]  V. Vaillant,et al.  Risk factors for the occurrence of sporadic Salmonella enterica serotype typhimurium infections in children in France: a national case-control study. , 2000, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[41]  L. Hutwagner,et al.  Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[42]  J. P. Davis,et al.  An increase in sporadic and outbreak-associated Salmonella enteritidis infections in Wisconsin: the role of eggs. , 1999, The Journal of infectious diseases.

[43]  Tine Hald,et al.  Attributing the human disease burden of foodborne infections to specific sources. , 2009, Foodborne pathogens and disease.

[44]  L. Willocks,et al.  Salmonella virchow PT 26 infection in England and Wales: a case control study investigating an increase in cases during 1994 , 1996, Epidemiology and Infection.

[45]  T. Halasa,et al.  Meta-analysis of dry cow management for dairy cattle. Part 2. Cure of existing intramammary infections. , 2009, Journal of dairy science.

[46]  C. Medus,et al.  Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: a case-control study in five FoodNet Sites, 2002–2003 , 2006, Epidemiology and Infection.

[47]  L. Hutwagner,et al.  Prior antimicrobial agent use increases the risk of sporadic infections with multidrug-resistant Salmonella enterica serotype Typhimurium: a FoodNet case-control study, 1996-1997. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[48]  T. Hald,et al.  Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. , 2010, Foodborne pathogens and disease.

[49]  L. Slutsker,et al.  Breast-feeding decreases the risk of sporadic salmonellosis among infants in FoodNet sites. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[50]  K. Mølbak,et al.  Risk factors for sporadic infection with Salmonella enteritidis, Denmark, 1997-1999. , 2002, American journal of epidemiology.

[51]  T. Humphrey,et al.  Risk factors for salmonella food poisoning in the domestic kitchen – a case control study , 2002, Epidemiology and Infection.

[52]  R. Reporter,et al.  Epidemic Salmonella enteritidis infection in Los Angeles County, California. The predominance of phage type 4. , 1996, The Western journal of medicine.

[53]  G. Smith,et al.  Bias in meta-analysis detected by a simple, graphical test , 1997, BMJ.

[54]  J. Crump,et al.  Salmonella enterica serotype Javiana infections associated with amphibian contact, Mississippi, 2001 , 2004, Epidemiology and Infection.

[55]  P. Kass,et al.  Disease determinants of sporadic salmonellosis in four northern California counties. A case-control study of older children and adults. , 1992, Annals of epidemiology.

[56]  D. Swerdlow,et al.  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. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[57]  C. Ferguson Evidence for publication bias in video game violence effects literature: A meta-analytic review , 2007 .

[58]  T. Crume,et al.  Highly resistant Salmonella Newport-MDRAmpC transmitted through the domestic US food supply: a FoodNet case-control study of sporadic Salmonella Newport infections, 2002-2003. , 2006, The Journal of infectious diseases.

[59]  G. Kapperud,et al.  Epidemiology of Salmonella typhimurium O:4-12 infection in Norway: evidence of transmission from an avian wildlife reservoir. , 1998, American journal of epidemiology.

[60]  R. Orwin A fail-safe N for effect size in meta-analysis. , 1983 .