Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 19, Number 1—January 2013

Cronobacter Infections Not from Infant Formula, Taiwan

On This Page
Article Metrics
citations of this article
EID Journal Metrics on Scopus

Cite This Article

To the Editor: Species of the genus Cronobacter are relatively heterogeneous at the phenotypic and molecular levels (1). In 2012, the following 7 Cronobacter species had been defined: C. sakazakii, C. malonaticus, C. turicensis, C. dublinensis, C. muytjensii, C. condimenti, and C. universalis (2). These opportunistic pathogens cause bacteremia and meningitis in neonates and are associated with necrotizing enterocolitis (3); ≈30% of infants with Cronobacter bacteremia or meningitis have died (4). Cronobacter spp. primarily infect infants, but infections among immunocompromised patients, particularly elderly patients, have been reported (5). Although these organisms are ubiquitous in the environment and have been isolated from a variety of foods, Cronobacter spp. infections in infants have been epidemiologically associated with ingestion of contaminated powdered infant formula (6). Few reports of C. sakazakii infections in adults have been published.

During 2002–2011, a total of 5 C. sakazakii isolates, 1 from each of 5 patients, were identified at the National Taiwan University Hospital in northern Taiwan (Table). These isolates were identified as belonging to the C. sakazakii group by use of 2 systems: PMIC/ID-30 (Becton Dickinson Diagnostic Systems, Sparks, MD, USA) and the Vitek 2 System GN card (bioMérieux Inc., La Balme les Grottes, France). The phenotypic profiles that use 14 biochemical characteristics to differentiate 7 species and 3 subspecies of C. dublinensis within Cronobacter gen. nov. (C. sakazakii group) have been described (2). Although we did not apply the 14 biochemical tests to differentiate the 5 isolates (2), the isolates’ lack of indole production and dulcitol utilization, obtained by use of Enterotube II (Becton Dickinson Diagnostic Systems), was compatible with identification of the following 3 species or subspecies: C. sakazakii, C. malonaticus, or C. dublinensis subsp. lausannensis (2). Results of partial 16S rRNA gene sequence analysis with primers 8FPL and 1492RPL indicated that the isolates were probably C. sakazakii (7), and results of a 2-step rpoB-based PCR that used 2 sets of primer pairs (Csakf/Csakr and Cmalf/Cmalr) confirmed that the isolates were C. sakazakii (8).

Serogroups of the 5 C. sakazakii isolates were determined by using 5 primer pairs specific to the wehC, wehI, and wzx genes (9). Of these 5 isolates, 3 were serogroup O1, and 2 were not typeable (not serogroups O1, O2, or O3).

Results of disk-diffusion susceptibility testing showed that all isolates were susceptible to cefotaxime, cefepime, piperacillin–tazobactam, ertapenem, imipenem, meropenem, ciprofloxacin, gentamicin, and amikacin and that all were resistant to cefazolin. The random amplified polymorphic DNA patterns generated by arbitrarily primed PCR that used 2 random oligonucleotide primers (M13 and ERIC1) differed among the 5 isolates, indicating that these 5 C. sakazakii strains were not clonally related (10).

The clinical and microbiological characteristics of the 5 patients (4 adult, 4 male) with C. sakazakii infection are summarized in the Table. Primary bacteremia was found in 2 patients, pneumonia in 2 (predominant growth of C. sakazakii from purulent sputum samples), and acute cholecystitis in 1.

The nonadult patient was a 2-month-old boy with congenital heart disease. Because of apnea and cyanosis, he was sent to an emergency department and later received assisted ventilation and supportive care in an intensive care unit. He was extubated on day 11 of hospitalization; however, fever and increased purulent sputum were noted on day 18. Bacterial culture of the suctioned sputum specimen yielded C. sakazakii. Before being hospitalized, the boy had been fed reconstituted powdered infant formula (Nestlé H.A.1, Gold; Nestlé Taiwan Ltd., Taipei, Taiwan) by mouth without other supplemental nutrition. During hospitalization, he received infant formula made by the hospital nutritional department through nasogastric tube. Although the powdered infant formula was not tested for C. sakazakii, initial sputum culture disclosed viridans group streptococci, and C. sakazakii was isolated from sputum obtained on day 18 of hospitalization. Thus, C. sakazakii from this infant might not have been associated with contaminated powdered infant formula.

Among the 4 adult patients, 3 had underlying solid organ malignancy and had received immunosuppressive drugs., and the other had bacteremia and died of cardiac arrest at arrival at the emergency department. The sources of C. sakazakii infection in the 1 nonimmunocompromised adult and the infant remain unclear; further research is needed to identify the source of C. sakazakii infections in Taiwan.


Hsih-Yeh Tsai, Chun-Hsing Liao, Yu-Tsung Huang, Ping-Ing Lee, and Po-Ren HsuehComments to Author 
Author affiliations: Author affiliations: Far Eastern Memorial Hospital, New Taipei City, Taiwan (H.-Y. Tsai, C.-H. Liao, Y.-T. Huang); National Taiwan University College of Medicine, Taipei, Taiwan (H.-Y. Tsai, Y.-T. Huang, P.-I. Lee, P.-R. Hsueh)



  1. Iversen  C, Waddington  M, On  SL, Forsythe  S. Identification and phylogeny of Enterobacter sakazakii relative to Enterobacter and Citrobacter species. J Clin Microbiol. 2004;42:536870. DOIPubMedGoogle Scholar
  2. Joseph  S, Cetinkaya  E, Drahovska  H, Levican  A, Figueras  MJ, Forsythe  SJ. Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. Int J Syst Evol Microbiol. 2012;62:127783. DOIPubMedGoogle Scholar
  3. Yan  QQ, Condell  O, Power  K, Butler  F, Tall  BD, Fanning  S. Cronobacter species (formerly known as Enterobacter sakazakii) in powdered infant formula: a review of our current understanding of the biology of this bacterium. J Appl Microbiol. 2012;113:115. Epub 2012 Apr 11. DOIPubMedGoogle Scholar
  4. Bowen  AB, Braden  CR. Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis. 2006;12:11859. DOIPubMedGoogle Scholar
  5. Skovgaard  N. New trends in emerging pathogens. Int J Food Microbiol. 2007;120:21724. DOIPubMedGoogle Scholar
  6. Healy  B, Cooney  S, O’Brien  S, Iversen  C, Whyte  P, Nally  J, Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. Foodborne Pathog Dis. 2010;7:33950. DOIPubMedGoogle Scholar
  7. Lai  CC, Cheng  A, Huang  YT, Chung  KP, Lee  MR, Liao  CH, Escherichia fergusonii bacteremia in a diabetic patient with pancreatic cancer. J Clin Microbiol. 2011;49:40012. DOIPubMedGoogle Scholar
  8. Stoop  B, Lehner  A, Iversen  C, Fanning  S, Stephan  R. Development and evaluation of rpoB based PCR systems to differentiate the six proposed species within the genus Cronobacter. Int J Food Microbiol. 2009;136:1658. DOIPubMedGoogle Scholar
  9. Jarvis  KG, Grim  CJ, Franco  AA, Gopinath  G, Sathyamoorthy  V, Hu  L, Molecular characterization of Cronobacter lipopolysaccharide O-antigen gene clusters and development of serotype-specific PCR assays. Appl Environ Microbiol. 2011;77:401726. DOIPubMedGoogle Scholar
  10. Hsueh  PR, Teng  LJ, Lee  LN, Yu  CJ, Yang  PC, Ho  SW, Melioidosis: an emerging infection in Taiwan? Emerg Infect Dis. 2001;7:42833.PubMedGoogle Scholar




Cite This Article

DOI: 10.3201/eid1901.120774

Related Links


Table of Contents – Volume 19, Number 1—January 2013

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.



Please use the form below to submit correspondence to the authors or contact them at the following address:

Po-Ren Hsueh, Departments of Laboratory Medicine and Internal Medicine, National Taiwan University Hospital, #7, Chung-Shan South Rd, Taipei 100, Taiwan

Send To

10000 character(s) remaining.


Page created: December 20, 2012
Page updated: December 20, 2012
Page reviewed: December 20, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.