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Cronobacter infections not from infant formula, Taiwan.
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MedLine Citation:
PMID:  23260041     Owner:  NLM     Status:  MEDLINE    
Hsih-Yeh Tsai; Chun-Hsing Liao; Yu-Tsung Huang; Ping-Ing Lee; Po-Ren Hsueh
Publication Detail:
Type:  Case Reports; Letter    
Journal Detail:
Title:  Emerging infectious diseases     Volume:  19     ISSN:  1080-6059     ISO Abbreviation:  Emerging Infect. Dis.     Publication Date:  2013 Jan 
Date Detail:
Created Date:  2012-12-24     Completed Date:  2013-06-03     Revised Date:  2013-07-11    
Medline Journal Info:
Nlm Unique ID:  9508155     Medline TA:  Emerg Infect Dis     Country:  United States    
Other Details:
Languages:  eng     Pagination:  167-9     Citation Subset:  IM    
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MeSH Terms
Bacterial Typing Techniques
Cronobacter sakazakii / classification,  genetics*,  isolation & purification
Enterobacteriaceae Infections / diagnosis,  microbiology*
Infant Formula
Middle Aged
RNA, Ribosomal, 16S / classification,  genetics,  isolation & purification
Reg. No./Substance:
0/RNA, Ribosomal, 16S

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

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Journal Information
Journal ID (nlm-ta): Emerg Infect Dis
Journal ID (iso-abbrev): Emerging Infect. Dis
Journal ID (publisher-id): EID
ISSN: 1080-6040
ISSN: 1080-6059
Publisher: Centers for Disease Control and Prevention
Article Information
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Print publication date: Month: 1 Year: 2013
Volume: 19 Issue: 1
First Page: 167 Last Page: 169
PubMed Id: 23260041
ID: 3557994
Publisher Id: 12-0774
DOI: 10.3201/eid1901.120774

Cronobacter Infections Not from Infant Formula, Taiwan Alternate Title:Cronobacter Infections, Taiwan
Hsih-Yeh Tsai
Chun-Hsing Liao
Yu-Tsung Huang
Ping-Ing Lee
Po-Ren Hsueh
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)
Correspondence: Address for correspondence: Po-Ren Hsueh, Departments of Laboratory Medicine and Internal Medicine, National Taiwan University Hospital, #7, Chung-Shan South Rd, Taipei 100, Taiwan; email:

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.


Suggested citation for this article: Tsai H-Y Liao C-H, Huang Y-T, Lee P-I, and Ren Hsueh PR. Cronobacter infections not from infant formula, Taiwan [letter]. Emerg Infect Dis [Internet]. 2013 Jan [date cited].

1. . IversenC, WaddingtonM, OnSL, ForsytheS. Identification and phylogeny of Enterobacter sakazakii relative to Enterobacter and Citrobacter species.J Clin Microbiol. Year: 2004;42:5368–7010.1128/JCM.42.11.5368-5370.200415528745
2. . JosephS, CetinkayaE, DrahovskaH, LevicanA, FiguerasMJ, ForsytheSJ. 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. Year: 2012;62:1277–8310.1099/ijs.0.032292-022661070
3. . YanQQ, CondellO, PowerK, ButlerF, TallBD, FanningS. 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. Year: 2012;113:1–15 Epub 2012 Apr 11. 10.1111/j.1365-2672.2012.05281.x22420458
4. . BowenAB, BradenCR. Invasive Enterobacter sakazakii disease in infants.Emerg Infect Dis. Year: 2006;12:1185–910.3201/eid1708.05150916965695
5. . SkovgaardN. New trends in emerging pathogens.Int J Food Microbiol. Year: 2007;120:217–2410.1016/j.ijfoodmicro.2007.07.04617976849
6. . HealyB, CooneyS, O’BrienS, IversenC, WhyteP, NallyJ, et al. Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen.Foodborne Pathog Dis. Year: 2010;7:339–5010.1089/fpd.2009.037919958103
7. . LaiCC, ChengA, HuangYT, ChungKP, LeeMR, LiaoCH, et al. Escherichia fergusonii bacteremia in a diabetic patient with pancreatic cancer.J Clin Microbiol. Year: 2011;49:4001–210.1128/JCM.05355-1121918030
8. . StoopB, LehnerA, IversenC, FanningS, StephanR. Development and evaluation of rpoB based PCR systems to differentiate the six proposed species within the genus Cronobacter.Int J Food Microbiol. Year: 2009;136:165–810.1016/j.ijfoodmicro.2009.04.02319467725
9. . JarvisKG, GrimCJ, FrancoAA, GopinathG, SathyamoorthyV, HuL, et al. Molecular characterization of Cronobacter lipopolysaccharide O-antigen gene clusters and development of serotype-specific PCR assays.Appl Environ Microbiol. Year: 2011;77:4017–2610.1128/AEM.00162-1121531829
10. . HsuehPR, TengLJ, LeeLN, YuCJ, YangPC, HoSW, et al. Melioidosis: an emerging infection in Taiwan?Emerg Infect Dis. Year: 2001;7:428–3311384520

[TableWrap ID: T1] Table  Characteristics of 5 patients with Cronobacter sakazakii infections, National Taiwan University Hospital, Taiwan, 2002–2011*
Patient age/sex Year of diagnosis Underlying medical conditions Clinical
presentation Infection type Outcome Isolation site Isolate GenBank accession no. Isolate serogroup
77 y/M 2002 Laryngeal cancer, diabetes mellitus, pulmonary tuberculosis Cardiac arrest at arrival at emergency department Primary bacteremia Died Blood FJ947061.1 O1
72 y/M 2002 Gastric cancer Fever Primary bacteremia Survived Blood JF330153.1 NT
2 mo/M 2005 Congenital heart disease Fever Pneumonia Survived Sputum F330133.1 O1
37 y/M 2008 None Abdominal pain Acute cholecystitis Survived Bile JF330153.1 NT
64 y/F 2011 Breast cancer Hemoptysis Pneumonia Survived Sputum GU727684.1 NT

*All isolates were identified as C. sakazakii I (99% identity) by 16S sequencing. NT, not typeable (not serogroups O1, O2, or O3).

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Keywords: Keywords: Cronobacter sakazakii, infection, Taiwan, bacteria, adults, immunocompromised, infant formula.

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