A Focus on Salmonella -- Updated Version

On this page... Introduction Classification Natural Reservoirs and Transmission Mechanism of Infection Antimicrobial Resistance Salmonellosis Foodborne Disease Outbreaks Research at the USDA Agricultural Research Service References Detection Methods This technical fact sheet illustrates the following key points about Salmonella: Leading cause of bacterial foodborne illness which accounts for 31 percent of all food-related deaths. Has more than 2,400 serovars which are potentially pathogenic and are identified based on the types of antigens present. Causes three types of Salmonellosis: gastroenteritis, typhoid fever, and bacteremia, which are most commonly caused by consumption of contaminated food and water. Emergence of antimicrobial resistant strains has lead to an increase in the prevalence of human infections and has limited the possibility of effective treatment. Research is focused on determining resistance trends as well as identifying and controlling vehicles of transmission on the farm, during transportation, and in abattoirs and processing plants. Salmonella, the leading cause of bacterial foodborne illnesses in the United States (U.S.), is the causative agent of Salmonellosis. Responsible for approximately 1.4 million non-typhoidal illnesses in the U.S. annually including 40, 000 confirmed cases and 400 deaths, Salmonellosis is the most common cause of enteric (intestinal) infections and accounts for 31 percent of all food-related deaths.14, 17 In addition, an estimated 12 to 33 million cases of typhoid fever, a more serious and fatal form of Salmonellosis, occurs globally each year and is endemic in many developing countries of the Indian subcontinent, South and Central America, and Africa.68 Salmonella is also the most prominent pathogen associated with bacterial foodborne outbreaks in the U.S., accounting for 24 percent of all food outbreaks and 18 percent of produce-related outbreaks between 1990 and 2005.7 A recent survey from 1996 to 2007 estimated that approximately 33 outbreaks were associated with Salmonella-contaminated fruits and vegetables.6 The 2008 Jalapeno and Serrano Pepper Outbreak was the largest foodborne outbreak in more than a decade which infected 1,400 people in 43 states. 13, 24 The ongoing 2009 Peanut Butter and Peanut-containing Products Outbreak has caused 691 illnesses and 9 deaths in 46 states as of March 17, 2009. This outbreak has lead to the largest recall of human food items in the U.S. resulting in over 2,100 products being voluntarily recalled by more than 200 companies.29 The high frequency of Salmonella outbreaks makes it a public health burden representing a significant cost to many countries. In the U.S., the cost associated with Salmonella outbreaks is estimated at 3 billion dollars annually. In recent years, the emergence of antimicrobial-resistant Salmonella strains has lead to an increase in the total prevalence of human infections and has limited the possibilities for effective treatment. 66, 10 Back to top Classification Salmonella are gram negative, facultatively anaerobic, non-spore forming, rod shaped bacteria that are motile (with a few exceptions) by means of peritrichous flagella. They are catalase positive, oxidase negative, and chemo-organotrophic with the ability to metabolize nutrients by both respiratory and fermentative pathways.50, 23 This pathogen grows on citrate, forming acetate, formate, and carbon dioxide as products, and catabolizing D-glucose with the production of acid and gas.4, 23 In addition, Salmonella readily generate hydrogen sulfide gas in both triple sugar iron and lysine agar media.37, 54 The genus Salmonella is a member of the family Enterobacteriaceae and consists of very closely related bacteria, many of which cause disease in human and animals. The DNA of this genus is most closely related to other genera of the Enterobacteriaceae family: Escherichia, Shigella, and Citrobacter.51, 54 It is comprised of two species: Salmonella bongori and Salmonella enterica. S. enterica is further divided into six subspecies which are known by subspecies names and Roman numerals (i.e. S. enterica subsp. enterica I). These subspecies are differentiated on the basis of biochemical traits and genomic similarities and contain multiple serovars (serotypes). Currently, more than 2,400 Salmonella serovars have been identified based on the presence of three major types of antigens: somatic (O) or cell wall antigens; flagellar (H) antigens; and surface antigens.49, 54 Somatic (O) or Cell Wall Antigens -- This type includes lipopolysaccharide-protein chains on the external surface of the bacterial outer membrane. They are heat stable, alcohol resistant, and hydrophilic which enables the bacteria to form stable suspensions in saline solutions.54 In S. enterica, 46 types of O antigens are present, which differ in sugar composition and in linkages between sugars and O units.21 Flagellar (H) Antigens -- This type represents the determinant groups in the flagellar protein. They are heat and alcohol-labile proteins, and individual Salmonella strains may produce one (monophasic) or two (diphasic) sets of flagellar antigens. Most serovars alternately express two sets of antigens, i.e., phase 1 and phase 2 antigens.23 Surface (Envelope) Antigens -- This type is commonly observed in other genera of enteric bacteria (e.g., Escherichia coli and Klebsiella) and may be found in some Salmonella serovars. A well known surface antigen, the Vi antigen, is heat labile occurring in only three Salmonella serovars: Typhi, Paratyphi C, and Dublin.54 All Salmonella serotypes are considered potentially pathogenic. Some serotypes are host- specific, but the many can affect different hosts. The known serotypes of Salmonella may be grouped depending on the host range such as:53 Those highly adapted to human hosts -- This group includes S. typhi and S. paratyphi types A, B, and C which are pathogenic only in humans. Those adapted to animal hosts -- This group includes two common strains, S. dublin and S. choleraesuis, which also cause disease in humans. Those unadapted to specific hosts -- This group constitutes S. enteritidis and includes > 2000 serotypes that cause gastroenteritis. They account for 85 percent of all Salmonella infections in the U.S. S. enterica Serovars S. enterica serovars cause intestinal diseases and represent more than 99.5 percent of the Salmonella serotypes isolated from humans and other warm-blooded animals. The three main serovars of S. enterica are:54, 51 S. enterica serovar Typhi (S. typhi) -- This bacterium is the causative agent of typhoid fever. It is not widespread in the U.S. but is very common in developing countries. It can only infect humans and no other host has been identified. S. enterica serovar Typhimurium (S. typhimurium) -- This Salmonella species is one of the most common causes of foodborne illnesses in the U.S. It causes a typhoid-like disease in mice and does not cause as severe a disease in humans as S. typhi. S. enterica serovar Enteritidis (S. enteritidis) -- This bacterium is the most common cause of foodborne illness in the U.S. It usually infects chicken flocks, spreads from hen to hen, and rapidly transmits through the food chain causing the disease in humans. This foodborne disease is almost identical to that of S. typhimurium which is very closely related. Back to top Natural Reservoirs and Transmission Salmonella is a zoonotic pathogen and is widespread in humans and animals worldwide. The serovars of Salmonella can be found predominantly in one particular host, can be ubiquitous or can have an unknown habitat. For example, S. typhi and paratyphi are strictly human pathogens while all other non-typhoid Salmonella species (Salmonella enterica) are ubiquitous in the environment and reside in the intestinal tracts of animals.54 The pathogen has large and varied animal reservoirs, the most common are chickens, turkeys, pigs, and cows. Many domestic animals (e.g. ducks, dogs, cats, pet turtles), birds, reptiles, flies, and rats are also potential sources.65 Imported birds and animals may also serve to introduce different Salmonella species to the local area resulting in an increase in its prevalence. 2 Salmonella exists in human and animal carrier states. Approximately 3 percent of persons infected with S. typhi and less than 1 percent of non-typhoidal cases become chronic carriers of Salmonella. The carrier state may last from many weeks to years; however, many humans and animals just serve as reservoirs and passive carriers of Salmonella without showing symptoms of the disease.32, 27 Salmonella species are often found in aquatic environments: sewage, freshwater, marine coastal water, and groundwater. Contaminated water is the most common source of S. typhi. The pathogen can survive for long periods in natural waters, and the persistence of epidemic Salmonella strains (e.g. S. typhi, S. typhimurium) is of great concern to public health.3 Modes of Transmission Fecal-Oral -- The most common mode of transmission of Salmonella strains is through ingestion of contaminated food or water. Contamination comes from animal and human feces that contact the food during processing or harvesting.22 S. enteritidis and S. typhimurium are transmitted by this route through foods such as eggs, meats and dairy products. Animal foods that are not thoroughly cooked, and fruits and vegetables that are not thoroughly washed are also found to be vehicles of transmission.55 S. typhi and S. paratyphi are mainly transmitted by fecally contaminated water. For example, the fertilization of crops with untreated sludge or sewage effluents transmits the pathogen. In addition, shellfish harvested from contaminated waters are also a common source of Salmonella.33, 30 Person-to-Person -- This mode of transmission occurs when a infected persons do not thoroughly wash their hands after using the toilet. For example, infected food handlers and health care providers may contaminate food during preparation, or while feeding a patient, if their hands have not been washed thoroughly.65 The epidemiology of typhoid fever primarily involves person-to-person spread because the associated organisms lack an animal reservoir. In contrast, non-typhoidal Salmonella have enormous animal reservoirs and transmit through other modes. Animal-to-Animal -- Contact with newly acquired farm animals, the use of contaminated food and water sources, and pastureland at the farm facilitates this type of transmission. The stress and overcrowded conditions associated with the transport of animals to the slaughterhouse increase the shed and spread of bacteria.25 In addition, cross infection at the abattoir leads to widespread occurrence of Salmonella in animals and subsequently in meats. The infected animals on the farm may be only 0.5 percent, but this may increase to 35 percent after 2 to 5 days in the abbatoir.41 Animal-to-Human -- Salmonella can be acquired directly from pets (e.g. cats and dogs), reptiles, and birds. The feces of pets, especially those with diarrhea, contain Salmonella and humans can become infected if they do not wash their hands after contact with pets or pet feces.15 The pets may suffer Salmonellosis as a reverse zoonosis, with infection transmitted from human-to-pet and subsequently back to other humans. Salmonella can also be found in healthy dogs and cats at rates of up to 36 percent and 18 percent, respectively.52 Reptiles such as turtles, lizards, and snakes harbor Salmonella and an estimated 6 percent of all sporadic human cases of Salmonella infection are associated with reptiles.52 Many chicks and young birds carry the pathogen. The bacteria are shed in the environment from infected birds through nasal or ocular secretions, fecal materials, and feather dust; and, are transmitted to humans most frequently through the inhalation of contaminated air.2 Transmission through Poultry Production Systems Poultry is considered one of the most important Salmonella reservoirs and a prominent asymptomatic Salmonella carrier in the human food chain.47 A few percent of birds entering the poultry plant may harbor Salmonella in their intestinal tract, but after processing 30 to 35 percent may be infected. As a result, Salmonella are commonly found on egg shells, and in the contents of clean fresh eggs. Even, a high percentage of processed products such as egg powder are contaminated with Salmonella.41 Modes of Transmission through Poultry Plants Vertical Transmission -- The transovarian transmission of the pathogen from hens to eggs. It rapidly increases the Salmonella prevalence and allows cross-contamination in poultry flocks.47 Horizontal -- The direct contact of uninfected birds with infected birds, or indirect contact through contaminated drinking water and feed.47 Common Routes of Transmission Feed -- An important source of horizontal transmission if contaminated by feces, feathers, or airborne Salmonella. The feed ingredients and dust in the feed can be a main source of Salmonella contamination.35 The high risk ingredients are rapeseed meal, corn gluten meal, meat and bone meal including imported meat meal and tapioca.39 Eggborne Sources -- Eggs and egg products are important sources of vertical transmission. S. enteritidis is the primary pathogen that frequently causes egg associated human illnesses.11 The pathogen is also carried in the large intestine of the adult-laying hens and is shed in their feces leading to contamination of the egg shell after the egg is laid. In addition, contamination may also occur by horizontal transmission or by direct contamination of reproductive organs with S. enteritidis before the egg is laid. This causes the laying of contaminated eggs and the hatching of infected chicks.47 Other Sources -- Numerous potential sources of Salmonella exist in the commercial laying house environment. Egg belts, egg collectors, ventilation fans, and flush water have been identified as sources of contamination. The presence of mice also increases the spread of the pathogen.47 Back to top Mechanism of Infection Salmonella infection most commonly begins with the ingestion of contaminated food or water and can cause illness ranging from gastroenteritis to typhoid fever.46 The severity of illness in infected individuals is primarily determined by the virulence mechanisms of the infecting strain. Pathogenic Salmonella serotypes possess several virulence factors which include:45 Acid Tolerance -- ability to survive the pH of the stomach Cell Adhesion and Invasion -- ability to attach and invade cells Defense Mechanisms -- ability to defend against host's response to attack Intracellular Replication -- ability to replicate intracellularly Toxin Elaboration -- ability to produce toxins After ingestion, Salmonella bacteria exhibit an adaptive acid tolerance response that enables them to survive their passage through the acidic pH environment of the stomach. When they reach the intestine, they attach to specialized epithelial cells (M cells) of the Peyer's patches by means of fimbriae.68 This results in the bacterial colonization of the lower intestine (ileum and cecum). Salmonella bacteria then invade host cells by a process known as bacterial-mediated endocytosis which is distinct from receptor-mediated endocytosis, a process by which many other pathogens enter host cells.45 This process induces host cell membrane ruffling and is dependent on the rearrangement of the host cell cytoskeleton, and involves an increase in cellular inositol phosphate and calcium levels. The membrane ruffles non-specifically engulf the bacteria and internalize them into the cell by macropinocytosis.26 This is an example of signal transduction where molecules secreted by the invasive microorganism lead to profound structural changes in the targeted host cells.37 Attachment and invasion are under distinct genetic control and involve multiple genes in both chromosomes and plasmids.23 Depending on the invading strain and associated virulence factors, the infection process after invasion commonly takes place in the following two ways: Gastroenteritis Typhoid Fever Pathogenesis of Gastroenteritis (non-typhoidal strains) In addition to the invasion of the intestinal epithelial barrier, S. enteriditis and S. typhimurium induce a secretory response in the intestinal epithelium and initiate recruitment and transmigration of neutrophils into the intestinal lumen.45 This causes epithelial cells to synthesize and release several proinflammatory cytokines, including interleukin-1 (IL-1), interleukin-6 (IL-6), interleukin-8 (IL-8), which evoke an acute inflammatory response leading to intestinal fluid secretion and diarrhea.36, 31 Depending on the serotype and the effectiveness of the host defense, some bacteria may also spread to the liver, spleen, gallbladder, or central nervous system. However, the nontyphoid serovars are killed promptly in extraintestinal sites due to lack of human-specific virulence factors. Therefore, the most common nontyphoid Salmonella infection, gastroenteritis, remains confined to the intestine.46 Pathogenesis of Typhoid Fever (typhoidal strains) Following invasion of the intestinal epithelium, S. typhi and S. paratyphi enter macrophages by macropinocytosis, and subsequently activate virulence mechanisms that evade microbicidal functions of the macrophages. This permits pathogen survival and replication in the intracellular environment.45 The infected macrophages (with bacteria inside them) spread to the mesenteric lymph nodes and throughout the body via systemic circulation. They are then taken up by the reticuloendothelial system which confine and control the spread of the organism. However the typhi serotype may be released into the blood stream and other organs including the spleen, liver, gallbladder, kidneys and central nervous system resulting in bacteremia and clinical symptoms of typhoid.46 S. paratyphi can also cause enteric fever but severity of disease is less than that caused by S. typhi.40 Toxins (non-typhoidal strains and typhoidal strains) Both typhoidal and non-typhoidal Salmonella strains may produce both a thermolabile enterotoxin and a cytotoxin that affect the organism's ability to cause disease. The enterotoxin is released into the intestinal lumen resulting in the loss of intestinal fluids while the cytotoxin inhibits protein synthesis.19 Both of these toxins are presumed to play a role in the diarrheal symptoms of Salmonellosis.54 Back to top Antimicrobial Resistance The emergence and spread of antimicrobial-resistant Salmonella strains, particularly those that are resistant to multiple antimicrobial drugs (multidrug-resistant or MDR), have become a public health issue worldwide.1, 43 Antimicrobial resistance in Salmonella results in an additional ~30,000 infections in the U.S. annually leading to about 300 hospitalizations and 10 deaths. The death rate of persons with MDR infections was reported to be ten times higher than the general population.66 Of the ten serotypes most commonly isolated from human infections in the U.S., as reported by the Centers for Disease Control and Prevention (CDC), eight serotypes include at least some isolates that are resistant to five or more antimicrobial drugs.1 The most common MDR Salmonella serotypes are: Typhimurium, Heidelberg, and Newport.44 The two main factors which lead to the emergence and spread of antimicrobial resistance are: Genetic Elements Use/Misuse of Antimicrobials Genetic Elements Antimicrobial resistance genes confer resistance to antibiotics or disinfectants. These genes are found on two genetics elements in bacteria: plasmids and integrons. Plasmids -- The resistance genes associated with plasmids confer antibiotic resistance to beta-lactams, aminoglycosides, tetracyclines, sulfonamides, and trimethoprim and have been found on different plasmid types. Many of these plasmids also carry multiple antibiotic resistance genes that are transferable to other Salmonella strains and bacterial species.1 Integrons -- The resistance genes associated with integrons confer resistance to several antibiotics and disinfectants such as aminoglycosides, chloramphenicol, beta-lactams, macrolides, quaternary ammonium, and trimethoprim. An integron itself is not mobile but it is transferred in the presence of mobile plasmids and is found in multiple Salmonella serotypes.23 Use and Misuse of Antimicrobials Antimicrobials are commonly used and misused in the following ways:8 Treatment of microbial infections in humans, plants, and animals Prophylactic drug regimens in healthy humans, plants, and animals Enhancement of growth rate and feed conversion in food animals These types of uses and misuses result in MDR strains because they exert a selective pressure (survival of the fittest) on Salmonella bacteria populations. Bacteria that cannot resist die and those that survive pass on the resistance gene to the next generation. The transmission of the resistance gene over generations leads to increased resistance over time. The effective control and surveillance of MDR Salmonella strains are required to minimize the health risks in the population worldwide. This can be achieved by: Preventing transmission of resistant bacteria and resistance determinants from animal to humans Using antibiotics in food animals and humans in a prudent manner Educating farmers and food handlers in the principles of safe food production and handling Following good husbandry, hygiene, and abattoir practices at all stages in the food production chain For more information on the control and surveillance of antimicrobial-resistant bacteria, please view the report from Joint FAO/OIE/WHO Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance. Back to top Detection Methods Methods for the isolation and identification of Salmonella in food samples are categorized into two types: Conventional Methods Rapid Methods Conventional Methods Conventional methods for Salmonella detection require up to five days and are based on the cultural, biochemical, and serological properties of Salmonella.5, 67 The procedures for conventional methods are available from several regulatory bodies including the Food and Drug administration (FDA), United Sates Department of Agriculture (USDA), and Association of Official Analytical Chemists (AOAC). Standard conventional methods consist of five distinct steps: Non-Selective Enrichment (Pre-enrichment) --Pre-enrichment in a non-selective broth medium is done for recovery of stressed or sublethally injured Salmonella which may arise from exposure to heat, freezing, desiccation, preservatives, high osmotic pressure or wide temperature fluctuations in food processing operations. This step allows for the proliferation of Salmonella to detectable levels. The most common pre-enrichment broths are lactose and brilliant green. 33, 42 Selective Enrichment -- Selective enrichment involves the inoculation of pre-enrichment culture into enrichment broths. Enrichment broths recommended for Salmonella a include tetrathionate brilliant green (TBG) and selenite cystine (SC). This step facilitates the recovery of Salmonella on plating media while inhibiting the growth of competitive microorganisms.33, 42 Selective Plating -- Selective plating of enrichment cultures onto selective agar media is done for the presumptive identification of Salmonella colonies on the basis of distinct biochemical reactions. Plating to highly selective media also allows for the development of discrete Salmonella colonies while inhibiting the growth of other bacteria. Standard plating media include brilliant green (BGA), brilliant green sulfa (BGS), xylose-lysine-desoxycholate (XLD), and Hektoen enteric (HE) agars. These media indicate acid production from lactose and/or sucrose utilization through color change. Bismuth sulfite (BSA) is another highly selective medium on which Salmonella typically produce hydrogen sulfide and appear as charcoal black colonies.37 Biochemical Screening -- Biochemical screening involves a series of biochemical tests for further confirmation of presumptive Salmonella colonies. Typical Salmonella colonies have the following characteristics which are used in biochemical screening:67 Produce acid from glucose but not from lactose or sucrose in triple sugar iron (TSI) agar medium. Decarboxylate lysine to cadaverine (alkaline product) in lysine iron agar (LIA) medium. Generate hydrogen sulfide in TSI agar and LIA. Do not ferment lactose or sucrose in XLD and HE. The inability of Salmonella to hydrolyze urea, produce indole from tryptophan, and to grow in potassium cyanide broth are also useful in biochemical characterization.67 Serological Identification/Confirmation -- Serological identification is done for the confirmation of colonies biochemically suspected of being Salmonella. The step involves the reaction of somatic (O) and flagellar (H) polyvalent and single-grouping antisera with the suspected isolates. Mixing Salmonella cells with H antisera gives a characteristic pattern of agglutination (Salmonella are loosely attached to each other by their flagella and can be dissociated by shaking).54 In contrast, the reaction of Salmonella cells with O antisera may not result in agglutination because surface antigens may mask O antigens. Therefore, thermal solubilization of surface antigens is necessary for serological confirmation of O antigens by agglutination.34, 23 Rapid Methods Rapid methods for Salmonella detection in foods offer detection times as low as 18 hours, and are more convenient and less labor-intensive than conventional methods. Extensive research has resulted in the development of many commercially available rapid methods based on the following techniques and methodologies:37, 48 Colorimetric and fluorometric enzyme-linked immunosorbent assays (ELISA) DNA probe hybridization Immunoimmobilization of motile Salmonella Latex agglutination Polymerase chain reaction (PCR) Salmonella -specific phages Although rapid methods require less time than traditional culture procedures, they are currently used as a screening tool only. Standard cultural, serological, and biochemical methods are still in use for definitive identification of Salmonella serotypes. Research continues to develop specific, rapid, and reliable methods to detect Salmonella serotypes.42 Back to top Salmonellosis Salmonellosis is a foodborne bacterial disease caused bySalmonella. The disease is widespread and human infections vary depending upon the following:54 Serovar Strain Host status Infectious dose Nature of the contaminated food The infectious dose depends upon the host status (age and health) and the strain type.28 Studies involving healthy human volunteers indicated that a median dose of 1 million bacteria is required to produce a disease.46 However, infection may result from ingesting as low as fifteen to twenty cells depending on the strain virulence and the host health status.28, 54 Susceptible populations are at a higher risk of acquiring Salmonella infections than healthy adults. These include:55 Infants and young children Pregnant women and their unborn babies Elderly people People with weakened immune systems (such as those with HIV/AIDS, cancer, diabetes, kidney disease, and transplant patients) Salmonellosis occurs as one of the three different forms of illness: gastroenteritis, typhoid (enteric) fever, and bacteremia. Gastroenteritis -- Infection with non-typhoidal Salmonella usually causes gastroenteritis similar to that caused by other bacterial enteric pathogens. The incubation period is 6 to 48 hours after ingestion of contaminated food or water. Symptoms include:46, 68 Fever* and chills Nausea and vomiting Headache and Myalgia Abdominal cramping and diarrhea** *Fever generally resolves within 48 hours. ** Diarrhea is typically self-limiting, lasting 3 to 7 days and is rarely bloody. Typhoid (enteric) Fever -- Infection with S. typhi usually causes typhoid fever. The incubation period ranges from 5 to 21 days following infection through contaminated water or animal products or contact with an infected person or carrier.38 The duration of the illness is about 4 to 6 weeks and common symptoms include:46, 40 Fever Headache Generalized aches and pains Anorexia Weakness Mental confusion Sore throat Malaise Abdominal pain Constipation or pea soup diarrhea People with typhoid fever usually have a sustained fever as high as 103oF to 104oF (39oC to 40oC). In some cases severe symptoms may also occur which include: 38 Rose spots -- Appearance of slightly raised, rose-colored spots on the upper chest Bradycardia -- Slowing of heartbeat Hepatosplenomegaly -- Enlargement of liver and spleen Bacteremia -- This form of illness typically affects susceptible populations which are at a higher risk of developing serious complications. It occurs when Salmonella enters the blood stream and circulates through the body. Common symptoms include:38, 46 Prolonged or recurrent fever Meningitis Sepsis Focal infections Complications of Salmonella Infections In healthy individuals Salmonella infections are self-limiting and non-fatal as opposed to susceptible populations where infections can be dangerous and lead to fatal outcomes. Some of the complications that occur in susceptible populations may include:38, 17 Reiter's Syndrome -- An inflammatory condition that can lead to chronic arthritis. It is characterized by eye irritation, painful urination, and inflammation of joints. Meningitis -- An infection of the tissues surrounding the brain and spinal cord. Septicemia -- An infection of the bloodstream. Endocarditis -- The inflammation of the heart lining or valves. Osteomyelitis -- An infection of the bones or bone marrow. Treatment of Salmonellosis In healthy people Salmonella infections usually resolve in 5 to 7 days and do not require any specific treatment other than oral fluids. Since antibiotic treatments may increase the risk of becoming a carrier, they are not routinely used to treat uncomplicated non-typhoidal Salmonella gastroenteritis.15, 68 However, in people with weakened immune systems and in cases of typhoid fever, the infection can be severe and fatal; therefore treatment is essential. The treatment options include:38 Fluid replacement -- Minerals such as sodium, potassium and calcium that maintain the balance of fluids are lost in persistent diarrhea and need to be replaced. This can be done either by drinking lots of liquids or receiving fluids intravenously in cases of serious fluid loss. This will help in rehydration and proper functioning of the body. Diet restrictions -- Milk products should be avoided to reduce abdominal pains and stomach-soothing foods such as bananas, rice, applesauce and toast should be substituted for other foods. Antibiotics -- These are administered only if the infection spreads from the intestine to other body parts. The duration of antibiotic treatments vary depending on the form of illness, and range from 14 days for enteric fever to six weeks for bacteremia. The antibiotics include: Ciprofloxacin (Cipro) Sulfamethoxazole and trimethoprim combination (Bactrim) Ceftriaxone (Rocephin) Amoxicillin (Amoxil) Physicians should be aware that antibiotic resistance is increasingly reported in various Salmonella strains and those patients who are prescribed antibiotics are at higher risk for acquiring antimicrobial-resistant Salmonellosis.17 Antidiarrheals -- These medications alleviate diarrhea by slowing down intestinal movements and increasing fluid absorption. These drugs include loperamide, bismuth subsalicylate, and diphenoxylate. Vaccination against Typhoid Fever -- For those traveling to developing nations, vaccines are now available to reduce the risk of typhoid fever. For more information about these vaccines, please visit CDC -- Getting Vaccinated. Prevention of Salmonellosis The CDC has guidelines, What can a person do to prevent Salmonellosis, for both the general population and high risk individuals in order to prevent Salmonellosis. For additional information to prevent typhoid fever, please visit CDC -- How can you Avoid Typhoid Fever. The USDA Food Safety and Inspection Service (FSIS) has developed a Salmonella Question and Answer: How Can Consumers Prevent Salmonellosis? Salmonella Contamination in Foods Salmonella may be associated with all kinds of foods. Foods that have been reported as vehicles of Salmonella infection are:28 Raw meats, poultry, and eggs Milk and dairy products Fish, shrimp, and frog legs Yeast, coconut, cake mixes, dried gelatin, cocoa, and chocolate Cream-filled desserts and toppings Peanut butter and peanut paste Sauces and salad dressings Raw fruits and vegetables Since the intestine is the natural habitat of Salmonella serovars, raw animal foods are the common Salmonella sources. These include poultry, eggs, egg products, meat, meat products, and unpasteurized milk or dairy products. However, in recent years Salmonella has also been associated with raw fruits and vegetables such as cantaloupes, tomatoes and alfalfa sprouts. Raw plant foods may also be contaminated with Salmonella when fertilized with untreated sludge or irrigated and washed with contaminated water. Salmonella can occur in other foods as a result of cross-contamination with raw foods or contamination from humans, animals, birds, or reptiles. For example, it has been found in dry and dehydrated foods (e.g., cocoa, chocolate, dry milk, spices, and cereal products) and in acid food products (e.g., non-pasteurized orange juice). Back to top Foodborne Disease Outbreaks An estimated 96 percent of all Salmonella cases are caused by foods. A wide range of foods has been implicated in foodborne Salmonella outbreaks. Several of the large outbreaks that have recently occurred were associated with dairy products, fruits, and vegetables.27 Of the many sectors within the meat industry, poultry and eggs remain predominant vehicles of Salmonella infection in many countries. Egg-associated Salmonella serotype (S. enteritidis) is responsible for the largest number of outbreaks and cases in the U.S.12 Between 1993 and 1999, an average of 80 percent of confirmed S. enteritidis outbreaks in the U.S. were reported to be egg-associated.9 In Europe, 68.2 percent of S. enteritidis outbreaks were traced to egg and egg products.27 The lists of national and international outbreaks summarized below, demonstrate that several Salmonella serovars can be associated with a wide range of foods worldwide. Selected Foodborne Outbreaks in North America The following list of national outbreaks indicates that Salmonella serotypes are not confined to a particular food group but are widespread in variety of foods including milk and dairy products, fruits and vegetables, eggs, and meat. The contamination of these foods directly with Salmonella or cross-contamination on the farm, at processing plants and distribution systems have resulted in several Salmonella outbreaks in the past two decades. 2009 U.S. Ongoing Peanut Butter (Ingredient driven) Outbreak 16 Contaminated peanut butter and peanut paste and all products manufactured from them Serovar was S. typhimurium Resulted in 691 confirmed cases and 9 deaths (as of March 17, 2009) Contamination occurred at the processing plant 2008 U.S. Raw Jalapeno and Serrano Pepper Outbreak 13 Contaminated Mexican-grown raw jalapeno and serrano peppers were the confirmed sources, initially tomatoes were suspected Serovar was S. saintpaul Resulted in 1,400 confirmed cases Contamination source was irrigation water on the farm 2007 U.S. Veggie Booty Outbreak 18 Contaminated Veggie Bootie Serovar was S. wandsworth Resulted in 65 confirmed cases Contamination was due to contaminated seasoning mix used in Veggie Booty 2001 U.S. Tuna Salad Outbreak 23 Contaminated tuna salad Serovar was S. enteritidis Resulted in 688 confirmed cases Contamination was due to contaminated hard boiled eggs in tuna salad 1999 U.S. and Canada Orange Juice Outbreak 37 Contaminated orange juice Serovar was S. muenchen Resulted in more than 200 confirmed cases Contamination was due to distribution of unpasteurized juice 1997 U.S. Stuffed Ham Outbreak 37 Contaminated stuffed hams Serovar was S. heidelberg Resulted in 746 confirmed cases and one death Contamination was due to bulk cooking and cooling of stuffed hams under inadequate time and temperature conditions. 1994 U.S. Ice cream Outbreak 23 Contaminated ice cream Serovar was S. enteritidis PT8 Resulted in 740 confirmed cases Contamination was due to transportation of pasteurized ice cream mix in an unsanitized truck that had previously carried raw eggs (cross-contamination) 1985 U.S. Pasteurized Fluid Milk Outbreak 37 Contaminated pasteurized milk Serovar was S. typhimurium Resulted in 16,284 confirmed cases and 7 deaths Contamination was due to seemingly (never ascertained) faulty cross-connections between raw and pasteurized milk lines (cross-contamination) 1984 Canada Cheddar Cheese Outbreak 23 Contaminated cheddar cheese Serovar was S. typhimurium PT 10 Resulted in 2,700 confirmed cases Contamination was due to mixing of raw and pasteurized milk (cross-contamination) in the cheese plant For additional foodborne outbreak information and statistics in the U.S., visit Foodnet -- Foodborne Diseases Active Surveillance Network. Selected International Foodborne Outbreaks The following list of international outbreaks indicates that eggs are the prominent food vehicles of Salmonella. In addition, imported seeds and spices have also been implicated as the source in some outbreaks. 2003 England, Wales, and Scotland Egg Sandwich Outbreak 20, 23 Contaminated pre-packed egg and mayonnaise sandwiches Serovar was S. bareilly Resulted in more than 186 confirmed cases Contamination was due to eggs and raw egg mayonnaise 2002 Spain Custard-filled Pastry Outbreak 23 Contaminated pastries filled with vanilla cream Serovar was S. enteritidis PT6 Resulted in 1,435 confirmed cases Contamination was due to cross-contamination of the bakery supply by fresh shell eggs 2001 Norway and Sweden Fish Outbreak 23 Contaminated fish gratin Serovar was S. livingstone Resulted in 60 confirmed cases and 3 deaths Contamination was due to egg powder ingredient used for the fish gratin 1994 Finland and Sweden Alfaalfa Sprouts Outbreak 37 Contaminated alfalfa sprouts Serovar was S. bovismorbificans Resulted in 492 confirmed cases Contamination was due to seeds imported from Australia 1993 Germany Paprika Chips Outbreak 23 Contaminated potato chips with paprika as one of the ingredients Serovars were S. saintpaul, S. aviana, and S. rubislaw Resulted in more than 670 confirmed cases Contamination was due to paprika imported from South America For additional international foodborne outbreak information, visit the Program for Monitoring Emerging Diseases of the International Society of Infectious Disease. Back to top Research at the USDA Agricultural Research Service The USDA Agricultural Research Service (ARS) is actively involved in food safety research related to Salmonella under the National Food Safety Program 108. This research program provides the means to ensure that the food supply is safe and secure for consumers and that food and feed meet foreign and domestic regulatory requirements. The following ARS research units conduct research on Salmonella: Pre-Harvest Food Safety and Enteric Diseases Research Unit Livestock Behavior Research Unit Food Safety Intervention Technologies Research Unit Produce Safety and Microbiology Research Unit Bacterial Epidemiology and Antimicrobial Resistance Research Unit Egg Safety and Quality Research Unit Food and Feed Safety Research Unit Environmental Microbial and Food Safety Laboratory Southeast Watershed Research Laboratory Some of the Salmonella research projects being conducted at these ARS units are: Molecular Analysis of Salmonella Virulence, Antibiotic Resistance, and Host Response Location: Pre-Harvest Food Safety and Enteric Diseases Research Unit Project Objectives59 Investigate the molecular mechanisms that coordinate virulence and antibiotic resistance in Salmonella obtained from cattle (DT104 and S. dublin) and swine (DT104 and S. choleraesuis). Characterize the molecular mechanisms involved in Salmonella survival, colonization and pathogenicity in relation to various host (swine and cattle) factors such as stress, gastric pH, and protozoa. Investigate the molecular basis for swine resistance to Salmonella colonization by characterizing the immunological aspects of infection. Accomplishments59 Determined that key immune response system (NFkappaB) is suppressed during infection of pig by Salmonella. This suppression may provide a strategy for S. typhimurium to evade a strong immune response by the pig. Suggested that this immune evasion could contribute to the ability of S. typhimurium to establish a subclinical (carrier) infection in the pig. Identified a potential mechanism by which S. typhimurium eludes a strong inflammatory response to establish a carrier status in swine via suppression of the NFkappaB immune response system in antigen presenting cells. Handling and Transport Stress Interactions with Pathogen Biology in Swine and Cattle Location: Livestock Behavior Research Unit Project Objectives57 Identify physiological, immunological, endocrinological and gastrointestinal- microbiological alterations which occur in infected livestock when subjected to common managerial stressors. Understand how handling and transportation stress influence livestock pathogens, such as Salmonella and Campylobacter, which have the potential to detrimentally affect human health. Accomplishments57 Plasmid pAK1-lux (S. Typh-lux) used to image S. typhimurium in swine intestine. Suggested that new methods to determine the uptake or invasion by S. typhimurium are needed to understand where these pathogens colonize or hide, particularly as related to stressors associated with common management practices. Characterized photon emissions and stability properties of S. Typh-lux transformed with 2 photon generating plasmids for use in vivo biophotonic paradigms. Validated the use of pAK1-lux (S. Typh-lux) to visualize S. typhimurium trafficking using traditional plate counts correlated with photonic emissions in the duodenum, jejunum, ileum, and large intestines of pigs. Mechanism of Inactivation of Foodborne Pathogens by Alternative Food Processing Technologies Location: Food Safety Intervention Technologies Research Unit Project Objectives58 Compare mechanisms of inactivation of S. typhimurium by three non-thermal processing technologies, pulsed electric field (PEF), pulsed ultraviolet radiation (PUV) and super-critical carbon dioxide (ScCO2). Accomplishments58 The population of S. typhimurium LT-2 in early stationary phase (12 hours) decreased by 1-1.5 log after treatment with PEF. Extracted sufficient quantity of ribonucleic acid (RNA) from the samples to proceed with complementary DNA (cDNA) preparation for microarray procedure. Optimization of treatment will take place to further this study. Salmonella enterica Interactions with Fresh Produce Location: Produce Safety and Microbiology Research Unit Project Objectives62 Identification of S. enterica genes that are involved in the growth and survival of the pathogen on post-harvest lettuce at room temperature and under cold stress, and in soft rot lesions. Accomplishments62 Determination of gene expression profile of Salmonella while in soft rot lesions on leafy greens. Measured the expression of candidate genes by Quantitative Reverse Transcription Polymerase Chain Reaction (QRT-PCR). Provided evidence for the role of above pathways in the colonization of rot-affected leaves by the foodborne pathogen. The laboratory fully developed and tested all genetic tools required to identify Salmonella genes that are upregulated on cut lettuce at cold and warm temperatures. Epidemiology of Antimicrobial Resistance of Foodborne Pathogens & Other Bacterial Isolates of Animal Origin as Part of National Antimicrobial Resistance Monitoring System (NARMS) Location: Bacterial Epidemiology and Antimicrobial Resistance Research Unit Project Objectives 56 Assess the epidemiology of Salmonella in animals to determine the frequency, phenotypic and genotypic characteristics. Determine trends of resistance present in Salmonella populations. Define areas best suited for these interventions. Accomplishments 56 Speciated/serotyped over 4,000 Salmonella isolates. Tested all the serotyped Salmonella for susceptibility to a custom-made panel of antimicrobials which are important in veterinary and human medicine. Generated an annual NARMS report and posted it to the website (http://www.ars.usda.gov/Main/docs.htm?docid=6750). Continued to expand pulsed-field gel electrophoresis (PFGE) testing of Salmonella isolates as part of USDAVetNet. Mutational Analysis of Salmonella enterica in Broiler and Egg Laying Chickens Location: Egg Safety and Quality Research Unit Project Objectives60 Determine critical genetic determinants that impact the ability of S. enterica to contaminate the eggs of hens and to otherwise propagate in the poultry environment. Accomplishments60 Determined that chickens are resistant to carrying high Salmonella loads as compared to rodents. Suggested that mouse might be a host that amplifies Salmonella on farm which substantiates the importance of efforts to control rodent populations to decrease egg contamination. System Dynamics of Salmonella and Campylobacter in Chill Tank During Broiler Processing Location: Food and Feed Safety Research Unit Project Objectives63 Identify Salmonella and Campylobacter contamination levels on broiler carcasses prior to entry and after leaving the chill immersion system. Accomplishments63 Determined that cutting the broiler carcasses in half, longitudinally, and evaluating these samples before and after chill immersion, was the most effective method for determining Salmonella and Campylobacter status. The results of this project will develop a better understating of how the targeted bacteria contaminate otherwise pathogen-free carcasses entering the chill tanks, and will facilitate efforts to develop methodology to significantly prevent this contamination. Pilot Study of Factors Affecting Maintenance of Mycobacterium, Salmonella, E. coli, and Listeria on Dairy Farms Location: Environmental Microbial and Food Safety Laboratory Project Objectives61 Identify and characterize a third dairy herd to be included in a Pilot Program that currently consists of two dairy herds and which focuses on the protocol development, laboratory set-up, program logistics, and database. Determine the impact of intervention strategies on Johne's disease dynamics, milk and beef quality (particularly with respect to zoonotic bacterial pathogens), economics and sustainability on dairy farms. Validate intervention strategies to support best management practices (BMPs). Optimize intervention and monitoring strategies in the given constraints on time, labor and financial resources in modern dairy herds. Create a national resource bank (data and biological specimens on well-characterized animals) for current and future monitoring and research on dairy cattle diseases. Accomplishments61 Sample collection continued according to the approved protocol. Farm surveys were completed within required time frame and samples were obtained and distributed as required. Identified cull cows as supershedders of Mycobacterium avium subsp. paratuberculosis (MAP) Collected additional environmental and fecal samples to document the effect of the supershedders elimination on the environmental load of MAP. Watershed Scale Transport of Salmonella, Campylobacter and Indicator Organisms in the Satilla River Basin Location: Southeast Watershed Research Laboratory Project Objectives64 Determine the effects of land use and waste water treatment facilities on pathogen and indicator organism transport in a Coastal Plain River Basin (Satilla River Basin). Determine if pathogens are associated with specific animal productions systems such as beef cattle or poultry houses. Determine if pathogens are associated with processing wastewater and whether they are effectively killed by wastewater treatment. Accomplishments64 Monthly sampling for pathogens, indicator organisms, and water chemistry parameters has been continued. Developed robust techniques to identify Campylobacter species through polymerase chain reaction (PCR) techniques. Compared PCR techniques to plating and selective media techniques. Sampling of runoff from fields and pastures showed the presence of pathogens. Storm flow sampling of watershed streams has confirmed the presence of pathogens. FSRIO Research Projects Database For additional USDA Salmonella Research Projects, please visit the FSRIO Research Projects Database. For additional Salmonella research projects conducted by other U.S. government and International agencies, please search the FSRIO Research Projects Database. Back to top References 1. Alcaine, S.D., L.D. Warnick, and M. Wiedmann. 2007. Antimicrobial Resistance in Nontyphoidal Salmonella. J. Food Prot. 70: 780-790. Abstract Retrieved February 22, 2009, from http://www.ncbi.nlm.nih.gov/pubmed/17388077. 2. Avian Biotech International. 2009. Salmonella. 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USDA Agricultural Research Service. 2009. Annual Report 2008: Mechanism of Inactivation of Foodborne Pathogens by Alternative Food Processing Technologies. Retrieved March 8, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=412432&showpars=true&fy=2008. 59. USDA Agricultural Research Service. 2009. Annual Report 2008: Molecular Analysis of Salmonella Virulence, Antibiotic Resistance, and Host Response. Retrieved March 8, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=409771&showpars=true&fy=2008. 60. USDA Agricultural Research Service. 2009. Annual Report 2008: Mutational Analysis of Salmonella enterica in Broiler and Egg Laying Chickens. Retrieved March 9, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=411676&showpars=true&fy=2008. 61. USDA Agricultural Research Service. 2009. Annual Report 2008: Pilot Study of Factors Affecting Maintenance of Mycobacterium, Salmonella, E. coli, and Listeria on Dairy Farms. Retrieved March 10, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=4090238. 62. USDA Agricultural Research Service. 2009. Annual Report 2008: Salmonella enterica Interactions with Fresh Produce. Retrieved March 9, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=411125&showpars=true&fy=2008. 63. USDA Agricultural Research Service. 2009. Annual Report 2008: System dynamics of Salmonella and Campylobacter in Chill Tank during Broiler Processing. Retrieved March 10, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=411448&showpars=true&fy=2008. 64. USDA Agricultural Research Service. 2009. Annual Report 2008: Watershed Scale Transport of Salmonella, Campylobacter and Indicator Organisms in the Satilla River Basin. Retrieved March 10, 2009, from http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=411060&showpars=true&fy=2008. 65. Vermont Department of Health. 2005. Salmonella. Retrieved February 14, 2009, from http://healthvermont.gov/prevent/salmonella/Salmonella.aspx. 66. World Health Organization. 2005. Drug-resistant Salmonella. Retrieved February 4, 2009, from http://www.who.int/mediacentre/factsheets/fs139/en/. 67. Yousef, A.E. and C. Carlstrom, eds. 2003. Food Microbiology: A Laboratory Manual. Wiley-Interscience, Singapore. Preview Retrieved February 24, 2009, from http://tinyurl.com/cvl4fn. 68. Zapor, M. and D.P.Dooley. 2009. Salmonellosis. Retrieved February 2, 2009, from http://emedicine.medscape.com/article/228174-print. Back to top

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