Enterobacter, Cronobacter, and Pantoea Species

Microbiology And Epidemiology

The recent taxonomic re-classification of the former Enterobacteriaceae family places the genera Enterobacter and Cronobacter as members of the Enterobacteriaceae family, while Pantoea has been reassigned to the Erwinaceae family. The genus Enterobacter has undergone significant taxonomic revision. Although there are more than 15 named species, molecular techniques likely will identify additional species. Many former members of the genus Enterobacter have been transferred to other genera in the family Enterobacteriaceae, including the Klebsiella, Serratia, Hafnia, and Pantoea genera . Some have been transferred to new genera, including Lelliottia , Pluralibacter, and Kosakonia . Most notably, the former Enterobacter areogenes is now Klebsiella aerogenes . Despite the new designation of K. aerogenes , we will discuss it here with other members of the Enterobacter cloacae group, given the implications for identification and antimicrobial susceptibility.

The genus Pantoea has been proposed to accommodate several organisms with significant biochemical and nucleic acid diversity that formerly were included in the heterogeneous taxon called the Enterobacter agglomerans group. There are more than 20 species, with P. agglomerans and P. ananatis most commonly associated with human infections. Some commercial biochemical identification systems include P. agglomerans or P. agglomerans group in their databases, but they may not accurately differentiate among Pantoea species.

The Enterobacter spp. most commonly recovered from human sources include E. cloacae, K. aerogenes, and to a lesser extent, P. agglomerans group, Cronobacter spp., E. gergoviae, and E. asburiae . E. cloacae is by far the most common clinical isolate. A number of newly named species (formerly included in the E. cloacae group) are difficult to differentiate using biochemical test methods. Organisms formerly classified as E. sakazakii comprised a diverse group and are renamed as Cronobacter spp., which account for at least seven named species, of which C. sakazakii and C. malonaticus are most frequently isolated from human infections. Some commercial biochemical identification systems use the terms E. cloacae group and C. sakazakii group to describe these closely related and difficult to distinguish organisms.

Improved identification methods are needed. Matrix-assisted laser desorption/ionization–time of flight (MALDI-TOF) mass spectrometry demonstrates overall good performance in the identification of gram-negative bacilli. This technique is promising to differentiate among Enterobacter, Cronobacter, and Pantoea species.

Enterobacter, Cronobacter, and Pantoea spp. are non-fastidious in nature and grow on blood and chocolate agar and selective media for enteric bacteria. On MacConkey agar E. cloacae and K. aerogenes commonly appear as pink, lactose-fermenting, mucoid colonies similar in appearance to Klebsiella pneumoniae and Klebsiella oxytoca. Most isolates of Cronobacter spp. and P. agglomerans group organisms produce a non-diffusible, yellow pigment, which often is more intense when grown on enriched media at 25°C versus 35°C. Colonies of Cronobacter can appear dry, wrinkled, and leathery on some media.

Most isolates of Enterobacter spp . are motile, use citrate as a sole carbon source, and give a positive Voges-Proskauer (VP) test result but do not produce indole or hydrogen sulfide. With the exception of the P. agglomerans group organisms, most isolates have ornithine decarboxylase (ODC) activity. Motility and ornithine reactions help to differentiate Enterobacter spp. from the common human isolates of Klebsiella spp . , though K. aerogenes is motile and positive for ODC.

Commercial or conventional biochemical identification systems usually help in identifying and differentiating E. cloacae, K. aerogenes, P. agglomerans, and Cronobacter spp., but the other species present a greater challenge and are not all represented in the databases of commercial systems. The laboratory report of Enterobacter spp. or Cronobacter spp. may be sufficient for most clinical purposes, although knowledge of the specific species can be important in the setting of a potential healthcare-associated outbreak or when the clinical significance of the isolate is questioned.

Enterobacter spp. and Pantoea spp. are common in the gastrointestinal tract of humans and other mammals, and can be found in water, sewage, soil, plant material, and foods. Even the more common human isolates, E. cloacae and K. aerogenes, have been described as having ubiquitous animal and environmental distributions. Pantoea spp. are commonly associated with and can cause disease in plants.

In humans, Enterobacter spp. and Pantoea spp. are opportunistic pathogens and are among the most common causes of nosocomial pneumonia, urinary tract infection, surgical wound infection, and central-line-associated bloodstream infection (CLABSI). These organisms frequently colonize the skin, respiratory, urinary, and gastrointestinal tracts of hospitalized patients. These sites act as portals of entry for the establishment of localized or systemic disease. Enterobacter spp. and Pantoea spp. also cause community-acquired urinary tract, skin, soft tissue, and other infections, although at much lower rates than other gram-negative bacilli such as E. coli, Proteus spp., and Klebsiella spp. Community-acquired infections due to P. agglomerans have been associated with foreign bodies, in particular plant thorn and wood splinter injuries.

Enterobacter spp. accounted for 5% of all bacterial pathogens and 9% of gram-negative bacilli in more than 4000 episodes of nosocomial or community-acquired bloodstream infections (BSIs) in North America and Latin America in 1997. Of almost 75,000 gram-negative bacilli recovered from BSIs in patients in intensive care units (ICUs) in the US between 1993 and 2004 , Enterobacter spp. accounted for 14% of isolates.

Two US studies indicate that Enterobacter spp. represent the fourth and seventh most common pathogens causing BSI in pediatric ICUs (PICUs) and neonatal ICUs (NICUs), respectively. ^, A 2003 US study of ICU nosocomial bacterial infections reported that Enterobacter spp. accounted for 10% of pneumonia, 4% of BSI, 9% of surgical site, and 7% of urinary tract infections due to gram-negative bacilli. Enterobacter spp. also accounted for 15% of all gram-negative BSIs in children in Israel. An outbreak of E . gergoviae among adult kidney transplant recipients was associated with a common source of contamination, which was presumed to be urinary catheters or stents.

An endogenous source of Enterobacter spp. is most common in nosocomial infections. Approximately 40% of infants are fecal carriers of Klebsiella or Enterobacter spp. on discharge from NICUs. Colonization in nursery settings has been associated with overcrowding, inadequate handwashing, low birth weight, prematurity, endotracheal intubation, prolonged hospitalization, contaminated infant formula or parenteral nutrition fluid, and the use of antibiotics or central venous catheters (CVCs). Risk factors for infection include immunosuppression from any cause, prematurity, use of devices (e.g., CVC, endotracheal tube, urinary catheter), and prior use of antibiotics. The role of microbial virulence factors in the pathogenicity of these organisms has been reviewed.

Clinical Manifestations