Salmonella

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This page is about microbiologic aspects of the organism(s).  For clinical aspects of the disease, see Salmonellosis.

Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: João André Alves Silva, M.D. [2] Jolanta Marszalek, M.D. [3]

Overview

Salmonella is a rod-shaped, facultative intracellular, gram-negative enterobacteria. Salmonella species shows motility, produces hydrogen sulfide, and only 1% is able to ferment lactose. It may be isolated from the stool of infected patients, and grown in culture media, such as MacConkey agar and deoxycholate agar. Salmonella enters the body through contaminated food or water, and invades the intestinal epithelial cells, causing inflammation.

This bacterium may be classified into 2 different species: Salmonella enterica and Salmonella bongori. Salmonella enterica is divided in 6 different subspecies, of which I, contains most pathogenic serotypes for humans. Salmonella may be serogrouped into more than 2500 serovars with polyvalent antisera, according to the capsular antigen, polysaccharide O antigens, and flagellar antigens. The bacteria show tropism for the epithelial cells of the gastrointestinal tract, macrophages, dendritic cells, and neutrophils. Different serotypes of Salmonella may have different natural reservoirs, some have humans as their only natural reservoir (serotypes Sendai and Typhi), while others (serotype Dublin) may infect humans and cattle.

Taxonomy

Cellular organism; Bacteria; Proteobacteria; Gammaproteobacteria; Enterobacteriales; Enterobacteriaceae

Biology

Computer-generated image of three drug-resistant non-typhoidal Salmonella bacteria. Adapted from Public Health Image Library (PHIL), Centers for Disease Control and Prevention.

Colonial growth pattern displayed by Salmonella enterica subsp. arizonae, formerly Salmonella choleraesuis and Arizona hinshawii bacteria grown on a blood agar culture plate Adapted from Public Health Image Library (PHIL), Centers for Disease Control and Prevention.

Salmonella is a gram-negative, facultative intracellular, anaerobic, non-spore-forming bacillus. It measures 2 to 3 by 0.4 to 0.6 μm. Salmonella is a non-lactose fermenting bacterium. It reduces nitrates, produces acid on glucose fermentation and does not produce cytochrome oxidase. Due to the presence of flagella, almost all salmonella species are motile. 1% of the bacteria is able to ferment lactose, which may be responsible for its non-detection in some culture media.

For the isolation of salmonella in culture, freshly passed stool are preferred. Common media for the growth of salmonella include: MacConkey agar, deoxycholate agar, and xylose-lysine-deoxycholate agar.

When the sample has a low number of bacteria, special enrichment broths, such as the selenite-based enrichment broth, may be used to raise the number of bacteria.

Infectious Cycle

Salmonella enterica enters the body through the mouth, by ingestion of contaminated food and water. For the bacteria to cause disease, an inoculum of about 50 000 pathogens is often required. Once in the intestine, the bacteria will first infect the apical epithelium. Salmonella will then initiate bacterial mechanisms that allow invasion of the host cells, inducing inflammatory changes, such as:

• Diffuse and focal infiltration of PMN
• Crypt abscesses
• Necrosis of the epithelium
• Fluid secretion
• Edema

Different serovars will have different preferable intestinal locations. An example is the enterocolitis at the terminal ileum, cecum, and proximal colon caused by serovar Typhimurium. Intestinal disease is marked by neutrophil migration to the intestinal epithelium. This recruitment is done by the secretion of interleukin-8, induced by Salmonella.

Classification

Before 1983 Salmonella was classified in several species. However, its genome study has shown high levels of DNA similarities among different types of salmonella, which leads to the actual classification of salmonella in 2 different species:

Salmonella enterica

• Contains six subspecies - I, II, IIIa, IIIb, IV, and VI:
  • I - enterica
  • II - salamae
  • III - arizonae
  • IIIb - diarizonae
  • IV - houtenae
  • VI - indica
• Subspecies I contains most pathogenic serotypes for humans
• Subspecies IIIa and IIIb, formerly belonging to the genus Arizonae, are responsible for rare human infections

Salmonella bongori

• Formerly subspecies V

Serovars

Salmonella subspecies may be serogrouped into more than 2500 serovars with polyvalent antisera. For this division the following bacterial structures are considered:

• Capsular antigen
• Polysaccharide O antigens
• Flagellar antigens

Different salmonella serotypes may also be distinguished in culture, according to their different metabolism of sugars. Different serovars may also have different disease manifestations. For example, Salmonella enterica, serovar Typhimurium is the causative agent of typhoid fever, and is not associated with classical salmonellosis.

Tropism

In vitro, Salmonella is able to interact with different types of cells. However, in vivo, the bacteria was found to enter only certain human cells, namely:

• Epithelial cells of the gastrointestinal tract - first cells to be infected by Salmonella
• Macrophages - where Salmonella survives and replicates
• Dendritic cells - relevant for dissemination of bacteria in the initial stages of infection, yet, they are not considered adequate reservoirs for Salmonella at latter stages
• Neutrophils - interaction is based on the immune response against the bacteria, hence this might not be considered true tropism

Differential diagnosis

Salmonella gastroenteritis must be differentiated from other causes of viral, bacterial, and parasitic gastroentritis.

Organism			Age predilection	Travel History	Incubation Size (cell)	Incubation Time	History and Symptoms			Diarrhea type8				Food source	Specific consideration
							Fever	N/V	Cramping Abd Pain	Small Bowel	Large Bowel	Inflammatory	Non-inflammatory
Viral	Rotavirus		<2 y	-	<102	<48 h	+	+	-	+			+	-	Mostly in day cares, most common in winter.
	Norovirus		Any age	-	10 -103	24-48 h	+	+	+	+			+	-	Most common cause of gastroenteritis, abdominal tenderness,
	Adenovirus		<2 y	-	105 -106	8-10 d	+	+	+	+			+	-	No seasonality
	Astrovirus		<5 y	-		72-96 h	+	+	+	+			+	Seafood	Mostly during winter
Bacterial	Escherichia coli	ETEC	Any age	+	108 -1010	24 h	-	+	+	+			+	-	Causes travelers diarrhea, contains heat-labile toxins (LT) and heat-stable toxins (ST)
		EPEC	<1 y	-	10†	6-12 h	-	+	+	+			+	Raw beef and chicken	-
		EIEC	Any ages	-	10†	24 h	+	+	+		+		+	Hamburger meat and unpasteurized milk	Similar to shigellosis, can cause bloody diarrhea
		EHEC	Any ages	-	10	3-4 d	-	+	+		+	+		Undercooked or raw hamburger (ground beef)	Known as E. coli O157:H7, can cause HUS/TTP.
		EAEC	Any ages	+	1010	8-18 h	-	-	+		+		+	-	May cause prolonged or persistent diarrhea in children
	Salmonella sp.		Any ages	+	1	6 to 72 h	+	+	+		+	+		Meats, poultry, eggs, milk and dairy products, fish, shrimp, spices, yeast, coconut, sauces, freshly prepared salad.	Can cause salmonellosis or typhoid fever.
	Shigella sp.		Any ages	-	10 - 200	8-48 h	+	+	+		+	+		Raw foods, for example, lettuce, salads (potato, tuna, shrimp, macaroni, and chicken)	Some strains produce enterotoxin and Shiga toxin similar to those produced by E. coli O157:H7
	Campylobacter sp.		<5 y, 15-29 y	-	104	2-5 d	+	+	+		+	+		Undercooked poultry products, unpasteurized milk and cheeses made from unpasteurized milk, vegetables, seafood and contaminated water.	May cause bacteremia, Guillain-Barré syndrome (GBS), hemolytic uremic syndrome (HUS) and recurrent colitis
	Yersinia enterocolitica		<10 y	-	104 -106	1-11 d	+	+	+		+	+		Meats (pork, beef, lamb, etc.), oysters, fish, crabs, and raw milk.	May cause reactive arthritis; glomerulonephritis; endocarditis; erythema nodosum. can mimic appendicitis and mesenteric lymphadenitis.
	Clostridium perfringens		Any ages		> 106	16 h	-	-	+		+		+	Meats (especially beef and poultry), meat-containing products (e.g., gravies and stews), and Mexican foods.	Can survive high heat,
	Vibrio cholerae		Any ages	-	106-1010	24-48 h	-	+	+	+			+	Seafoods, including molluscan shellfish (oysters, mussels, and clams), crab, lobster, shrimp, squid, and finfish.	Hypotension, tachycardia, decreased skin turgor. Rice-water stools
Parasites	Protozoa	Giardia lamblia	2-5 y	+	1 cyst	1-2 we	-	-	+	+			+	Contaminated water	May cause malabsorption syndrome and severe weight loss
		Entamoeba histolytica	4-11 y	+	<10 cysts	2-4 we	-	+	+		+	+		Contaminated water and raw foods	May cause intestinal amebiasis and amebic liver abscess
		Cryptosporidium parvum	Any ages	-	10-100 oocysts	7-10 d	+	+	+	+			+	Juices and milk	May cause copious diarrhea and dehydration in patients with AIDS especially with 180 > CD4
		Cyclospora cayetanensis	Any ages	+	10-100 oocysts	7-10 d	-	+	+	+			+	Fresh produce, such as raspberries, basil, and several varieties of lettuce.	More common in rainy areas
	Helminths	Trichinella spp	Any ages	-	Two viable larvae (male and female)	1-4 we	-	+	+		+		+	Undercooked meats	More common in hunters or people who eat traditionally uncooked meats
		Taenia spp	Any ages	-	1 larva or egg	2-4 m	-	+	+	+			+	Undercooked beef and pork	Neurocysticercosis: Cysts located in the brain may be asymptomatic or seizures, increased intracranial pressure, headache.
		Diphyllobothrium latum	Any ages	-	1 larva	15 d	-	-	-	+			+	Raw or undercooked fish.	May cause vitamin B12 deficiency

8Small bowel diarrhea: watery, voluminous with less than 5 WBC/high power field

Large bowel diarrhea: Mucousy and/or bloody with less volume and more than 10 WBC/high power field
† It could be as high as 1000 based on patient's immunity system.

The table below summarizes the findings that differentiate inflammatory causes of chronic diarrhea

Cause	History	Laboratory findings	Diagnosis	Treatment
Diverticulitis	Bloody diarrhea Left lower quadrant abdominal pain Abdominal tenderness on physical examination Low grade fever	Leukocytosis Elevated serum amylase and lipase Sterile pyuria on urinalysis	Abdominal CT scan with oral and intravenous (IV) contrast	bowel rest, IV fluid resuscitation, and broad-spectrum antimicrobial therapy which covers anaerobic bacteria and gram-negative rods
Ulcerative colitis	Diarrhea mixed with blood and mucus, of gradual onset. Signs of weight loss Rectal urgency Tenesmus Blood is often noticed on underwear Different degrees of abdominal pain	Anemia Thrombocytosis A high platelet count Elevated ESR (>30mm/hr) Low albumin	Endoscopy	Induction of remission with mesalamine and corticosteroids followed by the administration of sulfasalazine and 6-Mercaptopurine depending on the severity of the disease.
Entamoeba histolytica	Abdominal cramps Diarrhea Passage of 3 - 8 semiformed stools per day Passage of soft stools with mucus and occasional blood Fatigue Intestinal gas (excessive flatus) Rectal pain while having a bowel movement (tenesmus) Unintentional weight loss	cysts shed with the stool	detects ameba DNA in feces	Amebic dysentery Metronidazole 500-750mg three times a day for 5-10 days Tinidazole 2g once a day for 3 days is an alternative to metronidazole Luminal amebicides for E. histolytica in the colon: Paromomycin 500mg three times a day for 10 days Diloxanide furoate 500mg three times a day for 10 days Iodoquinol 650mg three times a day for 20 days For amebic liver abscess: Metronidazole 400mg three times a day for 10 days Tinidazole 2g once a day for 6 days is an alternative to metronidazole Diloxanide furoate 500mg three times a day for 10 days must always be given afterwards.

Natural Reservoir

Different salmonella serovars may have different natural reservoirs. Common types of serovars of salmonella enterica that infect the human gastrointestinal tract include serovars Sendai, Typhi, and Paratyphi. Humans are their only natural reservoir. Other serotypes, such as serotype Dublin, have cattle as their natural reservoir, but has also the capacity to cause infection in humans.

Drug Side Effect

• Vedolizumab

Related Chapters

• 1984 Rajneeshee bioterror attack
• List of foodborne illness outbreaks
• Food Testing Strips

Gallery

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  Salmonella bacteria in tetrathionate enrichment broth stained using direct FA staining technique. From Public Health Image Library (PHIL).

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  Salmonella bacteria in tetrathionate enrichment broth stained using direct FA staining technique. From Public Health Image Library (PHIL).

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  Triple sugar iron agar (TSI) tested for Salmonella (H2S+) and (H2S-); Citrobacter sp. and S. arizonae. From Public Health Image Library (PHIL).

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  Gram-negative bacilli, or rod-shaped Salmonella sp. bacteria. From Public Health Image Library (PHIL).

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  SEM depicts a number of red-colored Salmonella sp. bacteria invading a mustard-colored ruffled immune cell. From Public Health Image Library (PHIL).