Bad Bug Book – Foodborne Pathogenic Microorganisms and Natural Toxins – Second Edition

Salmonella is a motile, non-sporeforming, Gram- negative, rod-shaped bacterium in the family Enterobacteriaceae and the tribe Salmonellae. Non-motile variants include S. Gallinarum and S. Pullorum. The genus Salmonella is divided into two species that can cause illness in humans:

Image (c) Dennis Kunkel Microscopy, Inc.

• S. enterica

• S. bongori
Salmonella enterica, which is of the greatest public 
health concern, is comprised of six subspecies:

o S. enterica subsp. enterica (I)

o S. enterica subsp. salamae (II)

o S. enterica subsp. arizonae (IIIa)

o S. enterica subsp. diarizonae (IIIb)

o S. enterica subsp. houtenae (IV)

o S. enterica subsp. indica (VI)

Salmonella is further subdivided into serotypes,
based on the Kaufmann-White typing scheme first
published in 1934, which differentiates Salmonella
strains by their surface and flagellar antigenic
properties. Salmonella spp. are commonly referred
to by their serotype names. For example,
Salmonella enterica subsp. enterica is further
divided into numerous serotypes, including S.
Enteritidis and S. Typhimurium, which are
common in the U.S. (Note that species names are
italicized, but serotype names are not.)

Kaufmann first proposed the scheme, 44 serotypes had been discovered. As of 2007, the number of serotypes discovered was 2,579.

2. Disease

Salmonella can cause two types of illness, depending on the serotype:
(1) nontyphoidal salmonellosis and (2) typhoid fever, both of which are described below. The 
symptoms of nontyphoidal salmonellosis can be quite unpleasant, but this illness is generally self-limiting among healthy people with intact immune systems (although it can cause life- threatening illness even in healthy people). Typhoid fever is more serious and has a higher mortality rate than does nontyphoidal salmonellosis.

Nontyphoidal Salmonellosis

• Caused by serotypes other than S. Typhi and S. Paratyphi A.

• Mortality: Generally less than 1%; however, S. Enteritidis has a 3.6% mortality rate in outbreaks in nursing homes and hospitals, with the elderly being particularly affected.

• Onset: 6 to 72 hours after exposure.

• Infective dose: As low as one cell, depending on age and health of host and strain 
differences among members of the genus.

• Symptoms: Nausea, vomiting, abdominal cramps, diarrhea, fever, headache.

• Duration: Symptoms generally last 4 to 7 days, with acute symptoms usually lasting 1 to 2 days or longer, depending on host factors, the dose ingested, and strain characteristics.

• Complications: (1) Dehydration and electrolyte imbalance may occur as a result of diarrhea and vomiting. This can lead to death in the very young, the elderly, and the immunocompromised, if not treated promptly. (2) In 2% of culture-proven cases, reactive arthritis (i.e., arthritis from an immune reaction to the infection – an autoimmune response – rather than directly from the infection itself) may follow 3 to 4 weeks after the onset of acute symptoms. Indications of reactive arthritis may include, for example, joint inflammation, urethritis, uveitis, and/or conjunctivitis. (3) Nontyphoidal Salmonella can sometimes escape from the gastrointestinal tract into the body and cause blood poisoning (septicemia) or infect the blood, internal organs, and/or joints (bacteremia). S. Dublin is sometimes associated with this complication.

• Route of entry: oral (e.g., ingestion of contaminated food, fecal particles, or contaminated water).

• Pathway: Penetration and passage of Salmonella organisms from gut lumen into epithelium of small intestine, where inflammation occurs. There is evidence that enterotoxin may be produced, perhaps within enterocytes.

Typhoid Fever

• Caused by serotypes S. Typhi and S. Paratyphi A, both of which are found only in humans.

• Mortality: Untreated, as high as 10%.

• Onset: Generally 1 to 3 weeks, but may be as long as 2 months after exposure.

• Infective dose: Fewer than 1,000 cells.

• Symptoms: High fever, from 103° to 104°F; lethargy; gastrointestinal symptoms, including abdominal pains and diarrhea or constipation; headache; achiness; loss of appetite. A rash of flat, rose-colored spots sometimes occurs.

• Duration: Generally 2 to 4 weeks.

• Illness / Complications: Septicemia, with colonization of other tissues and organs; e.g., may lead to endocarditis. Septic arthritis may occur, in which the infection directly affects the joints and may be difficult to treat. Chronic infection of the gallbladder may occur, which may cause the infected person to become a carrier.

• Route of entry: Oral (e.g., ingestion of contaminated food, fecal particles, or contaminated water).

• Pathway: Penetration and passage of typhoid Salmonella organisms from gut lumen into epithelium of small intestine and into the bloodstream (i.e., septicemia), which may carry the organisms to other sites in the body, where inflammation occurs. There is evidence that enterotoxin may be produced, perhaps within enterocytes. 
3. Frequency of Disease 
Annually in the United States:

Nontyphoidal salmonellosis – A recent report from the Centers for Disease Control and Prevention (CDC) estimates that 1,027,561 cases of domestically acquired nontyphoidal salmonellosis occur annually in the U.S., when under-reporting and under-diagnosis are taken into account.

Typhoid fever – In terms of domestically acquired S. enterica serotype Typhi, the CDC recently estimated that a mean of 1,821 cases occur annually in the U.S. Additional cases in the U.S. are associated with foreign travel. The report estimates that 433 cases of typhoid fever in the U.S., overall (i.e., whether or not they are domestically acquired), are culture-confirmed. The last case of a foodborne, noncarrier-based typhoid outbreak in the U.S. was in 1999 and was associated with the tropical fruit mamey. 
4. Sources 
Salmonella is widely dispersed in nature. It can colonize the intestinal tracts of vertebrates, including livestock, wildlife, domestic pets, and humans, and may also live in environments such as pond-water sediment. It is spread through the fecal-oral route and through contact with contaminated water. (Certain protozoa may act as a reservoir for the organism). It may, for example, contaminate meat, farm-irrigation water (thus contaminating produce in the field), soil and insects, factory equipment, hands, and kitchen surfaces and utensils. 
Since S. Typhi and S. Paratyphi A are found only in human hosts, the usual sources of these organisms in the environment are drinking and/or irrigation water contaminated by untreated sewage. It is highly recommended that only potable water and cooked vegetables be consumed in areas where these organisms are endemic. 
Various Salmonella species have long been isolated from the outside of egg shells, but S. Enteritidis can be present inside the egg. This and other information strongly suggest vertical transmission; i.e., deposition of the organism on the albumen (egg white) side of the yolk-sack membrane (vitelline membrane) by an infected hen, prior to shell formation.

Outbreaks also have been linked to the handling of certain animals sometimes kept as pets, such as turtles, frogs, and chicks.

Food Sources

Although Salmonella traditionally was thought of as being associated with animal products in the past, fresh produce also has been the source of major outbreaks, particularly recently. The organism also survives well on low-moisture foods, such as spices, which have been the vehicles for large outbreaks.

A few examples of foods that have been linked to Salmonella illness include meats, poultry, eggs, milk and dairy products, fish, shrimp, spices, yeast, coconut, sauces, unpasteurized salad dressings, cake mixes, cream-filled desserts and toppings that contain raw egg, dried gelatin, peanut butter, cocoa, produce (fruits and vegetables, such as tomatoes, peppers, and cantaloupes), and chocolate.

Cross Contamination

Cross contamination occurs when Salmonella is spread from a contaminated source – a contaminated food, infected food handler or animal – to other foods or objects in the environment. An example of how this may occur is when potentially contaminated raw meats, poultry, seafood, produce, or eggs are not kept separate from each other during preparation or cooking, or when a food handler does not adequately clean utensils, surfaces, equipment, and hands after they have come into contact with these products.

The contamination can spread to factory and equipment surfaces, as well as kitchen surfaces and utensils. Cross contamination may occur at any point in the food process.

Cross contamination also may occur from handling pets or wildlife, such as turtles or frogs (or their water, soil, or food and water bowls), then handling food, food-preparation utensils, or other objects in the environment. (Even culinary frog legs have caused outbreaks of salmonellosis.)

5. Diagnosis

Serological identification of cultural isolates from stool. Genetic identification of approximately 100 Salmonella serotypes from pure culture is now possible, but the remaining 2,400-plus serotypes can be identified only through traditional serotyping.

6. Target Populations

Anyone, of any age, may become infected with Salmonella. Particularly vulnerable are people with weak immune systems, such as the very young and the elderly, people with HIV or chronic illnesses, and people on some medications; for example, chemotherapy for cancer or the immunosuppressive drugs used to treat some types of arthritis. People with HIV are estimated to have salmonellosis at least 20 times more than does the general population and tend to have recurrent episodes.

7. Foods Analysis

Isolation and detection methods have been developed for many foods having prior history of Salmonella contamination. Conventional culture and identification methods may require 4 to 6 days for presumptive results. To screen foods, several rapid methods are available, which require 1 to 2 days. These rapid methods include antibody and molecular (DNA or RNA) based assays, but in most cases, require a cultural means to confirm the presence of Salmonella, for regulatory purposes.

8. Examples of Outbreaks

For information on recent outbreaks, see the Morbidity and Mortality Weekly Reports from the Centers for Disease Control and Prevention (CDC).

9. Other Resources

• The CDC provides information about Salmonella, including information about preventing Salmonella Enteritidis infection, on avoiding salmonellosis from animal-handling, and typhoid fever.

• Loci index for genome Salmonella Enteritidis is available from GenBank.