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Food Poison Journal Food Poisoning Outbreaks and Litigation: Surveillance and Analysis

What is Salmonella?

Salmonella is a bacterium that causes one of the most common enteric (intestinal) infections in the United States – salmonellosis. [5] It has long been said that, in 1885, pioneering American veterinary scientist, Daniel E. Salmon, discovered the first strain of Salmonella. [5] Actually, Theobald Smith, research-assistant to Dr. Salmon, discovered the first strain of SalmonellaSalmonella cholerae suis. [25] But, being the person in charge, Dr. Salmon received credit for the discovery. [25] In any case, today the number of known strains of the bacteria totals over two thousand. [5, 6]

The term Salmonella refers to a group or family of bacteria that variously cause illness in humans. Salmonella serotype typhimurium and Salmonella serotype enteritidis are the most common in the United States. [5, 15, 26] Salmonella javiana is the fifth most common serotype in the United States and accounted for 3.4% of Salmonella isolates reported to the CDC during 2002. [24] According to one study:

During the 1980s, S. Enteritidis emerged as an important cause of human illness in the United States. In 1976, the incidence of S. Enteritidis was 0.55 per 100,000 population and represented only 5% of all Salmonella isolates. By 1985, this proportion reached 10%, and the rate increased to 2.4 per 100,000 population. During the same time, total Salmonella infection rates rose from 10.7 per 100,000 in 1976 to 24.3 in 1985. The highest rates of S. Enteritidis were seen in the Northeast, although rates in the western region also increased during this time.

The number of outbreaks of S. Enteritidis infection also increased during the 1980s, particularly in the northeastern United States. Laboratory subtyping of S. Enteritidis isolates from outbreaks indicated that phage types (PT) 8 and 13a were the most common phage types in the United States. Although PT4 was common in Europe, where it coincided with a large increase in S. Enteritidis infections, it was seen in the United States only among persons with a history of foreign travel. [26]

Of the Salmonella outbreaks that occurred from 1985 through 1999, “[f]ive hundred twenty-two (62%) outbreaks of S. Enteritidis infection were associated with food prepared at commercial food establishments (restaurants, caterers, delicatessens, bakeries, cafeteria, or market).” [26]

The Incidence of Salmonella Infections

In 2009, over 40,000 cases of Salmonella (13.6 cases per 100,000 persons) were reported to the Centers for Disease Control and Prevention (CDC) by public health laboratories across the nation, representing a decrease of approximately 15% from the previous year, but a 4.2% increase since 1996. [1] Overall, the incidence of Salmonella in the United States has not significantly changed since 1996. [2, 5]

Only a small proportion of all Salmonella infections are diagnosed and reported to health departments. [15] It is estimated that for every reported case, there are approximately 38.6 undiagnosed infections. [15] The CDC estimates that 1.4 million cases, 15,000 hospitalizations, and 400 deaths are caused by Salmonella infections in the U.S. every year. [3]

Salmonella can be grouped into more than 2,400 serotypes. [5] The two most common serotypes in the U.S. are S. Typhimurium and S. Enteritidis. S. Typhi, the serotype that causes typhoid fever, is uncommon in the U.S. [6] But, globally, typhoid fever continues to be a significant problem, with an estimated 12-33 million cases occurring annually. [5] Moreover, outbreaks in developing countries have a high death-rate, especially when caused by strains of the bacterium that are resistant to antibiotic treatment. [5]

Salmonella are found in the intestinal tract of wild and domesticated animals and humans. Some serotypes of Salmonella, such as S. Typhi and S. Paratyphi are only found in humans. [5] For ease of discussion, it is generally useful to group Salmonellae into two broad categories: typhoidal, which includes S. Typhi and S. Paratyphi, and non-typhoidal, which includes all other serotypes.

The Prevalence of Salmonella in Food and Elsewhere

Most Salmonella infections are caused by eating contaminated food, especially food from animal origins. [23] One study found that 87% of all confirmed cases of Salmonella were foodborne, with 10 percent from person-to-person infection and 3% caused by pets. [23] As explained in a comprehensive report issued by the USDA’s Economic Research Service:

Salmonella contamination occurs in a wide range of animal and plant products (table 3). Poultry products and eggs are frequently contaminated with S. enteritidis, while beef products are commonly contaminated with S. typhimurium. Other food sources of Salmonella may include raw milk or other dairy products and pork. Salmonella outbreaks also have been traced to contaminated vegetables, fruits, and marijuana.

Another study went into even greater detail in explaining the prevalence of Salmonella and the sources of human infection, stating as follows:

A food item was implicated in 389 (46%) outbreaks of S. Enteritidis infection from 1985 through1999; in 86 (22%) of these, more than one food item was implicated. Of the 371 outbreaks for which information was available, 298 (80%) were egg associated. This proportion ranged from 10 (71%) of 14 in 1985 to 19 (95%) of 20 in 1997. Of outbreaks caused by a single vehicle for which information was known, 243 (83%) of 294 were egg-associated, as were 55 (71%) of 77 outbreaks in which more than one food item was implicated.

Among single foods implicated in egg-associated outbreaks, 67 (28%) of 243 were foods that contained raw eggs (e.g., homemade ice cream, Caesar salad dressing, tiramisu, egg nog). Sixty-five (27%) of the outbreaks implicated traditional egg dishes such as omelets, French toast, pancakes, and foods that use egg batter, such as crab cakes, chile rellenos, egg rolls, and Monte Cristo sandwiches. Sixty-three (26%) outbreaks implicated dishes known to contain eggs, such as lasagna, ziti, and stuffing, which would have been expected to have been fully cooked but probably did not reach temperatures sufficient to kill S. Enteritidis. Thirty-six (15%) outbreaks implicated egg dishes that were “lightly cooked” (e.g., hollandaise sauce, meringue, cream pies). The food vehicles in 12 (5%) outbreaks were reported to contain eggs but could not be classified because information on how the dishes were prepared was not provided.

Seventy-three (20%) of the 371 confirmed outbreaks for which information was provided involved vehicles that did not contain eggs. Twenty (27%) of these outbreaks were associated with poultry (chicken or turkey), 8 (11%) with beef, and 6 (8%) with foods containing shrimp (3 outbreaks), bologna (1), pork (1), and pepper loaf (1). Other implicated foods included potatoes (3), beans (3), desserts (3), salad (3), macaroni and cheese (1), cheese sauce (1), goat cheese (1), chili (1), and a pureed diet (1). In 22 (30%) of the non–egg-associated outbreaks, more than one food was implicated. In four of these outbreaks, cross-contamination with raw eggs was suspected. [26]

In sum, food remains the most common vehicle for the spread of Salmonella, and eggs are the most common food implicated. [26] As one authority points out, “Studies showed that the internal contents of eggs can be contaminated with [Salmonella], and this contamination has been identified as a major risk factor in the emergence of human illness.” [26]. Part of this risk stems from the variety of ways that Salmonella can contaminate an egg. For example, the FDA has documented the following:

Bacteria can be on the outside of a shell egg. That’s because the egg exits the hen’s body through the same passageway as feces is excreted. That’s why eggs are required to be washed at the processing plant. All USDA graded eggs and most large volume processors follow the washing step with a sanitizing rinse at the processing plant. It is also possible for eggs to become infected by Salmonella Enteritidis fecal contamination through the pores of the shells after they’re laid. SE also can be inside an uncracked, whole egg. Contamination of eggs may be due to bacteria within the hen’s reproductive tract before the shell forms around the yolk and white. SE doesn’t make the hen sick. [29]

Chicken is also a major cause of Salmonella. Beginning in 1998, the publisher of Consumer Reports magazine has conducted surveys and tested chicken at retail for Salmonella and Campylobacter. Its 2009 study found 14% of broiler chickens at grocery stores to contain Salmonella. [28] A USDA Baseline Data Collection Program report done in 1994 documented Salmonella contamination on 20.0% of broiler-chicken carcasses [16]. However, in 2009 the same USDA data collection survey showed the prevalence of Salmonella in broiler chickens at 7.5%. [17] Additionally, turkey carries a lower risk with a prevalence of 1.66%.

While Salmonella comes from animal feces, fruits and vegetables can become contaminated. A common source is raw sprouts, which have been the subject of at least 30 reported outbreaks of foodborne illnesses since 1996. [30] The U.S. Department of Health and Human Services cautions against consuming raw sprouts under any circumstances: “Unlike other fresh produce, seeds and beans need warm and humid conditions to sprout and grow. These conditions are also ideal for the growth of bacteria, including Salmonella, Listeria, and E. coli.” [30]

Symptoms of Salmonella Infection

Salmonella infections can have a broad range of illness, from no symptoms to severe illness. The most common clinical presentation is acute gastroenteritis. Symptoms include diarrhea, and abdominal cramps, often accompanied by fever of 100°F to 102°F (38°C to 39°C). [4, 5] Other symptoms may include bloody diarrhea, vomiting, headache and body aches. The incubation period, or the time from ingestion of the bacteria until the symptoms start, is generally 6 to 72 hours; however, there is evidence that in some situations the incubation can be longer than 10 days. [6, 7] People with salmonellosis usually recover without treatment within 3 to 7 days. [5] Nonetheless, the bacteria will continue to be present in the intestinal tract and stool for weeks after recovery of symptoms—on average, 1 month in adults and longer in children. [6]

  1. Typhi and Paratyphi generally cause a bacteremic illness—Salmonella found in the blood—of long duration. This illness is called enteric, typhoid, or paratyphoid fever. [5] Symptoms start gradually, and include fever, headache, malaise, lethargy, and abdominal pain. In children, it can present as a non-specific fever. The incubation period for S. Typhi is usually 8 to 14 days, but it can range from 3 to 60 days. [5, 6] For S. Paratyphi infections, the incubation period is similar to that of non-typhoidal Salmonella, 1 to 10 days. [5,6]

Complications of Salmonella Infection

In approximately 5% of non-typhoidal infections, patients develop bacteremia. [5, 8] In a small proportion of those cases, the bacteria can cause a focal infection, where it becomes localized in a tissue and causes an abscess, arthritis, endocarditis, or other severe illness. Infants, the elderly, and immune-compromised persons are at greater risk for bacteremia or invasive disease. [5, 23] Additionally, infection caused by antimicrobial-resistant non-typhoidal Salmonella serotypes appears to be more likely to cause bloodstream infections. [9, 23]

Overall, approximately 20% of cases each year require hospitalization, 5% of cases have an invasive infection, and one-half of 1% die. Infections in infants and in people 65 years of age or older are much more likely to require hospitalization or result in death. [8] There is some evidence that Salmonella infections increase the risk of developing digestive disorders, including irritable bowel syndrome. [10]

Although most persons that become ill with diarrhea caused by Salmonella recover without any further problems, a small number of persons develop a complication often referred to as reactive arthritis. The terminology used to describe this type of complication has changed over time. The term “Reiter’s Syndrome” was used for many years, but has now fallen into disfavor. The precise proportion of persons that develop reactive arthritis following a Salmonella infection is unknown, with estimates ranging from 2 to 15%. [11] Symptoms of reactive arthritis include inflammation (swelling, redness, heat, and pain) of the joints, the genitourinary tract (reproductive and urinary organs), or the eyes.

More specifically, symptoms of reactive arthritis include pain and swelling in the knees, ankles, feet and heels. It may also affect wrists, fingers, other joints, or the lower back. Tendonitis (inflammation of the tendons) or enthesitis (inflammation where tendons attach to the bone) can occur. Other symptoms may include prostatitis, cervicitis, urethritis (inflammation of the prostate gland, cervix or urethra), conjunctivitis (inflammation of the membrane lining the eyelid) or uveitis (inflammation of the inner eye). Ulcers and skin rashes are less common. [12] Symptoms can range from mild to severe.

One study showed that on average, symptoms developed 18 days after infection. A small proportion of those persons (15%) had sought medical care for their symptoms, and two thirds of persons with reactive arthritis were still experiencing symptoms 6 months later. [13] Although most cases recover within a few months, some continue to experience complications for years. Treatment focuses on relieving the symptoms.

There are a lot of gaps in our knowledge surrounding this complication. Since there is no specific test for reactive arthritis, doctors rely on signs and symptoms of the patient in order to make the diagnosis. However, there are no clearly defined criteria or set of symptoms used to diagnose this condition. The role of genetics is also unclear. It is thought that the presence of a gene called human leukocyte antigen (HLA)-B27 predisposes a person to develop reactive arthritis, along with other autoimmune diseases; however, several studies have shown that many persons that develop reactive arthritis lack this genetic factor. [11]

Diagnosis of Salmonella Infections

Salmonella bacteria can be detected in stool. [5, 15] In cases of bacteremia or invasive illness, the bacteria can also be detected in the blood, urine, or on rare occasions in tissues. [5] The test consists of growing the bacteria in culture. [5, 6] A fecal, blood or other sample is placed in nutrient broth or on agar and incubated for 2-3 days. After that time, a trained microbiologist can identify the bacteria, if present, and confirm its identity by looking at biochemical reactions. Treatment with antibiotics before collecting a specimen for testing can affect bacterial growth in culture, and lead to a negative test result even when Salmonella causes the infection. [5]

Treatment for Salmonella Infection

Salmonella infections usually resolve in 3 to 7 days, and many times require no treatment. Persons with severe diarrhea may require rehydration, often with intravenous fluids. [4, 5] Antimicrobial therapy (or treatment with antibiotics) is not recommended for uncomplicated gastroenteritis. In contrast, antibiotics are recommended for persons at increased risk of invasive disease, including infants younger than 3 months of age. [4]

In situations in which antibiotics are needed, trimethoprim/sulfamethoxazole, ampicillin, or amoxicillin, are the best choices. [4, 5] Ceftriaxone, cefotaxime, or flouroquinolones are effective options for antimicrobial-resistant strains, although fluoroquinolones are not approved for persons less than 18 years of age. For persons with an infection in a specific organ or tissue (invasive disease), treatment with an expanded-spectrum cephalosporin is recommended, until it is known if the bacteria is susceptible to one of the more commonly used antibiotics listed above. For these rare situations, treatment with antibiotics for 4 weeks is generally recommended. For enteric fever, including S. Typhi infections, treatment for 14 days is recommended. The specific antibiotic chosen depends on the susceptibility of the bacteria and the response to treatment. [4]

References

  1. CDC, “Salmonella Annual Summary Tables 2009,” 2009, available online at

http://www.cdc.gov/ncezid/dfwed/PDFs/SalmonellaAnnualSummaryTables2009.pdf

  1. CDC, “Preliminary FoodNet Data on the Incidence of Infection with Pathogens Transmitted Commonly through Food—10 States, 2008,” MORBIDITY AND MORTALITY WEEKLY REPORT, Vol. 58, No. 14, pp. 333-37 (April 10, 2009), online at http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5813a2.htm
  2. Voetsch, Andrew, et al., “FoodNet Estimate of the Burden of Illness Caused By Non-Typhoidal Salmonella Infections in the United States,” CLINICAL INFECTIOUS DISEASES, Vol. 15, No. 38, Supplement 3, pp. S127-34 (April 15, 2004) available online at http://cid.oxfordjournals.org/content/38/Supplement_3/S127.long
    4. American Academy of Pediatrics, “Salmonella infections,” RED BOOK: 2006 Report of the Committee on Infectious Diseases, edited by L. K. Pickering, pp. 581–584 (27th ed. 2006).
  3. Miller, S. and Pegues, D., “Salmonella Species, Including Salmonella Typhi,” in Mandell, Douglas, and Bennett’s PRINCIPLES AND PRACTICE OF INFECTIOUS DISEASES, Sixth Edition, Chap. 220, pp. 2636-650 (2005).
  4. Behravesh, C.B., et al., “Salmonellosis,” in CONTROL OF COMMUNICABLE DISEASES MANUAL, 19th Edition, published by American Public Health Association, pp. 535-540. (Heymann, D, editor 2008).
  5. Medus, C, et al., “Salmonella Outbreaks in Restaurants in Minnesota, 1995 through 2003—Evaluation of the Role of Infected Foodworkers,” JOURNAL OF FOOD PROTECTION, Vol. 69, No. 8, pp. 1870-78 (Aug. 2006), article abstract and paid-access to full-text available online at http://www.ncbi.nlm.nih.gov/pubmed/16924912
  6. Jones, Timothy F., et al, “Salmonellosis Outcomes Differ Substantially By Serotype,” JOURNAL OF INFECTIOUS DISEASES, Vol. 198, No. 1, pp. 109-14 (July 1, 2008) at http://jid.oxfordjournals.org/content/198/1/109.full
  7. Varma, Jay K., et al., “Antimicrobial-Resistant Non-typhoidal Salmonella is Associated with Excess Bloodstream Infections and Hospitalizations, JOURNAL OF INFECTIOUS DISEASES, Vol. 191, No. 4,  pp. 554-61 (Feb. 15, 2005) available online at http://jid.oxfordjournals.org/content/191/4/554.long
  8. Mearin, F, et al., “Dyspepsia and Irritable Bowel Syndrome after a Salmonella Gastroenteritis outbreak: One-year Follow-up Cohort Study,” GASTROENTEROLOGY, Vol. 129, No. 1, pp. 98-104 (July 2005) article abstract and paid-access to full-text article available online at http://www.ncbi.nlm.nih.gov/pubmed/16012939.
  9. Townes, John M., “Reactive Arthritis after Enteric Infections in the United States: The Problem of Definition,” CLINICAL INFECTIOUS DISEASES, Vol. 50, Issue 2, pp. 247-54 (2010) available online at http://cid.oxfordjournals.org/content/50/2/247.long
  10. National Institute of Arthritis and Musculoskeletal and Skin Diseases, “Reactive Arthritis—Questions and Answers,” (online publication-date: April 2009), available at

http://www.niams.nih.gov/Health_Info/Reactive_Arthritis/default.asp#a (last accessed on July 20, 2011)

  1. Townes, John M., et al., “Reactive Arthritis Following Culture-Confirmed Infections with Bacterial Enteric Pathogens in Minnesota and Oregon: A Population-based Study,” ANNALS OF RHEUMATIC DISEASE, Vol. 67, No. 12, pp. 1689-96 (Dec. 2008) article abstract at http://www.ncbi.nlm.nih.gov/pubmed/18272671
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  6. USDA Food Safety and Inspection Service (FSIS), THE NATIONWIDE MICROBIOLOGICAL BASELINE DATA COLLECTION PROGRAM: YOUNG TURKEY SURVEY, Aug. 2008—July 2009, at http://www.fsis.usda.gov/PDF/Baseline_Data_Young_Turkey_2008-2009.pdf
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  16.       Consumers Union, “How Safe is that Chicken?” CONSUMER REPORTS (Jan. 2010), online at http://www.consumerreports.org/cro/magazine-archive/2010/january/food/chicken-safety/overview/chicken-safety-ov.htm
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  18.       Foodsafety.gov, “Sprouts: What You Should Know,” online at http://www.foodsafety.gov/keep/types/fruits/sprouts.html (last visited February 17, 2012).
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  20.       CDC, SALMONELLA: PREVENTION, Sep. 2010, available online at http://www.cdc.gov/salmonella/general/prevention.html
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