Essential Microbiology for Dentistry. 5th ed.

Chapter 15. Enterobacteria

Most of the commensal Gram-negative rods that inhabit the normal gastrointestinal tract, and sometimes cause disease, belong to the family Enterobacteriaceae. They are also colloquially termed coliforms. All species belonging to this family are Gram-negative, facultative anaerobes that ferment glucose. The major medically important species are listed in Table 15.1.

General characteristics of enterobacteria


Found in the human gut, at a density of approximately 10cells per gram of faeces. However, the predominant species in the gut is Bacteroides. Up to 15% of the population may harbour enterobacteria in the oral cavity, mostly as transient commensals. Their oral carriage rate may increase in old age, and in states leading to reduced salivary flow (xerostomia).


Rapidly growing cells 2 x 0.4 μm in size; may appear coccobacillary. Many species are motile and possess a capsule, especially on initial isolation. All species are endotoxigenic because of the lipopolysaccharide outer cell wall. They also possess pili and flagella, which mediate adhesion and locomotion, respectively (Fig. 15.1).

Culture and identification

Grow well on ordinary media (e.g., blood agar, MacConkey's agar), producing characteristic circular, convex and glistening/ mucoid colonies. Some motile species form swarming patterns on agar cultures. Most species are non-pigmented; a few produce red, pink, yellow or blue pigments.

Enterobacteriaceae ferment a large number of carbohydrates. This property, together with other biochemical tests, is used to identify and differentiate species.

Lactose fermentation

Growth on indicator media is used for the initial categorization of Enterobacteriaceae into two groups: lactose fermenters and lactose non-fermenters. Several selective media, such as MacConkey's and cystine-lactose-electrolyte-deficient (CLED) media, are available for this purpose. On MacConkey's agar, the lactose fermenters appear as pink colonies, whereas on CLED medium, the colour of lactose fermentation is yellow.

Other biochemical tests

Commercially available kit systems are routinely used to identify species of enterobacteria. The commonly available test systems are based on 10 (API 10E) or 20 (API 20E, Rapid E) biochemical tests (Fig. 15.2).

Serological tests

These are based on the antigens of the organisms. All species have the somatic (O) antigen, and most have the flagellar (H) antigen. The capsular (K) antigen is seen in some species. The antigens are useful in the classification of species and invaluable for epidemiological investigation of outbreaks of disease. Identification of strains within a species can also be done by bacteriophage typing, bacteriocin typing, plasmid analysis and polypeptide analysis.


All Enterobacteriaceae are potentially pathogenic. Patients who are immunosuppressed, undergoing mechanical or medical manipulation, and have underlying disease are most susceptible to infection.

Endotoxin shock

This can be precipitated in humans by the lipopolysaccharide, which all Enterobacteriaceae release when they are destroyed. Toxic lipopolysaccharide comprises lipid A, the core polysaccharide and the O antigen; the lipid A is responsible for most of the symptoms associated with endotoxic shock. The toxic effects of lipopolysaccharide are many and include fever, hypotension, intravascular coagulation and effects on the immune system. Large doses of endotoxin may cause death.


The antibiotic sensitivity patterns of enterobacteria are complex as they readily acquire resistance-coding plasmids. A spectrum of antibiotics are used, including ampicillin/amoxicillin, cephalosporins, aminoglycosides, trimethoprim, chloramphenicol and ciprofloxacin.


The tribe Eschericheae includes five genera: Escherichia, Salmonella, Shigella, Edwardsiella and Citrobacter. The most important human pathogens in this group, Escherichia coli and the Salmonella and Shigella species, are described here.

Escherichia coli

Habitat and transmission

Indigenous commensal of the human intestinal tract; transmission is either endogenous or exogenous.

Table 15.1 Enterobacteria commonly causing human disease


Representative species (no. of species)



E. coli (5)

Gastroenteritis, wound and urinary tract infection


S. dysenteriae S. flexneri S. boydii S. sonnei



S. typhi

S. typhimurium (7 subgroups)

Enteric fever (typhoid) Food poisoning


K. pneumoniae (7)





M. morganii (2) P mirabilis (4)

P. stuartii (5)

Urinary tract infection and other types of sepsis


Y pestis (11)

Plague, septicaemia, enteritis, etc.




C. freundii (4)

E. cloacae (13)

S. marcescens (10)

Low pathogenicity, opportunistic infections

Fig. 15.1 A scanning electron micrograph of Escherichia coli showing fimbriae and flagella (x10 000).

Fig. 15.2 Commercial identification kit for Enterobacteriaceae. This plate illustrates a colour reaction profile obtained after overnight incubation of the organism. The identity of the organism is Klebsiella pneumoniae.


Gram-negative rods, motile, sometimes capsulate, facultative anaerobe, bile-tolerant.

Culture and identification

Grows well on blood agar; ferments lactose (hence pink colonies on MacConkey's agar and yellow on CLED agar). Commercial kits, such as API 20E, are used in identification (Fig. 15.2). Biotyping systems are useful for strain delineation.


Escherichia coli is a major agent of sepsis; it causes the following diseases.

Urinary tract infection

Young women and elderly adults are the most susceptible. The disease varies from simple urethritis to serious pyelonephritis.

Diarrhoeal diseases

These range from simple diarrhoea to severe disease leading to excessive fluid loss and dehydration, which may be fatal in malnourished infants and elderly debilitated adults. Many strains of enteropathogenic Escherichia coli have powerful toxins and other mechanisms by which they cause diarrhoea:

 Enterotoxins: mainly two types, both coded by plasmids, one is heat-labile (LT) and is similar in action to the cholera toxin, and the other is heat-stable (ST).

 Enteroinvasiveness: some strains have the ability to invade intestinal epithelial cells and cause inflammation.

 Adhesive factors are produced by some strains enabling adhesion to mucosae; termed 'colonization factor antigens', these are mediated by plasmid-coded pili.

 Vero cytotoxicity is caused by strains that have the ability to induce cytopathic effects on Vero cells (grown in tissue culture). Verotoxin (VT) producers can cause diarrhoea with haemorrhagic symptoms (e.g., Escherichia coli O157).

Based on the above, diarrhoea-producing Escherichia coli can be divided into five types:

1. enteropathogenic Escherichia coli (EPEC)

2. enteroinvasive Escherichia coli (EIEC)

3. enterotoxigenic Escherichia coli (ETEC)

4. enterohaemorrhagic Escherichia coli (EHEC)

5. enteroaggregative Escherichia coli (EAEC).

Neonatal meningitis and septicaemia

Other infections Escherichia coli may cause include neonatal meningitis, septicaemia and wound infection, particularly after surgery of the lower intestinal tract.


The genus Salmonella has a bewildering spectrum of more than 2000 species living in the intestinal tract of humans, domesticated animals and poultry. Salmonella typhi and Salmonella paratyphi differ from others in that humans are the only known natural host.

Salmonella spp.

Habitat and transmission

Leading sources of salmonella infection are poultry products (i.e., flesh and eggs) and pet turtles (in the USA). Occupational salmonellosis affects veterinary and slaughterhouse workers. Infection is by ingestion of contaminated food, or person-to-person via the faecal-oral route. The carrier state, which develops in some after infection, is an important source of organisms.


Gram-negative, motile, non-sporing rods. All except Salmonella typhi are non-capsulate; facultative anaerobes.

Culture and identification

Culture on MacConkey's medium or deoxycholate citrate agar yields non-lactose-fermenting colonies. A combination of biochemical tests and serotyping is required for full identification. The latter is complex as salmonellae have a variety of antigens; notable are the O (somatic) and the H (flagellar) antigens; virulent strains, notably Salmonella typhi, have a capsular polysaccharide antigen designated the Vi (virulence) antigen. There are more than 1700 serotypes of Salmonella enteritidis.


The major types of salmonellosis (diseases due to Salmonella) are enteric fever, gastroenteritis and septicaemia.

Enteric fever (typhoid fever)

Caused by Salmonella typhi or Salmonella paratyphi A, B or C (see Chapter 26).


The most common form of salmonellosis, and can be due to any of the Salmonella enteritidis serotypes. Symptoms appear 10-24 h after ingestion of highly contaminated food or beverage. Nausea, vomiting, abdominal cramps, headache and diarrhoea are common.


Frequently caused by Salmonella dublin or Salmonella choleraesuis; a fulminant, sometimes fatal, disease independent of intestinal symptoms. Pneumonia, meningitis and osteomyelitis may result from haematogenous spread of the bacteria.

Treatment and prevention

Proper cooking of foods derived from animal sources. Typhoid vaccine, a killed suspension of Salmonella typhi, is available for those travelling to or living in areas where typhoid fever is endemic.


Shigella species cause bacillary dysentery. The genus is divided into four species (Shigella dysenteriae, Shigella sonnei, Shigella flexneri and Shigella boydii) and a variety of serotypes.

Shigella spp.

Habitat and transmission

The only reservoir is the human intestine. Infection is spread by the faecal-oral route under crowded conditions. A minute dose of the organisms is adequate to cause disease.


Gram-negative, non-motile rods (compare salmonellae); non-capsulate.

Culture and identification

All species grow well on ordinary media and are non-lactose fermenters (except Shigella sonnei, a slow lactose fermenter). Commercial kits are used in identification.


Although shigellae do not invade systemically like salmonellae, they locally invade the intestinal epithelium (ileum and colon). The resultant intense inflammatory response is characterized by bloody, mucopurulent diarrhoea (dysentery). Although no enterotoxin is produced, the exotoxin of Shigella species is neurotoxic.

Treatment and prevention

Severe dysentery is managed by fluid and electrolyte replacement. Antibiotics should be avoided as many strains are resistant to multiple antibiotics. Spread can be controlled by improving sanitation and personal hygiene to interrupt faecal-oral transmission; hand hygiene is critical.


A number of species belonging to this tribe, namely Klebsiella, Enterobacter and Serratia, are indigenous to the human intestinal and respiratory tracts. They are also occasionally isolated from the oral cavity and hence are considered transient oral commensals. They cause serious disease in immunocompromised patients, especially in hospital environments (nosocomial infection).

Klebsiella pneumoniae

As the name indicates, Klebsiella pneumoniae may sometimes cause a severe destructive pneumonia. It also causes nosocomial urinary tract infection. The virulence of the organism is mainly due to its large antiphagocytic capsule. This species is isolated from the oropharynx or gastrointestinal tract of about 5% of healthy people, and the isolation rate is higher in the hospitalized.

Enterobacter spp.

Enterobacter species are indigenous to the intestinal tract but can be found on plants and as free-living saprophytes. They may cause nosocomial urinary tract infection and very rarely a primary infection. Enterobacter cloacae and Enterobacter aero- genes are the most frequently isolated as transients in the oral cavity.

Serratia spp.

Serratia marcescens grows as characteristic magenta-coloured colonies. It may occasionally cause fatal disease in neonates, and in immunosuppressed and debilitated individuals.


Pseudomonas species are not enterobacteria, but they are included in this chapter for convenience as they are Gram-negative rods with somewhat similar properties. The genus contains a large number of species, but only a few are human pathogens. They are widely distributed in the environment and may cause disease, especially in hospital settings. Pseudomonas aeruginosa is the most important species to cause such infection and is a special problem in burns patients.

Pseudomonas aeruginosa

Habitat and transmission

Colonizes the human intestine in a few healthy individuals and in a large proportion of hospitalized patients. Colonizes environmental surfaces, especially under moist conditions. Thus, they are found in dental unit water lines, as harmless saprophytes.


Aerobic, Gram-negative rods, motile by means of polar flagella. Grow over a very wide temperature range, including room temperature.

Culture and identification

Grow easily on routine media, producing irregular, moist, iridescent colonies with a characteristic 'fishy' aroma. Identified using commercial kits.


Virulence factors identified include lipopolysaccharide endotoxin, an exotoxin, extracellular proteases and elastases, and an extracellular 'slime' that prevents phagocytosis.

Treatment and prevention

Although this species is resistant to most antimicrobials, it is sensitive to aminoglycosides and certain β-lactams (e.g., acylureidopenicillins), cephalosporins and polymyxin. Prevention is by good asepsis in hospitals and rational antibiotic therapy (to prevent emergence of resistant isolates).

Key facts

 Enterobacteriaceae are short Gram-negative rods, facultative anaerobes that ferment glucose and usually live in the intestinal tract.

 This extensive group of bacteria are classified according to their somatic (O) antigen (cell wall lipopolysaccharide), flagellar (H) antigen and capsular (K) antigen.

 Most, if not all, possess pili; capsules and flagella may be present.

 All produce endotoxin, and some produce powerful exotoxins.

 Escherichia coli is the predominant facultative inhabitant of the human intestinal tract.

 Diarrhoea-producing Escherichia coli can be divided into enteropathogenic (EPEC), enteroinvasive (EIEC), enterotoxigenic (ETEC), enterohaemorrhagic (EHEC) and enteroaggregative (EAEC) types.

Salmonellae and shigellae are responsible for a variety of gastrointestinal disorders.

Shigella is the cause of most dysentery in the West. Hundreds of species of Salmonella have been identified; they are the agents of typhoid fever, gastroenteritis and septicaemia.

Klebsiella, Enterobacter and Serratia, together with Escherichia coli, are indigenous to the human intestinal and respiratory tracts but are also occasionally isolated from the oral cavity; hence, they are considered to be transient oral commensals.

The latter groups may cause serious disease in hospital environments (nosocomial infection), particularly in compromised patients; these infections are often resistant to many antimicrobials.

Review questions (answers on p. 365)

Please indicate which answers are true, and which are false.

15.1 Enterobacteria:

A. are frequently implicated in periodontal infections

B. are Gram-variable

C. are an important cause of hospital-acquired infections

D. are found in the oral cavity of up to 25% of the population

E. are associated with ventilator-associated pneumonia

15.2 Escherichia coli:

A. produces a heat-labile and a heat-stable enterotoxin

B. causes neonatal meningitis

C. is a major pathogen causing nosocomial infections

D. strain O157 causes a diarrhoeal disease similar to cholera

E. can cause food poisoning

15.3 Which of the following organisms has a polysaccharide capsule?

A. Shigella sonnei

B. Klebsiella pneumoniae

C. Escherichia coli

D. Salmonella paratyphi

E. Bacillus anthracis

15.4 Pseudomonas aeruginosa:

A. is an important agent of nosocomial infections

B. is resistant to most antimicrobial agents

C. colonies produce a 'fruity' smell

D. in dental unit water lines cause significant morbidity

E. produces an extracellular slime that resists phagocytosis

Further reading

Brooks, J. F., Carroll, K. C., Butel, J. S., et al. (Eds.), (2013). Enteric Gram negative rods (Enterobacteriaceae). In Jawetz, Melnick & Adelberg's Medical microbiology (26th ed., pp. 229-244). New York: McGraw Hill. Chapter 15. [e-Book].

Sedgley, C., & Samaranayake, L. P. (1994). Oropharyngeal prevalence of Enterobacteriaceae in humans: A review. Journal of Oral Medicine and Oral Pathology, 23, 104-113.

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