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Human gastroenteritis outbreak associated with Escherichia albertii, Japan.
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MedLine Citation:
PMID:  23260717     Owner:  NLM     Status:  MEDLINE    
Although Escherichia albertii is an emerging intestinal pathogen, it has been associated only with sporadic human infections. In this study, we determined that a human gastroenteritis outbreak at a restaurant in Japan had E. albertii as the major causative agent.
Tadasuke Ooka; Eisuke Tokuoka; Masato Furukawa; Tetsuya Nagamura; Yoshitoshi Ogura; Kokichi Arisawa; Seiya Harada; Tetsuya Hayashi
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Publication Detail:
Type:  Journal Article; Research Support, Non-U.S. Gov't    
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:  144-6     Citation Subset:  IM    
University of Miyazaki, Miyazaki, Japan.
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MeSH Terms
Adhesins, Bacterial / genetics*
Bacterial Typing Techniques
Disease Outbreaks*
Electrophoresis, Gel, Pulsed-Field
Enterobacteriaceae Infections / epidemiology*,  microbiology
Escherichia / classification,  genetics*,  isolation & purification
Escherichia coli / classification,  genetics*,  isolation & purification
Escherichia coli Proteins / genetics*
Food Contamination
Food Microbiology
Gastroenteritis / epidemiology*,  microbiology
Japan / epidemiology
Sequence Analysis, DNA
Reg. No./Substance:
0/Adhesins, Bacterial; 0/Escherichia coli Proteins; 147094-99-3/eaeA protein, E coli

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: 144 Last Page: 146
PubMed Id: 23260717
ID: 3557987
Publisher Id: 12-0646
DOI: 10.3201/eid1901.120646

Human Gastroenteritis Outbreak Associated with Escherichia albertii, Japan Alternate Title:Human Gastroenteritis Associated with E. albertii
Tadasuke Ooka
Eisuke Tokuoka
Masato Furukawa
Tetsuya Nagamura
Yoshitoshi Ogura
Kokichi Arisawa
Seiya Harada
Tetsuya Hayashi
Author affiliations: University of Miyazaki, Miyazaki, Japan (T. Ooka, Y. Ogura, T. Hayashi);
Kumamoto Prefectural Institute of Public Health and Environmental Science, Kumamoto, Japan (E. Tokuoka, M. Furukawa, T. Nagamura, S. Harada);
University of Tokushima, Tokushima, Japan (K. Arisawa)
Correspondence: Address for correspondence: Tetsuya Hayashi, Division of Bioenvironmental Science, Frontier Science Research Center, University of Miyazaki, 5200 Kiyotake, Miyazaki 889-1692, Japan; email:

Escherichia albertii is an emerging human and bird pathogen that belongs to the attaching and effacing group of pathogens. This group of pathogens forms lesions on intestinal epithelial cell surfaces by the combined action of intimin, an eae gene–encoded outer membrane protein, and type III secretion system effectors (14).

Recently, we found that E. albertii represents a substantial proportion of the strains that had previously been identified as eae-positive Escherichia coli, enteropathogenic E. coli or enterohemorrhagic E. coli; 26 of the 179 eae-positive strains analyzed were found to be E. albertii (5). Furthermore, E. albertii is also a potential Shiga toxin 2f (Stx2f)–producing bacterial species (5). However, no E. albertii–associated gastroenteritis outbreak has been reported, which generates doubts regarding the clinical role of this microorganism. In this study, we revisited an outbreak of gastroenteritis that was presumed to have been caused by eae-positive atypical E. coli OUT:HNM (6) to determine if it was actually caused by E. albertii.

The Study

An outbreak of gastroenteritis occurred at the end of May 2011 in Kumamoto, Japan, among persons who attended 1 of 2 parties held in a Japanese restaurant on May 29. We reviewed case records for the 94 persons who attended the parties. A total of 48 persons became ill; 43 of them attended the first party (a total of 86 attended), and 5 attended the second party (a total of 8 attended). The ill participants had not eaten any food in common except for the meals served at the restaurant. The main symptoms of the patients were diarrhea (83%), abdominal pain (69%), fever (44%; mean temperature 37.2°C), and nausea (29%). The mean incubation period was 19 h.

A routine protocol to identify bacteria and viruses (Technical Appendix) was used by our laboratory to examine 54 fecal specimens from 44 party participants and 10 members of the restaurant kitchen staff (7 party participants and all of the kitchen staff were asymptomatic). Atypical E. coli (lactose negative; OUT:HNM) strains harboring the eae gene and E. coli OUT:H18 strains harboring the stx2d and astA (but not eae) genes were isolated from 24 and 3 specimen, respectively; 7 specimens yielded both strains (Table 1). The stx2-positive/eae-negative E. coli strains were found to be serotype O183 (a recently described O serotype) by agglutination testing with O183-specific antiserum (S. Iyoda, M. Ohnishi, unpub. data).

All atypical E. coli strains showed identical or nearly identical XbaI-digested DNA banding patterns by pulsed-field gel electrophoresis, and the 10 E. coli O183:H18 strains also exhibited identical patterns (Figure). The source of the infection was most likely the meals served in the restaurant, but a bacteriological examination of the meal or of the ingredients used to prepare the meal was not possible because none of the food was preserved for analysis.

The lactose-negative/eae-positive features of the OUT:HNM strains suggested that these strains might be E. albertii. We examined additional biochemical properties of these strains and found that they exhibited the E. albertii–specific features described (4,5). These features include nonmotility, inability to ferment xylose and lactose, and inability to produce β-D-glucuronidase. The E. coli O183:H18 strains demonstrated common phenotypic and biochemical properties of E. coli (7).

To determine whether the E. albertii–like OUT:HNM strains were E. albertii, we randomly selected 6 strains and determined their phylogeny by multilocus sequence analysis as described (5) (Technical Appendix Table). Results indicated that although the E. coli O183:H18 strain analyzed in parallel belongs to E. coli sensu stricto, the E. albertii–like OUT:HNM strains belong to the E. albertii lineage; all 6 strains showed identical sequences (Technical Appendix Figure).

We further examined the intimin subtype by sequencing the eae gene, the chromosome integration site of the locus of enterocyte effacement encoding the eae gene and a set of type III secretion system genes, and the presence and subtype of the cdtB gene as described (5). Results showed that the E. albertii strains had intimin σ, which is rarely identified in enteropathogenic E. coli or enterohemorrhagic E. coli; the locus of enterocyte effacement was integrated into the pheU tRNA gene; and the cdtB gene of the II/III/V subtype group was present. These features are consistent with recently described genetic features of E. albertii (5).

We divided the party participants into 4 groups according to strain isolation patterns and statistically assessed the association of strain isolation patterns with incidence of clinical symptoms (Table 2). The results indicated that persons infected with only E. albertii or persons infected with E. albertii and E. coli O183:H18 had diarrhea and abdominal pain more frequently than did uninfected persons (p<0.05) and that the incidence of asymptomatic carriers was lower among persons infected only with E. albertii.

Nucleotide sequences obtained in this study have been deposited in the DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank database. Accession numbers and other information on sequence analyses are shown in the Technical Appendix.


In this gastroenteritis outbreak, E. albertii or stx2-positive E. coli O183:H18 was isolated from 24 ill patients; both strains were isolated from 7 patients. Thus, although the responsible meal or food was not identified, it was most likely contaminated with these 2 microorganisms. The contribution or involvement of E. coli O183:H18 in this outbreak is unknown because there were 3 patients from whom only E. coli O183:H18 was isolated and because there were no differences in clinical symptoms between persons infected with E. coli O183:H18 and persons not infected (Tables 1, 2). In contrast, E. albertii was isolated from a larger number of patients, and many fecal specimens yielded only E. albertii (Table 1).

The proportion of persons who had clinical symptoms was also higher for E. albertii–positive party participants than for uninfected persons (Table 2). Therefore, it is plausible that E. albertii was the major causative pathogen of this outbreak. This information indicates that E. albertii can cause gastroenteritis outbreaks among humans (5).

More attention should be given to sporadic cases and outbreak cases caused by this emerging pathogen. It may also be informative to revisit past outbreak cases caused by eae-positive atypical E. coli if pathogens were recorded as being nonmotile, unable to ferment lactose and xylose, and unable to produce β-D-glucuronidase.

Technical Appendix

Protocol used to identify bacteria and viruses in fecal specimens obtained during a human gastroenteritis outbreak associated with Escherichia albertii, Japan.


Suggested citation for this article: Ooka T, Tokuoka E, Furukawa M, Nagamura T, Ogura Y, Arisawa K, et al. Human gastroenteritis outbreak associated with Escherichia albertii, Japan. Emerg Infect Dis [Internet]. 2013 Jan [date cited].


We thank Sunao Iyoda and Makoto Ohnishi for sharing their unpublished results of E. coli serotyping and Keigo Ekinaga, Haruki Tokunaga, and Ryuusei Higashi for providing materials and epidemiologic information.

This study was supported by a grant-in-aid for scientific research from MEXT Japan (Wakate-B, 23790480) to T.O. and a grant from the Yakult Foundation.

Dr Ooka is an assistant professor in the Department of Infectious Diseases, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan. His research interests include bacterial genomics and pathogenicity.

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6. . TokuokaE, FurukawaM, NagamuraT, HaradaS, EkinagaK, TokunagaH, et al. Food poisoning outbreak due to atypical EPEC OUT:HNM, May 2011—Kumamoto.Infectious Agents Surveillance Report.Year: 2012;33:8–9
7. . NataroJP, BoppCA, FieldsPI, KaperJB, StrockbineNA. Escherichia, Shigella, and Salmonella In: Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA, editors. Manual of clinical microbiology, 9th ed. Washington (DC): American Society for Microbiology Press; Year: 2007 p. 670–87.


[Figure ID: F1]

XbaI-digested pulsed-field gel electrophoresis profiles of isolates from fecal specimens collected from patients during an outbreak of human gastroenteritis associated with Escherichia albertii, Japan. Extra bands observed in 2 E. albertii isolates are indicated by arrowheads (only 1 or 2 band differences). The 2 E. coli O183:H18 and 6 E. albertii isolates indicated by numbers in boxes were subjected to multilocus sequence analysis (Technical Appendix). stx2d, Shiga toxin 2d gene; astA, enteroaggregative E. coli heat-stable toxin gene; eae, intimin gene. Lane M, Salmonella enterica serovar Braenderup strain H9812 (used as a DNA size standard); lanes P1, Party 1; lanes P2, Party 2; lanes KS, kitchen staff.

[TableWrap ID: T1] Table 1  Isolates from fecal specimens of party participants during outbreak of gastroenteritis associated with Escherichiaalbertii, Japan*
Isolate Origin of isolates
Participants, n = 44
Kitchen staff, n = 10
Symptomatic Asymptomatic No information Symptomatic Asymptomatic
E. albertii 21 1 0 0 2
E. albertii† and E. coli O183:H18‡ 7 0 0 0 0
E. coli O183:H18‡ 3 0 0 0 0
None 6 5 1 0 8

*None, negative for both pathogens.
†Initially identified as atypical (lactose negative) E. coli OUT:HNM harboring the intimin (eae) gene.
‡Initially identified as eae negative E. coli OUT:H18 harboring the Shiga toxin 2d and enteroaggregative E.coli heat-stable toxin genes.

[TableWrap ID: T2] Table 2  Clinical symptoms of party participants during outbreak of gastroenteritis associated with Escherichia albertii, by pathogen identified, Japan*
Symptom E. albertii, n = 21† E. albertii and E. coli O183:H18, n = 7 E. coli O183:H18, n = 3 None,‡ n =11§
Diarrhea 17 (81)¶ 7 (100)§ 1 (33) 4 (36)
Abdominal pain 16 (76)¶ 6 (86)§ 2 (67) 3 (27)
Nausea 5 (24) 5 (71)§ 0 1 (9)
Fever 8 (38) 4 (57) 2 (67) 4 (36)
None 1 (5)¶ 0 0 5 (45)

*Values are no. (%). None, negative for both pathogens. 
†One symptomatic person was excluded because no clinical record was available.
‡Negative for both pathogens.
§One person was excluded because no clinical record was available.
¶A 2-tailed Fisher exact test (p<0.05) showed significant differences between the groups from which E. albertii or E. coli O183:H18 was isolated and the groups from which they were not isolated.

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Keywords: Keywords: Escherichia albertii, enteric infections, bacteria, outbreak, human gastroenteritis, Japan.

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