Isolation and Identification Enterobacter asburiae from Consumed Powdered Infant Formula Milk (PIF) in the Neonatal Intensive Care Unit (NICU)

  • Jalal Mardaneh Department of Microbiology, School of Medicine, Gonabad University of Medical Sciences, Gonabad, Iran.
  • Mohammad Mehdi Soltan Dallal Mail Food Microbiology Research Center, Tehran University of Medical Sciences, Tehran, Iran. AND Divison of Bacteriology, Department of Pathobiology and Microbiology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
Powdered infant formula milk (PIF), Neonatal intensive care unit (NICU), E. asburiae


Enterobacter asburiae (E. asburiae) is a facultative anaerobic, non-spore-forming gram-negative rod-shaped bacterium belonging to the family of Enterobacteriaceae. It is an opportunistic pathogen that its strains are isolated from a variety of clinical and environmental specimens. Since powdered infant formula milk (PIF) is not a sterile product, it is an excellent medium for bacterial growth. The aim of this study was to isolate and identify E. asburiae from PIF in the neonatal intensive care unit (NICU) and determine antimicrobial susceptibility patterns of this bacterium. A total 125 PIF samples were purchased from drug stores between June 2011 to March 2012. E. asburiae was isolated according to FDA method. For final confirmation, biochemical tests embedded in the API-20E system were used. The drug susceptibility test was performed using the disc diffusion method according to CLSI recommendations. Out of the 125 PIF samples investigated, 2 (1.6%) samples were positive for E. asburiae. All isolated strains were uniformly susceptible to aztreonam, cefotaxim, amikacin, streptomycin, nalidixic acid, meropenem, tetracycline, ceftazidime, and colistin. Variable susceptibility was seen to the some antimicrobial agents tested. Each country should categorize its own designed guidelines for the preparation and handling of PIF adapted to the local environment. Moreover, the pathogenesis of the E. asburiae in infants hospitalized in NICU and other groups such as immunosuppressed patients and HIV infected individuals is uncertain and requires further study.


Hoffmann H, Stindl S, Ludwig W, et al. Reassignment of Enterobacter dissolvens to Enterobacter cloacae as E. cloacae subspecies dissolvens comb. nov and emended description of Enterobacter asburiae and Enterobacter kobei. Syst Appl Microbiol 2005;28(3):196-205.

Asis CA Jr, Adachi K. Isolation of endophytic diazotroph Pantoea agglomerans and nondiazotroph Enterobacter asburiae from sweetpotato stem in Japan. Lett Appl Microbiol 2004;38(1):19-23.

Cha SW, Heo JN, Park CK, et al. Enterobacter asburiae Pneumonia with Cavitation. J Korean Soc Radiol 2013;68(3):217-9.

Brenner DJ, McWhorter A, Kai A, et al. Enterobacter asburiae sp. nov., a new species found in clinical specimens, and reassignment of Erwinia dissolvens and Erwinia nimipressuralis to the genus Enterobacter as Enterobacter dissolvens comb. nov. and Enterobacter nimipressuralis comb. nov. J Clin Microbiol 1986;23(6):1114-20.

Farmer JJ 3rd, Davis BR, Hickman-Brenner FW, et al. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. J Clin Microbiol 1985;21(1):46-76.

Bi C, Rice JD, Preston JF. Complete fermentation of xylose and methylglucuronoxylose derived from methylglucuronoxylan by Enterobacter asburiae strain JDR-1. Appl Environ Microbiol 2009;75(2):395-404.

Paterson DL, Rossi F, Baquero F, et al. In vitro susceptibilities of aerobic and facultative gram-negative bacilli isolated from patients with intra-abdominal infections worldwide: the 2003 Study for Monitoring Antimicrobial Resistance Trends (SMART). J Antimicrob Chemother 2005;55(6):965-73.

Elbeltagy A, Nishioka K, Sato T, et al. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 2001;67(11):5285-93.

Siddiqui IA, Shaukat SS. Endophytic colonization of Phaseolus vulgaris by Pseudomonas fluorescens strain 89B-27 and Enterobacter asburiae strain JM22. Improv Plant Productivity by Rhizosphere Bacteria 1997;180(1):111-20.

McInroy JA, Kloepper JW. Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 1995;173(2):337-42.

Koth K, Boniface J, Chance EA, et al. Enterobacter asburiae and Aeromonas hydrophila: soft tissue infection requiring debridement. Orthopedics 2012;35(6):e996-9.

Stewart JM, Quirk JR. Community-acquired pneumonia caused by Enterobacter asburiae. Am J Med 2001;111(1):82-3.

Pitout JD, Moland ES, Sanders CC, et al. Beta-lactamases and detection of beta-lactam resistance in Enterobacter spp. Antimicrob Agents Chemother 1997;41(1):35-9.

Sheng WH, Badal RE, Hseuh PR. Distribution of Extended-spectrum β-lactamases (ESBLs), AmpC β- lactamases, and Carbapenemases among Enterobacteriaceae Isolates Causing Intra-abdominal Infections in Asia-Pacific: the Study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother 2013;57(7):2981-8.

Callaghan C. Infection control in the neonatal intensive care unit. Nurs Stand 2007;22(1):35-41.

Pratt RJ, Pellowe CM, Wilson JA, et al. epic2: national evidence-based guidelines for preventing healthcareassociated infections in NHS hospitals in England. J Hosp Infect 2007; 65(Suppl 1):S1-64.

Polin RA, Saiman L. Nosocomial Infections in the Neonatal Intensive Care Unit. Neo Rev 2003;4(3):81-9.

Mardaneh J, Soltan-Dallal MM. Isolation and Identification of E. cowanii from Powdered Infant Formula in NICU and Determination of Antimicrobial Susceptibility of Isolates. Iran J Pediatr 2014;24(3):261-6.

Mardaneh J, Soltan Dallal MM, Taheripoor M, et al. Isolation, Identification and Antimicrobial Susceptibility Pattern of Tatumella ptyseos Strains Isolated from Powdered Infant Formula Milk Consumed in Neonatal Intensive Care Unit: First Report from Iran. Jundishapur J Microbiol 2014;7(6):e10608.

Poorabbas B, Mardaneh J, Rezaei Z, et al. Nosocomial Infections: Multicenter surveillance of antimicrobial resistance profile of Staphylococcus aureus and gram negative rods isolated from blood and other sterile body fluids in Iran. Iran J Microbiol 2015;7(3):127-35.

Hewitt KM, Mannino FL, Gonzalez A, et al. Bacterial Diversity in Two Neonatal Intensive Care Units (NICUs). PLoS One 2013;8(1):e54703.

Akonor PT, Akonor MA. Food Safety Knowledge: The Case of Domestic Food Handlers in Accra. Eur J Nutr Food Saf 2013;3(3):99-111.

Mardaneh J, Dallal MM. Isolation, identification and antimicrobial susceptibility of Pantoea (Enterobacter) agglomerans isolated from consumed powdered infant formula milk (PIF) in NICU ward: First report from Iran. Iran J Microbiol 2013;5(3):263-7.

Abbasi P, Kargar M, Doosti A, et al. Characterization of Shiga-toxin producing E. coli (STEC) and enteropathogenic E.coli (EPEC) using multiplex Real- Time PCR assays for stx1 , stx2 , eaeA. Iran J Microbiol 2014;6(3):169-74.

Hassanzadeh P, Hassanzadeh Y, Mardaneh J, et al. Isolation of Methicillin-Resistant Staphylococcus aureus (MRSA) from HIV Patients Referring to HIV Referral Center, Shiraz, Iran, 2011-2012. Iran J Med Sci 2015;40(6):526-30.

Anvarinejad M, Pouladfar Gh, Japoni A, et al. Isolation and Antibiotic Susceptibility of the Microorganisms Isolated from Diabetic Foot Infections in Nemazee Hospital, Southern Iran. J Pathogen 2015;1-7.

How to Cite
Mardaneh J, Soltan Dallal MM. Isolation and Identification Enterobacter asburiae from Consumed Powdered Infant Formula Milk (PIF) in the Neonatal Intensive Care Unit (NICU). Acta Med Iran. 54(1):39-43.
Original Article(s)