Phenotypic Profiles of Enterotoxigenic Escherichia coli Associated with Early Childhood Diarrhea in Rural Egypt

ABSTRACT Enterotoxigenic Escherichia coli (ETEC) causes substantial diarrheal morbidity and mortality in young children in countries with limited resources. We determined the phenotypic profiles of 915 ETEC diarrheal isolates derived from Egyptian children under 3 years of age who participated in a 3-year population-based study. For each strain, we ascertained enterotoxin and colonization factor (CF) expression, the O:H serotype, and antimicrobial susceptibility. Sixty-one percent of the strains expressed heat-stable enterotoxin (ST) only, 26% expressed heat-labile enterotoxin (LT) alone, and 12% expressed both toxins. The most common CF phenotypes were colonization factor antigen I (CFA/I) (10%), coli surface antigen 6 (CS6) (9%), CS14 (6%), and CS1 plus CS3 (4%). Fifty-nine percent of the strains did not express any of the 12 CFs included in our test panel. Resistance of ETEC strains to ampicillin (63%), trimethoprim-sulfamethoxazole (52%), and tetracycline (43%) was common, while resistance to quinolone antibiotics was rarely detected. As for the distribution of observed serotypes, there was an unusually wide diversity of O antigens and H types represented among the 915 ETEC strains. The most commonly recognized composite ETEC phenotypes were ST CS14 O78:H18 (4%), ST (or LTST) CFA/I O128:H12 (3%), ST CS1+CS3 O6:H16 (2%), and ST CFA/I O153:H45 (1.5%). Temporal plots of diarrheal episodes associated with ETEC strains bearing common composite phenotypes were consistent with discrete community outbreaks either within a single or over successive warm seasons. These data suggest that a proportion of the disease that is endemic to young children in rural Egypt represents the confluence of small epidemics by clonally related ETEC strains that are transiently introduced or that persist in a community reservoir.

[1]  S. T. Cowan,et al.  Manual for the identification of medical bacteria. , 1960 .

[2]  J. Waitz Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically , 1990 .

[3]  D. Maneval,et al.  Characterization of enterotoxigenic Escherichia coli isolated from U.S. troops deployed to the Middle East , 1993, Journal of clinical microbiology.

[4]  J. Holmgren,et al.  Role of PCF8775 antigen and its coli surface subcomponents for colonization, disease, and protective immunogenicity of enterotoxigenic Escherichia coli in rabbits , 1988, Infection and immunity.

[5]  K. Mølbak,et al.  Enterotoxigenic Escherichia coli infections and diarrhea in a cohort of young children in Guinea-Bissau. , 2002, The Journal of infectious diseases.

[6]  N. Binsztein,et al.  Colonization factors of enterotoxigenic Escherichia coli isolated from children with diarrhea in Argentina , 1991, Journal of clinical microbiology.

[7]  M. Takahashi,et al.  [Increasing fluoroquinolone low-sensitivity in enterotoxigenic Escherichia coli isolated from diarrhea of overseas travelers in Tokyo]. , 2001, Kansenshogaku zasshi. The Journal of the Japanese Association for Infectious Diseases.

[8]  R. J. Berry,et al.  Studies on enterotoxigenic Escherichia coli isolated from persons without diarrhoea in Western Australia , 1983, Journal of Hygiene.

[9]  C. Hoge,et al.  Distribution of colonization factor antigens among enterotoxigenic Escherichia coli strains isolated from patients with diarrhea in Nepal, Indonesia, Peru, and Thailand , 1997, Journal of clinical microbiology.

[10]  N. Binsztein,et al.  Characterization of monoclonal antibodies against putative colonization factors of enterotoxigenic Escherichia coli and their use in an epidemiological study , 1993, Journal of clinical microbiology.

[11]  C. Gyles Escherichia coli in Domestic Animals and Humans , 1994 .

[12]  P. Echeverria,et al.  Case-control study of endemic diarrheal disease in Thai children. , 1989, The Journal of infectious diseases.

[13]  Mary Jane Ferraro,et al.  Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically : approved standard , 2000 .

[14]  W. Gaastra,et al.  Development and evaluation of genotypic assays for the detection and characterization of enterotoxigenic Escherichia coli. , 2003, Diagnostic microbiology and infectious disease.

[15]  J. Holmgren,et al.  Monoclonal antibodies against Escherichia coli heat-stable toxin (STa) and their use in a diagnostic ST ganglioside GM1-enzyme-linked immunosorbent assay , 1986, Journal of clinical microbiology.

[16]  G. Viboud,et al.  Colonization factors of enterotoxigenic Escherichia coli isolated from children in north India. , 1996, The Journal of infectious diseases.

[17]  H. Hallander,et al.  Analysis of incidence of infection with enterotoxigenic Escherichia coli in a prospective cohort study of infant diarrhea in Nicaragua , 1997, Journal of clinical microbiology.

[18]  I. Orskov,et al.  Escherichia coli O:H serotypes isolated from human blood. Prevalence of the K1 antigen with technical details of O and H antigenic determination. , 1975, Acta pathologica et microbiologica Scandinavica. Supplement.

[19]  M. Lahav,et al.  EnterotoxigenicEscherichia coli (ETEC) isolated in the Tel-Aviv (Israel) area , 2005, Medical Microbiology and Immunology.

[20]  A. Svennerholm,et al.  Colonization factors of human enterotoxigenic Escherichia coli (ETEC). , 1996, Trends in microbiology.

[21]  A. Svennerholm,et al.  Monoclonal antibodies against the different subcomponents of colonization factor antigen II of enterotoxigenic Escherichia coli , 1990, Journal of clinical microbiology.

[22]  H. Dupont,et al.  Patterns of loss of enterotoxigenicity by Escherichia coli isolated from adults with diarrhea: suggestive evidence for an interrelationship with serotype , 1977, Infection and immunity.

[23]  R. Frenck,et al.  High Disease Burden of Diarrhea Due to Enterotoxigenic Escherichia coli among Rural Egyptian Infants and Young Children , 2003, Journal of Clinical Microbiology.

[24]  B. Nagy,et al.  Enterotoxigenic Escherichia coli (ETEC) in farm animals. , 1999, Veterinary research.

[25]  S. T. Cowan,et al.  Cowan and Steel's manual for the identification of medical bacteria , 1993 .

[26]  M. Wolk,et al.  Enterotoxigenic Escherichia coli (ETEC) in hospitalised Arab infants from Judea area--west bank, Israel. , 1997, Public health.

[27]  A. Faruque,et al.  Prevalence of Toxin Types and Colonization Factors in Enterotoxigenic Escherichia coli Isolated during a 2-Year Period from Diarrheal Patients in Bangladesh , 2000, Journal of Clinical Microbiology.

[28]  R. Frenck,et al.  Development of pathogenicity-driven definitions of outcomes for a field trial of a killed oral vaccine against enterotoxigenic Escherichia coli in Egypt: application of an evidence-based method. , 2004, The Journal of infectious diseases.

[29]  B. Lowe,et al.  Prevalence of enteric pathogens among international travelers with diarrhea acquired in Kenya (Mombasa), India (Goa), or Jamaica (Montego Bay). , 2002, The Journal of infectious diseases.

[30]  N. Binsztein,et al.  Prospective Cohort Study of EnterotoxigenicEscherichia coli Infections in Argentinean Children , 1999, Journal of Clinical Microbiology.

[31]  M. Mathan,et al.  Etiology of acute diarrhoea among children in developing countries: a multicentre study in five countries. , 1991, Bulletin of the World Health Organization.

[32]  M. Blanco,et al.  Serotypes and colonization factors of enterotoxigenic Escherichia coli isolated in various countries , 1993, European Journal of Epidemiology.

[33]  A. Bauer,et al.  Antibiotic susceptibility testing by a standardized single disk method. , 1966, Technical bulletin of the Registry of Medical Technologists. American Society of Clinical Pathologists. Registry of Medical Technologists.

[34]  Subcommittee On Acute Gastroenteritis Practice parameter: the management of acute gastroenteritis in young children. American Academy of Pediatrics, Provisional Committee on Quality Improvement, Subcommittee on Acute Gastroenteritis. , 1996, Pediatrics.

[35]  L. Peruski,et al.  Phenotypic Diversity of EnterotoxigenicEscherichia coli Strains from a Community-Based Study of Pediatric Diarrhea in Periurban Egypt , 1999, Journal of Clinical Microbiology.

[36]  A. Siitonen,et al.  Prevention of travellers' diarrhoea by oral B-subunit/whole-cell cholera vaccine , 1991, The Lancet.

[37]  M. H. Reis,et al.  Production of heat-stable enterotoxin by the O128 serogroup of Escherichia coli , 1979, Infection and immunity.

[38]  M. Katouli,et al.  Aetiological studies of diarrhoeal diseases in infants and young children in Iran. , 1990, The Journal of tropical medicine and hygiene.

[39]  D. Evans,et al.  Hemagglutination of Human Group A Erythrocytes by Enterotoxigenic Escherichia coli Isolated from Adults with Diarrhea: Correlation with Colonization Factor , 1977, Infection and immunity.

[40]  M. Wolf,et al.  Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli , 1997, Clinical microbiology reviews.

[41]  T. Cheasty,et al.  Isolation of enterotoxigenic Escherichia coli from British troops in Saudi Arabia , 1995, Epidemiology and Infection.

[42]  J. Ruiz,et al.  Quinolone Resistance in EnterotoxigenicEscherichia coli Causing Diarrhea in Travelers to India in Comparison with Other Geographical Areas , 2000, Antimicrobial Agents and Chemotherapy.

[43]  M. Hibberd,et al.  Characterization of a putative colonization factor (PCFO166) of enterotoxigenic Escherichia coli of serogroup O166. , 1989, Journal of general microbiology.