The rabbit as a new reservoir host of enterohemorrhagic Escherichia coli.We investigated the prevalence of enterohemorrhagic Escherichia coli enterohemorrhagic Escherichia coli EHEC Any of the E coli serotypes–eg O29, O39, O145 that produces shiga-like toxins, causing bloody inflammatory diarrhea, evoking a HUS. See Escherichia coli O157:H7, Hemolytic uremic syndrome. (EHEC EHEC enterohemorrhagic Escherichia coli. EHEC Enterohemorrhagic Escherichia coli, see there ) in rabbits acquired from two commercial vendors and a local petting zoo. Fecal samples from 34 Dutch Belted (DB) and 15 New Zealand New Zealand (zē`lənd), island country (2005 est. pop. 4,035,000), 104,454 sq mi (270,534 sq km), in the S Pacific Ocean, over 1,000 mi (1,600 km) SE of Australia. The capital is Wellington; the largest city and leading port is Auckland. White (NZW NZW New Zealand White (rabbit breed) NZW NoordzeeWind NZW South Weymouth, Massachusetts (Airport Code) ) rabbits were cultured; and isolates were biotyped, serotyped, 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) ), and genotyped by repetitive-element sequence--based PCR (Rep-PCR). Seven (25%) of 28 DB rabbits acquired from one commercial source were positive for EHEC, including O153:H- and O153:H7. One (9%) of 11 NZW rabbits from the same source was positive for eae-, stx1+ O153 strains. In contrast, six DB rabbits from another commercial source and four rabbits from a petting zoo were negative for EHEC. Rep-PCR demonstrated that the O153 EHEC and O145 enteropathogenic enteropathogenic having pathogenicity for the intestine. enteropathogenic Escherichia coli strains of E. coli which cause enteritis by close association with enteric cells. Includes attaching and effacing E. coli. 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. were two distinct clones. Our study indicates that rabbits are a new reservoir host reservoir host n. A host that serves as a source of infection and potential reinfection of humans and as a means of sustaining a parasite when it is not infecting humans. of EHEC that may pose a zoonetic risk for humans. ********** 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. O157:H7 is a leading foodborne 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 associated with human illness, including hemorrhagic colitis hemorrhagic colitis n. Abdominal cramps and bloody diarrhea, without fever, attributed to a self-limited infection by a strain of Escherichia coli. and hemolytic uremic syndrome hemolytic uremic syndrome n. A syndrome in which hemolytic anemia and thrombocytopenia occur with acute renal failure, marked in children by sudden gastrointestinal bleeding, urine that contains red blood cells and is scanty in volume, and (HUS), the leading cause of acute renal failure acute renal failure Acute kidney failure Nephrology An abrupt decline in renal function, triggered by various processes–eg, sepsis, shock, trauma, kidney stones, drug toxicity-aspirin, lithium, substances of abuse, toxins, iodinated radiocontrast. in children (1). Similarly, non-O157 enterohemorrhagic E. coli (EHEC) serotypes have been 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 outbreaks of disease worldwide and are currently considered emerging pathogens by the World Health Organization (WHO) (2). Most EHEC infections in humans are foodborne, and the source of infection is an animal reservoir. Cattle and other ruminants are considered major reservoirs hosts of EHEC (3). Recent reports have also emphasized that farm animals and their environment pose a zoonotic Zoonotic A disease which can be spread from animals to humans. Mentioned in: Zoonosis risk for humans, based on outbreaks of E. coli O157:H7 infection among farm visitors (4). Identifying bacterial pathogens in natural hosts is important because they constitute potential reservoirs for zoonotic transmission (5). We recently described an outbreak of hemorrhagic Hemorrhagic A condition resulting in massive, difficult-to-control bleeding. Mentioned in: Hantavirus Infections hemorrhagic pertaining to or characterized by hemorrhage. diarrhea and hemolytic uremic syndrome (HUS) in Dutch Belted (DB) rabbits naturally infected with EHEC O153:H- (6). In the current study, we investigated the prevalence of EHEC in laboratory rabbits acquired from two commercial vendors and in rabbits from a local petting zoo to assess their potential as reservoir hosts. Materials and Methods Rabbits Fecal samples were collected from 34 DB and 15 New Zealand White (NZW) Pasteurella multocida--free laboratory rabbits acquired at various times from one commercial source. Fecal samples were also collected from six DB rabbits that were acquired from a second vendor and from four rabbits of various breeds that belonged to a local petting zoo. Bacterial Culture and Isolation Fecal pellets were homogenized ho·mog·e·nize v. ho·mog·e·nized, ho·mog·e·niz·ing, ho·mog·e·niz·es v.tr. 1. To make homogeneous. 2. a. To reduce to particles and disperse throughout a fluid. b. in tryptic tryp·tic adj. Relating to or resulting from trypsin. tryptic relating to or resulting from digestion by trypsin. soy broth (Remel, Lenexa, KS) and incubated at 37[degrees]C overnight. Each sample was then plated on Rainbow Agar Agar, in the Bible Agar (ā`gər), the same as Hagar. agar, substance obtained from seaweed agar (ä`gär, ā`–, ăg`är) O157 (Biolog, Hayward, CA) and incubated at 37[degrees]C for approximately 36 hours. Bacterial colonies were selected on the basis of color. Pink and purple colonies were selected and restreaked on MacConkey or blood agar plates (Remel) or both. All the E. coli isolates were confirmed biochemically and characterized by using API 20E strips (Biomerieux Vitek, Hazelwood, MO). Selected E. coli organisms were serotyped at the Pennsylvania State University Pennsylvania State University, main campus at University Park, State College; land-grant and state supported; coeducational; chartered 1855, opened 1859 as Farmers' High School. E. coli Reference Center (ECRC ECRC - European Computer-Industry Research Centre GmbH ). DNA Extraction and Polymerase Chain Reaction (PCR) Genomic DNA was extracted from bacteria by using InstaGene Matrix (Bio-Rad Laboratories, Hercules, CA). PCR primers and conditions to detect eae, stx1B, and stx2A and variants have been described previously (6). Southern Blot Analysis South·ern blot analysis n. An electrophoretic procedure used to separate and identify DNA sequences. Southern blot analysis was performed by using a Shiga toxin 1B (stx1B) probe generated by PCR amplification of EHEC O153:H- DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. to confirm stx1B in EHEC strains isolated from rabbits. Fifteen microliters of amplicon underwent electrophroresis through a 1.3 % agarose agarose more highly purified form of agar with similar uses to agar and widely used in the separation of nucleic acid fragments. gel and was transferred onto a Hybond N nylon membrane, as outlined by the manufacturer (Amersham, Piscataway, NJ). DNA was then cross-linked using the UV Stratalinker 1800 (Stratagene, La Jolla, CA). The fixed DNA was subsequently hybridized with the stx1B probe. The probe was labeled with horseradish peroxidase, exposed in the presence of luminol to Hyperfilm-ECL as outlined by the manufacturer (Amersham). High-Resolution Genotyping by Repetitive-Element Sequence-Based PCR (Rep-PCR) To perform Rep-PCR chromosomal profiling, genomic DNA was extracted from bacteria by using High Pure PCR Template Preparation Kit (Roche Diagnostics GmbH, Mannheim, Germany) and quantified by using a GeneQuant pro (Biochrom Ltd., Cambridge, UK) spectrophotometer spectrophotometer, instrument for measuring and comparing the intensities of common spectral lines in the spectra of two different sources of light. See photometry; spectroscope; spectrum. . Two primer pairs were used for the amplification reactions (7): REP1R-I (5'-IIIICGICGICATCIGGC-3'), REP2-I (5'-ICGICTTATCIGGCCTAC-3'); and ERICIR (5'-ATGTAAGCTCCTGGGGATTCAC-3'), ERIC2 (5'-AAGTAAGTGACTGGGGTGAGCG-3'). PCR reaction mixtures were prepared by using puReTaq Ready-To-Go PCR Beads (Amersham) containing 50 pmol of each primer and 1 [micro]L (100 ng) of DNA to a total volume of 25 [micro]L. Rep-PCR reactions were performed by using a Techne Genius (Techne Inc., Princeton, NJ) thermal cycler with the following conditions: for the REP primers, initial denaturation denaturation, term used to describe the loss of native, higher-order structure of protein molecules in solution. Most globular proteins exhibit complicated three-dimensional folding described as secondary, tertiary, and quarternary structures. (94[degrees]C, 7 min), followed by 30 cycles of denaturation (94[degrees]C, 30 s), annealing annealing (ənēl`ĭng), process in which glass, metals, and other materials are treated to render them less brittle and more workable. (40[degrees]C, 1 min), and extension (65[degrees]C, 8 min). A final extension (65[degrees]C, 16 min) completed the cycling protocol. For the ERIC primers, initial denaturation (95[degrees]C, 5 min) was followed by 35 cycles of denaturation (92[degrees]C, 45 s), annealing (51[degrees]C, 1 min), and extension (70[degrees]C, 10 min). A final extension (70[degrees]C, 20 min) completed the cycling protocol. PCR amplicons were visualized after electrophoresis in a 3% agarose gel and staining with ethidium bromide. Results Bacterial Cultures Rabbit fecal samples cultured on Rainbow agar O157 yielded E. coli colonies that ranged in color from pink to purple. No black colonies consistent with E. coli O157 were observed (8). Biochemical and molecular characterization of the rabbit E. coli strains is summarized in the Table. Most O153 strains were negative for rhamnose Rhamnose is a naturally-occurring deoxy sugar. It can be classified either as a methyl-pentose or a 6-deoxy-hexose. Rhamnose occurs in nature in its L-form as L-rhamnose (6-deoxy-L-mannose). This is unusual since most of the naturally-occurring sugars are in D-form. and sucrose. Some colonies of the O153:H- EHEC strain isolated from the first outbreak of HUS in DB rabbits (6) and a strain of unknown O 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. that showed autoagglutination were sorbitol sorbitol /sor·bi·tol/ (sor´bi-tol) a six-carbon sugar alcohol from a variety of fruits, found in lens deposits in diabetes mellitus. negative like most O157:H7 EHEC organisms isolated from humans. In addition, two O145:H- EPEC EPEC enteropathogenic Escherichia coli. EPEC Enteropathic Escherichia coli, see there were sorbitol negative. Prevalence of EHEC Strains Seven (25%) of 28 DB rabbits acquired from one commercial source were positive for eae+, stx1+ E. coli, including serotypes O153:H- and O153:H7. One (14%) of the 7 rabbits was infected with an EHEC of unknown O serotype that showed autoagglutination (DB 02-177, isolate 03-192) and was co-infected with enteropathogenic E. coli (EPEC) O145:H-. Eleven (39%) of the 28 DB rabbits were positive for EPEC O145H- or O145:H7. In addition, 1 (9%) of 11 NZW rabbits from the same source was positive for eae-, stx1+ O153:H-, and O153:H7 E. coli. All the E. coli strains were negative for stx2 and variants. In contrast, six DB rabbits from another commercial source and all four rabbits from the petting zoo were negative for EHEC and EPEC. Almost all of the eae-, stx1- E. coli belonged to serotype O7:H7. Southern Blot Analysis The presence of the stx1B amplicon was confirmed in O153:H- and O153:H7 E. coli. The O145:H- and O145:H7 isolates were confirmed to be negative for stx1B (Figure 1). [FIGURE 1 OMITTED] High-Resolution Genotyping by Rep-PCR Figure 2 shows the results obtained by Rep-PCR by using two different sets of primers, REP and ERIC. All the rabbit O153:H- and O153:H7 Stx-producing E. coli organisms tested, including eae- isolates from a NZW rabbit, produced identical amplification patterns that differed from those produced by two other O153:H- EHEC strains isolated from humans. Similarly, all the rabbit O145:H- and O145:H7 EPEC isolates produced identical amplification patterns that differed from those produced by a human and a bovine O145:H- EHEC. The EHEC isolated from the rabbit infected with EPEC O145:H- had an amplification pattern similar to that produced by the O153 strains. [FIGURE 2 OMITTED] Discussion In 2001, approximately 2 million rabbits were used as a food source (9). In addition, in 2000, laboratories used [greater than or equal to] 250,000 rabbits, and the domestic rabbit population in the United States was estimated at 9 million (9). Also, the rabbit is becoming an increasingly popular pet in U.S. households. In this study, we determined that 25% of the DB and 9% of the NZW rabbits from one commercial source of laboratory rabbits harbored Stx-producing E. coli O153:H- or O153:H7 in their feces. These findings raise concerns about the zoonotic risk for humans, given that rabbits are common companion animals, are used for biomedical research, and are an agricultural food source. DB rabbits are very popular in pet stores, are commonly used in rabbit shows, and are the second most common rabbit breed used in research after NZW rabbits (9). In addition, NZW rabbits are commonly used as a meat source in the United States. More studies are needed to assess the prevalence of these strains and other EHEC in agricultural, pet, and wild rabbit populations. Wild rabbits were also identified as vectors of a Stx-producing O157 E. coli strain that was isolated from cattle in an outbreak of hemorrhagic diarrhea and HUS involving visitors to a zoo (10). Our finding that most O153:H- and O153:H7 EHEC were unable to ferment rhamnose and sucrose indicates that these biochemical markers may be useful for the detection of these strains. For example, the inability to ferment rhamnose by some human EHEC strains has been applied to the development of selective isolation media (11). Rhamnose-negative rabbit EPEC strains appear to be highly pathogenic (12). Cattle are considered the primary reservoir host of O157 and non-O157 EHEC (13). Human infections have been linked to the presence of these bacteria in undercooked ground beef. In a recent study, the prevalence of non-O157 EHEC strains on beef carcasses was [greater than or equal to] 50%. Some isolates in that study also belonged to serotypes O153 and O145 (13). In addition, a study investigating the prevalence of non-O157 EHEC from human diarrheal samples in the United States demonstrated that non-O157 serotypes are at least as prevalent as serotype O157 (14). Serotype O145 has been isolated from diarrheic children in the United States and is a common non-O157 EHEC serotype isolated from HUS case-patients in Europe (15,16). Indeed, non-O157 serotypes are a leading cause of IIUS in Germany (17). Co-infection of EHEC and EPEC was also identified in one rabbit in this study. The EHEC and EPEC strains isolated from this rabbit appeared to belong to different serotypes. The high prevalence of these E. coli strains in rabbits and the occurrence of co-infection suggest that in vivo transduction transduction, in genetics: see recombination. Transduction (bacteria) A mechanism for the transfer of genetic material between cells. of EPEC by Stx-encoding bacteriophages from EHEC may naturally occur in this host (18). By performing Southern blot analysis, we confirmed the presence of stx1B in the O153:H- and O153:117 isolates, including the strain isolated from the rabbit infected with EPEC. In addition, by performing Rep-PCR analysis, we demonstrated that selected rabbit O153 EHEC and O145 EPEC isolates of the same O serotype represented two distinct clones. This apparent clonal nature of the isolates suggests transmission of E. coli between rabbits. Because these rabbit E. coli strains appeared to represent distinct clonal groups by Rep-PCR fingerprinting, their phylogenetic phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. relatedness to other strains was subsequently investigated by using multilocus sequence typing Multilocus sequence typing (MLST) is a technique in molecular biology for the typing of multiple loci. The procedure characterizes isolates of bacterial species using the DNA sequences of internal fragments of multiple (usually seven) housekeeping genes. . EHEC O153 and EPEC O145 belong to the EHEC 2 and EPEC 2 groups, respectively (T. S. Whittam, unpub. data). Rabbits may have become infected with these EHEC and EPEC strains from hay contaminated with cattle feces. Alternatively, rabbit-adapted E. coli strains may have been transduced by Stx-encoding bacteriophages from EHEC strains that transiently infected this rabbit colony. Previous experiments in NZW rabbits, in which purified Stx1 was infused intravenously, postulated that renal lesions did not develop in rabbits and that the rabbit model failed to replicate human HUS (19,20). We recently reported that glomerulonephritis glomerulonephritis: see nephritis. , tubular lesions, and renal glomerular glomerular /glo·mer·u·lar/ (glo-mer´u-ler) pertaining to or of the nature of a glomerulus, especially a renal glomerulus. glo·mer·u·lar adj. thrombotic microangiopathy, the hallmark of HUS, developed in DB rabbits naturally infected with EHEC (6). In the present study, however, HUS did not develop in most rabbits colonized Colonized This occurs when a microorganism is found on or in a person without causing a disease. Mentioned in: Isolation with EHEC. This result is consistent with human studies in which asymptomatic infection has been reported in household contacts of children with HUS and with studies showing that previous infection and frequent reexposure to E. coli O157:H7 may confer some protection against symptomatic illness (4,21). In summary, our findings indicate that rabbits are a newly recognized reservoir host of EHEC that poses a zoonotic risk to humans. These findings also provide an opportunity to develop a rabbit model to study the pathogenesis of EHEC-induced disease and HUS in a naturally susceptible reservoir host.
Table. Serotypes, biochemical, and molecular characterization
of Escherichia coli strains isolated from laboratory rabbits'
stx2 and
Source Rabbit Serotype API code stx1 variants eae
A DB 01-204 O153:H 5144162 + - +
O145:H 5144552 - - +
A DB 01-206 O145:H 5144552 - - +
A DB 01-207 O7:H- 5144572 - - -
A DB 01-208 O7:H- 5144572 - - -
A DB 01-210 O7:H- 5144572 - - -
A DB 01-211 O7:H- 5144572 - - -
A DB 02-171 O8:H- 5144572 - - -
O145:H- 5144572 - - +
A DB 02-181 O145:H- 5144572 - - +
O145:H- 5144672 - - +
O145:H- 4144572 - - +
A DB 02-182 O145:H- 5144572 - - +
O7:HM, O141:HM 5144572 - - -
A DB 02-174 O153:H- 5144542 + - +
A DB 02-175 O138:HM 5144572 - - -
O153:H- 5144542 + - +
A DB 02-172 O153:H- 5144542 + - +
A DB 02-169 O103:H2 5144572 - - -
A DB 02-177 O145:H- 5144572 - - +
A:H- 5144142 + - +
O145:H- 5144172 - - +
A DB 02-173 O145:H- 5144572 - - +
A DB 02-183 O153:H- 5144572 + - +
O153:H- 5144542 + - +
A DB 02-176 O7:H, O141:H- 5144572 - - -
A DB 02-179 O153:H7 5144542 + - +
A DB 02-2413 O145:H- 5144572 - - +
A DB 02-2368 O145:H- 5144572 - - +
A DB 02-10032 O145:H- 5144572 - - +
A DB 02-206 O145:H- 5144572 - - +
O145:H7 5144572 - - +
A DB 02-207 O145:H- 5144572 - - +
O145:H- 5144172 - - +
O145:H7 5144572 - - +
A DB 02-208 O153:H- 5144542 + - +
A DB 02-209 O8:H44 5144572 - - -
A DB 02-210 M:H- 7144172 - - -
O75:H- 5144172 - - -
A DB 02-212 O145:H- 5144572 - - +
A NZW 02-153 O7:H7 5144572 - - -
A NZW 02-186 O7:H7 5144572 - - -
A NZW 02-187 O7:H7 5144572 - - -
A NZW 02-188 O7:H7 5144572 - - -
A NZW 02-198 NT:H7 5144572 - - -
A NZW 02-199 O7:H7 5144572 - - -
A NZW 02-218 O86:H7 5144572 - - -
A NZW 02-222 O7:H7 7144573 - - -
A NZW 02-223 M:H7 7144572 - - -
A NZW 02-225 O7:H7 5144572 - - -
O145:H- 5144572 - - -
A NZW 02-227 O153:H- 5144542 + - -
O153:H7 5144542 + - -
B DB 02-228 O75:H- 5144172 - - -
B DB 02-231 O7:H7 5144572 - - -
B DB 02-232 O7:H7 5144572 - - -
B DB 02-233 O7:H7 5144572 - - -
(a) DB, Dutch Belted; NZW, New Zealand White: A, autoagglutination;
M, multiple; NT, did not wact with antisera.
Acknowledgments We thank David B. Schauer for critical review of the manuscript. This study was supported by NIH "Not invented here." See digispeak. NIH - The United States National Institutes of Health. grant T32-RR07036. References (1.) Hughes AK, Ergonal Z, Stricklett PK, Kohan DE. Molecular basis for high renal cell sensitivity to the cytotoxic effects of shigatoxin-1: upregulation of globotriaosylceramide expression. J Am Sac Nephrol 2002;13:2239-45. (2.) World Health Organization. Zoonotic non-O157 shiga toxin-producing Escherichia coli (STEC STEC shiga toxin-producing Escherichia coli. ). Report of a WHO scientific working group meeting. Berlin, Germany: Department of Communicable Disease Surveillance and Response, The Organization; 1998. (3.) Rabatsky-Ehr T, Dingman D, Marcus R, Howard R, Kinney A, Mshar P. Deer meat as the source for a sporadic case of Escherichia coli O157:H7 infection, Connecticut. Emerg Infect Dis 2002;8:525-7. (4.) Crump JA, Sulka AC, Langer AJ, Schaben C, Crielly AS, Gage R, et al. An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm. N Engl J Med 2002;347:555-60. (5.) Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis 2002;8:1468-73. (6.) Garcia A, Marini RP, Feng Y, Vitsky A, Knox KA, Taylor NS, et al. A naturally occurring rabbit model of enterohemorrhagic Escherichia coli-induced disease. J Infect Dis 2002; 186:1682-6. (7.) Versalovic J, Kapur V, Koeuth T, Mazurek GH, Whittam TS, Musser JM, et al. DNA fingerprinting of pathogenic bacteria by fluorophore-enhanced repetitive sequence-based polymerase chain reaction. Arch Pathol Lab Med 1995;119:23-9. (8.) Bettelheim KA. Studies of Echerichia coli cultured on Rainbow Agar O157 with particular reference to enterohaemorrhagic Escherichia coli (EHEC). Microbial microbial pertaining to or emanating from a microbe. microbial digestion the breakdown of organic material, especially feedstuffs, by microbial organisms. Immunol 1998;42:265-9. (9.) Grannis J. U.S. rabbit industry profile: USDA USDA, n.pr See United States Department of Agriculture. , APHIS, VS. Fort Collins (CD): Centers for Epidemiology and Animal Health, Center for Emerging Issues; 2002. (10.) Pritchard GC, Williamson S, Carson T, Bailey JR, Warner L, Willshaw G, et al. Wild rabbits--a novel vector for verocytotoxigenic Escherichia coli O157. Vet Rec 2001;149:567. (11.) Hiramatsu R, Matsumoto M, Miwa Y, Suzuki Y, Saito M, Miyazaki Y. Characterization of Shiga toxin--producing Escherichia coli O26 strains and establishment of selective isolation media for these strains. J Clin Microbial 2002;40:922-5. (12.) Camguilhem R, Milon A. Biotypes and O serogroups of Escherichia coli involved in intestinal infections of weaned rabbits: clues to diagnosis of pathogenic strains. J Clin Microbial 1989;27:743-7. (13.) Arthur TM, Barkocy-Gallagher GA, Rivera-Betancourt M, Koohmaraie M. Prevalence and characterization of non-O157 Shiga toxin-producing Escherichia coli on carcasses in commercial beef cattle processing plants. Appl Environ Microbial 2002:68:4847-52. (14.) Fey PD, Wickert RS, Rupp ME, Safranek TJ, Hinrichs SH. Prevalence of non-O157 Shiga toxin-producing Escherichia coli in diarrheal stool samples from Nebraska. Emerg Infect Dis 2000;6:530-3. (15.) Bokete TN, Whittam TS, Wilson RA, Clausen CR, O'Callahan CM, Moseley SL, et al. Genetic and phenotypic analysis of Escherichia coli with enteropathogenic characteristics isolated from Seattle children. J Infect Dis 1997;175:1382-9. (16.) Eklund M, Scheutz F, Siitonen A. Clinical isolates of non-O157 Shiga toxin-producing Escherichia coli: serotypes, virulence characteristics, and molecular profiles of strains of the same serotype. J Clin Microbial 2001;39:2829-34. (17.) Verweyen HM, Karch H, Allerberger F, Zimmerhackl LB. Enterohemorrhagic Escherichia coli (EHEC) in pediatric pediatric /pe·di·at·ric/ (pe?de-at´rik) pertaining to the health of children. pe·di·at·ric adj. Of or relating to pediatrics. hemolytic-uremic syndrome: a prospective study in Germany and Austria. Infection 1999;27:341-7. (18.) Acheson DW, Reidl J, Zhang X, Keusch GT, Mekalanos JJ, Waldor MK. In vivo transduction with shiga toxin 1-encoding phage phage: see bacteriophage. phage - A program that modifies other programs or databases in unauthorised ways; especially one that propagates a virus or Trojan horse. See also worm, mockingbird. The analogy, of course, is with phage viruses in biology. . Infect Immun 1998;66:4496-8. (19.) Zoja C, Corna D, Farina C, Sacchi G, Lingwood C, Doyle MP, et al. Verotoxin glycolipid Glycolipid One of a class of compounds having solubility properties of a lipid and containing one or more molecules of a covalently attached sugar. receptors determine the localization Customizing software and documentation for a particular country. It includes the translation of menus and messages into the native spoken language as well as changes in the user interface to accommodate different alphabets and culture. See internationalization and l10n. of microangiopathic process in rabbits given verotoxin-1. J Lab Clin Med 1992;120:229-38. (20.) Richardson SE, Rotman TA, Jay V, Smith CR, Becker LE, Petric M, et al. Experimental verocytotoxemia in rabbits. Infect Immun 1992:60:4154-67. (21.) Ludwig K, Sarkim V, Bitzan M, Karmali MA, Bobrowski C, Ruder H, et al. Shiga toxin-producing Escherichia coli infection and antibodies against Stx2 and Stx1 in household contacts of children with enteropathic hemolytic-uremic syndrome. J Clin Microbiol 2002:40:1773-82. Alexis Garcia * and James G. Fox * * Massachusetts Institute of Technology Massachusetts Institute of Technology, at Cambridge; coeducational; chartered 1861, opened 1865 in Boston, moved 1916. It has long been recognized as an outstanding technological institute and its Sloan School of Management has notable programs in business, , Cambridge, Massachusetts, USA Dr. Garcia is a postdoctoral fellow in the Division of Comparative Medicine at the Massachusetts Institute of Technology (MIT MIT - Massachusetts Institute of Technology ). His research interests include microbial pathogenesis and animal models of infection and neoplasia neoplasia /neo·pla·sia/ (-pla´zhah) the formation of a neoplasm. cervical intraepithelial neoplasia . Dr. Fox is professor and director of the Division of Comparative Medicine and professor in the Biological Engineering Division at MIT. Dr. Fox's research interests are centered on microbial pathogenesis and the role of chronic inflammation in cancer. Address for correspondence: Alexis Garcia, Division of Comparative Medicine, Massachusetts Institute of Technology, 77 Massachusetts Avenue, 16-820, Cambridge, MA 02139, USA; phone 617-253-1757, fax: 617-258-5708; email: agarcia@mit.edu |
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