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Scientific classification
Lignieres 1900

S. bongori
S. enterica

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Scientific classification
Lignieres 1900

S. bongori
S. enterica

Salmonella /ˌsælməˈnɛlə/ is a genus of rod-shaped, Gram-negative, non-spore-forming, predominantly motile enterobacteria with diameters around 0.8 to 1.5 µm, lengths from 2 to 5 µm, and peritrichous flagella, (flagella that are all around the cell body). They are chemoorganotrophs, obtaining their energy from oxidation and reduction reactions using organic sources, and are facultative anaerobes. There are only two species of Salmonella; Salmonella bongori and Salmonella enterica of which there are around six subspecies and innumerable serovars. Salmonella belongs to the same family as Escherichia, which has as a species E.coli. Most subspecies of Salmonella produce hydrogen sulfide,[1] which can readily be detected by growing them on media containing ferrous sulfate, such as is used in the triple sugar iron test (TSI). Most isolates exist in two phases: a motile phase I and a nonmotile phase II. Cultures that are nonmotile upon primary culture may be switched to the motile phase using a Cragie tube.[citation needed]

Salmonella is found worldwide in both cold-blooded and warm-blooded animals, and in the environment. They cause illnesses such as typhoid fever, paratyphoid fever, and food poisoning.[2]

Salmonella as pathogens[edit]

Salmonella bacteria are zoonotic and can be transferred between humans and other animals. Many infections are due to ingestion of contaminated food. For example, recent FDA studies link Guatemalan cantaloupes with Salmonella panama.[3] In speaking of other salmonella serotypes, enteritis Salmonella and Salmonella typhoid/paratyphoid Salmonella, the latter—because of a special virulence factor and a capsule protein (virulence antigen)—can cause serious illness, such as Salmonella enterica subsp. enterica serovar Typhi. Salmonella typhi is adapted to humans and does not occur in other animals.

Salmonella species are facultative intracellular pathogens[4] that enter cells via macropinosomes.[5]

Enteritis salmonellosis or food poisoning Salmonella[edit]

This is a group consisting of potentially every other serotype (over a thousand) of the Salmonella bacteria, most of which have never been found in humans. These are encountered in various Salmonella species, most having never been linked to a specific host, but can also infect humans. It is therefore a zoonotic disease.

The organism enters through the digestive tract and must be ingested in large numbers to cause disease in healthy adults. Gastric acidity is responsible for the destruction of the majority of ingested bacteria. Bacterial colonies may become trapped in mucus produced in the oesophagus.

Salmonellosis is a disease incurred by eating food (often raw or undercooked, or too frequently re-heated) which is contaminated by S. enterica. Infection usually occurs when a person ingests foods that contain a high concentration of the bacteria, similar to a culture medium. In otherwise healthy adults, the symptoms can be mild. Normally, no sepsis occurs, but it can occur exceptionally as a complication in the immunocompromised.

Virulent Salmonella organisms release outer membrane vesicles while coming in close encounter with animal host ileal epithelial cells, which are thought to ruffle the host cell surface, creating a corridor-passage for organisms to enter the cells. The organisms may then escape epithelial lining to be confronted by host macrophages. Host macrophages are also considered to be signalled by the pathogens via outer membrane vesicles to induce their own phagocytosis. In typhoidal mode, salmonellae replicate in phagosomes inside host macrophages and get released by inducing apoptosis in infected macrophages. Circulation of infected macrophages can assume dimensions of systemic infection. Ultrastructural studies support this mechanism of salmonella infection.[6] A comprehensive mechanism of release of outer membrane vesicles containing Salmonella/gram-negative pathogen toxins and allied biochemical signal molecules and their translocation into eukaryotic host/target cells, also implicating a new role assigned to type3 secretory system (T3SS)-like needle complexes of riveting bacterial outer and inner membranes to bubble out nanovesicles has been proposed.[7]

However, infants and young children are much more susceptible to infection, easily achieved by ingesting a small number of bacteria. In infants, contamination through inhalation of bacteria-laden dust is possible. After a short incubation period of a few hours to one day, the bacteria multiply in the intestinal lumen, causing an intestinal inflammation with diarrhea that is often mucopurulent (containing mucus or pus) and bloody. In infants, dehydration can cause a state of severe toxicity. Extraintestinal localizations are possible, especially Salmonella meningitis in children, osteitis, etc.

Enteritis Salmonella (e.g., Salmonella enterica subsp. enterica serovar enteritidis) can cause diarrhea, which usually does not require antibiotic treatment. However, in people at risk such as infants, small children, the elderly, Salmonella infections can become very serious, leading to complications. If these are not treated, HIV patients and those with suppressed immunity can become seriously ill. Children with sickle cell anaemia who are infected with Salmonella may develop osteomyelitis. Treatment of osteomyelitis, in this case, will be to use fluoroquinolones (Ciproflaxacin, Levofloxacin, etc. and Nalidixic acid).

Salmonella bacteria can survive for weeks outside a living body, and they are not destroyed by freezing.[8][9] Ultraviolet radiation and heat accelerate their demise; they perish after being heated to 55 °C (131 °F) for 90 min, or to 60 °C (140 °F) for 12 min.[10] To protect against Salmonella infection, heating food for at least ten minutes at 75 °C (167 °F) is recommended, so the centre of the food reaches this temperature.[11][12]

Most people with salmonellosis develop diarrhea, fever, vomiting, and abdominal cramps 12 to 72 hours after infection. In most cases, the illness lasts four to seven days, and most people recover without treatment. In some cases, though, the diarrhea may be so severe, the patient becomes dangerously dehydrated and must be taken to a hospital. At the hospital, the patient may receive intravenous fluids 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. The elderly, infants, and those with impaired immune systems are more likely to develop severe illness.

An infectious process can only begin after living salmonellae (not only their toxins) reach the gastrointestinal tract. Some of the microorganisms are killed in the stomach, while the surviving salmonellae enter the small intestine and multiply in tissues (localized form). By the end of the incubation period, the macro-organisms are poisoned by endotoxins released from the dead salmonellae. The local response to the endotoxins is enteritis and gastrointestinal disorder. In the generalized form of the disease, salmonellae pass through the lymphatic system of the intestine into the blood of the patients (typhoid form) and are carried to various organs (liver, spleen, kidneys) to form secondary foci (septic form). Endotoxins first act on the vascular and nervous apparatus, manifested by 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 water-salt metabolism, to decrease the circulating blood volume and arterial pressure, and to cause hypovolemic shock. Septic shock may 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.

Cell-free Salmonella toxins in ileum have been shown to cause ileal hemorrhaging,[13] which may cause toxins to leak into host circulation to cause ill-effects on target organs like liver. Apoptotosis like changes in liver hepatic cells have been noted.[14]

A small number of people afflicted with salmonellosis experience reactive arthritis, which can last months or years and can lead to chronic arthritis.

In Germany, food poisoning infections must be reported.[15] Between 1990 and 2005, the number of officially recorded cases decreased from approximately 200,000 to approximately 50,000 cases. In the USA, about 40,000 cases of Salmonella infection are reported each year.[16] According to the World Health Organization, over 16 million people worldwide are infected with typhoid fever each year, with 500,000 to 600,000 fatal cases.[citation needed]

The AvrA toxin injected by the type three secretion system of Salmonella Typhimurium works to inhibit the innate immune system by virtue of its serine/threonine acetyltransferase activity, and requires binding to eukaryotic target cell phytic acid (IP6).[17] This leaves the host more susceptible to infection. In a 2011 paper,[18] Yale University School of Medicine researchers described in detail how Salmonella is able to make these proteins line up in just the right sequence to invade host cells. "These mechanisms present us with novel targets that might form the basis for the development of an entirely new class of antimicrobials," said Professor Dr. Jorge Galan, senior author of the paper and the Lucille P. Markey Professor of Microbial Pathogenesis and chair of the Section of Microbial Pathogenesis at Yale. In the new National Institutes of Health-funded study, Galan and colleagues identify what they call a bacterial sorting platform, which attracts needed proteins and lines them up in a specific order. If the proteins do not line up properly, Salmonella, as well as many other bacterial pathogens, cannot "inject" them into host cells to commandeer host cell functions, the lab has found. Understanding how this machine works raises the possibility of new therapies that disable this protein delivery machine, thwarting the ability of the bacterium to become pathogenic. The process would not kill the bacteria as most antibiotics do, but would cripple its ability to do harm. In theory, this means bacteria such as Salmonella might not develop resistance to new therapies as quickly as they usually do to conventional antibiotics.


The genus Salmonella was named after Daniel Elmer Salmon, an American veterinary pathologist. While Theobald Smith was the actual discoverer of the type bacterium (Salmonella enterica var. Choleraesuis) in 1885, Dr. Salmon was the administrator of the USDA research program, and thus the organism was named after him by Smith.[19] Smith and Salmon had been searching for the cause of common hog cholera and proposed this organism as the causal agent. Later research, however, would show this organism (now known as Salmonella enterica) rarely causes enteric symptoms in pigs,[20] and was thus not the agent they were seeking (which was eventually shown to be a virus). However, related bacteria in the genus Salmonella were eventually shown to cause other important infectious diseases. The genus Salmonella was finally formally adopted in 1900 by J. Lignières for the many species of Salmonella, after Smith's first type-strain Salmonella cholera.

Salmonella nomenclature[edit]

Initially, each Salmonella "species" was named according to clinical considerations,[21] e.g., Salmonella typhi-murium (mouse typhoid fever), S. cholerae-suis. After it was recognized that host specificity did not exist for many species, new strains (or serovars, short for serological variants) received species names according to the location at which the new strain was isolated. Later, molecular findings led to the hypothesis that Salmonella consisted of only one species,[22] S. enterica, and the serovars were classified into six groups,[23] two of which are medically relevant. But as this now formalized nomenclature[24][25] is not in harmony with the traditional usage familiar to specialists in microbiology and infectologists, the traditional nomenclature is common. Currently, there are two recognized species: S. enterica, and S. bongori. In 2005 a third species was thought to be added Salmonella subterranean, but this has since been ruled out and is seen as another serovar.[26] There are six main subspecies recognised: enterica (I), salamae (II), arizonae (IIIa), diarizonae (IIIb), houtenae (IV), and indica (VI).[27] Historically, serotype (V) was bongori, which is now considered its own species.

The serovar (i.e. serotype) is a classification of Salmonella into subspecies based on antigens that the organism presents. It is based on the Kauffman-White classification scheme that differentiates serological varieties from each other. Serotypes are usually put into subspecies groups after the genus and species, with the serovars/serotypes capitalized but not italicized: an example is Salmonella enterica serovar Typhimurium. Newer methods for Salmonella typing and subtyping include genome-based methods such as pulsed field gel electrophoresis (PFGE), Multiple Loci VNTR Analysis (MLVA), Multilocus sequence typing (MLST) and (multiplex-) PCR-based methods.[28][29]

Growth kinetics[edit]

Mathematical models of salmonella growth kinetics have been developed for chicken, pork, tomatoes, and melons.[30][31][32][33][34] Salmonella reproduce asexually with a cell division rate of 20 to 40 minutes under optimal conditions.[citation needed]

Sources of infection[edit]

An infographic illustrating how Salmonella spreads from the farm

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

The most recent case of salmonella infection had been 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.[38]

Finally, the European Food Safety Authority (EFSA) highly recommends that when handling raw turkey meat consumers and people involved in the food supply chain shall pay attention to personal and food hygiene.[39]

New antibiotic-resistant strains[edit]

Non-typhoidal salmonella (iNTS) Africa, a new form of the germ, emerged in the southeast of the continent 75 years ago, followed by a second wave, which came out of central Africa 18 years later. The second wave of iNTS began 35 years ago, possibly in the Congo Basin, and early in the event picked up a gene making it resistant to the antibiotic chloramphenicol. There is an urgency to develop an effective salmonella vaccine because of the recent outbreaks in Africa of antibiotic-resistant strains of the food-borne bacteria that is killing hundreds of thousands of people there, as well as the heavy annual worldwide death toll each year. People with HIV are greatly affected. A recently identified set of antigens (molecules in the invading bacteria that trigger an immune response) that is common to both mice and humans, provide a foundation for developing a protective salmonella vaccine that could be on the market as early as 2016. This is good news because no new, effective antibiotics are on the horizon. In sub-Saharan the variant is the cause of an enigmatic disease called invasive non-typhoidal salmonella (iNTS), which affects Africa far more than other continents. Its genetic makeup is evolving into a more typhoid-like bacteria, able to efficiently spread around the human body.

Vaccine status[edit]

Researchers say they have paved the way toward an effective Salmonella vaccine by identifying eight antigenic molecules from human and mouse infections. These antigens provide the research community with a foundation for developing a protective salmonella vaccine. [40]

A recent study has tested a vaccine on chickens which offered efficient protection against salmonellosis.[41]


An estimated 142,000 Americans are infected each year with Salmonella Enteritidis from chicken eggs,[42] and about 30 die.[citation needed] 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.[43][44]

Nevertheless, such interior egg yolk contamination is theoretically unlikely.[45][46][47][48] Even under natural conditions, the rate of infection was very small (0.6% in a study of naturally contaminated eggs[49] and 3.0% among artificially and heavily infected hens[50]). However, the natural infection rate would result in roughly one in fourteen cartons (one dozen eggs) to contain at least one egg with interior egg yolk contamination.

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.[51]

See also[edit]


  1. ^ Clark MA, Barret EL (June 1987). "The phs gene and hydrogen sulfide production by Salmonella typhimurium.". J Bacteriology 169 (6): 2391–2397. 
  2. ^ Ryan KJ, Ray CG (editors) (2004). Sherris Medical Microbiology (4th ed.). McGraw Hill. pp. 362–8. ISBN 0-8385-8529-9. 
  3. ^ Rothschild, Mary. "Del Monte Sues FDA Over Cantaloupe Recall, Import Restrictions". Marler Clark. Retrieved 5 October 2012. 
  4. ^ Jantsch, J.; Chikkaballi, D.; Hensel, M. (2011). "Cellular aspects of immunity to intracellular Salmonella enterica". Immunological Reviews 240 (1): 185–195. doi:10.1111/j.1600-065X.2010.00981.x. PMID 21349094.  edit
  5. ^ Kerr, M. C.; Wang, J. T. H.; Castro, N. A.; Hamilton, N. A.; Town, L.; Brown, D. L.; Meunier, F. A.; Brown, N. F.; Stow, J. L.; Teasdale, R. D. (2010). "Inhibition of the PtdIns(5) kinase PIKfyve disrupts intracellular replication of Salmonella". The EMBO Journal 29 (8): 1331–1347. doi:10.1038/emboj.2010.28. PMC 2868569. PMID 20300065.  edit
  6. ^ Yashroy, Rakesh Chander (2007). "Mechanism of infection of a human isolate Salmonella (3,10:r:-) in chicken ileum: Ultrastructural study". Indian Journal of Medical Research 126: 558–566. 
  7. ^ YashRoy R.C. (2003) Eucaryotic cell intoxication by Gram-negative organisms: A novel bacterial outermembrane-bound nanovesicular exocytosis model for for Type III secretion system. Toxicology International, vol. 10(1), pp. 1-9.
  8. ^ Sorrells, K.M.; M. L. Speck and J. A. Warren (January 1970). "Pathogenicity of Salmonella gallinarum After Metabolic Injury by Freezing". Applied and Environmental Microbiology 19 (1): 39–43. PMC 376605. PMID 5461164. Retrieved 2010-08-19. "Mortality differences between wholly uninjured and predominantly injured populations were small and consistent (5% level) with a hypothesis of no difference." 
  9. ^ Beuchat, L. R.; E. K. Heaton (June 1975). "Salmonella Survival on Pecans as Influenced by Processing and Storage Conditions". Applied and Environmental Microbiology 29 (6): 795–801. PMC 187082. PMID 1098573. Retrieved 2010-08-19. "Little decrease in viable population of the three species was noted on inoculated pecan halves stored at -18, -7, and 5°C for 32 weeks." 
  10. ^ Goodfellow, S.J.; W.L. Brown (August 1978). "Fate of Salmonella Inoculated into Beef for Cooking". Journal of Food Protection Vol. 41 No.8 41 (8): 598–605. 
  11. ^ Partnership for Food Safety Education (PFSE) Fight BAC! Basic Brochure.
  12. ^ USDA Internal Cooking Temperatures Chart. The USDA has other resources available at their Safe Food Handling fact-sheet page. See also the National Center for Home Food Preservation.
  13. ^ YashRoy R.C. (2000) Salmonella 3,10:r:- toxicity in rabbit ileum and liver by light and electron microscopy. Indian Journal of Pathology and Microbiology, vol. 43(1), pp. 17-22
  14. ^ YashRoy R.C. (1994) Liver damage by intra-ileal treatment with Salmonella 3,10:r:- extract as studied by light and electron microscopy. Indian Journal of Animal Sciences, vol. 64(6), pp. 597-599.
  15. ^ § 6 and § 7 of the German law on infectious disease prevention, Infektionsschutzgesetz
  16. ^ Centers for Disease Control and Prevention
  17. ^ Mittal R, Peak-Chew SY, Sade RS, Vallis Y, McMahon HT (2010). "The Acetyltransferase Activity of the Bacterial Toxin YopJ of Yersinia Is Activated by Eukaryotic Host Cell Inositol Hexakisphosphate". J Biol Chem 285 (26): 19927–34. doi:10.1074/jbc.M110.126581. PMC 2888404. PMID 20430892. 
  18. ^ María Lara-Tejero, Junya Kato, Samuel Wagner,Xiaoyun Liu, and Jorge E. Galán (February 2011). "A Sorting Platform Determines the Order of Protein Secretion in Bacterial Type III Systems". Science Express 331 (6021): 1188. doi:10.1126/science.1201476. 
  19. ^ "FDA/CFSAN - Food Safety A to Z Reference Guide - Salmonella". FDA - Center for Food Safety and Applied Nutrition. 2008-07-03. Archived from the original on 2009-03-02. Retrieved 2009-02-14. 
  20. ^ S. Cholerasuis pathology. Accessed April 3, 2009
  21. ^ F. Kauffmann: Die Bakteriologie der Salmonella-Gruppe. Munksgaard, Kopenhagen, 1941
  22. ^ L. Le Minor, M. Y. Popoff: Request for an Opinion. Designation of Salmonella enterica. sp. nov., nom. rev., as the type and only species of the genus Salmonella. In: Int. J. Syst. Bacteriol., Bd. 37, 1987, S. 465–468
  23. ^ Reeves MW, Evins GM, Heiba AA, Plikaytis BD, Farmer JJ (February 1989). "Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov". J. Clin. Microbiol. 27 (2): 313–20. PMC 267299. PMID 2915026. 
  24. ^ "The type species of the genus Salmonella Lignieres 1900 is Salmonella enterica (ex Kauffmann and Edwards 1952) Le Minor and Popoff 1987, with the type strain LT2T, and conservation of the epithet enterica in Salmonella enterica over all earlier epithets that may be applied to this species. Opinion 80". Int. J. Syst. Evol. Microbiol. 55 (Pt 1): 519–20. January 2005. doi:10.1099/ijs.0.63579-0. PMID 15653929. 
  25. ^ Tindall BJ, Grimont PA, Garrity GM, Euzéby JP (January 2005). "Nomenclature and taxonomy of the genus Salmonella". Int. J. Syst. Evol. Microbiol. 55 (Pt 1): 521–4. doi:10.1099/ijs.0.63580-0. PMID 15653930. 
  26. ^ Agbaje M, Begum RH, et al. Evolution of Salmonella nomenclature: a critical note. Folia Microbiol (Praha). 2011 Nov;56(6):497-503. doi: 10.1007/s12223-011-0075-4. Epub 2011 Nov 4. PMID 22052214
  27. ^ Janda JM, Abbott SL (2006). "The Enterobacteria", ASM Press.
  28. ^ Porwollik, S (editor) (2011). Salmonella: From Genome to Function. Caister Academic Press. ISBN 978-1-904455-73-8. 
  29. ^ Achtman, M.; Wain, J.; Weill, F. O. X.; Nair, S.; Zhou, Z.; Sangal, V.; Krauland, M. G.; Hale, J. L.; Harbottle, H.; Uesbeck, A.; Dougan, G.; Harrison, L. H.; Brisse, S.; S. Enterica MLST Study Group (2012). "Multilocus Sequence Typing as a Replacement for Serotyping in Salmonella enterica". In Bessen, Debra E. PLoS Pathogens 8 (6): e1002776. doi:10.1371/journal.ppat.1002776. PMC 3380943. PMID 22737074.  edit
  30. ^ Dominguez, Silvia A. Modeling the Growth of Salmonella in Raw Poultry Stored under Aerobic Conditions. 
  31. ^ Carmen Pin. Modelling Salmonella concentration throughout the pork supply chain by considering growth and survival in fluctuating conditions of temperature, pH and a. doi:10.1016/j.ijfoodmicro.2010.09.025. 
  32. ^ Pan, Wenjing. Modeling the Growth of Salmonella in Cut Red Round Tomatoes as a Function of Temperature. 
  33. ^ Li, Di. Development and Validation of a_w Mathematical Model for Growth of Pathogens in Cut Melons. doi:10.4315/0362-028X.JFP-12-398. 
  34. ^ Li, Di. "Development and validation of a mathematical model for growth of salmonella in cantaloupe". 
  35. ^ "Reptile-Associated Salmonellosis --- Selected States, 1998--2002". Centers for Disease Control and Prevention. 12 December 2003. Retrieved 9 October 2011. 
  36. ^ 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". PubMed 99 (3): 399–402. PMID 9041295. 
  37. ^ "Ongoing investigation into reptile associated salmonella infections". Health Protection Report 3 (14). 9 April 2009. Retrieved 12 April 2009. 
  38. ^ Multi-country outbreak of Salmonella Stanley infections Update EFSA Journal 2012;10(9):2893 [16 pp.]. Retrieved 04/23/2013
  39. ^ Multi-Country Outbreak Of Salmonella In Europe SGS SafeGuards Bulletin, Retrieved 04/18/2013
  40. ^ "Discovery paves way for salmonella vaccine". UC Davis. 
  41. ^ Nandre, Rahul M.; Lee, John Hwa (Jan 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 (2): 425–431. PMID 24176491. 
  42. ^ "Playing It Safe With Eggs". FDA Food Facts. 2013-02-28. 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." 
  43. ^ Gantois, Inne; Richard Ducatelle, Frank Pasmans, Freddy Haesebrouck, Richard Gast, Tom J. Humphrey, Filip Van Immerseel (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" 
  44. ^ Humphrey, T. J. (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. Retrieved 2010-08-19. "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 salmonellas to invade yolk contents." 
  45. ^ Stokes, J.L.; W.W. Osborne, H.G. Bayne (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." 
  46. ^ Okamura, Masashi; Yuka Kamijima, Tadashi Miyamoto, Hiroyuki Tani, Kazumi Sasai, Eiichiroh Baba (2001). "Differences Among Six Salmonella Serovars in Abilities to Colonize Reproductive Organs and to Contaminate Egges 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."" 
  47. ^ Gast, RK; D.R. Jones, K.E. Anderson, R. Guraya, J. Guard, P.S. Holt (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. 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.--" 
  48. ^ Jaeger, Gerald (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" 
  49. ^ Humphrey, T.J.; A. Whitehead, A. H. L. Gawler, A. Henley and B. Rowe (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. Retrieved 2010-08-19. "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." 
  50. ^ Gast, Richard; Rupa Guraya, Jean Guard, Peter Holt, Randle Moore (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". Journal of Avian Diseases 51 (1): 40–44. PMID 17461265. 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)--." 
  51. ^ Cummings, PL; Sorvillo F, Kuo T (November 2010). "Salmonellosis-related mortality in the United States, 1990-2006". Foodborne pathogens and disease 7 (11): 1393–9. doi:10.1089/fpd.2010.0588. PMID 20617938. 

External links[edit]