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As of March 22, 1995, an addendum has been appended to this article.

Case 1

A herd of 50 crossbred cows and approximately 25 calves were affected by an epizootic of severe diarrhea. Initially, feces in the cows and calves were pasty and dark or bloody, and progressed over 2 to 3 days to a profuse, watery, fetid diarrhea. The affected animals became weak and recumbent, and eventually died. The epizootic persisted over a 14-day period, with 1 to 2 cases developing per day. Physical examination of several animals revealed anorexia, weight loss, moderate dehydration, nasal discharge, and various degrees of salivation. Rectal temperatures ranged from 36.7 to 40 C (98 to 104 F), and pulse and respiration rates were high. Several cows were observed to be drinking and urinating less than normal. One cow aborted a near-term fetus. Nine of 13 affected cows died and 1 of 4 affected calves died. Necropsies were performed on 6 cows and the calf. Consistent lesions of fibrinous hemorrhagic enterocolitis and multifocal necrotizing hepatitis were observed. A few animals had renal infarcts and nephrosis. Salmonella serogroup B was isolated from the intestinal contents of 4 of the 6 animals necropsied. The Salmonella organism was serotyped at the National Veterinary Services Laboratory as Salmonella subspecies I serotype typhimurium.

Specimens of water from a pond, water troughs, standing water around the troughs, a sink hole, and salt in a mineral feeder were obtained for culture of Salmonella. The bacterium was only isolated from the water around the watering trough.

A source of infection was not identified in the farm history. There had been no herd additions during the preceding year. There was, however, a history of mixing a bag of sour-smelling bone meal in the trace mineral salt, which was fed to the cows a week before the epizootic.

A definitive diagnosis of salmonellosis was made on the basis of multiple isolations of the same Salmonella serotype from 4 animals and environmental samplings, along with the compatible signs and lesions observed in the affected animals.

The owner and veterinary students asked the following questions of the attending clinician.

Q: Why did the first microbiology laboratory report the organism to be Salmonella serogroup B and then later report the organism to be Salmonella subspecies I serotype typhimurium?

A: There is much controversy over the nomenclature and classification of Salmonella. Studies have demonstrated that most strains of the group are highly related evolutionarily, and all strains are believed to belong to a single species. As a result of DNA studies, it has been suggested that salmonellae belong to a single species, S enterica.¹ Currently, there are 6 subgroups within the genus Salmonella. Salmonella subgroup I includes obligate parasites and pathogens of warm-blooded animals, including human beings. These salmonellae are most often associated with human and domestic animal disease. Subgroup II, subgroup IIIa, and subgroup IIIb are strains isolated from the environment and from cold-blooded animals and may cause disease in human beings. Subgroup IV and subgroup V also are isolated from the environment and cold-blooded animals but rarely are pathogenic to human beings.^2,3 The practice of using "species" names for well-known Salmonella serotypes is well accepted. For example, reporting an isolate as Salmonella typhimurium, rather than Salmonella subspecies I serotype typhimurium, provides the essential clinical and epidemiologic data. This type of terminology will be used in response to your subsequent questions.⁴

Most laboratories can isolate Salmonella, but identification of Salmonella requires many antisera, which can be expensive. Because of the time and expense of serotyping, many laboratories send isolates to reference laboratories in the United States for typing. It has been estimated that there are some 2,000 Salmonella serovars (serotypes), these serovars being identified by a series of agglutination reactions. Specific serovars are identified by the agglutination reactions of their heat-stable somatic O antigens and heat-labile flagellar H antigens. Most laboratories have kits to group salmonellae according to the O antigens. There are 4 major groups: B, C, D, and E.⁵ The Salmonella first identified was in serogroup B and was sent to a reference laboratory for further serotyping.

The initial grouping of Salmonella is generally more important microbiologically than epidemiologically because this helps direct which group antisera should be used for serotyping. Serotyping of the Salmonella involved in an individual or a herd is important in assessing the prognosis, because some serotypes are more pathogenic than others in the various species infected. Along with serotyping, it is helpful for epidemiologic investigations to subtype Salmonella further by antibiotic-susceptibility testing, biochemical reactions, phage typing, and plasmid analysis.⁶

Q: Could I acquire salmonellosis from the affected animals and, if so, how?

A: Yes. All Salmonella infections, except those caused by Salmonella typhi and paratyphi A and paratyphi C, are considered zoonoses. Salmonella typhi and paratyphi A and paratyphi C, which cause typhoid fever or enteric fever, are species specific to human beings and do not have a reservoir cycle in animals.⁷ Human and animal Salmonella infections are acquired by oral consumption of feces containing Salmonella or feedstuffs contaminated with Salmonella organisms.⁷ Salmonella epizootics in domestic animals usually are associated with the concentration of animals at a certain point, for example, in stockyards, breeding sheds, kennels, or catteries where high stocking densities and overcrowded facilities contribute to the spread of organisms.^8,9

In human beings, most Salmonella infections are acquired through contaminated food that has been improperly stored and/or improperly prepared and handled prior to consumption. Pork, beef, poultry, eggs, and milk products are commonly incriminated.¹⁰ Vegetables that are grown in soils fertilized or contaminated with human or animal feces containing Salmonella are a potential source of infection if not properly cleaned prior to consumption.

Pets that are in close contact with people are also a possible source of infection.¹¹ Average rates of Salmonella infections in dogs and cats surveyed from 1947 to 1965 were 14% and 2%, respectively.¹⁰ Pet tortoises and terrapins frequently have been associated with human salmonellosis, especially in children¹²; however, the frequency of salmonellosis in children 1 to 9 years old has decreased since the establishment of legislation banning the sale of pet turtles.¹³ Salmonella has been isolated from rabbits, monkeys, guinea pigs, parakeets, and snakes.¹⁰ Although Salmonella has been isolated from various pet animal species, it is difficult to assess the true risk of acquiring infection resulting in disease, because the number of organisms isolated from the various species was not reported and, more important, the infective dose is difficult to define.

To avoid infection, hands should be washed thoroughly with soap after handling animals or materials contaminated with feces, ie, clothing footwear, and animal bedding. Animals that have diarrhea should be isolated, especially from children, until well.

Q: How prevalent is salmonellosis in the human population and what are the most common serotypes in human cases?

A: The number of Salmonella isolations reported to the Centers for Disease Control (CDC) on a yearly basis has shown a general upward trend. In 1986, 42,028 isolates were reported to CDC.¹⁴ The true prevalence of infection is underestimated, however, because for every reported case in which an isolate was obtained, there are probably 50 to 100 unreported cases. It has been estimated that between 2 to 4 million Americans are infected yearly with Salmonella.¹³

Salmonella species are widespread throughout the United States, with some species being isolated more frequently in certain regions. For example, S dublin has been isolated most frequently west of the Rocky Mountains, especially in California, but an increasing number of isolates are being reported east of the Rocky Mountains.^10,15 Likewise, S enteritidis has been isolated most frequently in the Northeast, but recently, isolates have been frequently reported in the mid-Atlantic and Southern states.¹⁶

Although all Salmonella are potentially pathogenic for human beings, the 10 most frequently reported serotypes constitute approximately three quarters of all reported isolates.^14,17 The following serotypes were the most common isolates reported to CDC in the years 1984 to 1986: S typhimurium, S enteritidis, S heidelberg, S newport, S infantis, and S agona.¹⁴

Specific Salmonella serotypes have been associated with the consumption of certain foods. For example, S enteritidis is often associated with the consumption of eggs, and food containing raw eggs and S dublin is often associated with the consumption of raw milk.^16,18 Most serotypes, however, can be associated with a variety of foods. For example, in 1986, S heidelberg was isolated from lupine beans in Massachusetts, roast pork in Delaware, frozen pasta in the Northeast, and chicken in Oklahoma, Wisconsin, and Hawaii.¹⁴

Q: Were the clinical signs observed typical of Salmonella infections in animals?

A: There are 5 basic infection patterns of salmonellosis in animals. The first, primary salmonellosis, is caused by a particular Salmonella in a particular species. The Salmonella type and species involved will determine the clinical signs. Clinical infection may induce septicemia, acute enteritis, and chronic enteritis.

Septicemia develops in young and aged animals and commonly in adult horses.¹⁹ Clinical signs of septicemia include depression, prostration, high fever, and death within 24 to 48 hours after onset of clinical signs. Diarrhea may or may not develop.

Acute enteritis is the most common disease entity in adult animals infected with Salmonella. Animals will be pyrexic, anorectic, and have profuse diarrhea accompanied by dehydration, toxemia, and weight loss. Feces are putrid smelling, contain large amounts of mucus, with or without blood, and may contain fibrinous casts. Pregnant animals may abort. Without early treatment, the case fatality rate commonly is 75%. Acute enteritis may result in subsequent pneumonia and polyarthritis.¹⁰

Chronic enteritis usually succeeds an acute episode, but may develop initially. Chronic enteritis is associated with chronic weight loss as well as intermittent or persistent fever and diarrhea that may contain blood, mucus, and fibrinous casts.

The second form of salmonellosis develops in animals with concurrent disease, changes in physiologic states, and stress attributed to transport, housing, or surgery.²⁰

The third form is a chronic carrier state in which individuals who have recovered from clinical illness are normal, but excrete organisms for several weeks or months.²⁰

The fourth form is a temporary carrier state in which the organisms, having been continually picked up in the environment by means of contaminated feed or excretors housed in the same environment, are shed. This is often the form found in slaughter animals and animals coming from a stockyard or kennel.¹⁰

The fifth form is a latent infection in which organisms are isolated from the mesenteric lymph nodes of healthy animals at slaughter. This form of infection probably results from repeated ingestion of contaminated feed.²¹

Q: How does clinical salmonellosis appear in human beings?

A: In human beings, Salmonella of animal origin causes an intestinal infection characterized by sudden onset of fever, myalgia, cephalalgia, abdominal cramps, nausea, vomiting, and diarrhea.¹⁷ Blood in the feces is not commonly associated with Salmonella infections, as in animals, and bacteremia is rare.¹⁰ Dehydration and electrolyte imbalances may be severe in the young and elderly. In adults, the disease is self limiting in 2 to 4 days, with full recovery in about a week.

Salmonella infections may also induce enteric fever (bacteremia) or a septic syndrome. This may follow gastroenteritis or may be seen initially in healthy adults.¹⁷ In infants, the elderly, and immunocompromised patients, bacteremia may be transient, but does need to be treated vigorously. Any of the Salmonella may induce such infection, but S choleraesuis is the most commonly isolated serotype.¹⁷

Salmonella may also induce a localized infection in any organ or tissue of the body. This clinical syndrome may be the initial sign of Salmonella infection or may be secondary to bacteremia. Bronchopneumonia, endocarditis, pyelonephritis, osteomyelitis, arthritis, or meningitis may result from this localized infection. Many experiencing this syndrome are newborns, infants, or those having concurrent underlying disease.¹⁷

Q: Are there factors, such as age, that make animals and human beings more susceptible to Salmonella infections?

A: Neonates, old animals, and animals with concurrent infections are more susceptible to infection resulting in disease. Animals undergoing the physiologic stress of transportation, exercise, malnutrition, feed changes, pregnancy, or surgery are also more susceptible to infection resulting in clinical disease.^9,22

Infants < 1 year old and the elderly are most susceptible to infection. People taking antibiotics are also at a greater risk, because antibiotic treatment alters the normal enteric bacterial flora that serves as a protective mechanism against Salmonella infections.²³ People with debilitating disease such as chronic infections, neoplasia, hemopoietic disorders, immunoincompetence, and gastrointestinal tract disorders are also more susceptible to infection resulting in clinical disease.²⁴

Q: What is the treatment for clinical salmonellosis?

A: There is varying opinion among veterinary clinicians on how to treat clinical salmonellosis. It is agreed that oral or parenteral administration of fluids, electrolytes, and buffers is important to correct dehydration and balance electrolyte losses and acid-base abnormalities. Intestinal absorbents and protectants, such as activated charcoal and kaolin, may be helpful in some cases.^8,19,20

The use of antimicrobials in acute salmonellosis, however, is controversial. Antimicrobials do not eliminate the carrier state and may contribute to the development of antibiotic-resistant strains. Results tend to be poor if treatment is not administered until late in the disease; however, a high cure rate is obtained if the proper antimicrobial treatment is begun early.²⁰ Horses with the severe diarrheal form of salmonellosis are often treated with antimicrobials because subsequent bacteremia is common in foals and may develop in adults.¹⁹ Mortality can be as high as 50% in horses and 20 to 50% in other domestic species.^5,20

Much of the controversy regarding use of antimicrobials appears to stem from reports in the human literature that their use induces drug-resistant Salmonella and prolongs the shedding of the organism after abatement of clinical signs.^25,26 Giving antimicrobials to domestic animals has induced resistant Salmonella. However, prolonged fecal shedding of Salmonella after antimicrobial treatment of enteric disease has not been detected.²⁷

Treatment of Salmonella gastroenteritis in human beings usually is limited to the correction of dehydration and electrolyte imbalances and relief of abdominal pain. Electrolyte-rich fluids administered orally are generally all that is required, because the disease tends to be self limiting.¹⁷ Human salmonellosis caused by S typhi or S choleraesuis, however, is treated vigorously with antimicrobials and for prolonged periods as these organisms often cause septicemia.¹⁷

Infants, the elderly, and debilitated patients with severe symptoms may also warrant antimicrobial treatment along with supportive fluid treatment. Bacteremic people and people with localized infections are given antimicrobials.¹⁷

Q: Can I sell these cattle for slaughter?

A: Animals with acute enteritis should not be sent to slaughter. Clinically ill animals would be condemned on antemortem inspection and would not be allowed into the slaughtering area. These animals would also infect the environment in the holding yard. Other animals could then ingest organisms or carry them into the slaughterhouse on their haircoats and extremities, allowing for the possibility of contamination of clean carcasses.

Animals that have recovered and regained sufficient weight can be sent to slaughter. Animals would be examined antemortem and, if deemed healthy by the inspector, would be slaughtered. If no gross lesions are observed in the carcass or viscera during postmortem inspection, the carcass would be passed and graded without further inspection or testing.

Q: Where did my cattle acquire this infection?

A: Potential sources of on-farm infections include rodents, birds, contaminated water, and pasture, with the major sources being feedstuffs and infected carrier animals. The animals had been on the same pasture and had had access to the same water source for the past 3 months; no new animals had been added to the herd in the past year. In the history, a bag of sour-smelling bone meal had been mixed in the trace mineral salt. Bone, meat, fish, and feather meal are often contaminated with Salmonella organisms.^28,29 Although these products are heated and cooked during processing, they are often recontaminated after processing. These types of meals are conducive to dissemination of infectious organisms to a large population from a single source.^23,30 Unfortunately, there was no bone meal or mineral mix available for culture. Although not conclusive by any means, it was speculated that the foul-smelling bone meal was likely the source of infection.

Q: How can Salmonella be controlled in the environment?

A: Salmonella is difficult to control because of its ability to survive in the environment and because of animal carrier hosts. Salmonella is often found in water sources as a result of contamination by effluent from slaughterhouses, water treatment plants, infected animals defecating into the water supply, and runoff from manure-fertilized fields.^8,18,31 Potentially contaminated and stagnant water sources should be avoided and made inaccessible to animals. The use of fresh water free of organic material may reduce exposure to Salmonella, because it is unlikely that the organism can survive more than 3 weeks in such water, however Salmonella may remain viable for up to 9 months in pond and stagnant water.¹⁸

Management of manure should be directed to heating and drying, because Salmonella is sensitive to both of these processes.¹⁸ The bacterium, however, can remain viable on pasture in feces, and in the soil for up to 7 months.²⁰ Freezing will decrease survival, but some organisms will be viable after thawing. Salmonella-contaminated concrete areas, metal waterers, and equipment should be cleaned and then disinfected with common phenolic, chlorine, or iodine-based disinfectants.³²

Because the stress of transport will cause an increase in shedding of organisms in carrier animals, newly transported animals should be quarantined for 4 weeks after arrival to reduce the chance of exposure of organisms to resident animals and contamination of the environment.^33,34

Q: Is there a way to identify and eliminate carrier animals?

A: Identification of carrier animals is difficult because they only shed organisms periodically. Animals that recover from non-host-adapted Salmonella infections may shed the organism for a few weeks to 2 to 3 months after resolution of clinical disease.^22,27,35 Animals from which the organism is isolated after several months probably reflect recontamination from the environment rather than an active carrier state¹⁸; however, animals infected with host-adapted Salmonella, eg, S dublin in cattle and S pullorum in chickens, may remain true carriers for life.^31,36 Animals should not be considered free of infection until 3 successive attempts to isolate the organism every 14 days have failed.²⁰ In such cases, samples should be incubated in enrichment broth, eg, tetrathionate or selenite, to enhance isolation.⁴ Screening by serologic testing alone has had poor results in detecting individuals with non-host-adapted Salmonella species and variable results for host-adapted Salmonella species.^4,10,20

Case 2

Two children developed fever, chills, diarrhea, and abdominal cramps. The children were hospitalized 2 days after the onset of illness and Salmonella typhimurium was isolated from fecal specimens obtained from both children. Two days before the onset of illness, the father, who worked on a dairy farm, had brought home some raw milk, which was used to make cake frosting. The children and father ate the frosting. The father developed clinical signs similar to those of the children 20 days after the initial signs were seen in the children. Salmonella typhimurium was also isolated from the father's feces. In the preceding 4 months, there had been 5 cases of diarrhea among dairy cows on the farm where the father worked. Two of the ill cows survived, one died, and the other 2 were shipped for slaughter. Fecal specimens were obtained from 8 dairy cows and 2 calves. Salmonella typhimurium was isolated from a calf and from one of the recovered cows.³⁷

The farmer and members of the affected family asked the following questions of the local veterinarian.

Q: How does milk become contaminated with Salmonella?

A: Milk can be contaminated in a variety of ways. Cattle may excrete the organism in their milk during the febrile stage of clinical salmonellosis.²⁰ Active carriers may secrete infected milk intermittently, especially those cattle infected with S dublin and S muenster.³⁸ Both of these organisms have adapted to and colonize the bovine mammary gland. Although S typhimurium usually is not excreted in the milk, except during the febrile stage of clinical disease, it has been reported to have been persistently isolated from the milk of a healthy cow.³⁸

Milk is most likely to be contaminated by infected feces from either an animal with clinical salmonellosis or a healthy carrier animal during the milking process. Additional sources of contamination during milking are use of polluted water or dirty equipment. People who lack personal hygiene skills and have clinical salmonellosis or are chronic shedders of the organism may also contaminate milk.³⁹

Q: Could this epidemic have been prevented by pasteurizing the milk?

A: Yes. Effective pasteurization kills Salmonella in milk.²⁴ Although there have been reported epidemics of salmonellosis in Illinois; from the consumption of pasteurized milk,⁴⁰ it was speculated that the milk was contaminated after pasteurization by addition of raw milk through a faulty valve in the pipe system.⁴¹ Infected human beings handling milk, the use of contaminated water, cartons, or bottles, and reexposure of pasteurized milk to raw milk have all been associated with Salmonella epidemics resulting from ingestion of pasteurized milk.¹⁸

Q: What should I do to reduce the chances of Salmonella contaminating my milk?

A: Bulk-tank milk samples could be subjected to bacteriologic culturing for Salmonella. If Salmonella is repeatedly isolated from the tank, and improper cleaning and contaminated water have been eliminated as possible sources, testing the milk of individual cows may reveal persistent shedders and these animals should be culled. Use of feces for bacteriologic culturing is not recommended because of cost, and many intermittent shedders would be negative. Also, some animals from which Salmonella is isolated may not be true carriers but only temporary carriers. Udders should be clipped and teats thoroughly cleaned of fecal residue prior to milking. Cows suffering from clinical signs of diarrhea should be milked separately from the herd and their milk discarded. The use of water in the parlor should be kept to a minimum to reduce aerosolization of organisms and spreading of fecal material. Milkers should thoroughly wash their hands prior to milking and after using the restroom. Milkers with diarrheal disease should not milk until clinical symptoms subside.

Q: Could the Salmonella infection have come from the eggs used to make the cake?

A: It is possible, as S typhimurium infection has been associated with eggs and egg products, but baking would have killed any Salmonella, if present. Also, if Grade A shell eggs had been used, S enteritidis would have more likely been the Salmonella involved.¹⁶

Q: Are S typhimurium and S enteritidis epidemics commonly associated with eggs?

A: During the 1960s, S typhimurium infection associated with eggs was epidemic in the United States. The number of S typhimurium infections associated with eggs has been greatly reduced since establishment of the federal grading and disinfection programs in the 1970s.¹⁶

Salmonella enteritidis infection has increased nationwide, like most Salmonella infections, but in the past 12 years has increased six-fold in the northeastern United States. In the Northeast, 77% of the S enteritidis epidemics were associated with eggs or foods made with egg products.¹⁶ As is the case with most foodborne epidemics, most Salmonella epidemics are a result of improper cooking and/or improper storage and handling of the raw or cooked product.

Q: How are eggs contaminated with Salmonella?

A: For most Salmonella serotypes, eggshells are contaminated by feces containing Salmonella organisms; the organism enters the egg through cracks or shell defects.¹⁶ The risk of contamination by fecal soiling has been reduced by the currently established egg inspection, disinfecting, and grading programs.

In human beings, most Salmonella infections are acquired through consumption of animal products.⁷ The animals associated with these products often acquire their infection from contaminated animal feed. Salmonella enteritidis was not recognized in 3,000 isolates of Salmonella from animal feed, indicating that S enteritidis, unlike other Salmonella, is not primarily transmitted by fecal contamination.

Some researchers believe that Salmonella, especially S enteritidis may also be shed in the yolk of the egg prior to shell deposition, ie, transovarian transmission.⁴²

Q: How frequently are eggs contaminated with S enteritidis?

A: It is not known how frequently eggs are contaminated by S enteritidis or by any other Salmonella. The organisms may be intermittently shed into the yolk by hens colonized by Salmonella, much like intermittent shedding of organisms in milk by carrier cows.⁴²

Although the number of contaminated Grade A shell eggs is minimal, pooling eggs increases the likelihood of inclusion of a contaminated egg.⁴³ All reported cases of egg-associated S enteritidis have involved the consumption of pooled eggs.

Q: How can Salmonella infections associated with eggs be avoided in people?

A: One should avoid eating raw eggs. Eggs should be cooked thoroughly; boiled for 7 minutes, poached for 5 minutes, or fried on each side for 3 minutes. "Sunnyside" eggs may contain Salmonella because no duration of frying killed all the Salmonella organisms in experimentally infected eggs.⁴⁴ In food recipes that call for the use of raw eggs, eg, homemade ice cream, mayonnaise, and eggnog, pasteurized eggs should be substituted. Pasteurized eggs should also be used in nursing homes and hospitals because those populations are at a greater risk for death from S enteritidis infection.¹⁶ As with any foodstuff, eggs and prepared-egg foodstuffs should be stored at < 4.4 C (40 F) or > 60 C (140 F).

Case 3

Students and some employees of a school experienced an epidemic of diarrhea accompanied by nausea, vomiting, abdominal cramps, and fever. Twenty-two students and employees were hospitalized for gastroenteritis. Salmonella was isolated from 32 of 40 individuals with gastroenteritis, S heidelberg from 27, and S stanley from 5. Illness was strongly associated with eating chicken from the school cafeteria. The chicken had been thawed at room temperature the night before cooking and was cooked for 2 hours at a dial setting of 177 C (350 F). The chicken was left to cool overnight in the warm oven and was served the next day.⁴⁵

The kitchen workers and school board asked the following questions of health department staff and a veterinary food safety inspector.

Q: Isn't poultry microbiologically examined before passing meat inspection?

A: No. Microbiologic examination of poultry and red meat is not part of the routine inspection; however, limited surveys have revealed the rate of Salmonella contamination to be 35.2% in poultry, 1% in beef, and 12% in pork.⁴⁶ The differences in the rate of contamination between poultry and red meat may be a result of the methods used for microbiologic analysis. Microbiologic analysis of poultry is performed by using a whole-bird rinse, where the outside and inside of the carcass is sampled, which increases the success of isolation of the organism compared with analyzing a 25-g specimen of chopped beef or pork.⁴⁶

Q: Because poultry has the highest rate of contamination, is it responsible for most of the Salmonella epidemics associated with consumption of meat?

A: The CDC reported that from 1973 to 1984, chicken was responsible for 5% of the foodborne Salmonella epidemics, turkey for 9%, beef for 19%, pork for 7%, and dairy products for 6%.⁴⁶ It has been estimated that the number of organisms in contaminated meat is low, ie, 1/100 g. For most people, this rate of contamination is below the infective dose, although currently it is difficult to define an infective dose.⁴⁶

Q: How did the chicken become infected with Salmonella?

A: Salmonella can contaminate meat in several ways. Carrier birds, without signs of disease, entering the slaughter facility may contaminate equipment and carcasses by means of fecal leakage from the cloaca and from improper evisceration. Contamination may also occur during defeathering, from soiled feathers, and during carcass travel through the chilling tanks.¹⁰ Red meat carcasses may be contaminated by improper evisceration and soiled hair coats and manure brought into the slaughter area. Once a carcass is contaminated, organisms can be spread to other carcasses via hands, knives, and other processing equipment.

Q: Shouldn't cooking have killed the Salmonella in the chicken?

A: An internal temperature of 74 C (165 F) is needed to kill Salmonella.⁴⁵ In this case, to test the cooking process, a pan of beans was cooked in the same manner as the chicken; after 2 hours of cooking, the temperature in the middle of the pan was only 29 C (84 F), clearly not high enough to have killed the Salmonella.⁴⁵ It is important that ovens be properly functioning and that a meat thermometer be used to ensure proper cooking, especially when cooking large pieces of meat.

Meat may also be recontaminated after cooking by contacting contaminated hands, counter surfaces, or utensils that were initially contaminated by the meat prior to cooking. Uncooked foodstuffs, such as salads, may be contaminated by the contaminated meat via the same methods. It is therefore important that possibly contaminated equipment and surfaces be cleaned prior to contacting other foods.⁴⁷

Q: What measures should be taken to control and prevent foodborne Salmonella epidemics?

A: Meat, meat products, eggs, egg products, and dairy products should be stored at temperatures < 4.4 C (40 F). Prior to serving, food dishes should be stored at < 4.4 C (40 F) or > 60 C (140 F) to avoid bacterial multiplication. Frozen meat should be thawed at refrigerator temperatures (4.4 C or 40 F) and served soon after cooking. Meat that is cooked and allowed to cool should be heated to an internal temperature > 74 C (165 F) before serving.⁴⁵

Q: Can dogs and cats acquire salmonellosis through raw or undercooked contaminated meat?

A: Yes. All meat should be cooked as if being used for human consumption.¹⁰ All prepared foods for pets should be stored and cooked as previously recommended.

Discussion

Salmonellosis is an economic concern of agriculture as well as of modern society. Farmers realize an economic loss attributed to treatments, loss of productivity, and deaths caused by Salmonella. Society suffers an economic loss in lost productive days and, in some instances, cost incurred because of hospitalization.

It is difficult to estimate the risk of acquiring Salmonella infections from animals and from foods of animal origin. Many factors, such as infective dose, serotype, age, immune status, and the presence or absence of other disease states, have an influence on one's susceptibility to infection.

It is not economically feasible to produce animals free of Salmonella infection. Control of foodborne salmonellosis can be accomplished in 2 ways: reducing salmonellosis in the animal population by good animal husbandry and feeding practices and educating the public in the proper handling, preparation, and storage of food.

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22. Smith BP. Salmonella infections in horses. Compend Contin Educ Pract Vet 1981; 3:S4-S13.

23. Cohen ML, Tauxe RV. Drug resistant Salmonella in the United States: an epidemiologic prospective. Science 1986; 234:964-969.

24. Williams LP, Hobbs BC. Enterobacteriaceae infections. In Hubbert WT, ed. Diseases transmitted from animals to man. 6th ed. Springfield, Ill: Charles C Thomas, Publisher, 1975; 33-89.

25. Askeroff B, Bennet J. Effect of antibiotic therapy in acute salmonellosis on the fecal excretion of salmonellae. N Engl J Med 1969; 281:636-640.

26. Dixon JMS. Effect of antibiotic on duration of excretion of Salmonella typhimurium by children. Br Med J [Clin Res] 1965; 2:1343-1345.

27. Wilcock B, Olander H. Influences of oral antibiotic feeding on the duration and severity of clinical disease, growth performances, and pattern of shedding in swine inoculated with Salmonella typhimurium. J Am Vet Med Assoc 1978; 172:472-477.

28. Vaughn JB, Williams LP Jr, LeBlanc DR, et al. Salmonella in a modern broiler operation: a longitudinal study Am J Vet Res 1974; 35:737-741.

29. Bensink JC. Salmonella contamination of meat and bone meal. Aust Vet J 1979; 55:13-15.

30. Bensink JC, Boland PH. Possible pathways of contamination of meat and bone meal with Salmonella. Aust Vet J 1979; 55:521-524.

31. Ruben RH, Weinstein L. Salmonellosis. New York: Stratton International Medical Book Corp, 1977; 25.

32. Sojka WJ, Thomson PD, Hudson EB. Extraction of Salmonella dublin by adult bovine carriers. Br Vet J 1974; 130:482-487.

33. Robinson RA. Salmonellosis control and prevention in food animals at the producer level, in Proceedings Nat Salmonellosis Semi. US Anim Health Assoc, 1978.

34. Williams LP, Newell KW. Salmonella excretion in joy riding pigs. Am J Pub Health 1970; 50:926-929.

35. Rings MD. Salmonellosis in calves. Vet Clin North Am [Food Anim Pract] 1985; 1:529-540.

36. Snoeyenbos GH. Pullorum disease In: Hofstad MS, ed. Diseases of poultry. 8th ed. Ames: Iowa State University Press, 1984; 66-78.

37. Salmonellosis--Kentucky. MMWR 1977; 26:239.

38. Ogilvie TH. The persistent isolation of Salmonella typhimurium from the mammary gland of a cow. Can Vet J 1986; 27:329-331.

39. Marth EH. Salmonellae and salmonellosis associated with milk and milk products, a review. J Dairy Sci 1969; 52:283-315.

40. Milk-borne salmonellosis--Illinois. MMWR 1985; 34:200.

41. Sun M. Illinois traces cause of Salmonella outbreak. Science 1985; 228:972-973.

42. Snoeyenbos GH, Smyser CF, Van Roekel H. Salmonella infections of the ovary and peritoneum of chickens. Avian Dis 1969; 13:668-670.

43. Peel B. Occurrence of salmonellas in raw and pasteurized liquid whole egg. Queensland J Agric Anim Sci 1977; 33:13-21.

44. Baker RC, Hogarty S, Poon W, et al. Survival of Salmonella typhimurium and Staphylococcus aureus in eggs cooked by different methods. Poultry Sci 1983; 62:1211-1216.

45. Salmonellosis in a school system--Oklahoma. MMWR 1987; 36:74-75.

46. Houston DL. USDA and Salmonella control, in proceedings. 91st Annu Meet US Anim Health Assoc 1987; 445-450.

47. Hagstad HV, Hubbert WT. Food quality control, foods of animal origin. 1st ed. Ames: Iowa State University Press, 1986; 73-75, 97.

Addendum (1995)

In the United States, Salmonella species are the second most common cause of bacterial diarrhea in human beings, causing an estimated 200,000 cases/yr.¹ Currently 2,296 serovars (serotypes) are recognized²; S enteritidis, typhimurium, newport, heidelberg, and hadar were the serotypes from human sources reported most frequently to the CDC in 1991. The most common Salmonella serotypes from nonhuman sources reported to the CDC and USDA in 1990-91 were S enteritidis, typhimurium, heidelberg, hadar and choleraesuis.^3,4

Most cases of salmonellosis in human beings in the United States are associated with consumption of contaminated food from animal sources.⁵ Disease episodes have been associated with consumption of contaminated meat, raw milk, and raw or undercooked eggs. Farm animals and pets are potential sources of Salmonella spp, especially younger animals with diarrhea. Although fecal/oral transmission or ingestion is the major route of infection, salmonellosis has been acquired through inhalation. Transmission via inhalation has been documented in infants and calves where Salmonella organisms were aerosolized via vacuum sweepers and high-pressure cleaning sprayers, respectively.^6,7 Inhalation may be the major route of transmission of S choleraesuis in swine.⁸

Animals at risk of acquiring infections are neonates, old animals, and animals with concurrent infections. Animals undergoing the physiologic stress of transportation, exercise, malnutrition, pregnancy, or surgery or those housed under intense animal husbandry conditions also are at increased risk of infection.^9,10

Human infants less than 1 year old and the elderly are most susceptible to infection. Individuals given immunosuppressive therapy or antimicrobial therapy within the preceding 30 days, and persons with sickle cell anemia, neoplasia, or acquired immunodeficiency syndrome are likewise at increased risk of becoming infected.¹¹ Individuals at increased risk of acquiring Salmonella infections and/or those caring for them should be made aware of proper food handling, cooking, and storage techniques. Because pets may also be a source of infection for these individuals, pets with signs of diarrhea should be examined by a veterinarian. Young pups and kittens with diarrhea have an increased chance of shedding Salmonella organisms; therefore, selection of an older animal for a pet should be recommended to high risk individuals.^9,12,13 Because of the high prevalence of Salmonella shedding by reptiles, they should not be kept as pets by high-risk individuals.¹⁴ To avoid infection, hands should be washed thoroughly after handling animals or materials contaminated with feces. Pets should be fed a high-quality commercial pet food. Pets may shed Salmonella organisms acquired by consuming contaminated foods; therefore, if supplemental foods are fed, the food should undergo the same handling and cooking procedures as if it were to be consumed by the pets owner.

Most Salmonella infections in human beings develop after consumption of contaminated food that has been improperly stored and/or improperly prepared and handled. Some Salmonella serovars are commonly associated with specific food products. Since 1988, S enteritidis has been the first or second most frequently reported isolate from human beings.¹⁵ Infections attributable to S enteritidis are associated with consumption of grade A shell eggs. Eggshells may be contaminated with feces that contain Salmonella bacteria. The organism then infects eggs by entering through cracks or shell defects. The risk of contamination by feces has been reduced by currently established egg inspection, disinfecting, and grading programs.¹⁶ Salmonella enteritidis, however, is shed in the yolk via transovarian transmission, prior to shell deposition. The bacteria may be intermittently shed for short periods into the yolks by hens colonized by S enteritidis.^17-19 Initial S enteritidis episodes were confined to the northeast section of the United States during the 70s, but the number of episodes associated with eggs and this organism have increased annually in all sections of the United States since the mid 1980s. In 1990, the USDA began to identify infected layer farms through the use of environmental and internal organ bacteriologic culturing, in an attempt to control human S enteritidis episodes associated with eggs. Specimens of the environment and from chickens on farms are obtained for culture after the farm has been identified as the source from which the eggs implicated in a human disease episode originated. If S enteritidis is isolated from the environment, eggs are required to be sent to breaker plants for pasteurization. The presence of S enteritidis is then confirmed in the flock by culturing specimens of internal organs of hens.²⁰ Trace back of the implicated eggs to the farm of origin is difficult because of the practice of blending eggs from multiple layer farms.

The infection prevalence of S enteritidis in table eggs is estimated to be 0.01%.¹⁵ Even though S enteritidis is present in eggs, most exposures do not result in clinical illness. Development of illness depends on the number and pathogenicity of organisms consumed and susceptibility of the individual. In a worst case scenario, an estimated 1 human case might develop for every 240,000 eggs consumed.²⁰ Although most reported S enteritidis episodes are associated with consumption of batched eggs, consumption of a single egg may lead to clinical disease in an individual. A study investigating sporadic S enteritidis infections indicated that 37% of clinical infections were attributed to eating undercooked fried eggs.²¹ Although everyone is susceptible to S enteritidis infections, the serotype appears to be more virulent in the elderly and HIV-infected individuals.⁵ Hospitals and nursing homes, therefore, should pasteurize eggs, because the pasteurization process kills S enteritidis. To kill S enteritidis, eggs need to be thoroughly cooked (ie, until all the liquid yolk is solidified). Soft-scrambled eggs and those fried sunny side up or over easy may contain viable S enteritidis.²² Boiling eggs for 8 minutes did not kill S enteritidis in experimentally infected eggs; however, viable organisms were not isolated after eggs were boiled for 9 minutes. Storage/handling of eggs is also important in controlling infections. Salmonella enteritidis did not multiply in infected eggs kept at refrigeration temperature of 4.4 C (40 F), but a generation time of 60 minutes was observed in eggs kept at room temperature. Eggs inoculated with 10² organisms/g contained 10⁸ organisms/g after being kept at room temperature for 24 hours. The importance of proper storage and cooking of eggs cannot be overemphasized.²³

The most serious health risk to the public comes from the slaughter of sick animals and animals that are apparently healthy, but are Salmonella carriers. Sick animals should be detected on antemortem inspection as unfit for slaughter. Healthy animals that are colonized externally or internally are slaughtered and are potentially a source of contamination in the slaughter facility. During the slaughtering process, fecal material either from the gastrointestinal tract or from soiled hides may contaminate carcasses. The amount of carcass contamination is dependent on the cleanliness of the slaughter facility and competency of the slaughter house personnel during the slaughtering process.

Two potential sources of infection for animals are feedstuffs and infected carrier animals. Processed feeds, especially those derived from animal products, such as bone, blood, and feather meal, may be contaminated with Salmonella organisms.^23,24 The contamination is generally a result of recontamination after processing. Feedstuffs produced on the farm are also susceptible to being contaminated prior to feeding. In some intensive management systems, the alleyway between groups of animals may be used as a thoroughfare through which manure is transported from one area of the farm to another and may also serve as the feedbunk. On these farms, fecal material may be lost in transport, then feed may be spread over it at the next feeding. Equipment that is used to move feed from a storage area to the feeding area may also be used to move manure or remove dead or disabled animals. As a result, the feed-handling equipment would be contaminated with fecal material potentially containing Salmonella organisms. Birds and rodents may serve as a mechanical means of transporting Salmonella organisms from different locations on a farm through contamination of feedstuffs. Because salmonellae are excreted in animal feces, proper manure handling is critical. Unfortunately, as a result of intensified livestock production manure removal has become a challenge. Manure is used as a substitute for fertilizer on crop and pasture land. Runoff from this fertilized land has the potential to contaminate water supplies as well as adjacently grazed pastures. Composted manure is used as bedding, and composted poultry litter is used in cattle feed. The process of composting kills Salmonella organisms.²⁵ Unfortunately, the organisms may remain viable for up to 7 months if manure is not properly composted.²⁶ They can be present and persist in the farm environment even though animals do not manifest clinical signs of disease or production losses associated with Salmonella spp.²⁷

Identification of carrier animals in a population has been difficult, because bacteriologic culture has been the main means of diagnosis. Infected animals may not consistently shed the organism; as a result, culturing is likely to underestimate the true prevalence. Immunologic tests have been developed that can identify cattle as carriers of or being exposed to Salmonella spp on the basis of a persistent serum IgG titer against Salmonella lipopolysaccharides.²⁸ results of a study using serum and milk ELISA indicted that 1 or more cows had recently been exposed to Salmonella spp on 75% of the study farms. Salmonella sp was isolated from only 11.7% of the study farms.²⁸

Disease has been associated with consumption of milk. Although pasteurization kills Salmonella organisms, episodes have been associated with pasteurized milk being contaminated with raw milk.^29,30 Salmonella spp, therefore, need to be controlled at the farm level. The organisms have been isolated from 8.9% of bulk tanks.³¹ Milk can be contaminated in a variety of ways. Cows may excrete the organism in the milk during the febrile stage of clinical salmonellosis. Active carriers may secrete infected milk intermittently, especially those infected with host-adapted Salmonella spp, such as S dublin.³² Nonhost-adapted serovars, S enteritidis, muenster, and typhimurium have also been found in milk that was traced to cows with subclinical mammary gland infections.²⁸ Teat skin is, however, the more important source of nonhost-adapted serovars.³³ The teats are contaminated from the environment, and the organism is transferred to the milk if the teats are not washed properly. The number of organisms in the cow's bedding has been correlated with the number of organisms found in the bulk tank.³⁴ Proper management of the housing area and proper milking hygiene must be established to decrease contamination of the bulk tank.

As the populations of the elderly, immunocompromised, and HIV-infected individuals increase in size, the number of Salmonella infections is also likely to increase. To prevent infections, personal and food hygiene practices must be emphasized. Hands should be thoroughly washed after handling pets and raw foods potentially contaminated with Salmonella bacteria. Foods should be kept refrigerated until prepared for consumption. To kill Salmonella organisms, meat should be cooked to an internal temperature of 74 C (165 F) and eggs should be cooked until no liquid yolk remains. Cooked foods, if not eaten immediately after cooking, should be kept at temperatures above 60 C (140 F) until consumed. Cooked products and raw products, such as vegetables, should not be recontaminated after cooking or contaminated after rinsing by contact with contaminated hands, cooking utensils, or counter surfaces. Farm management practices that decrease the transmission of Salmonella spp on the farm need to be implemented. Emphasis should be placed on environmental sanitation and the acquisition, storage, and feeding of feedstuffs free from Salmonella contamination.

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