Enterotoxin-producing Escherichia coli O169:H41, United States.From 1996 to 2003, 16 outbreaks of enterotoxigenic Escherichia coli Enterotoxigenic Escherichia Coli (ETEC) is a type of Escherichia coli that can cause Traveler's diarrhea. A number of pathogenic isolates are termed ETEC, but the main hallmarks of this type of bacteria are expression of one or more enterotoxins and presence of (ETEC ETEC enterotoxigenic Escherichia coli. ETEC Enterotoxic Escherichia coli, see there ) infections in the United States and on cruise ships were confirmed. E. coli E. coli: see Escherichia coli. E. coli in full Escherichia coli Species of bacterium that inhabits the stomach and intestines. E. coli can be transmitted by water, milk, food, or flies and other insects. serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. O169:H41 was identified in 10 outbreaks and was the only serotype in 6. This serotype was identified in 1 of 21 confirmed ETEC outbreaks before 1996. ********** Enterotoxigenic Escherichia coli (ETEC) is an important cause of diarrhea in the developing world and among travelers and is increasingly recognized as a cause of outbreaks in the United States (1). Dalton et al. reviewed confirmed ETEC outbreaks that occurred both in the United States and among passengers on cruise ships that docked in U.S. ports from 1975 through 1995 (2). Twenty-one such outbreaks caused by 17 different ETEC serotypes occurred during this period; 7 (33%) occurred among cruise ship passengers (2). Because laboratory tests for the identification of ETEC are not widely available, outbreaks caused by ETEC may escape recognition, and healthcare workers may miss opportunities for treatment and prevention. To improve recognition of ETEC outbreaks, Dalton proposed that specimens from outbreaks of gastroenteritis gastroenteritis: see enteritis. gastroenteritis Acute infectious syndrome of the stomach lining and intestines. Symptoms include diarrhea, vomiting, and abdominal cramps. that meet certain criteria be referred for ETEC testing at a public health reference laboratory. These outbreaks include those for which routine stool cultures have not yielded an etiologic agent and those which are characterized by an incubation period incubation period n. 1. See latent period. 2. See incubative stage. Incubation period of 24 to 48 hours, a duration of illness [greater than or equal to] 60 hours, and a diarrhea-to-vomiting prevalence ratio of [greater than or equal to] 2.5 (2). The Study For the 8-year period 1996 through 2003, we reviewed all suspected ETEC outbreaks solely or jointly investigated by the Foodborne and Diarrheal Diseases Branch at the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. (CDC See Control Data, century date change and Back Orifice. CDC - Control Data Corporation ). In accordance with Dalton et al., we defined a confirmed ETEC outbreak as one in which ETEC isolates of the same serotype were isolated from [greater than or equal to] 3 ill persons and no other viral or bacterial pathogens were identified, or one in which ETEC isolates of the same serotype were isolated from [greater than or equal to] 10 ill persons and no more than one other bacterial or viral pathogen was identified in a single stool specimen. Stool specimens collected during these investigations were routinely cultured for Salmonella, Shigella shigella Any of the rod-shaped bacteria that make up the genus Shigella, which are normal inhabitants of the human intestinal tract and can cause dysentery, or shigellosis. Shigellae are gram-negative (see gram stain), non-spore-forming, stationary bacteria. S. , Campylobacter Campylobacter Genus of gram-negative spiral-shaped bacteria infecting mammals. Many species, especially C. fetus, cause miscarriage in sheep and cattle. C. jejuni is a common cause of food poisoning. Sources include meats (particularly chicken) and unpasteurized milk. , E. coli O157:H7, Yersinia Yersinia A genus of bacteria in the Enterobacteriaceae family. The bacteria appear as gram-negative rods and share many physiological properties with related Escherichia coli. Of the 11 species of Yersinia, Y. pestis, Y. enterocolitica, and Y. , and Vibrio vibrio Any of a group of aquatic, comma-shaped bacteria in the family Vibrionaceae. Some species cause serious diseases in humans and other animals. They are gram-negative (see spp. In many instances, these specimens were also tested for noroviruses. To identify ETEC, patient specimens were plated to MacConkey agar, and individual colonies or sweeps of confluent con·flu·ent adj. 1. Flowing together; blended into one. 2. Merging or running together so as to form a mass, as sores in a rash. growth were tested by polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) ) for heat-labile (LT) and heat-stable (ST) enterotoxin enterotoxin /en·tero·tox·in/ (en´ter-o-tok?sin) 1. a toxin specific for the cells of the intestinal mucosa. 2. a toxin arising in the intestine. 3. genes (3). Using standard methods, we serotyped LT- or ST-positive isolates for O and H antigens. ETEC isolates were tested by the disk-diffusion method for susceptibility to ampicillin ampicillin (ăm'pĭsĭl`ĭn), a penicillin-type antibiotic that is effective against both gram-negative microorganisms and gram-positive microorganisms such as Escherichia coli. , amoxicillin/clavulanic acid, ceftriaxone ceftriaxone /cef·tri·ax·one/ (cef?tri-ak´son) a semisynthetic, ß–resistant, third-generation cephalosporin effective against a wide range of gram-positive and gram-negative bacteria, used as the sodium salt. , chloramphenicol chloramphenicol (klōr'ămfĕn`əkŏl'), antibiotic effective against a wide range of gram-negative and gram-positive bacteria (see Gram's stain). It was originally isolated from a species of Streptomyces bacteria. , ciprofloxacin ciprofloxacin /cip·ro·flox·a·cin/ (sip?ro-flok´sah-sin) a synthetic antibacterial effective against many gram-positive and gram-negative bacteria; used as the hydrochloride salt. cip·ro·flox·a·cin n. , gentamicin gentamicin /gen·ta·mi·cin/ (jen?tah-mi´sin) an aminoglycoside antibiotic complex isolated from bacteria of the genus Micromonospora, , kanamycin kanamycin /kan·a·my·cin/ (kan?ah-mi´sin) an aminoglycoside antibiotic derived from Streptomyces kanamyceticus, effective against aerobic gram-negative bacilli and some gram-positive bacteria, including mycobacteria; used as the , nalidixic acid nalidixic acid /nal·i·dix·ic ac·id/ (nal-i-dik´sik) a synthetic antibacterial agent used in the treatment of genitourinary infections caused by gram-negative organisms. na·li·dix·ic acid n. , streptomycin streptomycin (strĕp'tōmī`sĭn), antibiotic produced by soil bacteria of the genus Streptomyces and active against both gram-positive and gram-negative bacteria (see Gram's stain), including species resistant to other , sulfisoxazole, tetracycline tetracycline (tĕ'trəsī`klēn), any of a group of antibiotics produced by bacteria of the genus Streptomyces. They are effective against a wide range of Gram positive and Gram negative bacteria, interfering with protein , and trimethoprim-sulfamethoxazole (4). A PCR-restriction fragment length polymorphism test was used to identify the H41 gene in selected nonmotile E. coli O169 isolates (5). Conclusions During the 8-year study period, CDC received isolates from 59 outbreaks for ETEC testing. Sixteen met the criteria for our definition of a confirmed ETEC outbreak; three occurred on international cruise ships that docked in U.S. ports and 12 occurred in the United States (Table). We identified ETEC in specimens from six other outbreaks that did not meet these criteria, either because ETEC isolates of the same serotype were isolated from only two persons (n = 2) or because we isolated additional bacteria/ pathogens from the specimens (n = 4). The 16 ETEC outbreaks had a median of 41 ill persons per outbreak (range 5-916), for a total of 2,865 patients. From 81% to 100% of ill persons in each outbreak reported diarrhea; less frequently reported symptoms included abdominal cramps (66%-90%), fever (0%-73%), nausea (44%-70%), and vomiting (0%-33%). In the 15 outbreaks in which diarrhea and vomiting were reported, the median "diarrhea-to-vomiting prevalence ratio" (the percentage of patients who reported diarrhea divided by the percentage of patients who reported vomiting) was 7.7 (range 2.9-undefined: the upper limit of the range is undefined because in two outbreaks all ill persons interviewed denied vomiting). In nine outbreaks with sufficient data, incubation periods among individual patients were 5-158 hours. The median incubation period was 24-48 hours for 10 of the 12 outbreaks for which it could be calculated. The duration of illness, reported in 11 outbreaks, was 0.3-21 days. The median duration of illness was [greater than or equal to] 60 hours in 11 of the 13 outbreaks for which it could be calculated. A vehicle was implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. in 11 (69%) outbreaks. Unbottled ship's water or beverages containing ice prepared on board the ship were implicated in 2 of the 3 outbreaks on cruise ships that had docked in foreign ports. The source of the third international cruise ship outbreak was not determined. Although no problems with chlorination chlorination Public health Addition of chlorinated compounds to drinking water as disinfectants. Cf Ozonation. of bunkered water were documented in the two outbreaks, this problem has been seen in previous waterborne ETEC outbreaks aboard cruise ships (6). Basil served on board ship was implicated as the source of ETEC in the remaining cruise ship outbreak (on a ship that docked only in U.S. ports). One other outbreak was attributed to a flesh herb (parsley) served raw (7). Salads made with raw vegetables were implicated in four other domestic outbreaks. If we define a strain as each ETEC serotype identified during an outbreak that has a unique antimicrobial resistance pattern, we identified a total of 30 strains representing eight different serotypes in specimens from the 16 outbreaks (Table). In five outbreaks, we isolated more than one ETEC serotype. Heat-stable toxin heat-stable toxin one of two plasmid-encoded toxins produced by Escherichia coli. (ST)-producing E. coli O169:H41 was the most commonly identified serotype. This serotype was identified as the only pathogen in specimens from six outbreaks in the United States and was identified along with other ETEC serotypes in four additional outbreaks. Three of these four outbreaks occurred on international cruise ships. In 21 previously reported ETEC outbreaks, E. coli O169:H41 bad been isolated only once, from an outbreak that occurred among international cruise ship passengers in 1995, in which another ETEC serotype predominated (2). By all of the basic epidemiologic and clinical characteristics that we analyzed, outbreaks in which E. coli O169:H41 was identified alone, or in combination with other serotypes, did not appear to differ from outbreaks in which this emerging strain was not identified. Resistance to antimicrobial agents remained common among ETEC isolates (Table). Twenty-four (80%) of the 30 strains were resistant to tetracycline, 11 (38%) were resistant to sulfisoxazole, 4 (13%) were resistant to ampicillin, and 2 (7%) were resistant to trimethoprim-sulfamethoxazole. All strains of O169:H41 were resistant to tetracycline, and two were also resistant to at least one additional antimicrobial drug. Only two outbreaks were caused exclusively by pan-sensitive ETEC strains (7%). A comparison of ETEC outbreaks reported to CDC from 1996 through 2003 with those from previous years shows that outbreaks on cruise ships and in the United States continue to occur and that antimicrobial resistance among ETEC isolates remains common. Raw vegetables and herbs have been increasingly implicated as the vehicles for ETEC outbreaks in recent years. This finding is in keeping with an increase in produce-associated outbreaks among other foodborne bacterial pathogens (8). Finally, a new ETEC serotype, ST-producing O169:H41, has become predominant. The first report of O169:H41 was in association with a foodborne outbreak in 1991 in Japan, where this serotype continues to be isolated (9-11). Hamada reported four outbreaks that occurred from June 1997 to August 1998; the largest of these outbreaks had a 57% attack rate and resulted in approximately 2,800 cases. All four outbreaks occurred at either restaurants or catered events (11). Contaminated wakame wa·ka·me n. A brown seaweed (Undaria pinnatifida) native to the coasts of China, Japan, and Korea, having a short stipe and pinnately divided blades, extensively used in Asian cooking. [Japanese.] seaweed was implicated in one of the outbreaks and considered the likely cause in another (11). Nishakawa et al. report that O169:H41 has become the most prevalent ETEC serotype in Japan (12). In 1995, CDC detected this serotype for the first time during an outbreak on a Caribbean cruise ship. It was identified during two additional Caribbean cruise ship outbreaks before causing a domestic outbreak in Minnesota in 1997. In addition to being identified in 10 of the 16 ETEC outbreaks that met our criteria, O169:H41 was also a predominant serotype in 4 of the 6 ETEC outbreaks that did not meet our criteria for a confirmed outbreak, either because the serotype was isolated from two persons only or because an additional pathogen was also isolated in the outbreak. The emergence and eventual predominance of O169:H41 in the United States and Japan may have important implications for ETEC vaccine producers. Nishikawa et al. characterized strains of O169:H41 from Japan and reported that they are not clonal and that they possess a novel colony-forming factor (12). From 1996 through 1999, laboratory-confirmed ETEC outbreaks represented 0.2% of all foodborne outbreaks reported to CDC (13). This number is likely to be an underestimate because special diagnostic tests are required to confirm ETEC. Seventy-one percent of outbreaks of foodborne illness reported to CDC during this period were of unknown cause. In a previous study, Hall et al. demonstrated that the epidemiologic and clinical syndrome in 1.1% of outbreaks of unknown cause reported to CDC from 1982 through 1989 was compatible with infections caused by ETEC or STEC STEC shiga toxin-producing Escherichia coli. (14). ETEC is also responsible for some episodes of sporadic diarrheal disease. When researchers systematically looked for it, they isolated ETEC from 1.4% of stool samples from patients visiting urban and rural health maintenance organization clinics in Minnesota for diarrhea (15). Our data suggest that the clinical criteria proposed by Dalton et al. for suspecting ETEC as a cause of an outbreak of unknown cause (median incubation 24-48 hours, mean or median duration >60 hours, and diarrhea-to-vomiting prevalence ratio [greater than or equal to] 2.5) remain valid. The epidemiology of ETEC outbreaks in the United States is changing, but the incidence of these outbreaks does not appear to be decreasing. Researchers cannot use routine stool cultures to detect ETEC, and delays in stool sample collection for [greater than or equal to] 7 days greatly reduces yield (16,17). For outbreaks that meet the clinical profile and for which routine stool diagnostic tests have not yielded an enteric enteric /en·ter·ic/ (en-ter´ik) within or pertaining to the small intestine. en·ter·ic adj. 1. Of, relating to, or within the intestine. 2. pathogen, physicians and public health authorities should send E. coli isolates to reference laboratories, such as CDC, for ETEC testing.
Table. Characteristics of enterotoxigenic Escherichia coli (ETEC)
outbreaks, (a) United States, 1996-2003
Setting
No. Mo/y Location (reference) Presumed source No. ill
1 3/96 Caribbean Cruise ship Drinking water 652
2 4/97 Caribbean Cruise ship Drinking water, 429
(5) ice
3 4/97 California Restaurant Beans, 41
enchilada, tacos,
rice, tortilla
chips
4 6/97 Massachusetts Boxed Tomato, 33
lunch mozzarella salad
5 7/97 Minnesota Catered Fresh vegetables 15
party
6 4/98 Mexico-Hawaii Cruise ship -- 397
7 6/98 Illinois Catered Potato, 916
parties macaroni, egg
salads
8 8/98 Minnesota Restaurant Parsley 66
(6)
9 9/98 Minnesota Restaurant -- 5
10 5/00 Washington Cruise Ship Basil 100
11 6/00 New York Banquet -- 40
12 7/00 Utah Wedding -- 45
rehearsal
13 7/01 Wisconsin Catered Quesadillas, 21
party fajitas, nacho
chips, beans
14 8/01 Illinois Catered -- 24
patty
15 10/02 Oregon Catered Garlic chicken 40
party lasagna
16 8/03 Tennessee Catered Catfish, coleslaw 41
party
Median
% Median illness
Diarrhea % incubation, duration,
No. Mo/y (bloody) Vomiting h (range) days (range)
1 3/96 98 (9) 19 -- --
2 4/97 100 (6) 14 -- >3
3 4/97 95 17 24 (5-85) 2 (0.3-4)
4 6/97 97 33 48 (24-96) 3.7 (1-7)
5 7/97 100 13 37 (8-158) 3.2 (0.4-6)
6 4/98 96 33 -- --
7 6/98 100 8 50 (40-76) 5 (2-9)
8 8/98 100 (0) 6 25 8
9 9/98 100 (0) 0 48 6
10 5/00 100 5 40 (27-67) 10 (0.5-21)
11 6/00 97 (0) 3 48 (24-96) 3 (1-8)
12 7/00 100 29 33 (18-59) 2.3 (1-3)
13 7/01 100 -- 38 (9-70) 6 (1-8)
14 8/01 100 0 -- --
15 10/02 98 (13) 15 72 (24-144) 5
16 8/03 81 (0) 5 2 2.5
No Serotype/toxin Antimicrobial
No. Mo/y isolates type (b) resistance (c)
1 3/96 6 O169:H41/ST Tc
1 O6:H16/LT,ST Sensitive
1 O27:H7/ST St, Su, Tc
1 O34:H10/ST Tc
2 4/97 8 O169:H41/ST Tc
3 O148:H28/ Tc
LT,ST
1 O78:H12/ST Ch, St, Su,
Tc, TmS
1 O27:H7/ST St, Su, Tc
3 4/97 11 O27:H7/ST Sensitive
4 6/97 5 O25:NM/ST Sensitive
5 7/97 4 O169:H41/ST Tc
6 4/98 3 O6:H16/LT,ST Sensitive
1 O6:H16/LT,ST St, Tc
2 O169:H41/ST Tc
O148:H28/ St, Su, Tc
1 LT,ST
O148:H28/ Tc
1 LT, ST
1 O27:H7/ST St, Su, Tc
7 6/98 11 O6:H16/LT,ST Sensitive
8 8/98 7 O6:H16/LT,ST Ap, St, Su,
Tc
1 O159:H4/LT Ap, St, Su,
Tc, TmS
1 O27:H7/ST St, Su, Tc
9 9/98 3 O169:H41/ST St, Su, Tc
10 5/00 3 O169:H41/ST Tc
11 6/00 5 O169:H41/ST Tc
12 7/00 5 O27:H7/ST St, Su, Tc
13 7/01 3 O169:H41/ST Tc
14 8/01 3 O169:H41/ST Ap, Tc
1 O169:H41/ST Tc
2 O6:H16/LT,ST Sensitive
1 O25:NM/ST Ap
15 10/02 3 O27:H7/ST St, Su, Tc
16 8/03 12 0169:H49 Tc
(a) An outbreak is defined as [greater than or equal to] 3 ill persons
infected with the same ETEC serotype and no other viral or bacterial
pathogens, or [greater than or equal to] 10 ill persons with the same
serotype and no more than one other bacterial or viral pathogen
identified.
(b) NM, nonmotile; LT, heat-labile toxin; ST, heat-stable toxin.
(c) Ap, ampicillin; Ch, chloramphenicol; St, streptomycin; Su,
sulfisoxazole; Tc, tetracycline; TmS, trimethoprim-sulfamethoxazole.
Acknowledgments We thank the staff of the local and state health departments and the Vessel Sanitation Program Vessel Sanitation Program See Sanitation score. at the Centers for Disease Control and Prevention, who participated in the investigations summarized in this manuscript. References (1.) Cohen cohen or kohen (Hebrew: “priest”) Jewish priest descended from Zadok (a descendant of Aaron), priest at the First Temple of Jerusalem. The biblical priesthood was hereditary and male. MB, Giannella RA. Enterotoxigenic Escherichia coli. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL, editors. Infections of the gastrointestinal tract gastrointestinal tract n. The part of the digestive system consisting of the stomach, small intestine, and large intestine. Gastrointestinal tract . 2nd ed. Philadelphia: Lippincott Williams & Wilkins; 2002. p. 579-94. (2.) Dalton CB, Mintz ED, Wells JG, Bopp CA, Tauxe RV. Outbreaks of anterotoxigenic Escherichia coli Escherichia coli (ĕsh'ərĭk`ēə kō`lī), common bacterium that normally inhabits the intestinal tracts of humans and animals, but can cause infection in other parts of the body, especially the urinary tract. infection in American adults: a clinical and epidemiologic profile. Epidemiol Infect 1999;123:9-16. (3.) Olsvik O, Strockbine NA. PCR detection of heat-stable, heat-labile, and Shiga-like toxin genes in Escherichia coli. In: Persing CH, Smith TF, Tenover FC, White TJ, editors. Diagnostic molecular microbiology. Washington: American Society for Microbiology The American Society for Microbiology (ASM) is a scientific organization, based in the United States although with over 43,000 members throughout the world. It is the largest single life science professional organization and its members include those whose interests encompass basic ; 1993. p. 271-6. (4.) National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial disk susceptibility tests. Approved Standard. 5th ed. NCCLS NCCLS National Committee for Clinical Laboratory Standards doc. M2-A5 (ISBN ISBN abbr. International Standard Book Number ISBN International Standard Book Number ISBN n abbr (= International Standard Book Number) → ISBN m 1-56238-208-X). Villanova (PA): The Committee; 1993. (5.) Fields PI, Blom K, Hughes HJ, Helsel LO, Feng P, Swaminathan B. Molecular characterization of the gene encoding H antigen in Escherichia coli and development of a PCR-restriction fragment length polymorphism test for identification of E. coli O157:H7 and O157:NM. J Clin Microbiol 1997;35:1066-70. (6.) Daniels NA, Niemann J, Karpati A, Parashar UD, Greene KD, Wells JG, et al. Traveler's diarrhea Traveler's Diarrhea Definition The occurrence of multiple loose bowel movements in someone traveling to an area outside their usual surroundings (usually from temperate industrialized regions to tropical areas), is known as Traveler's diarrhea (TD). at sea: three outbreaks of waterborne enterotoxigenic Escherichia coli (ETEC) on cruise ships. J Infect Dis 2000;181:1491-5. (7.) Naimi TS, Wicklund JH, Olsen SJ, Krause G, Wells JG, Bartkus JM, et al. Concurrent outbreaks of Shigella sonnei Shigella son·ne·i n. Sonne bacillus. Shigella sonnei Shigella group D Microbiology The most commonly isolated, least virulent Shigella serotype and enterotoxiganic Escherichia coli infections associated with parsley: implications for surveillance and outbreak control. J Food Prot 2003;66:535-41. (8.) Tauxe RV, Kruse H, Hedberg CW, Potter M, Madden J, Wachmuth K. Microbial microbial pertaining to or emanating from a microbe. microbial digestion the breakdown of organic material, especially feedstuffs, by microbial organisms. hazards and emerging issues associated with produce. J Food Prot 1997;60:1400-8. (9.) Ando K, Itaya T, Aoki A, Saito A, Masaki H, Tokumura Y, et al. An outbreak of food poisoning food poisoning, acute illness following the eating of foods contaminated by bacteria, bacterial toxins, natural poisons, or harmful chemical substances. It was once customary to classify all such illnesses as "ptomaine poisoning," but it was later discovered that caused by enterotoxiganic E. coli O169:H41. Jpn J Food Microbiol 1993;10:77 81. (10.) Nishikawa Y. Heat-stable enterotoxin producing E. coli O169:H41 in Japan. Emerg Infect Dis 1995;1:61. (11.) Hamada K, Tsuji H, Shimada K, Aoki Y. Outbreaks of heat stable enterotoxin-producing E. coli O169 in Kinki district in Japan: epidemiological analysis by pulsed-field electrophoresis. Jpn J Infect Dis 1999;52:165-7. (12.) Nishikawa Y, Helander A, Ogasawara J, Moyer NP, Hanaoka M, Hase A, Yasukawa A. Epidemiology and properties of heat-stable enterotoxin producing Escherichia coli serotype O169:H41. Epidemiol infect 1998;121:31-42. (13.) Centers for Disease Control and Prevention. U.S. foodborne disease outbreaks. 2002 [cited 2003 Jan 21]. Available from: http://www.cdc.gov/ncidod/dbmd/outbreak/us_outb.htm. (14.) Hall JA, Goulding JS, Bean NH, Tauxe RV. Epidemiologic profiling: evaluating foodborne outbreaks for which no pathogen was isolated by routine laboratory testing: United States, 1982-9. Epidemiol Infect 2001;127:381-7. (15.) Gahr P, Sullivan M, Smith K, Besser J, Hedberg C. A case-control study case-control study, n an investigation employing an epidemiologic approach in which previously existing incidents of a medical condition are used in lieu of gathering new information from a randomized population. of enterotoxigenic en·ter·o·tox·i·gen·ic adj. Of or being an organism containing or producing an enterotoxin. Enterotoxigenic E. coli infections in Minnesota residents. In: Abstracts of the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy Antimicrobial Agents and Chemotherapy (print-ISSN 0066-4804, CODEN AMACCQ; canceled ISSN 0074-9923, canceled CODEN AACHAX) is an academic journal published by the American Society for Microbiology. ; Chicago, Illinois; 2001 Dec 16-19; Abstract 766. Washington: American Society for Microbiology; 2001. (16.) Gorbach SL, Kean BH, Evans DG, Bessudo D. Travelers' diarrhea and toxigenic toxigenic /tox·i·gen·ic/ (tok?si-jen´ik) 1. producing or elaborating toxins. 2. derived from or containing toxins. tox·i·gen·ic adj. Producing a poison; toxicogenic. Escherichia coli. N Engl J Med 1975;292:933-6. (17.) Ryder RW, Sack DA, Kapikian AZ, McLaughlin JC, Chakraborty J, Mizanur Rahman AS, et al. Enterotoxigenic Escherichia coli and Reo-virus-like agent in rural Bangladesh. Lancet 1976;1:659-63. Mark E. Beatty, * Cheryl A. Bopp, * Joy G. Wells, * Kathy D. Greene, * Nancy D. Puhr, * and Eric D. Mintz * * Centers for Disease Control and Prevention, Atlanta, Georgia, USA Dr. Beatty, a pediatrician, is a preventive medicine resident at the Centers for Disease Control and Prevention. His research interests include enteric pathogens. Address for correspondence: Mark E. Beatty, Centers for Disease Control and Prevention, Mailstop A38, 1600 Clifton Road, Atlanta, Georgia USA, 30333; fax: 404-639-2205; email: zbn5@cdc.gov |
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