Foodborne Illness Incidence Rates and Food Safety Risks for Populations of Low Socioeconomic Status and Minority Race/Ethnicity: A Review of the Literature
While foodborne illness is not traditionally tracked by race, ethnicity or income, analyses of reported cases have found increased rates of some foodborne illnesses among minority racial/ethnic populations. In some cases ( Listeria, Yersinia) increased rates are due to unique food consumption patterns, in other cases ( Salmonella, Shigella, Campylobacter) it is unclear why this health disparity exists. Research on safe food handling knowledge and behaviors among low income and minority consumers suggest that there may be a need to target safe food handling messages to these vulnerable populations. Another possibility is that these populations are receiving food that is less safe at the level of the retail outlet or foodservice facility. Research examining the quality and safety of food available at small markets in the food desert environment indicates that small corner markets face unique challenges which may affect the quality and potential safety of perishable food. Finally, a growing body of research has found that independent ethnic foodservice facilities may present increased risks for foodborne illness. This review of the literature will examine the current state of what is known about foodborne illness among, and food safety risks for, minority and low socioeconomic populations, with an emphasis on the United States and Europe.
References
[1]
Scallan, E.; Hoekstra, R.M.; Angulo, F.; Tauxe, R.V.; Widdowson, M.-A.; Roy, S.L.; Jones, J.L.; Griffin, P.M. Foodborne illness acquired in the United States—Major pathogens. Emerg. Infect. Dis. 2011, 17, 7–15.
[2]
Bytzer, P.; Howell, S.; Leemon, M.; Young, L.J.; Jones, M.P.; Talley, N.J. Low socioeconomic class is a risk factor for upper and lower gastrointestinal symptoms: A population based study in 15,000 Australian adults. Gut 2001, 49, 66–72, doi:10.1136/gut.49.1.66.
[3]
Borgnolo, G.; Barbone, F.; Scornavacca, G.; Franco, D.; Vinci, A.; Iuculano, F. A case-control study of Salmonella gastrointestinal infection in Italian children. Acta Paediatr. 1996, 85, 804–808, doi:10.1111/j.1651-2227.1996.tb14155.x.
[4]
Olowokure, B.; Hawker, J.; Weinberg, J.; Gill, N.; Sufi, F. Deprivation and hospital admission for infectious intestinal diseases. Lancet 1999, 353, 807–808, doi:10.1016/S0140-6736(99)00611-X.
[5]
Jalava, K.; Ollgren, J.; Eklund, M.; Siitonen, A.; Kuusi, M. Agricultural, socioeconomic and environmental variables as risks for human verotoxigenic Escherichia coli (VTEC) infection in Finland. BMC Infect. Dis. 2011, 11, doi:10.1186/1471-2334-11-275.
[6]
Gillespie, I.A.; Mook, P.; Little, C.L.; Grant, K.A.; Mclaughlin, J. Human Listeriosis in England, 2001–2007: Association with neighborhood deprivation. Euro Surveill. 2010, 15, 19609:1–19609:10.
[7]
Shiferaw, B.; Shallow, S.; Marcus, R.; Segler, S.; Soderlund, D.; Hardnett, F.; Van Gilder, T. Trends in population-based active surveillance for Shigellosis and demographic variability in FoodNet sites, 1996–1999. Clin. Infect. Dis. 2004, 38 (Suppl 3), S175–S180, doi:10.1086/381584.
[8]
Lay, J.; Varma, J.; Vugia, D.; Jones, T.; Zansky, S.; Marcus, R.; Segler, S.; Medus, C.; Blythe, D.; The EIP FoodNet Working Group. Racial and Ethnic Disparities in Foodborne Illness, 2000. Infectious Diseases Society of America: Chicago, IL, USA, 2000.
[9]
Marcus, R.; Rabatsky-Ehr, T.; Lay, J.; Mohle-Boetani, J.; Farley, M.; Shiferaw, B.; Hawkins, M.; Zansky, S.; Jones, T.; Hadler, J. Age, Ethnic and Racial Disparity in Salmonella Serotype Enteritidis (SE): FoodNet, 1998–2000. In Proceedings of International Conference on Emerging Infectious Diseases, Atlanta, GA, USA, 24–27 March 2002.
[10]
Chang, M.; Groseclose, S.; Zaidi, A.; Braden, C. An ecological analysis of sociodemographic factors associated with the incidence of Salmonellosis, Shigellosis, and E. coli o157:H7 infections in US counties. Epidemiol. Infect. 2009, 137, 810–820, doi:10.1017/S0950268808001477.
[11]
Centers for Disease Control and Prevention. Foodborne Disease Active Suiveillance Network (FoodNet). Available online: http://www.cdc.gov/foodnet/ (accessed on 15 June 2013).
[12]
Hardnett, F.P.; Hoekstra, R.M.; Kennedy, M.; Charles, L.; Angulo, F.J. Epidemiologic issues in study design and data analysis related to foodnet activities. Clinic Infect. Dis. 2004, 38, S121–S126, doi:10.1086/381602.
[13]
Centers for Disease Control and Prevention. FoodNet Reports. Available online: http://www.cdc.gov/foodnet/data/reports.html (accessed on 16 June 2013).
[14]
Ray, S.M.; Ahuja, S.D.; Blake, P.A.; Farley, M.M.; Samuel, M.; Fiorentino, T.; Swanson, E.; Cassidy, M.; Lay, J.C.; Van Gilder, T. Population-based surveillance for Yersinia enterocolitica infections in foodnet sites, 1996–1999: Higher risk of disease in infants and minority populations. Clinic Infect. Dis. 2004, 38, S181–S189, doi:10.1086/381585.
[15]
Jackson, K.A.; Biggerstaff, M.; Tobin-D’Angelo, M.; Sweat, D.; Klos, R.; Nosari, J.; Garrison, O.; Boothe, E.; Saathoff-Huber, L.; Hainstock, L. Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant, Hispanic women. J. Food Prot. 2011, 74, 949–953, doi:10.4315/0362-028X.JFP-10-536.
[16]
Linnan, M.J.; Mascola, L.; Lou, X.D.; Goulet, V.; May, S.; Salminen, C.; Hird, D.W.; Yonekura, M.L.; Hayes, P.; Weaver, R.; Audurier, A.; Plikaytis, B.D.; Fannin, S.L.; Kleks, A.; Broome, C.V. Epidemic listeriosis associated with Mexican-style cheese. New England Journal of Medicine 1988, 319, 823–828, doi:10.1056/NEJM198809293191303.
[17]
Bermudez-Millan, A.; Perez-Escamilla, R.; Damio, G.; Gonzalez, A.; Segura-Perez, S. Food safety knowledge, attitudes, and behaviors among Puerto Rican caretakers living in Hartford, Connecticut. J. Food Prot. 2004, 67, 512–516.
[18]
Dharod, J.M.; Perez-Escamilla, R.; Paciello, S.; Venkitanarayanan, K.; Bermudez-Millan, A.; Damio, G. Critical control points for home prepared “chicken and salad” in Puerto Rican households. Food Prot. Trends 2007, 27, 544–552.
[19]
Henley, S.C.; Stein, S.E.; Quinlan, J.J. Identification of unique food handling practices that could represent food safety risks for minority consumers. J. Food Prot. 2012, 75, 2050–2054, doi:10.4315/0362-028X.JFP-12-146.
[20]
Kwon, J.; Wilson, A.N.S.; Bednar, C.; Kennon, L. Food safety knowledge and behaviors of women, infant, and children (WIC) program participants in the United States. J. Food Prot. 2008, 71, 1651–1658.
[21]
Meer, R.R.; Misner, S.L. Food safety knowledge and behavior of expanded food and nutrition education program participants in Arizona. J. Food Prot. 2000, 63, 1725–1731.
[22]
Trepka, M.J.; Murunga, V.; Cherry, S.; Huffman, F.G.; Dixon, Z. Food safety beliefs and barriers to safe food handling among WIC program clients, Miami, Florida. J. Nut. Educ. Behav. 2006, 38, 371–377, doi:10.1016/j.jneb.2006.05.022.
[23]
Wenrich, T.; Cason, K.; Lv, N.; Kassab, C. Food safety knowledge and practices of low income adults in Pennsylvania. Food Prot. Trends 2003, 23, 326–335.
[24]
Zenk, S.; Schulz, A.; Israel, B.; James, S.; Bao, S.; Wilson, M. Neighborhood racial composition, neighborhood poverty, and the spatial accessibility of supermarkets in metropolitan Detroit. Amer. J. Public Health 2005, 95, 660–667, doi:10.2105/AJPH.2004.042150.
[25]
Moore, L.; Diez Roux, A. Associations of neighborhood characteristics with location and type of food stores. Amer. J. Public Health 2006, 96, 325–331, doi:10.2105/AJPH.2004.058040.
[26]
Hilmers, A.; Hilmers, D.C.; Dave, J. Neighborhood disparities in access to healthy foods and their effects on environmental justice. Amer. J. Public Health 2012, 102, 1644–1654, doi:10.2105/AJPH.2012.300865.
[27]
U.S. Department of Agriculture, Economic Research Service. Access to Affordable and Nutritious Food: Measuring and Understanding Food Desets and Their Consequences. 2009. Available online: http://www.ers.usda.gov/media/242675/ap036_1.pdf (accessed on 16 June 2013).
[28]
U.S. Department of Agriculture, Economic Research Service. Characteristics and Influential Factors of Food Deserts. 2012. Available online: http://www.ers.usda.gov/publications/err-economic-research-report/err140.aspx#.UdDb99jNnsI (accessed on 16 June 2013).
[29]
Signs, R.J.; Darcey, V.L.; Carney, T.A.; Evans, A.A.; Quinlan, J.J. Retail food safety risks for populations of different races, ethnicities, and income levels. J. Food Prot. 2011, 74, 1717–1723, doi:10.4315/0362-028X.JFP-11-059.
[30]
Koro, M.E.; Anandan, S.; Quinlan, J.J. Microbial quality of food available to populations of differing socioeconomic status. Amer. J. Prev. Med. 2010, 38, 478–481, doi:10.1016/j.amepre.2010.01.017.
[31]
Kwon, J.; Roberts, K.R.; Shanklin, C.W.; Liu, P.; Yen, W.S.F. Food safety trianing needs assessment for independent ethnic restaurants: Review of health inspection data in Kansas. Food Prot. Trends 2010, 30, 412–421.
[32]
Darcey, V.L.; Quinlan, J.J. Use of geographic information systems technology to track critical health code violations in retail facilities available to populations of different socioeconomic status and demographics. J. Food Prot. 2011, 74, 1524–1530, doi:10.4315/0362-028X.JFP-11-101.
[33]
Roberts, K.; Kwon, J.; Shanklin, C.; Liu, P.; Yen, W. Food safety practices lacking in independent ethnic restaurants. J. Cul. Sci. Tech. 2011, 9, 1–16, doi:10.1080/15428052.2011.549041.
[34]
Macartney, S.; Bishaw, A.; Fontenot, K. Poverty Rates for Selected Detailed Race and Hispanic Groups by State and Place: 2007–2011. U.S. Department of Commerce, United States Census Bureau: Washington, DC, USA, 2013.
[35]
Ailes, E.; Scallan, E.; Berkelman, R.L.; Kleinbaum, D.G.; Tauxe, R.V.; Moe, C.L. Do differences in risk factors, medical care seeking, or medical practices explain the geographic variation in Campylobacteriosis in foodborne diseases active surveillance network (FoodNet) sites? Cli. Infect. Dis. 2012, 54, S464–S471, doi:10.1093/cid/cis050.
[36]
Gilliss, D.; Cronquist, A.B.; Cartter, M.; Tobin-D’Angelo, M.; Blythe, D.; Smith, K.; Lathrop, S.; Zansky, S.; Cieslak, P.R.; Dunn, J.; et al. Incidence and trends of infection with pathogens transmitted commonlyh through food—Foodborne diseases active surveillance network, 10 U.S. Sites, 1996–2012. MMWR 2013, 62, 283–287.
[37]
Samuel, M.C.; Vugia, D.J.; Shallow, S.; Marcus, R.; Segler, S.; McGivern, T.; Kassenborg, H.; Reilly, K.; Kennedy, M.; Angulo, F. Epidemiology of sporadic Campylobacter infection in the United States and declining trend in incidence, FoodNet 1996–1999. Clin. Infect. Dis. 2004, 38, S165–S174, doi:10.1086/381583.
[38]
Calva, J.J.; Ruiz-Palacios, G.M.; Lopez-Vidal, A.B.; Ramos, A.; Bojalil, R. Cohort study of intestinal infection with Campylobacter in Mexican children. Lancet 1988, 331, 503–506, doi:10.1016/S0140-6736(88)91297-4.
[39]
Martin, P.M.V.; Mathiot, J.; Ipero, J.; Kirimat, M.; Georges, A.J.; Georges-Courbot, M. Immune response to Campylobacter jejuni and Campylobacter coli in a cohort of children from birth to 2 years of age. Infect. Immun. 1989, 57, 2542–2546.
[40]
Pazzaglia, G.; Bourgeois, A.L.; Diwany, K.E.; Nour, N.; Badran, N.; Hablas, R. Campylobacter diarrhoea and an association of recent disease with asymptomatic shedding in Egyptian children. Epidem. Infect. 1991, 106, 77–82, doi:10.1017/S0950268800056466.
[41]
Blaser, M.J.; Sazie, E.; Williams, L.P., Jr. The influence of immunity on raw milk—Associated Campylobacter infection. JAMA 1987, 257, 43–46, doi:10.1001/jama.1987.03390010047026.
[42]
Domingues, A.R.; Pires, S.M.; Halasa, T.; Hald, T. Systematic review: Source attribution of human Campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Epidem. Infect. 2012, 140, 970–981, doi:10.1017/S0950268811002676.
[43]
Mughini Gras, L.; Smid, J.H.; Wagenaar, J.A.; de Boer, A.G.; Havelaar, A.H.; Friesema, I.H.M.; French, N.P.; Busani, L.; van Pelt, W. Risk factors for Campylobacteriosis of chicken, ruminant, and environmental origin: A combined case-control and source attribution analysis. PLoS One 2012, 7, doi:10.1371/journal.pone.0042599.
[44]
White, A.J.; Kinlin, L.; Johnson, C.; Spain, C.V.; Ng, V.; Fisman, D. Environmental determinants of Campylobacteriosis risk in Philadelphia from 1994 to 2007. EcoHealth 2009, 6, 200–208, doi:10.1007/s10393-009-0246-9.
[45]
Swaminathan, B.; Gerner-Smidt, P. The epidemiology of human Listeriosis. Microb. Infect. 2007, 9, 1236–1243, doi:10.1016/j.micinf.2007.05.011.
[46]
MacDonald, P.D.M.; Whitwam, R.E.; Boggs, J.D.; MacCormack, J.N.; Anderson, K.L.; Reardon, J.W.; Saar, J.R.; Graves, L.M.; Hunter, S.B.; Sobel, J. Outbreak of Listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican style cheese. Clin. Infect. Dis. 2005, 40, 677–682, doi:10.1086/427803.
[47]
Lay, J.; Varma, J.; Marcus, R.; Jones, T.; Tong, S.; Medus, C.; Samuel, M.; Cassidy, P.; Hardnett, F.; Barden, C. Higher incidence of Listeria infections among Hispanics: FoodNet, 1996–2000. In Proceedings of International Conference on Emerging Infectious Diseases, Atlanta, GA, USA, 24–27 March 2002.
[48]
Jackson, K.A.; Iwamoto, M.; Swerdlow, D. Pregnancy-associated Listeriosis. Epidem. Infect. 2010, 138, 1503–1509, doi:10.1017/S0950268810000294.
[49]
Silk, B.J.; Date, K.A.; Jackson, K.A.; Pouillot, R.; Holt, K.G.; Graves, L.M.; Ong, K.L.; Hurd, S.; Meyer, R.; Marcus, R. Invasive Listeriosis in the foodborne diseases active surveillance network (FoodNet), 2004–2009: Further targeted prevention needed for higher-risk groups. Clin. Infect. Dis. 2012, 54, S396–S404, doi:10.1093/cid/cis268.
[50]
U.S. Food and Drug Administration. Preventing Listeriosis in Pregnant Hispanic Women in the U.S. Available online: http://www.fda.gov/Food/FoodborneIllnessContaminants/PeopleAtRisk/ucm062993.htm (accessed on 23 June 2013).
[51]
Centers for Disease Control and Prevention. Listeria. Available online: http://www.cdc.gov/listeria/resources/index.html (accessed on 23 June 2013).
[52]
Pouillot, R.; Hoelzer, K.; Jackson, K.A.; Henao, O.L.; Silk, B.J. Relative risk of Listeriosis in foodborne diseases active surveillance network (FoodNet) sites according to age, pregnancy, and ethnicity. Clin. Infect. Dis. 2012, 54, S405–S410, doi:10.1093/cid/cis269.
[53]
Taylor, E.V.; Holt, K.G.; Mahon, B.E.; Ayers, T.; Norton, D.; Gould, L.H. Ground beef consumption patterns in the United States, FoodNet, 2006 through 2007. J. Food Prot. 2012, 75, 341–346, doi:10.4315/0362-028X.JFP-11-333.
[54]
Patil, S.R.; Cates, S.; Morales, R. Consumer food safety knowledge, practices, and demographic differences: Findings from a meta-analysis. J. Food Prot. 2005, 68, 1884–1894.
[55]
Ong, K.L.; Gould, L.H.; Chen, D.L.; Jones, T.F.; Scheftel, J.; Webb, T.H.; Mody, R.K.; Mahon, B.E. Changing epidemiology of Yersinia enterocolitica infections: Markedly decreased rates in young Black children, foodborne diseases active surveillance network (FoodNet), 1996–2009. Clin. Infect. Dis. 2012, 54, S385–S390, doi:10.1093/cid/cis053.
[56]
Methchock, B.; Lonsway, D.R.; Carter, G.P.; Lee, L.A.; McGowan, J.E. Yersinia enterocolitica: A frequent stool isolate from children in an urban hospital in the southeast United States. J. Clin. Microbiol. 1991, 29, 2868–2869.
[57]
Bottone, E.J. Current trends in Yersinia enterocolitica isolates in the New York city area. J. Clin. Microbiol. 1983, 17, 63–67.
[58]
Scallan, E.; Jones, T.F.; Cronquist, A.; Thomas, S.; Thomas, S.; Frenzen, P.; Hoefer, D.; Medus, C.; Angulo, F.J.; FoodNet Working Group. Factors associated with seeking medical care and submitting a stool sample in estimating the burden of foodborne illness. Foodborne Pathog. Dis. 2006, 3, 432–438, doi:10.1089/fpd.2006.3.432.
[59]
Fein, S.B.; Lando, A.M.; Levy, A.S.; Teisl, M.F.; Noblet, C. Trends in U.S. Consumers’ safe handling and consumption of food and their risk perceptions, 1988 through 2010. J. Food Prot. 2011, 74, 1513–1523, doi:10.4315/0362-028X.JFP-11-017.
[60]
Patrick, M.E.; Mahon, B.E.; Zansky, S.M.; Hurd, S.; Scallan, E. Riding in shopping carts and exposure to raw meat and poultry products: Prevalence of, and factors associated with, this risk factor for Salmonella and Campylobacter infection in children younger than 3 years. J. Food Prot. 2010, 73, 1097–1100.
[61]
Dharod, J.M.; Paciello, S.; Bermudez-Millan, A.; Venkitanarayanan, K.; Damio, G.; Perez-Escamilla, R. Bacterial contamination of hands increases risk of cross-contamination among low-income Puerto Rican meal preparers. J. Nut Educ. Behav. 2009, 41, 389–397, doi:10.1016/j.jneb.2008.11.001.
[62]
Dharod, J.M.; Pérez-Escamilla, R.; Bermúdez-Millán, A.; Segura-Pérez, S.; Damio, G. Influence of the fight bac! Food safety campaign on an urban Latino population in Connecticut. J. Nut Educ. Behav. 2004, 36, 128–134, doi:10.1016/S1499-4046(06)60149-8.
[63]
Baker, E.; Schootman, M.; Barnidge, E.; Kelly, C. The role of race and poverty in access to foods that enable individuals to adhere to dietary guidelines. Prev. Chronic Dis. 2006, 3, 1–11.
[64]
Baker, E.A.; Kelly, C.; Barnidge, E.; Strayhorn, J.; Schootman, M.; Struthers, J.; Griffith, D. The garden of Eden: Acknowledging the impact of race and class in efforts to decrease obesity rates. Amer. J. Public Health 2006, 96, 1170–1174, doi:10.2105/AJPH.2004.049502.
[65]
Zenk, S.N.; Schulz, A.J.; Israel, B.A.; James, S.A.; Bao, S.; Wilson, M.L. Fruit and vegetable access differs by community racial composition and socioeconomic position in Detroit, Michigan. Ethn. Dis. 2006, 16, 275–280.
[66]
Pham, M.T.; Jones, A.Q.; Sargeant, J.M.; Marshall, B.J.; Dewey, C.E. Specialty food safety concerns and multilingual resource needs: An online survey of public health inspectors. Foodborne Path. Dis. 2010, 7, 1457–1462, doi:10.1089/fpd.2010.0580.
[67]
Webber, C.B.; Sobal, J.; Dollahite, J.S. Shopping for fruits and vegetables. Food and retail qualities of importance to low-income households at the grocery store. Appetite 2010, 54, 297–303, doi:10.1016/j.appet.2009.11.015.
[68]
Andreyeva, T.; Middleton, A.E.; Long, M.W.; Luedicke, J.; Schwartz, M.B. Food retailer practices, attitudes and beliefs about the supply of healthy foods. Public Health Nutr. 2011, 14, 1024–1031, doi:10.1017/S1368980011000061.
[69]
Mauer, W.A.; Kaneene, J.B.; DeArman, V.T.; Roberts, C.A.; Miller, R.; Pong, L.; Dickey, T.E. Ethnic-food safety concerns: An online survey of food safety professionals. J. Environ. Health 2006, 68, 32–38.
[70]
Food Marketing Institute. Access to Healthier Foods: Opportunities and Challenges for Food Retailers in Underserved Areas. Available online: http://www.fmi.org/docs/health-wellness-research-downloads/access_to_healthier_foods.pdf?sfvrsn=2 (accessed on 13 September 2011).
[71]
Pothukuchi, K.; Mohamed, R. Explaining disparities in food safety compliance by food stores: Does community matter? Agr. Hum. Values 2008, 25, 319–332.
[72]
Yapp, C.; Fairman, R. Factors affecting food safety compliance within small and medium-sized enterprises: Implications for regulatory and enforcement strategies. Food Contr. 2004, 17, 42–51.
[73]
Medeiros, P.; Wilcock, A. Public health inspector bias and judgement during inspections of food service premises. Food Prot. Trends 2006, 26, 930–940.
[74]
Taking on “Food Deserts”. Available online: http://www.letsmove.gov/blog/2010/02/24/taking-food-deserts (accessed on 20 December 2010).
[75]
TRF. Pennsylvania Fresh Food Financing Initiative. Available online: http://www.trfund.com/resource/downloads/Fresh_Food_Financing_Initiative_Comprehensive.pdf (accessed on 13 June 2013).
[76]
Oliveira, V.; Frazao, E. The WIC Program: Background, Trends, and Economic Issues; United States Department of Agriculture: Washingtong, DC, USA, 2009.
[77]
Sivapalasingam, S.; Friedman, C.R.; Cohen, L.; Tauxe, R.V. Fresh produce: A growing cause of outbreaks for foodborne illness in the United States, 1973–1997. J. Food Prot. 2004, 67, 2342–2353.
[78]
Morland, K.; Wing, S.; Diez Roux, A.; Poole, C. Neighborhood characteristics associated with the location of food stores and food service places. Amer. J. Prev. Med. 2002, 22, 23–29, doi:10.1016/S0749-3797(01)00403-2.
Simonne, A.H.; Nille, A.; Evans, K.; Marshall, M.R. Ethnic food safety trends in the United States based on CDC foodborne illness data. Food Prot. Trends 2004, 24, 590–604.
[81]
Rudder, A. Food safety and the risk assessment of ethnic minority food retail businesses. Food Contr. 2006, 17, 189–196, doi:10.1016/j.foodcont.2004.10.017.
[82]
Niode, O.; Bruhn, C.; Simonne, A.H. Insight into Asian and Hispanic restaurant manager needs for safe food handling. Food Contr. 2011, 22, 34–42, doi:10.1016/j.foodcont.2010.06.006.
