CPH 601—Spring 2015
Helen Sauer
Salmonella—Prevalence and Prevention Strategies
Background/History
Salmonella is a bacteria commonly found in the intestinal tracts of humans and animals, including reptiles, farm animals, and rodents. In 1885, Dr. Theobald Smith, a Department of Agriculture researcher investigating hog cholera, is the first to identify Salmonella enterica, formerly called Salmonella choleraesui. Dr. Smith worked under Dr. Daniel E. Salmon, who became the bacteria’s namesake.1
There are around 2,500 different serotypes of Salmonella bacteria. Salmonella can be grouped into typhoidal (S. Typhi and S. Paratyphi) and non-typhoidal (including Typhimurium and Enteritidis, the most common serotypes in the United States.2
In the early 20th century, Irish immigrant Mary Mallon was identified as the first asymptomatic carrier of typhoid. Now an infamous public health case study, “Typhoid Mary” infected an estimated 51 people with typhoid fever over the course of her career before being forcibly quarantined by state public health officials. In spring 1985, 168,000 to 197,000 people were sickened with salmonellosis in northern Illinois, comprising the largest outbreak of Salmonella food poisoning in United States history. Investigators determined the cause to be Salmonella typhimurium strain of bacteria associated with the Hillfarm Dairy in Melrose Park, Illinois. 3 Salmonella has also been used as a tool of bioterrorism. In 1984, 751 individuals were deliberately poisoned by salad bars at 10 Oregon restaurants. Followers of Indian mystic guru Bhagwan Shree Rajneesh hoped to incapacitate the voting population of the city so that their own candidates would win the 1984 Wasco County elections. 4
Prevalence
Salmonella causes salmonellosis, one of the most common foodborne illnesses in the world. The WHO estimates that tens of millions of people contract salmonellosis each year, resulting in around 100,000 fatalities. In the US, around 42,000 cases are reported per year, representing an estimated 1.4 million total cases and around 400 deaths.5 Cases are likely underreported as salmonellosis can result in relatively mild illness in healthy adults. Young children, the elderly and the immunocompromised are the most likely to have severe infections.6
Salmonella Typhi causes typhoid fever, which is largely obsolete in the United States (due to widespread vaccination), but still results in an estimated 12-33 million cases and 600,000 deaths per year in developing countries.7 As of 2000, more than 90% of the morbidity and mortality associated with typhoid fever occurred in Asia, including Pakistan, India, Vietnam, China, and Indonesia.8 The CDC advises travelers to this region be vaccinated.
Mechanism of Toxicity
Pathogenesis
Salmonella are usually associated with hosts, but have been found to be able to survive on surfaces for weeks. In most cases, Salmonella bacteria are ingested through food or water contaminated with human or animal excreta. Organisms travel to the distal small bowel, where microphages ingest the organism and spread it to the lymph nodes, spleen, and liver.9

Figure 1
Distinct from many other bacteria that can produce toxins, Salmonella itself is toxic. A lipopolysaccharide in Salmonella triggers an allergic reaction, but the symptoms experienced are the body’s reaction to the resulting infection. Figure 1 illustrates Salmonella bacteria being ingested by microphages as well as direct invasion of the epithelial cells, leading to inflammation and local/systemic dissemination in the intestine and other organs.

Clinical presentation
Infections from Salmonella usually produce one of three distinct illnesses: nontyphoidal enterocolitis, nontyphoidal focal disease, or typhoid (enteric) fever. Enterocolitis from non-typhiodal Salmonella strains usually results in loose and bloodless stool for 6-72 hours, but can result in large-volume, cholera-like diarrhea for 3 to 7 days in severe cases. 48-hour fever, abdominal cramps, chills, and heachache are common for nontyphoidal enterocolitis.10 The second manifestation, nontyphoidal focal disease, can occur with or without the presence of bacteremia (Salmonella bacteria in the blood).It results in pain in the affected organ, commonly the GI tract, endothelial surfaces like heart valves, lungs, joints, bones, or soft tissue. Organs compromised by preexisting conditions are particularly susceptible.10
Infection from typhoid and paratyphoid strains cause up to four weeks of fever, rash, fatigue, dry cough and headache, and sometimes diarrhea and vomiting. Between 10 and 15% of patients develop the most severe form of the disease, which results in multisystem toxemia. After 2-3 weeks of these symptoms, more grave complications may occur, including intestinal hemorrhage or perforation.11
Exposure Level and Risk Assessment
Exposure Levels
Salmonella bacteria are commonly found in raw poultry and eggs, but can also be present in raw meat, unpasteurized dairy, and raw vegetables and fruit. They can also be spread through contact with human feces. Additionally, household pets such as cats and particularly birds and reptiles can be Salmonella carriers. 12
In a study of 11 salmonellosis outbreaks in the United States, the actual doses required for infection were calculated to be <103 organisms in six cases; the outbreaks with higher doses involved very high rates of attack and short periods of incubation. 13 A 2001 study of dose-response relationship in rats, illness was only observed in animals exposed to doses of 10(8) cfu or more. At lower doses, changes in the gastrointestinal tract were observed, but did not result in full-blown salmonellosis.14 Assuming children under 5 years of age represented a more susceptible population, it was estimated that at the doses observed in Salmonella outbreaks (approximately 2 and 4 log CFU/g), the susceptible population was 1.8 to 2.3 times more likely to get ill.15
An infected person can carry Salmonella bacteria for days or even months, even while asymptomatic. People treated with oral antibiotics and children tend to carry the bacteria longer, presenting significant risks for schools and daycares.16
Risk Assessment
Study conducted in 1990 following severe Salmonella Enteritidis outbreak linked to contaminated eggs in the US found that less than 1 in 1000 eggs from “infected” flocks are contaminated. An infected hen laid one contaminated egg in every 200, resulting in an endemic level of 1 in 10,000 to 14,000 eggs produced. For healthy adults who eat fully cooked eggs, risk for illness is one in every 1.6 million eggs consumed. Risk is stated to be higher for the immunosuppressed and for those who consume raw or partially cooked eggs.14
As salmonellosis is one of the most common foodborne illnesses, there are ample toolkits for determining Salmonella risk, especially in relation to poultry. The objective is to reduce “farm-to-table” transmission. USDA offers an Egg Production module to determine quantitative microbial risk assessment for SE in shell eggs and egg products, illustrated below.17

Source: USDA/FSIS Shell Eggs Processing and Distribution Module
Standard USDA recommendations for liquid whole eggs are pasteurization at 60 degrees Celsius for 3.5 minutes. The following figure uses linear regression to illustrate the reduction in Salmonella Enteritidis infections following pasteurization at varying temperatures.

Source: USDA/FSIS Shell Eggs Processing and Distribution Module

Risk for typhoid or paratyphoid fever is very low in the US due to vaccination, and the risk of typhoid fever is highest for travelers to southern Asia (6–30 times higher than for all other destinations).18 Generally, more bacteria are required for the development of typhoid vs paratyphoid fever. In Southeast Asia, urbanization has increased the risk of typhoid and paratyphoid fevers. In a study conducted in Jakarta, Indonesia, consuming food from street vendors was found to be associated increased odds of paratyphoid fever (Odds Ratio 3.34), as well as recent flooding in the community (Odds Ratio 4.52). Independent risk factors for typhoid included no use of soap for handwashing (Odds Ratio 1.91), sharing food from the same plate (Odds Ratio 1.93), and no toilet in the household (Odds Ratio 2.20).19
Preventing/Controlling Exposure
Controlling at the Source and Along the Path
In recent years, the USDA has developed stricter standards for poultry processing units in response to rising salmonellosis outbreaks. In 2015, the USDA’s Food Safety and Inspection Service passed new pathogen reduction standards for chicken parts, ground chicken, and ground turkey, aimed at achieving a 30 percent reduction in illnesses from Salmonella.20 Standards for ground products will be more stringent than those for whole poultry products, as the risk of Salmonella contamination increases with processing. As of 2010, eggs from commercial flocks that are known to be infected are pasteurized instead of being sold as grade A shell eggs. The rule also includes refrigeration requirements during storage and transportation. 21 Additionally, state agencies and authorized laboratories of the USDA certify participating breeding flocks and hatcheries of chickens that lay eggs as SE clean (“tested free”). (CDC, 2010)
Following Salmonella outbreaks linked to peanut butter in 2009, 2012, and 2014, new techniques were developed to sanitize machinery following contamination that have been proven effective. In laboratory experiments, no Salmonella was detected in environmental samples on XLD (<0.16 log CFU/cm2) following application of the hot oil and 60% isopropanol sanitation solution (±quaternary ammonium compounds). 22
Controlling at the individual level
Standard recommendations for avoiding Salmonella contamination include storing poultry, meats, and eggs at ≤40° F (≤4° C), discarding cracked eggs, thoroughly cooking poultry and eggs, choosing pasteurized eggs and dairy products, and washing produce before consumption.23 The incidence of Salmonella contamination changed from 30% at retail to 0.16% after cooking to 4% at consumption. 24
CDC recommendations include thorough handwashing after handing raw meat and poultry. Kitchen utensils, countertops, and cutting boards that have come in contact with raw meat and poultry should be washed with warm, soapy water to reduce the risk of cross contamination. Handwashing procedures should be used following contact with household pets such as reptiles or birds or their excrement. The CDC recommends that the elderly, immunocompromised, and small children and infants avoid direct contact with these sorts of household pets as their risk of severe Salmonella infection is greater.23
Summary
Salmonella constitutes a major public health risk in the United States and abroad. Infections from non-typhi Salmonella have increased 10% in recent years.25 Typhoid has largely been eliminated through vaccination in the United States, but remains a major source of illness and mortality in developing countries. Along with following standard recommendations for handling raw meat and poultry, closer monitoring of industrial food processing and increased internal controls could help prevent large-scale infection. However, published studies have not ascertained a strong link between free-range and organic practices and lower Salmonella incidence (versus traditional commercial practices). 26 Future research should concentrate on best management practices for poultry production, economical and effective sanitation methods for food processing equipment, and public education for restaurant workers and households on the importance of thorough cooking and timely refrigeration. Widespread typhoid vaccination should be emphasized for Asian nations.

1. Schultz M. Theobald Smith. Emerging Infectious Diseases. 2008;14.
2. CDC. Preliminary FoodNet Data on the Incidence of Infection with Pathogens Transmitted Commonly Through Food --- 10 States, 2008. In: CDC, ed. Morbidity and Mortality Weekly Report. Vol 58. Atlanta: CDC; 2008:333-337.
3. Van J. `85 Salmonella Outbreak Largest Ever, Study Says. Chicago Tribune, 1987.
4. Bovsun M. 750 sickened in Oregon restaurants as cult known as the Rajneeshees spread salmonella in town of The Dalles. Daily News, 2013.
5. WHO. Salmonella (non-typhoidal); 2013.
6. CDC. Salmonella: Technical Information. 2013.
7. Voetsch G, Angulo, Monica M. Farley, Sue Shallow, Ruthanne Marcus, Paul R. Cieslak, Valerie C. Deneen, Robert V. Tauxe. FoodNet Estimate of the Burden of Illness Caused by Nontyphoidal Salmonella Infections in the United States. Clinical Infectious Diseases. 2004;38(Supplement 3).
8. R Leon Ochiai a CJAa, M Carolina Danovaro-Holliday a, Dong Baiqing b, Sujit K Bhattacharya c, Magdarina D Agtini d, Zulfiqar A Bhutta e, Do Gia Canh f, Mohammad Ali a, Seonghye Shin a, John Wain g, Anne-Laure Page a, M John Albert h, Jeremy Farrar i, Remon Abu-Elyazeed j, Tikki Pang k, Claudia M Galindo a, Lorenz von Seidlein a, John D Clemens a, the Domi Typhoid Study Group. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bulletin of the World Health Organization. 2000;86.
9. Falkow F. Salmonella as an Intracellular Parasite. Molecular Microbiology. 1989;3(12):1833-1841.
10. Salmonella Infection.
11. CDC. Typhoid Fever. 2013.
12. Bäumler ea. Tracing the Origins of Salmonella Outbreaks. Science. 2000;287:50-52.
13. Blaser MJ NL. A Review of Human Salmonellosis: I. Infective Dose. Clinical Infectious Diseases. 1982;4(6):1096-1106.
14. Havelaar GJ, Takumi K, Koedam MA, Dufrenne JB, van Leusden FM, de La Fonteyne L, Bousema JT, Vos JG. A rat model for dose-response relationships of Salmonella Enteritidis infection. Journal of Applied Microbiology. 2001;91(3):442-452.
15. AgricultureOrganization Fa. Hazard characterization and exposure assessment of Salmonella spp. in broilers and eggs.
16. Salmonellosis.
17. B. K. Hope ARB, E. D. Edel, A. T. Hogue, W. D. Schlosser, R. Whiting‖, R. M. McDowell andR. A. Morales. An Overview of the Salmonella Enteritidis Risk Assessment for Shell Eggs and Egg Products. Risk Analysis. 2002;22(2):203-218.
18. Gupta SK MF, Omondi MW, Whichard JM, Fields PI, Gerner-Smidt P, et al. Laboratory-based surveillance of paratyphoid fever in the United States: travel and antimicrobial resistance. Clinical Infectious Diseases. 2008;46(11):1656-1663.
19. Albert M. Vollaard MSA, MD, MSc; Henri A. G. H. van Asten, MD, MPH; Suwandhi Widjaja, MD, PhD; Leo G. Visser, MD, PhD; Charles Surjadi, MD, PhD; Jaap T. van Dissel, MD, PhD. Risk Factors for Typhoid and Paratyphoid Fever in Jakarta, Indonesia. JAMA. 2004;291(22):2607-2615.
20. USDA. USDA Proposes New Measures to Reduce Salmonella and Campylobacter in Poultry Products. In: USDA, ed. Washington, DC; 2015.
21. CDC. Salmonella serotype Enteritidis; 2010.
22. Grassoa EM, Stephen F. Groveb, Lindsay A. Halikc, Fletcher Arrittd, Susanne E. Kellerc. Cleaning and sanitation of Salmonella-contaminated peanut butter processing equipment. Food Microbiology. 2015;46:100-1063.
23. CDC. Prevention.
24. Oscar. A quantitative risk assessment model for Salmonella and whole chickens. Food Microbiology. 2004;93:231-247.
25. CDC. No Progress in Salmonella During Past 15 Years. In: CDC, ed. Atlanta; 2011.
26. Bailey JS1 CD. Salmonella prevalence in free-range and certified organic chickens. Journal of Food Protection. 2005;68(11):2451-2453.