Salmonellosis

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Salmonellosis
SalmonellaNIAID.jpg
Electron micrograph showing Salmonella typhimurium (red) invading cultured human cells
Specialty Infectious disease
Symptoms Diarrhea, fever, abdominal cramps, vomiting [1]
Complications Reactive arthritis, irritable bowel syndrome [2]
Usual onset0.5–3 days post exposure [1]
Duration4–7 days [1]
TypesTyphoidal, nontyphoidal [1]
Causes Salmonella [1]
Risk factors Old, young, weak immune system, bottle feeding, proton pump inhibitors [1]
Diagnostic method Stool test, blood tests [3] [1]
Differential diagnosis Other types of gastroenteritis [2]
PreventionProper preparation and cooking of food and supervising contact between young children and pets [4]
Treatment Fluids by mouth, intravenous fluids, antibiotics [1]
Frequency1.35 million non–typhoidal cases per year (US) [1]
Deaths90,300 (2015) [5]

Salmonellosis is a symptomatic infection caused by bacteria of the Salmonella type. [1] It is the most common disease to be known as food poisoning (though the name refers to food-borne illness in general), these are defined as diseases, usually either infectious or toxic in nature, caused by agents that enter the body through the ingestion of food. In humans, the most common symptoms are diarrhea, fever, abdominal cramps, and vomiting. [1] Symptoms typically occur between 12 hours and 36 hours after exposure, and last from two to seven days. [4] Occasionally more significant disease can result in dehydration. [4] The old, young, and others with a weakened immune system are more likely to develop severe disease. [1] Specific types of Salmonella can result in typhoid fever or paratyphoid fever. [1] [3] Typhoid fever and paratyphoid fever are specific types of salmonellosis, known collectively as enteric fever, [6] and are, respectively, caused by salmonella typhi & paratyphi bacteria, which are only found in humans. [7] Most commonly, salmonellosis cases arise from salmonella bacteria from animals, [8] and chicken is a major source for these infections. [9]

Contents

There are two species of Salmonella: Salmonella bongori and Salmonella enterica with many subspecies. [4] However, subgroups and serovars within a species may be substantially different in their ability to cause disease. This suggests that epidemiologic classification of organisms at the subspecies level may improve management of Salmonella and similar pathogens. [10] [11] [12]

Both vegetarian and non-vegetarian populations are susceptible to Salmonella infections due to the consumption of contaminated meat and milk. [13] Infection is usually spread by consuming contaminated meat, eggs, water or milk. [14] Other foods may spread the disease if they have come into contact with manure. [4] A number of pets including cats, dogs, and reptiles can also carry and spread the infection. [4] Diagnosis is by a stool test or blood tests. [1] [3]

Efforts to prevent the disease include the proper washing, preparation, and cooking of food to appropriate temperature. [4] Mild disease typically does not require specific treatment. [4] More significant cases may require treatment of electrolyte problems and intravenous fluid replacement. [1] [4] In those at high risk or in whom the disease has spread outside the intestines, antibiotics are recommended. [4]

Salmonellosis is one of the most common causes of diarrhea globally. [2] In 2015, 90,300 deaths occurred from nontyphoidal salmonellosis, and 178,000 deaths from typhoidal salmonellosis. [5] In the United States, about 1.35 million cases and 450 deaths occur from non-typhoidal salmonellosis a year. [1] In Europe, it is the second most common foodborne disease after campylobacteriosis. [2]

Immunological parameters of infection

From an immunological point of view Salmonellosis is an infection caused by gram-negative bacteria infiltrating epithelial cells of the small intestine in the distal ileum whereby inducing acute inflammatory response called enteritis. [15] Salmonella can infect M-cells population overlying the Payer’s patches in the intestine, cells located in lamina propria of the intestinal mucosa and other epithelial cells. [15] After infecting cells in Peyer's patches, Salmonella can move to the mesenteric lymph nodes. This happens because lymphatic vessels are responsible for draining fluids, cells, and microbes from the intestinal tissues and carrying them to these lymph nodes. This process requires migration dependent on a factor known as CCR7. Once in the mesenteric lymph nodes, Salmonella can then enter the bloodstream, leading to a systemic infection that spreads throughout the body. [16] Virulence of the Salmonella is given by the Salmonella Pathogenicity Island 1 (SPI-1). [17] This needle-like structure, formed by a set of proteins, is known as the Type III secretion system. It enables Salmonella to effectively invade neighboring cells by injecting bacterial proteins directly into them, facilitating its spread and evasion of the host's immune defenses. [18] The first cells recruited to the Salmonella infection site are neutrophils, monocytes, and dendritic cells. Neutrophils play a key role in early defense against Salmonella, preventing its spread into the bloodstream. Studies in mice have shown that without neutrophils, there's an increase in the extracellular bacterial load during Salmonella infection. Moreover, these cells are essential for producing IFN-γ in the intestinal mucosa, which is crucial for controlling Salmonella Typhimurium through an IFN-γ-dependent mechanism. [19] Several other pro-inflammatory cytokines have been also observed after the infection of the epithelia such as IL-1α, TNFα, IL-12, IL-18 and IL-15, affecting the body-temperature by inducing fever, increase mucus production, activation of B and T leukocytes and polymorphonuclear leukocytes and macrophages recruitment to the site of infection. [20] Resident macrophages can also recognize flagellin and activate NLRC4 inflammasome complex to activate caspase-1 and IL-1β and IL-18 release. [21] Recruited monocytes are specifically adapted to regulating bacterial replication through the production of antimicrobial molecules (anti-microbial factors such as iNOS, TNF-α and IL-1β), however, they exhibit limited capability as antigen-presenting cells. [22] While monocytes help in containing the bacteria initially, the inability to effectively present antigens can delay or weaken the activation of T cells, which are necessary for a strong and specific immune response. In contrast, dendritic cells experience maturation through both direct pathways, mediated by bacteria, and indirect pathways, facilitated by cytokines in vivo, enhancing their ability to present antigens optimally. In a study focusing on the interaction between dendritic cells and intestinal epithelial cells, it was observed that when intestinal epithelial cells are stimulated by flagellin (a component of bacterial flagella, like those found in Salmonella), they trigger a specific response. This response involves the release of a molecule called CCL20. CCL20 is known to attract DCs, a type of immune cell. As a result, dendritic cells migrate towards the site of flagellin stimulation in the intestines. Recruitment of these cells to follicles plays a crucial role in initiating early T-cells mediated responses to Salmonella infection. [23] T–cell activation is limited to the draining mesenteric lymph nodes within 9–12 h since the initial infection as in any other lymph node activated T-cells specific to Salmonella were not detected. [24] Protective immunity against Salmonella appears to be primarily mediated by CD4+ T cells. This is evident in mice lacking a thymus, αβ T cells, MHC class-II, or T-bet+ Th1 cells, as they demonstrate an inability to resolve the infection. [25] [26] Clearly Th1 response is crucial in response and clearance of Salmonella infection since mice depleted from T-bet or IFN-γ are unable to combat Salmonellosis. The presence of different cytokines in combination with cytokines produced from Th1 cells however suggests additional effect of Th17 response. IL-22 and IL-17 are contributing to protection against Salmonella by its mucosal production and antimicrobial peptides expression (IL-22) as well regulation of mucosal host defense and neutrophil recruitment (IL17) demonstrated by IL-17A deficient mice infected with Salmonella. [27] [28] Conversely, mice lacking B-cells or γδ T cells can successfully clear the primary attenuated Salmonella infection, but a robust B-cell response is essential for resolving virulent Salmonella infections. [29] Different study revealed that B-cells are essential for protective immunity against Salmonella independent of antibody secretion because B-cells unable to secrete antibodies were still protective against Salmonella, suggesting that B-cells can serve as antigen presenting cells in this context and activate T-cells responses. [30] Further experiments focused on CD8+ cytotoxic lymphocytes revealed their crucial role in Salmonella clearance. Depletion of CD8+ T cells resulted in the failure to resolve the infection in mice. [31] These findings strongly suggest that CD4+-mediated protection is facilitated by the contribution of CD8+ cytotoxic T cells in the immune response against Salmonella. The investigation of immune memory revealed robust bacterial clearance facilitated by both CD4+ and CD8+ responses. Interestingly, this memory was not sufficient in adoptive transfer into other mice, despite possessing a potent response. However, when serum transfer was employed, the observed response indicated the crucial antibody-dependent role in secondary Salmonella infections. [32] Immunocompromised individuals (for example AIDS, malnutrition or those taking immunosuppressive treatment) are more susceptible to salmonellosis and contribute to bacteremia caused by neutropenia in immunocompromised individuals comparing immunocompetent ones. [33]

Signs and symptoms

Enteritis

After a short incubation period of a few hours to one day, the bacteria multiply in the small intestine, causing an intestinal inflammation (enteritis). Most people with salmonellosis develop diarrhea, fever, vomiting, and abdominal cramps 12 to 72 hours after infection. [34] Diarrhea is often watery and non-bloody but may be mucoid and bloody. [35] In most cases, the illness lasts four to seven days, and does not require treatment. In some cases, though, the diarrhea may be so severe that the patient becomes dangerously dehydrated and must be hospitalized. At the hospital, the patient may receive fluids intravenously to treat the dehydration, and may be given medications to provide symptomatic relief, such as fever reduction. In severe cases, the Salmonella infection may spread from the intestines to the blood stream, and then to other body sites, and can cause death, unless the person is treated promptly with antibiotics.[ citation needed ]

In otherwise healthy adults, the symptoms can be mild. Normally, no sepsis occurs, but it can occur exceptionally as a complication in the immunocompromised. However, in people at risk such as infants, small children, and the elderly, Salmonella infections can become very serious, leading to complications. In infants, dehydration can cause a state of severe toxicity. Extraintestinal localizations are possible, especially Salmonella meningitis in children, osteitis, etc. Children with sickle-cell anemia who are infected with Salmonella may develop osteomyelitis. Treatment of osteomyelitis, in this case, will be to use fluoroquinolones (ciprofloxacin, levofloxacin, etc., and nalidixic acid).[ citation needed ]

Those whose only symptom is diarrhea usually completely recover, but their bowel habits may not return to normal for several months. [36]

Typhoid fever

Typhoid fever occurs when Salmonella bacteria enter the lymphatic system and cause a systemic form of salmonellosis. Endotoxins first act on the vascular and nervous apparatus, resulting in increased permeability and decreased tone of the vessels, upset thermal regulation, vomiting, and diarrhea. In severe forms of the disease, enough liquid and electrolytes are lost to upset the fluid balance, cause an electrolyte imbalance, decrease the circulating blood volume and arterial pressure, and cause hypovolemic shock. Septic shock may also develop. Shock of mixed character (with signs of both hypovolemic and septic shock) are more common in severe salmonellosis. Oliguria and azotemia develop in severe cases as a result of renal involvement due to hypoxia and toxemia. [34]

Long-term

Salmonellosis is associated with later irritable bowel syndrome [37] and inflammatory bowel disease. [38] Evidence however does not support it being a direct cause of the latter. [38]

A small number of people afflicted with salmonellosis experience reactive arthritis, which can last months or years and can lead to chronic arthritis. [39] In sickle-cell anemia, osteomyelitis due to Salmonella infection is much more common than in the general population. Though Salmonella infection is frequently the cause of osteomyelitis in people with sickle-cell, it is not the most common cause, which is Staphylococcus infection. [40]

Those infected may become asymptomatic carriers, but this is relatively uncommon, with shedding observed in only 0.2 to 0.6% of cases after a year. [41]

Causes

An infographic illustrating how Salmonella bacteria spread from the farm Prevention of Salmonella from the farm to table infographic.png
An infographic illustrating how Salmonella bacteria spread from the farm

Salmonella bacteria can survive for some time without a host; they are frequently found in polluted water, with contamination from the excrement of carrier animals being particularly important.[ citation needed ]

The European Food Safety Authority highly recommends that when handling raw turkey meat, consumers and people involved in the food supply chain should pay attention to personal and food hygiene. [47]

An estimated 142,000 Americans are infected each year with Salmonella Enteritidis from chicken eggs, [48] and about 30 die. [49] The shell of the egg may be contaminated with Salmonella by feces or environment, or its interior (yolk) may be contaminated by penetration of the bacteria through the porous shell or from a hen whose infected ovaries contaminate the egg during egg formation. [50] [51]

Nevertheless, such interior egg yolk contamination is theoretically unlikely. [52] [53] [54] [55] Even under natural conditions, the rate of infection was very small (0.6% in a study of naturally contaminated eggs [56] and 3.0% among artificially and heavily infected hens [57] ).

Prevention

The US Food and Drug Administration (FDA) has published guidelines to help reduce the chance of food-borne salmonellosis. [58] Food must be cooked to 145–165 °F (63–74 °C), and liquids such as soups or gravies should be boiled when reheating. Freezing kills some Salmonella, but it is not sufficient to reliably reduce them below infectious levels. While Salmonella is usually heat-sensitive, it acquires heat-resistance in high-fat environments such as peanut butter. [59]

Vaccine

Antibodies against nontyphoidal Salmonella were first found in Malawi children in research published in 2008. The Malawian researchers identified an antibody that protects children against bacterial infections of the blood caused by nontyphoidal Salmonella. A study at Queen Elizabeth Hospital in Blantyre found that children up to two years old develop antibodies that aid in killing the bacteria. This could lead to a possible Salmonella vaccine for humans. [60]

A 2014 study tested a vaccine on chickens which offered efficient protection against salmonellosis. [61]

Vaccination of chickens against Salmonella essentially wiped out the disease in the United Kingdom. A similar approach was considered in the United States, but the Food and Drug Administration decided not to mandate vaccination of hens. [62]

Treatment

Electrolytes may be replenished with oral rehydration supplements (typically containing salts sodium chloride and potassium chloride).[ citation needed ]

Appropriate antibiotics, such as ceftriaxone, may be given to kill the bacteria, but are not necessary in most cases. [41] Azithromycin has been suggested to be better at treating typhoid in resistant populations than both fluoroquinolone drugs and ceftriaxone. There are recommendations on choice of antibiotic to avoid promoting antibiotic resistance.[ citation needed ]

There is no evidence of benefit of treating healthy people with diarrhea due to non-typhoidal salmonellosis. However, the evidence for the very young, very old or people with severe diseases are uncertain. [63]

Epidemiology

United States

Salmonellosis annually causes, per CDC estimation, about 1.35 million illnesses, 26,500 hospitalizations, and 420 deaths in the United States every year. [64] About 142,000 people in the United States are infected each year with Salmonella Enteritidis specifically from chicken eggs, and about 30 die. [49]

In 2010, an analysis of death certificates in the United States identified a total of 1,316 Salmonella-related deaths from 1990 to 2006. These were predominantly among older adults and those who were immunocompromised. [65] The U.S. government reported as many as 20% of all chickens were contaminated with Salmonella in the late 1990s, and 16.3% were contaminated in 2005. [66]

The United States has struggled to control salmonella infections, with the rate of infection rising from 2001 to 2011. In 1998, the USDA moved to close plants if salmonella was found in excess of 20 percent, which was the industry's average at the time, for three consecutive tests. [67] Texas-based Supreme Beef Processors, Inc. sued on the argument that Salmonella is naturally occurring and ultimately prevailed when a federal appeals court affirmed a lower court. [67] These issues were highlighted in a proposed Kevin's Law (formally proposed as the Meat and Poultry Pathogen Reduction and Enforcement Act of 2003), of which components were included the Food Safety Modernization Act passed in 2011, but that law applies only to the FDA and not the USDA. [67] The USDA proposed a regulatory initiative in 2011 to Office of Management and Budget. [68]

Salmonella is found in 8% of the chicken parts tested by the USDA and 25% of ground chicken. [69]

Europe

An outbreak of salmonellosis started in Northern Europe in July 2012, caused by Salmonella thompson. The infections were linked to smoked salmon from the manufacturer Foppen, where the contamination had occurred. Most infections were reported in the Netherlands; over 1060 infections with this subspecies and four fatalities were confirmed. [70] [71]

A case of widespread infection was detected mid-2012 in seven EU countries. Over 400 people had been infected with Salmonella enterica serovar Stanley (S. Stanley) that usually appears in the regions of Southeast Asia. After several DNA analyses seemed to point to a specific Belgian strain, the "Joint ECDC/E FSA Rapid Risk Assessment" report detected turkey production as the source of infection. [72]

In Germany, food poisoning infections must be reported. [73] Between 1990 and 2005, the number of officially recorded cases decreased from about 200,000 to about 50,000.[ citation needed ]

Elsewhere

In March 2007, around 150 people were diagnosed with salmonellosis after eating tainted food at a governor's reception in Krasnoyarsk, Russia. Over 1,500 people attended the ball on March 1 and fell ill as a consequence of ingesting Salmonella-tainted sandwiches.[ citation needed ]

In Singapore about 150 people fell sick after eating Salmonella-tainted chocolate cake produced by a major bakery chain in December 2007. [74]

South Africa reported contamination of its poultry carcasses by Salmonella. Egypt showed that Salmonella was predominant in poultry along with other non-typhoid strains. In Indonesia, the isolation of Salmonella Typhi was the main focus, while other serovars were also included from poultry. In India, Salmonella was predominant in poultry. Romania reported Salmonella serovars in poultry that affect humans. [75]

History

Both salmonellosis and the microorganism genus Salmonella derive their names from a modern Latin coining after Daniel E. Salmon (1850–1914), an American veterinary surgeon. He had help from Theobald Smith, and together they found the bacterium in pigs.[ citation needed ]

Salmonella enterica was possibly the cause of the 1576 cocliztli epidemic in New Spain. [76]

Four-inch regulation

The "Four-inch regulation" or "Four-inch law" is a colloquial name for a regulation issued by the U.S. FDA in 1975, restricting the sale of turtles with a carapace length less than four inches (10 cm). [77]

The regulation was introduced, according to the FDA, "because of the public health impact of turtle-associated salmonellosis". Cases had been reported of young children placing small turtles in their mouths, which led to the size-based restriction.[ citation needed ]

Regulation elsewhere

FSSAI regulation

The FSSAI has been established under the Food Safety and Standards Act, 2006, which is a consolidating statute related to food safety and regulation in India. FSSAI is responsible for protecting and promoting public health through the regulation and supervision of food safety. The major importance of the FSSAI License is that it ensures that the food is verified chemically and hence is safe to consume. 'Health before wealth' is a common quote as well as fact. Therefore, anything related directly to health is a matter of great sensitivity. [78]

Research

Bacteriophage treatment

Therapy with phages or bacteriophages (viruses that infect bacteria) has been proposed as a treatment for Salmonella infections. Bacteriophages have a number of advantages over other alternatives: (i) high efficacy in killing bacteria, (ii) minimal or no side effects, (iii) no allergic effects, (iv) production is rapid and inexpensive, and (v) they are host-specific and therefore do not affect the intestinal microbiota or other saprophytic bacteria in the environmental milieu.

The use of bacteriophages is effective in the prevention and treatment of bacterial pathogens in animals. In the specific case of poultry, good results have been obtained by reducing the infection of Salmonella, E. coli and Campylobacter. Until now, the use of phage therapy to control Salmonella in poultry could reduce, but not completely eliminate bacterial colonisation. [79]

Bacteriophages are suitable to prevent or reduce the colonization of pathogenic bacteria and therefore diseases in cattle, [80] where phages are supplied either individually or in cocktail to farm animals, the routes and methods of application were examined by various authors and the application of phages through oral tube feeding or feed intake showed a reduction of pathogenic bacteria without affecting the intestinal microbiota of the host. [81] Current research is focused on improved phage delivery in a manner that avoids decreasing phage titer due to destabilization or inactivation by gastric pH extremes.

See also

Related Research Articles

<span class="mw-page-title-main">Typhoid fever</span> Disease caused by the bacteria Salmonella Typhi

Typhoid fever, also known simply as typhoid, is a disease caused by Salmonella enterica serotype Typhi bacteria, also called SalmonellaTyphi. Symptoms vary from mild to severe, and usually begin six to 30 days after exposure. Often there is a gradual onset of a high fever over several days. This is commonly accompanied by weakness, abdominal pain, constipation, headaches, and mild vomiting. Some people develop a skin rash with rose colored spots. In severe cases, people may experience confusion. Without treatment, symptoms may last weeks or months. Diarrhea may be severe, but is uncommon. Other people may carry it without being affected, but are still contagious. Typhoid fever is a type of enteric fever, along with paratyphoid fever. Salmonella enterica Typhi is believed to infect and replicate only within humans.

<i>Salmonella</i> Genus of prokaryotes

Salmonella is a genus of rod-shaped (bacillus) gram-negative bacteria of the family Enterobacteriaceae. The two known species of Salmonella are Salmonella enterica and Salmonella bongori. S. enterica is the type species and is further divided into six subspecies that include over 2,600 serotypes. Salmonella was named after Daniel Elmer Salmon (1850–1914), an American veterinary surgeon.

<span class="mw-page-title-main">Coddled egg</span> Egg lightly cooked in a water bath

In cooking, coddled eggs are eggs that have been cracked into a ramekin or another small container, placed in a water bath or bain-marie and gently or lightly cooked just below boiling temperature. They can be partially cooked, mostly cooked, or hardly cooked at all. Poached eggs are similar to coddled eggs but cooked by submersion in water, rather than being placed in a water bath.

<span class="mw-page-title-main">Psittacosis</span> Infectious disease in humans

Psittacosis—also known as parrot fever, and ornithosis—is a zoonotic infectious disease in humans caused by a bacterium called Chlamydia psittaci and contracted from infected parrots, such as macaws, cockatiels, and budgerigars, and from pigeons, sparrows, ducks, hens, gulls and many other species of birds. The incidence of infection in canaries and finches is believed to be lower than in psittacine birds.

<i>Salmonella enterica</i> Species of bacterium

Salmonella enterica is a rod-shaped, flagellate, facultative anaerobic, Gram-negative bacterium and a species of the genus Salmonella. It is divided into six subspecies, arizonae (IIIa), diarizonae (IIIb), houtenae (IV), salamae (II), indica (VI), and enterica (I). A number of its serovars are serious human pathogens; many of them are serovars of Salmonella enterica subsp. enterica.

<span class="mw-page-title-main">Foodborne illness</span> Illness from eating spoiled food

Foodborne illness is any illness resulting from the contamination of food by pathogenic bacteria, viruses, or parasites, as well as prions, and toxins such as aflatoxins in peanuts, poisonous mushrooms, and various species of beans that have not been boiled for at least 10 minutes.

<span class="mw-page-title-main">Asymptomatic carrier</span> Organism which has become infected with a pathogen but displays no symptoms

An asymptomatic carrier is a person or other organism that has become infected with a pathogen, but shows no signs or symptoms.

Enteric fever is a medical term encompassing two types of salmonellosis, which, specifically, are typhoid fever and paratyphoid fever. Enteric fever is a potentially life-threatening acute febrile systemic infection and is diagnosed by isolating a pathogen on culture. Typhoid fever is caused by the salmonella enterica bacteria, serotype typhi, while paratyphoid fever is caused by the salmonella enterica bacteria, serotype paratyphi A, B, or C. These salmonella enterica bacteria serovar that cause enteric fever only have human hosts, as opposed to other types of salmonellosis-causing salmonella bacteria which often have animal reservoirs.

<span class="mw-page-title-main">Serotype</span> Distinct variation within a species of bacteria or virus or among immune cells

A serotype or serovar is a distinct variation within a species of bacteria or virus or among immune cells of different individuals. These microorganisms, viruses, or cells are classified together based on their surface antigens, allowing the epidemiologic classification of organisms to a level below the species. A group of serovars with common antigens is called a serogroup or sometimes serocomplex.

<span class="mw-page-title-main">Paratyphoid fever</span> Bacterial infection caused by one of the three types of Salmonella enterica

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<span class="mw-page-title-main">Pathogenic bacteria</span> Disease-causing bacteria

Pathogenic bacteria are bacteria that can cause disease. This article focuses on the bacteria that are pathogenic to humans. Most species of bacteria are harmless and are often beneficial but others can cause infectious diseases. The number of these pathogenic species in humans is estimated to be fewer than a hundred. By contrast, several thousand species are part of the gut flora present in the digestive tract.

<span class="mw-page-title-main">2008 United States salmonellosis outbreak</span> Disease outbreak in the United States

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<span class="mw-page-title-main">Eggs as food</span> Edible animal product

Humans and their hominid ancestors have consumed eggs for millions of years. The most widely consumed eggs are those of fowl, especially chickens. People in Southeast Asia began harvesting chicken eggs for food by 1500 BCE. Eggs of other birds, such as ducks and ostriches, are eaten regularly but much less commonly than those of chickens. People may also eat the eggs of reptiles, amphibians, and fish. Fish eggs consumed as food are known as roe or caviar.

<span class="mw-page-title-main">Pasteurized eggs</span> Packaged eggs pre-processed with medium heat

Pasteurized eggs are eggs that have been pasteurized in order to reduce the risk of foodborne illness in dishes that are not cooked or are only lightly cooked. They may be sold as liquid egg products or pasteurized in the shell.

<i>Salmonella enterica <span style="font-style:normal;">subsp.</span> enterica</i> Subspecies of bacterium

Salmonella enterica subsp. enterica is a subspecies of Salmonella enterica, the rod-shaped, flagellated, aerobic, Gram-negative bacterium. Many of the pathogenic serovars of the S. enterica species are in this subspecies, including that responsible for typhoid.

The 2012 outbreak of Salmonella took place in 15 places worldwide with over 2,300 strains identified.

Salmonellosis annually causes, per CDC estimation, about 1.2 million illnesses, 23,000 hospitalizations, and 450 deaths in the United States every year.

Melita Alison Gordon is a gastroenterologist who works on invasive gut pathogens and tropical gastrointestinal disease. She leads the Malawi Liverpool Wellcome Trust Salmonella and Enterics Group. Gordon was awarded the British Society of Gastroenterology Sir Francis Avery Jones Research Medal in 2011.

<span class="mw-page-title-main">Milk borne diseases</span>

Milk borne diseases are any diseases caused by consumption of milk or dairy products infected or contaminated by pathogens. Milk borne diseases are one of the recurrent foodborne illnesses—between 1993 and 2012 over 120 outbreaks related to raw milk were recorded in the US with approximately 1,900 illnesses and 140 hospitalisations. With rich nutrients essential for growth and development such as proteins, lipids, carbohydrates, and vitamins in milk, pathogenic microorganisms are well nourished and are capable of rapid cell division and extensive population growth in this favourable environment. Common pathogens include bacteria, viruses, fungi, and parasites and among them, bacterial infection is the leading cause of milk borne diseases.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 "Salmonella". CDC. 13 November 2019. Archived from the original on 6 May 2022. Retrieved 5 May 2022.
  2. 1 2 3 4 Hald T (2013). Advances in microbial food safety: 2. Pathogen update: Salmonella. Elsevier Inc. Chapters. p. 2.2. ISBN   9780128089606. Archived from the original on 2017-09-10.
  3. 1 2 3 "Salmonella Infections". MedlinePlus. Archived from the original on 30 April 2017. Retrieved 7 May 2017.
  4. 1 2 3 4 5 6 7 8 9 10 "Salmonella (non-typhoidal)". World Health Organization. December 2016. Archived from the original on 20 April 2017. Retrieved 7 May 2017.
  5. 1 2 Wang H, Naghavi M, Allen C, Barber RM, Bhutta ZA, Carter A, et al. (October 2016). "Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015". Lancet. 388 (10053): 1459–1544. doi:10.1016/s0140-6736(16)31012-1. PMC   5388903 . PMID   27733281.
  6. Qamar FN, Hussain W, Qureshi S (2022). "Salmonellosis Including Enteric Fever". Pediatric Clinics of North America. 69 (1): 65–77. doi:10.1016/j.pcl.2021.09.007. PMID   34794677. S2CID   244281295.
  7. "Typhoid & Paratyphoid Fever | CDC Yellow Book 2024".
  8. "Salmonella and Food". 5 June 2023.
  9. "Chicken and Food Poisoning". 14 November 2023.
  10. Cohn AR, Cheng RA, Orsi RH, Wiedmann M (13 May 2021). "Moving Past Species Classifications for Risk-Based Approaches to Food Safety: Salmonella as a Case Study". Frontiers in Sustainable Food Systems. 5: 652132. doi: 10.3389/fsufs.2021.652132 .
  11. O'Hagan M (10 September 2021). "Salmonella: Why it's a chicken and egg thing". Knowable Magazine. doi: 10.1146/knowable-091021-1 . S2CID   239248124 . Retrieved 13 September 2021.
  12. Ricke SC (February 2021). "Strategies to Improve Poultry Food Safety, a Landscape Review". Annual Review of Animal Biosciences. 9 (1): 379–400. doi: 10.1146/annurev-animal-061220-023200 . PMID   33156992. S2CID   226275729.
  13. Centers for Disease Control and Prevention (CDC) (June 2002). "Outbreak of multidrug-resistant Salmonella newport--United States, January-April 2002". MMWR. Morbidity and Mortality Weekly Report. 51 (25): 545–548. PMID   12118534.
  14. "Salmonella". World Health Organization. Archived from the original on 17 April 2017. Retrieved 7 May 2017.
  15. 1 2 House D, Bishop A, Parry C, Dougan G, Wain J (October 2001). "Typhoid fever: pathogenesis and disease". Current Opinion in Infectious Diseases. 14 (5): 573–578. doi:10.1097/00001432-200110000-00011. ISSN   0951-7375. PMID   11964878. S2CID   33369729.
  16. Voedisch S, Koenecke C, David S, Herbrand H, Förster R, Rhen M, Pabst O (August 2009). "Mesenteric lymph nodes confine dendritic cell-mediated dissemination of Salmonella enterica serovar Typhimurium and limit systemic disease in mice". Infection and Immunity. 77 (8): 3170–3180. doi:10.1128/IAI.00272-09. ISSN   1098-5522. PMC   2715677 . PMID   19506012.
  17. Jones BD, Falkow S (September 1994). "Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization". Infection and Immunity. 62 (9): 3745–3752. doi:10.1128/iai.62.9.3745-3752.1994. ISSN   0019-9567. PMC   303026 . PMID   8063389.
  18. Espina M, Olive AJ, Kenjale R, Moore DS, Ausar SF, Kaminski RW, Oaks EV, Middaugh CR, Picking WD, Picking WL (August 2006). "IpaD Localizes to the Tip of the Type III Secretion System Needle of Shigella flexneri". Infection and Immunity. 74 (8): 4391–4400. doi:10.1128/IAI.00440-06. ISSN   0019-9567. PMC   1539624 . PMID   16861624.
  19. Conlan JW (March 1996). "Neutrophils prevent extracellular colonization of the liver microvasculature by Salmonella typhimurium". Infection and Immunity. 64 (3): 1043–1047. doi:10.1128/iai.64.3.1043-1047.1996. ISSN   0019-9567. PMC   173878 . PMID   8641757.
  20. Eckmann L, Kagnoff MF (1 November 2001). "Cytokines in host defense against Salmonella". Microbes and Infection. 3 (14): 1191–1200. doi:10.1016/S1286-4579(01)01479-4. ISSN   1286-4579. PMID   11755407.
  21. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A (June 2006). "Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf". Nature Immunology. 7 (6): 569–575. doi:10.1038/ni1344. ISSN   1529-2908. PMID   16648853. S2CID   11172068.
  22. Rydström A, Wick MJ (1 May 2007). "Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection". Journal of Immunology. 178 (9): 5789–5801. doi:10.4049/jimmunol.178.9.5789. ISSN   0022-1767. PMID   17442963.
  23. Pham OH, McSorley SJ (January 2015). "Protective host immune responses to Salmonella infection". Future Microbiology. 10 (1): 101–110. doi:10.2217/fmb.14.98. ISSN   1746-0913. PMC   4323267 . PMID   25598340.
  24. McSorley SJ, Asch S, Costalonga M, Reinhardt RL, Jenkins MK (March 2002). "Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection". Immunity. 16 (3): 365–377. doi: 10.1016/s1074-7613(02)00289-3 . ISSN   1074-7613. PMID   11911822.
  25. Ravindran R, Foley J, Stoklasek T, Glimcher LH, McSorley SJ (1 October 2005). "Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection". Journal of Immunology. 175 (7): 4603–4610. doi:10.4049/jimmunol.175.7.4603. ISSN   0022-1767. PMID   16177105.
  26. Weintraub BC, Eckmann L, Okamoto S, Hense M, Hedrick SM, Fierer J (June 1997). "Role of alphabeta and gammadelta T cells in the host response to Salmonella infection as demonstrated in T-cell-receptor-deficient mice of defined Ity genotypes". Infection and Immunity. 65 (6): 2306–2312. doi:10.1128/iai.65.6.2306-2312.1997. ISSN   0019-9567. PMC   175320 . PMID   9169768.
  27. Schulz SM, Köhler G, Holscher C, Iwakura Y, Alber G (September 2008). "IL-17A is produced by Th17, gammadelta T cells and other CD4- lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance". International Immunology. 20 (9): 1129–1138. doi:10.1093/intimm/dxn069. ISSN   1460-2377. PMID   18599501.
  28. Lee S, McLachlan JB, Kurtz JR, Fan D, Winter SE, Baumler AJ, Jenkins MK, McSorley SJ (January 2012). "Temporal expression of bacterial proteins instructs host CD4 T cell expansion and Th17 development". PLOS Pathogens. 8 (1): e1002499. doi: 10.1371/journal.ppat.1002499 . ISSN   1553-7374. PMC   3262010 . PMID   22275869.
  29. Mastroeni P, Simmons C, Fowler R, Hormaeche CE, Dougan G (January 2000). "Igh-6−/− (B-Cell-Deficient) Mice Fail To Mount Solid Acquired Resistance to Oral Challenge with Virulent Salmonella enterica Serovar Typhimurium and Show Impaired Th1 T-Cell Responses to Salmonella Antigens". Infection and Immunity. 68 (1): 46–53. doi:10.1128/IAI.68.1.46-53.2000. ISSN   0019-9567. PMC   97100 . PMID   10603367.
  30. Nanton MR, Way SS, Shlomchik MJ, McSorley SJ (15 December 2012). "Cutting edge: B cells are essential for protective immunity against Salmonella independent of antibody secretion". Journal of Immunology. 189 (12): 5503–5507. doi:10.4049/jimmunol.1201413. ISSN   1550-6606. PMC   3518619 . PMID   23150714.
  31. Lee S, Dunmire S, McSorley SJ (17 December 2012). "MHC class-I-restricted CD8 T cells play a protective role during primary Salmonella infection". Immunology Letters. 148 (2): 138–143. doi:10.1016/j.imlet.2012.10.009. ISSN   0165-2478. PMC   3540194 . PMID   23089550.
  32. Mastroeni P, Villarreal-Ramos B, Hormaeche CE (September 1993). "Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells". Infection and Immunity. 61 (9): 3981–3984. doi:10.1128/iai.61.9.3981-3984.1993. ISSN   0019-9567. PMC   281103 . PMID   8359920.
  33. Tumbarello M, Tacconelli E, Caponera S, Cauda R, Ortona L (September 1995). "The impact of bacteraemia on HIV infection. Nine years experience in a large Italian university hospital". The Journal of Infection. 31 (2): 123–131. doi:10.1016/s0163-4453(95)92110-9. ISSN   0163-4453. PMID   8666842.
  34. 1 2 Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Bäumler AJ (2001). "Animal models of Salmonella infections: enteritis versus typhoid fever". Microbes and Infection. 3 (14–15): 1335–1344. doi: 10.1016/s1286-4579(01)01495-2 . PMID   11755423.
  35. "Nontyphoidal Salmonella Infections - Infectious Diseases - Merck Manuals Professional Edition". Merck Manuals Professional Edition. Retrieved 2018-09-15.
  36. "What is Salmonellosis?". US Center of Disease Control and Prevention. 2019-02-08. Archived from the original on 2014-03-31.
  37. Smith JL, Bayles D (July 2007). "Postinfectious irritable bowel syndrome: a long-term consequence of bacterial gastroenteritis". Journal of Food Protection. 70 (7): 1762–1769. doi: 10.4315/0362-028X-70.7.1762 . PMID   17685356. S2CID   42240663.
  38. 1 2 Mann EA, Saeed SA (January 2012). "Gastrointestinal infection as a trigger for inflammatory bowel disease". Current Opinion in Gastroenterology. 28 (1): 24–29. doi:10.1097/mog.0b013e32834c453e. PMID   22080823. S2CID   800248.
  39. Schmitt SK (June 2017). "Reactive Arthritis". Infectious Disease Clinics of North America (Review). 31 (2): 265–277. doi:10.1016/j.idc.2017.01.002. PMID   28292540.
  40. Burnett MW, Bass JW, Cook BA (February 1998). "Etiology of osteomyelitis complicating sickle cell disease". Pediatrics. 101 (2): 296–297. doi:10.1542/peds.101.2.296. PMID   9445507.
  41. 1 2 "Nontyphoidal Salmonella Infections". Merck Manual. Archived from the original on 2016-09-19. Retrieved 2016-09-19.
  42. Goldberg J (24 February 2012). "Are the bacteria that make food smell and taste bad the same ones that make you sick?". Tufts.edu. Retrieved 28 May 2018.
  43. Di Bella S, Capone A, Bordi E, Johnson E, Musso M, Topino S, et al. (July 2011). "Salmonella enterica ssp. arizonae infection in a 43-year-old Italian man with hypoglobulinemia: a case report and review of the literature". Journal of Medical Case Reports. 5 (1): 323. doi: 10.1186/1752-1947-5-323 . PMC   3156765 . PMID   21781321.
  44. "Reptile-Associated Salmonellosis—Selected States, 1998–2002". Centers for Disease Control and Prevention. 12 December 2003. Archived from the original on 6 October 2011. Retrieved 9 October 2011.
  45. Mermin J, Hoar B, Angulo FJ (March 1997). "Iguanas and Salmonella marina infection in children: a reflection of the increasing incidence of reptile-associated salmonellosis in the United States". Pediatrics. 99 (3): 399–402. doi:10.1542/peds.99.3.399. PMID   9041295.
  46. "Ongoing investigation into reptile associated salmonella infections". Health Protection Report. 3 (14). 9 April 2009. Archived from the original on 29 April 2009. Retrieved 12 April 2009.
  47. "Multi-country outbreak of Salmonella Stanley infections Update". EFSA Journal. 10 (9): 2893. 21 September 2012. doi: 10.2903/j.efsa.2012.2893 .
  48. "Playing It Safe With Eggs". FDA Food Facts. 2013-02-28. Archived from the original on 2013-03-01. Retrieved 2013-03-02. The U.S. Food and Drug Administration (FDA) estimates that 142,000 illnesses each year are caused by consuming eggs contaminated with Salmonella.
  49. 1 2 Black J, O'Keefe E (2009-07-08). "Administration Urged to Boost Food Safety Efforts". Washington Post . Archived from the original on 2011-06-04. Retrieved 2009-07-07.
  50. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Van Immerseel F (July 2009). "Mechanisms of egg contamination by Salmonella Enteritidis". FEMS Microbiology Reviews. 33 (4): 718–738. doi: 10.1111/j.1574-6976.2008.00161.x . PMID   19207743. Eggs can be contaminated on the outer shell surface and internally. Internal contamination can be the result of penetration through the eggshell or by direct contamination of egg contents before oviposition, originating from infection of the reproductive organs. Once inside the egg, the bacteria need to cope with antimicrobial factors in the albumen and vitelline membrane before migration to the yolk can occur
  51. Humphrey TJ (January 1994). "Contamination of egg shell and contents with Salmonella enteritidis: a review". International Journal of Food Microbiology. 21 (1–2): 31–40. doi:10.1016/0168-1605(94)90197-X. PMID   8155476. Salmonella enteritidis can contaminate the contents of clean, intact shell eggs as a result of infections of the reproductive tissue of laying hens. The principal site of infection appears to be the upper oviduct. In egg contents, the most important contamination sites are the outside of the vitelline membrane or the albumen surrounding it. In fresh eggs, only a few salmonellae are present. As albumen is an iron-restricted environment, growth only occurs with storage-related changes to vitelline membrane permeability, which allows salmonellae to invade yolk contents.
  52. Stokes JL, Osborne WW, Bayne HG (September 1956). "Penetration and Growth of Salmonella in Shell Eggs". Journal of Food Science. 21 (5): 510–518. doi:10.1111/j.1365-2621.1956.tb16950.x. Normally, the oviduct of the hen is sterile and therefore the shell and internal contents of the egg are also free of microorganisms (10,16). In some instances, however, the ovaries and oviduct may be infected with Salmonella and these may be deposited inside the egg (12). More frequently, however, the egg becomes contaminated after it is laid.
  53. Okamura M, Kamijima Y, Miyamoto T, Tani H, Sasai K, Baba E (2001). "Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens". Avian Diseases. 45 (1): 61–69. doi:10.2307/1593012. JSTOR   1593012. PMID   11332500. when hens were artificially infected to test for transmission rate to yolks: "Mature laying hens were inoculated intravenously with 106 colony-forming units of Salmonella enteritidis, Salmonella typhimurium, Salmonella infantis, Salmonella hadar, Salmonella heidelberg, or Salmonella montevideo to cause the systemic infection. Salmonella Enteritidis was recovered from three yolks of the laid eggs (7.0%), suggesting egg contamination from the transovarian transmission of S. enteritidis."
  54. Gast RK, Jones DR, Anderson KE, Guraya R, Guard J, Holt PS (August 2010). "In vitro penetration of Salmonella Enteritidis through yolk membranes of eggs from 6 genetically distinct commercial lines of laying hens". Poultry Science. 89 (8): 1732–1736. doi: 10.3382/ps.2009-00440 . PMID   20634530. Archived from the original on 2011-07-24. Retrieved 2010-08-20. In this study, egg yolks were infected at the surface of the yolk (vitelline membrane) to determine the percentage of yolk contamination (a measure used to determine egg contamination resistance, with numbers lower than 95% indicating increasing resistance): Overall, the frequency of penetration of Salmonella Enteritidis into the yolk contents of eggs from individual lines of hens ranged from 30 to 58% and the mean concentration of Salmonella Enteritidis in yolk contents after incubation ranged from 0.8 to 2.0 log10 cfu/mL.
  55. Jaeger G (Jul–Aug 2009). "Contamination of eggs of laying hens with S. Enteritidis". Veterinary Survey (Tierärztliche Umschau). 64 (7–8): 344–348. Retrieved 2010-08-20. The migration of the bacterium into the nutritionally rich yolk is constrained by the lysozyme loaded vitelline membrane, and would need warm enough storage conditions within days and weeks. The high concentration on of antibodies of the yolk does not inhibit the Salmonella multiplication. Only seldom does transovarian contamination of the developing eggs with S. enteritidis make this bacterium occur in laid eggs, because of the bactericidal efficacy of the antimicrobial peptides
  56. Humphrey TJ, Whitehead A, Gawler AH, Henley A, Rowe B (June 1991). "Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs". Epidemiology and Infection. 106 (3): 489–496. doi:10.1017/S0950268800067546. PMC   2271858 . PMID   2050203. Over 5700 hens eggs from 15 flocks naturally infected with Salmonella enteritidis were examined individually for the presence of the organism in either egg contents or on shells. Thirty-two eggs (0·6%) were positive in the contents. In the majority, levels of contamination were low.
  57. Gast RK, Guraya R, Guard-Bouldin J, Holt PS, Moore RW (March 2007). "Colonization of specific regions of the reproductive tract and deposition at different locations inside eggs laid by hens infected with Salmonella enteritidis or Salmonella heidelberg". Avian Diseases. 51 (1): 40–44. doi:10.1637/0005-2086(2007)051[0040:cosrot]2.0.co;2. PMID   17461265. S2CID   20428394. Archived from the original on 2010-03-10. Retrieved 2010-08-20. when hens are artificially infected with unrealistically large doses (according to the author): In the present study, groups of laying hens were experimentally infected with large oral doses of Salmonella Heidelberg, Salmonella Enteritidis phage type 13a, or Salmonella Enteritidis phage type 14b. For all of these isolates, the overall frequency of ovarian colonization (34.0%) was significantly higher than the frequency of recovery from either the upper (22.9%) or lower (18.1%) regions of the oviduct. No significant differences were observed between the frequencies of Salmonella isolation from egg yolk and albumen (4.0% and 3.3%, respectively).
  58. "Salmonella Questions and Answers". USDA Food Safety and Inspection Service. 2006-09-20. Archived from the original on 2009-01-15. Retrieved 2009-01-21.
  59. "FDA issues peanut safety guidelines for foodmakers". Reuters. 2009-03-10. Archived from the original on 2009-03-12.
  60. MacLennan CA, Gondwe EN, Msefula CL, Kingsley RA, Thomson NR, White SA, et al. (April 2008). "The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children". The Journal of Clinical Investigation. 118 (4): 1553–1562. doi:10.1172/JCI33998. PMC   2268878 . PMID   18357343.
  61. Nandre RM, Lee JH (January 2014). "Construction of a recombinant-attenuated Salmonella Enteritidis strain secreting Escherichia coli heat-labile enterotoxin B subunit protein and its immunogenicity and protection efficacy against salmonellosis in chickens". Vaccine. 32 (3): 425–431. doi:10.1016/j.vaccine.2013.10.054. PMID   24176491.
  62. Neuman W (2010-08-24). "U.S. Forgoes Salmonella Vaccine for Egg Safety". The New York Times. ISSN   0362-4331. Archived from the original on 2016-04-17. Retrieved 2016-03-12.
  63. Onwuezobe IA, Oshun PO, Odigwe CC (November 2012). "Antimicrobials for treating symptomatic non-typhoidal Salmonella infection". The Cochrane Database of Systematic Reviews. 11 (11): CD001167. doi:10.1002/14651858.CD001167.pub2. PMC   6532567 . PMID   23152205.
  64. "Salmonella Questions and Answers | CDC". www.cdc.gov. 2023-04-23.
  65. Cummings PL, Sorvillo F, Kuo T (November 2010). "Salmonellosis-related mortality in the United States, 1990-2006". Foodborne Pathogens and Disease. 7 (11): 1393–1399. doi:10.1089/fpd.2010.0588. PMID   20617938.
  66. Burros M (March 8, 2006). "More Salmonella Is Reported in Chickens". The New York Times. Archived from the original on January 9, 2016. Retrieved 2007-05-13.
  67. 1 2 3 "Salmonella Lurks From Farm to Fork « News21 2011 National Project". foodsafety.news21.com. Archived from the original on 2016-06-02. Retrieved 2016-09-18.
  68. "Ground Turkey Recall Shows We Still Need Kevin's Law | Food Safety News". 2011-08-12. Archived from the original on 2016-10-09. Retrieved 2016-09-18.
  69. Simon B, Yeung M, Grabell I, Hwang M (29 October 2021). "America's Food Safety System Failed to Stop a Salmonella Epidemic. It's Still Making People Sick". ProPublica. Retrieved 2021-11-03.
  70. Veelgestelde vragen Salmonella Thompson 15 oktober 2012, Rijksinstituut voor Volksgezondheid en Milieu [Frequently asked questions Salmonella Thompson 15 October 2012, Netherlands Institute for Public Health and the Environment].
  71. "Salmonella besmetting neemt verder af, 2 november 2012, Rijksinstituut voor Volksgezondheid en Milieu" [Salmonella infections continue to decline 2 November 2012, Netherlands Institute for Public Healthand the Environment].
  72. European Centre for Disease Prevention and Control, European Food Safety Authority (2012). "Multi-country outbreak of Salmonella Stanley infections Update". EFSA Journal. 10 (9): 2893. doi:10.2903/j.efsa.2012.2893. Archived from the original on 2014-04-13.
  73. § 6 and § 7 of the German law on infectious disease prevention, Infektionsschutzgesetz
  74. Hong L (7 December 2007). "PrimaDeli food poisoning cases increase to 153". Channel NewsAsia. Archived from the original on 8 December 2007.
  75. Barbour EK, Ayyash DB, Alturkistni W, Alyahiby A, Yaghmoor S, Iyer A, et al. (January 2015). "Impact of sporadic reporting of poultry Salmonella serovars from selected developing countries". Journal of Infection in Developing Countries. 9 (1): 001–007. doi: 10.3855/jidc.5065 . PMID   25596565.
  76. Vågene ÅJ, Herbig A, Campana MG, Robles García NM, Warinner C, Sabin S, et al. (March 2018). "Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico". Nature Ecology & Evolution. 2 (3): 520–528. Bibcode:2018NatEE...2..520V. doi:10.1038/s41559-017-0446-6. PMID   29335577. S2CID   3358440.
  77. "Human Health Hazards Associated with Turtles". U.S. Food and Drug Administration. Archived from the original on 2007-06-09. Retrieved 2007-06-29.
  78. "The Food Safety and Standards Authority of India (FSSAI)".
  79. Oechslin F (June 2018). "Resistance Development to Bacteriophages Occurring during Bacteriophage Therapy". Viruses. 10 (7): 351. doi: 10.3390/v10070351 . PMC   6070868 . PMID   29966329.
  80. García P, Martínez B, Obeso JM, Rodríguez A (December 2008). "Bacteriophages and their application in food safety". Letters in Applied Microbiology. 47 (6): 479–485. doi:10.1111/j.1472-765x.2008.02458.x. PMID   19120914. S2CID   30899476.
  81. Olson EG, Micciche AC, Rothrock MJ, Yang Y, Ricke SC (2022). "Application of Bacteriophages to Limit Campylobacter in Poultry Production". Frontiers in Microbiology. 12: 458721. doi: 10.3389/fmicb.2021.458721 . PMC   8766974 . PMID   35069459.