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Preventing Foodborne Illness: Salmonellosis

Keith R. Schneider, Renée Goodrich-Schneider, Bruna Bertoldi, and Susanna Richardson

This is one in a series of fact sheets discussing common foodborne pathogens of interest to food handlers, processors, and retailers.

What causes a Salmonella-associated foodborne illness?

Salmonella is a bacterium that can cause diarrheal illness in people. Illnesses caused by Salmonella-contaminated food have been identified for more than 100 years (Crum-Cianflone 2008). In 2007, the Centers for Disease Control and Prevention (CDC) estimated that there were 1.2 million cases and approximately 450 deaths associated with Salmonella-contaminated food each year (Scallan et al. 2011). While most go unreported, a significant number, especially those associated with larger outbreaks, are clearly identified to be caused by the ingestion of Salmonella-contaminated food. It was estimated that in 2004 alone, the total economic burden caused by Salmonella infections in the United States (US) was $1.6–$5.3 billion (Scallan et al. 2011).

Outbreaks Associated with Salmonella

Fresh produce has become a larger part of the nation's daily diet, but with this increase in consumption, a rise in the number of foodborne illness associated with fresh produce has also been seen (Sivapalasingam et al. 2004). Recently in 2015, an outbreak of Salmonella enterica serovar Poona was linked to cucumbers (CDC 2016). During the summer of 2015 and continuing into 2016, illnesses were reported in 40 states across the US. A fresh produce company from California that distributed cucumbers throughout the US, mostly to retailers, food service companies, and wholesalers, was implicated in the outbreak (FDA 2016). To date, 907 total cases were reported which have led to 204 hospitalizations and 6 deaths.

In another outbreak in the fall of 2012, Salmonella Bredeney was associated with a nut butter company located in New Mexico. The contamination resulted in 42 ill individuals, 10 of whom needed hospitalization. The ages of those affected ranged from 1 to 79. Twenty states were affected in this outbreak (CDC 2012a). Approximately 100 different types of items made with nuts (e.g., almond butter, peanut butter, cashew butter, blanched peanut, and others) were recalled by the company. Subsequent secondary recalls resulted from the use of contaminated nuts as ingredients (CDC 2012a).

During the summer and fall of 2010, approximately 2,000 people contracted salmonellosis from the consumption of shell eggs (not dried or powdered eggs). Eggs have been associated with Salmonella contamination for many years, but this recent outbreak was one of the largest in recent history. After investigation, the farms that supplied the eggs were identified as the source of contamination (CDC 2010).

Tomatoes had historically been implicated in foodborne salmonellosis outbreaks, especially during the late 1990s and early 2000s. However, there has not been a significant salmonellosis outbreak linked to tomatoes since 2006, where contaminated tomatoes sickened 183 people (CDC 2006). It was during this time many new protocols, such as Florida's (2007) Tomato Good Agricultural Practices (T-GAPs) program were introduced. These programs were designed to ensure the safe production, processing, and handling of tomatoes. This focus on good agricultural practices has led to a vast reduction of microbial contamination and outbreaks on tomatoes (Kokkinakis et al. 2007). Recently, FDA enacted the Food Safety Modernization Act (FSMA), a sweeping new set regulations designed to protect against foodborne illnesses (FDA 2011). One such regulation under the umbrella of FSMA is the Produce Safety Rule (FSMA SEC.105). This new rule will bring mandatory GAPs to all potentially hazardous produce commodities in hopes of reducing the number of foodborne illnesses associated with fresh produce.

What type of bacterium is Salmonella?

Salmonella are typically motile, non-spore-forming, Gram-negative, rod-shaped bacteria (Murray et al. 2007). Currently, there are 2,463 types (serovars) of Salmonella (ASM 2016). Salmonella Typhi and Paratyphi are the serovars that cause typhoid fever, usually a more severe disease than those caused by the other non-typhoidal Salmonella. Salmonella is widespread in the environment and is associated with all animal species, including mammals, birds, reptiles, and amphibians. It has been found in water, soil, insects, animal feces, raw meats, poultry, seafood, and on factory and kitchen surfaces. While these are common sources, Salmonella has been isolated from numerous other food sources as well (Murray et al. 2007).

How is Salmonella spread?

A variety of foods have caused salmonellosis outbreaks, including poultry, meats, eggs, milk products, fruit juice, fish, shrimp, frog legs, yeast, coconut, sauces and salad dressing, cake mixes, breakfast cereal, cream-filled desserts and toppings, dried gelatin, peanut butter, cocoa, chocolate, and dried spices. Salmonella incidence is much higher in raw agricultural products than in cooked or processed food products. Salmonella can be present in foods as a result of cross-contamination with raw foods, or from contamination from humans, animals, birds, or reptiles (Sanyal et al. 1997). Because of the microorganism's ability to survive in a wide range of environments, Salmonella has been found in dry and dehydrated foods (e.g., cocoa, chocolate, dry milk, spices, and cereal products) (Komitopoulou and Peñaloza 2008) and in acidic food products (e.g., non-pasteurized orange juice) (Jain et al. 2009). Thus, preventative measures are extremely important in all food handling and processing steps.

Symptoms of salmonellosis

Acute symptoms of salmonellosis may include nausea, vomiting, abdominal cramps, diarrhea, fever, and headache. Typically, symptoms develop 12–72 hours after ingestion of contaminated food. Most people infected usually recover without treatment after four to seven days (CDC 2012b). As with many foodborne pathogens, young children, the elderly, and the immunocompromised are the most likely targets of Salmonella infections. Depending on host factors, such as the age and health of the host, the infective dose has been estimated to be less than a thousand cells for many of the strains (Blaser and Newman 1982) and as low as 15–20 cells for some strains (FDA 2012a).

In a small percentage of cases, people infected with Salmonella can develop chronic, long-term problems associated with the illness. Reactive arthritis may begin three to four weeks after onset of acute symptoms; arthritic symptoms can be debilitating and last for six months or more (Scallan et al. 2011).

High-Risk Populations for Salmonellosis

All age groups are susceptible to infections, but salmonellosis has a more severe effect on the elderly, infants, and anyone whose immune systems are already compromised by other factors (Jacobs et al. 1985). The frequency of salmonellosis in AIDS patients, for example, is estimated to be 20 times higher than that of the general population (Celum et al. 1987). For food products being supplied to school lunch programs, nursing homes, or hospitals, a more rigorous quality assurance program might be necessary. More demanding standards may include increased sanitation, stricter rules governing personal hygiene, and/or increased microbial testing of finished product(s).

Sanitation Methods for Minimizing the Risk of Salmonellosis in the Plant or Food Establishment

Clean

Use hot, soapy water and a sanitizer to wash hands and food-contact surfaces often. Wash hands, cutting boards, dishes, and utensils after they come in contact with raw food. Clean liquid spills in the refrigerator, especially spills from products associated with Salmonella.

  • Ensure employees wash hands before, during, and after handling any food, particularly raw meat and poultry.
  • Sanitize all utensils, cutting boards, and work surfaces with an approved sanitizing agent before and after use.
  • Clean food-contact surfaces such as refrigerator shelving if they come in contact with possible sources of Salmonella contamination.
  • Wash all vegetables and fruits thoroughly before consumption.

Separate

Treat all RTE (ready-to-eat) foods, raw meat, poultry, and seafood as possible sources of contamination. Keep these types of foods separate from items that are not traditionally cooked or potentially can be eaten raw, such as vegetables, fruits, breads, and other already prepared, edible foods. This reduces the chance of cross-contamination.

  • The utensils used for raw and cooked foods should be separate.
  • Meats and other potential sources of contamination should be stored in places that rest below storage areas for foods that may be consumed raw.
  • Rewrap open packages carefully or store in leak-proof containers to prevent cross-contamination.

Cook

Heat foods to safe temperatures. The 2013 FDA Food Code recommends cooking most potentially hazardous foods to an internal temperature of 165ºF or above for at least 15 seconds (refer to Sections 3–4: Destruction of Organisms of Public Health Concern, Subparts 3-401 and 3-501 of the 2013 FDA Food Code, for specific details on cooking temperatures) (FDA 2013).

Proper cooking and personal hygiene, good sanitation, and preventing cross-contamination of raw and cooked food are the best measures to control Salmonella. Recommendations to reduce the incidence of foodborne salmonellosis include the following:

  • Do not store food in the temperature danger zone between 41ºF and 135ºF. The refrigerator should be at 41ºF or colder. All food should be refrigerated promptly.
  • Completely cook or boil foods like hot dogs and poultry products until they become steaming hot (165ºF or above).

Storage

Try to limit room temperature exposure of food to 2 hours or less before returning perishables and RTE foods to the refrigerator or freezer.

  • Cover all food to prevent cross-contamination.
  • Place all cooked food in the refrigerator within one hour of cooking.
  • Place uncooked meat, poultry, fish, or other raw products below cooked or RTE foods in the refrigerator to prevent cross-contamination.
  • Maintain the refrigerator temperature at or below 41ºF, and keep the refrigerator clean.
  • Observe strictly the "use by" or "best by" dates on refrigerated items.

Good Practices for Food Product Receiving, Handling, Processing, and Storage

The FDA, under the new FSMA regulations, defines current Good Manufacturing Practices for food (cGMPs) in title 21 of CFR (Code of Federal Regulations) part 117 (FDA 2015), formerly 21 CFR 110 (FDA 2012b). These cGMPs outline the minimum required general sanitation practices in FDA-inspected food handling and processing facilities. It is recommended that more specific and stringent standard operating procedures (SOPs) be developed for individual facilities. Sanitation recommendations for food service and retail food facilities, outlined in the FDA Food Code (FDA 2013), have been adopted into many state and local regulations. As there may be some variation in FDA Food Code adoption, it is important that each facility check with the appropriate state and/or local regulatory authority. The Florida statutes can be found online at http://www.leg.state.fl.us/statutes/. Title 33, Chapter 509 specifies some of these regulations.

In addition to setting and adhering to strict sanitation requirements in the facility, a retail establishment should also develop SOPs for receiving and storing food products and ingredients. If food processing is being done, appropriate controls and requirements should be established and strictly adhered to. The FDA Food Code outlines appropriate processing and cooking requirements for many food products processed in a retail facility. However, if certain high-risk food products (e.g., sushi, fresh juice, specialty meats, and others) are processed in the retail establishment, rather than in a more traditional processing facility, additional controls and the issuance of a "variance" by the regulatory authority is required before processing can occur (FDA 2013). The growing retail practice of cooking/preparing/packaging foods traditionally processed in controlled plant environments raises safety concerns. Any processing of food at the retail level needs to be closely monitored.

As an establishment becomes cleaner, it becomes harder to detect foodborne pathogens and testing becomes more limited in its ability to prevent foodborne illness. This is why programs that promote and monitor the use of barriers and/or hurdles are so important. When instituted properly, these activities reduce the risk of foodborne illness. Nothing can be done to completely eliminate bacterial contamination, short of irradiation. Since most consumers prefer a fresh product, programs should be implemented that reduce the probability of illness to a miniscule point.

Receiving

Specifications for receiving can be found in Section 3-202.11 of the 2013 Food Code (FDA 2013). The following guidelines cover the basic points that should be addressed:

  • Potentially Hazardous Food (PHF) should be at a temperature of 41ºF or below when received, unless specified by law (e.g., milk, shellfish).
  • Raw shell eggs should be received at an ambient air temperature of 45ºF or less.
  • PHFs that are received hot should be at a temperature of 135ºF or above.
  • PHF should be received with no evidence of temperature abuse, such as thawing.

Processing

One of the easiest ways to prevent foodborne salmonellosis is ensuring that foods are cooked thoroughly. It should be noted that certain foods that are typically served uncooked—raw eggs (used in Caesar salad dressings, homemade mayonnaise, raw cookie dough, etc.) and fresh vegetables—would obviously not benefit from the cooking process. For these items, other factors, such as sanitation, worker hygiene, and proper storage, take on much greater importance.

  • When a recipe calls for using raw eggs (e.g., Caesar salad dressing), try to purchase a pasteurized egg product.
  • Cook eggs, fish, meat, or foods containing these items to an internal temperature of 145ºF or above for a minimum of 15 seconds.
  • Cook ground meat products to an internal temperature of 155ºF or above for a minimum of 15 seconds.
  • Cook poultry to an internal temperature of 165ºF or above for a minimum of 15 seconds.
  • Reheat previously cooked material to an internal temperature of 165ºF.

Storage

Once an item has been received and/or processed, it will proceed to storage (or display). There are some general guidelines governing these practices as well.

  • Frozen food should remain frozen until it is used.
  • If frozen food is displayed in a refrigerated case, the food should remain at 41ºF or below.
  • Frozen food should be thawed at a temperature of 41ºF or below. Food can also be thawed under running water at a temperature of 70ºF or below. Lastly, the product can be thawed as part of the cooking process.
  • Product must be cooled adequately. Refer to sections 3-501.14 and 3-501.15 of the 2013 Food Code.
  • Hold cooked product above 135ºF while displaying, and under 41ºF while storing.
  • Properly label all stored product.

For more, consult the 2013 Food Code (FDA 2013).

Personal Hygiene

Wash your hands! The majority of foodborne illness, such as salmonellosis, is caused by poor personal hygiene, particularly a lack of proper hand washing. Dirty hands can contaminate food. Although hands may look clean, the bacteria that cause illness are too small to be seen. Whenever you are preparing food and you come in contact with items that are not part of the assembly process, rewash your hands. The same is true even when wearing gloves. THERE IS NO FIVE-SECOND RULE WHEN IT COMES TO FOOD SAFETY! Millions of bacteria and other germs can be transferred on contact. Following is a list of instances when you should wash your hands:

  • Before handling, preparing, or serving food
  • Before handling clean utensils or dishware
  • After using the restroom
  • After touching your face, cuts, or sores
  • After smoking/eating/drinking
  • After handling raw meat, especially poultry
  • After touching unclean equipment, working surfaces, soiled clothing, soiled wiping cloths, etc.
  • After collecting and/or taking out the garbage

Your facility may have even stricter requirements with which you must comply to ensure food safety.

What is the proper procedure for hand washing?

  • Wet your hands with warm water.
  • Apply soap and wash your hands for 20 seconds.
  • Rinse and dry with a single-use paper towel.
  • Use the paper towel to shut off the water.

References

Blaser, M. J., and L.S. Newman. 1982. "A Review of Human Salmonellosis: Infective Dose". Clinical Infectious Diseases 4(6):1096–1106.

Brenner, F.W, R.G. Villar, F.J. Angulo, R. Tauxe, and B. Swaminathan. 2000. "Salmonella Nomenclature". Journal of Clinical Microbiology 38(7):2465-2467.

Centers for Disease Control and Prevention (CDC). 2006. "Salmonellosis-Outbreak Investigation, October 2006". Division of Bacterial and Mycotic Diseases. Accessed June 14, 2016. https://www.cdc.gov/salmonella/2006/tomatoes-11-2006.html

Centers for Disease Control and Prevention(CDC). 2016. "Multistate Outbreak of Salmonella Poona Infections Linked to Imported Cucumbers." Accessed June 14, 2016. https://www.cdc.gov/salmonella/poona-09-15/index.html

Centers for Disease Control and Prevention (CDC). 2010. "Investigation Update: Multistate Outbreak of Human Salmonella Enteritidis Infections Associated with Shell Eggs (Final Update)". Accessed June 14, 2016. June 14, 2016. https://www.cdc.gov/salmonella/2010/shell-eggs-12-2-10.html

Centers for Disease Control and Prevention (CDC). 2012a. "Multistate Outbreak of Salmonella Bredeney Infections Linked to Peanut Butter Manufactured By Sunland, Inc (Final Update)". National Center for Emerging and Zoonotic Infectious Diseases. Division of Foodborne, Waterborne, and Environmental Diseases. Accessed June 14, 2016. https://www.cdc.gov/salmonella/bredeney-09-12/

Centers for Disease Control and Prevention (CDC). 2012b. "Salmonella". National Center for Emerging and Zoonotic Infectious Diseases. Division of Foodborne, Waterborne, and Environmental Diseases. Accessed June 14, 2016. https://www.cdc.gov/salmonella/

Celum, C.L., R.E. Chaisson, G.W. Rutherford, J.L. Barnhart, and D.F. Echenberg. 1987. "Incidence of Salmonellosis in Patients with AIDS". The Journal of Infectious Diseases 156(6):998–1002.

Crum-Cianflone, N.F. 2008. "Salmonellosis and the Gastrointestinal Tract: More than Just Peanut Butter". Current Gastroenterology Reports 10(4):424–431.

Food and Drug Administration (FDA). 2013. FDA 2013 Food Code. Accessed June 14, 2016: https://www.fda.gov/media/87140/download

Food and Drug Administration (FDA). 2012a. "Bad Bug Book 2nd Edition: Foodborne Pathogenic Microorganisms and Natural Toxins Handbook". Center for Food Safety and Applied Nutrition. Accessed June 14, 2016: https://www.fda.gov/food/foodborne-pathogens/bad-bug-book-second-edition

Food and Drug Administration (FDA). 2012b. Code of Federal Regulations Title 21-Part 110. Department of Health and Human Services. Accessed June 14, 2016. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=110&showFR=1

Food and Drug Administration (FDA). 2015. Code of Federal Regulations Title 21-Part 117. Department of Health and Human Services. Accessed June 14, 2016. https://www.federalregister.gov/documents/2015/09/17/2015-21920/current-good-manufacturing-practice-hazard-analysis-and-risk-based-preventive-controls-for-human

Food and Drug Administration (FDA). 2016a. FDA Investigates Multistate Outbreak of Salmonella Poona linked to Cucumbers. Accessed. June 14, 2016. https://www.fda.gov/food/outbreaks-foodborne-illness/fda-investigated-multistate-outbreak-salmonella-poona-linked-cucumbers#what

Food and Drug Administration (FDA). 2016b. FDA Food Safety Modernization Act (FSMA). Accessed March 18, 2016. https://www.fda.gov/food/guidance-regulation-food-and-dietary-supplements/food-safety-modernization-act-fsma

Food and Drug Administration (FDA). 2016c. Produce Safety Rule. Accessed March 18, 2016. https://www.fda.gov/food/food-safety-modernization-act-fsma/full-text-food-safety-modernization-act-fsma#SEC105

Jacobs, J.L., J.W. Gold, H. W. Murray, R.B. Roberts, and D. Armstrong. 1985. "Salmonella Infections in Patients with the Acquired Immunodeficiency Syndrome". Annals of Internal Medicine 102(2):186–188.

Jain, S., S.A. Bidol, J.L. Austin, E. Berl, F. Elson, M. LeMail-Williams, M. Deasy III, et al. 2009. "Multistate Outbreak of Salmonella Typhimurium and Saintpaul Infections Associated with Unpasteurized Orange Juice—United States, 2005". Clinical Infectious Diseases 48(8):1065–1071.

Kokkinakis, E., G. Boskou, G.A. Fragkiadakis, A. Kokkinaki, and N. Lapidakis. 2007. "Microbiological Quality of Tomatoes and Peppers Produced under the Good Agricultural Practices Protocol AGRO 2-1 & 2-2 in Crete, Greece". Food Control 18(12):1538–1546.

Komitopoulou, E., and W. Peñaloza. 2008. "Fate of Salmonella in Dry Confectionery Raw Materials". Journal of Applied Microbiology 106(6):1892–1900.

Mritunjay, S.J. and V. Kumar. 2015. "Fresh Farm Produce as a Source of Pathogens: A Review". Research Journal Environmental Toxicology 9(2):59-70.

Jorgensen J.H, and M.A. Pfaller, eds. 2015. Manual of Clinical Microbiology (11th ed.). Washington DC: ASM Press.

Sanyal, D., T. Douglas, and R. Roberts. 1997. "Salmonella Infection Acquired from Reptilian Pets". Archives of Disease in Childhood. 77:345–346.

Scallan, E., R.M. Hoekstra, F.J. Angulo, R.V. Tauxe, M.A. Widdowson, S.L. Roy, J.L. Jones, and P.M. Griffin. 2011. "Foodborne Illness Acquired in the United States — Major Pathogens". Emerging Infectious Diseases 17(1):7–15.

Sivapalasingam, S., C.R. Friedman, L. Cohen, and R.V. Tauxe. 2004. "Fresh Produce: A Growing Cause of Outbreaks of Foodborne Illness in the United States, 1973 Through 1997". Journal of Food Protection 67(10):2342-2353.

Resources

Adhikari, B., F. Angulo, and M. Meltzer. 2004. "Economic Burden of Salmonella Infections in the United States". American Agricultural Economics Association 2004 Annual meeting, Denver, CO, August 2004. https://ageconsearch.umn.edu/record/20050.

CDC (Centers for Disease Control and Prevention). 2009. "FoodNet Facts and Figures: Number of Infections and Incidence per 100,000 Persons". CDC Foodnet. Accessed June 15, 2016. https://www.cdc.gov/foodnet/factsandfigures/incidence.html.

Florida Administrative Code & Florida Administrative Register. 2010. Rule Chapter: 5G-6: Tomato Inspection. Accessed June 20, 2016: https://www.flrules.org/gateway/ChapterHome.asp?Chapter=5G-6.

DuPage County Health Department. "Handwashing." Accessed June 15, 2016. http://www.dupagehealth.org/handwashing.

San Diego State University. "Salmonella.org." Accessed June 15, 2016. http://www.salmonella.org.