Escherichia Coli As a Pathogen in Dogs and Cats Lothar Beutin

Escherichia coli as a pathogen in dogs and cats Lothar Beutin

To cite this version:

Lothar Beutin. Escherichia coli as a pathogen in dogs and cats. Veterinary Research, BioMed Central, 1999, 30 (2-3), pp.285-298. hal-00902570

HAL Id: hal-00902570 https://hal.archives-ouvertes.fr/hal-00902570 Submitted on 1 Jan 1999

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article

Escherichia coli as a pathogen in dogs and cats

Lothar Beutin

Robert Koch-Institut, Division of Emerging Bacterial Pathogens, Nordufer 20, 13353 Berlin, Germany

(Received 16 October 1998; accepted 17 December 1998)

Abstraet-Certain strains of Escherichia coli behave as pathogens in dogs and cats causing gastro- intestinal and extra-intestinal diseases. Among the five known groups of diarrhoeagenic E. coli, namely enteropathogenic E. coli (EPEC), enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), shiga-toxin producing E. cnli (STEC) and enteroaggregative E. coli (EAggEC), only EPEC and ETEC were clearly associated with enteric disease in young dogs. ETEC isolates from diarrhoeic dogs were found to be positive for the hcat-stable enterotoxins STa and STb but negative for heat-labile enterotoxin (LT). Canine ETEC were found to be different from those of other animals and humans by their serotypes, production of alpha-haemolysin and adhesive factors and by the production of uncharacterized types of cntcrt>tt>xins by some ETEC. Canine EPEC could be distin- guished from EPEC of humans or other animals by their serotypes and by the eae-protein intimin which mediates intimate adherence of EPEC to intestinal mucosa cells. STEC were occasionally isolated from faeces of healthy and diarrhoeic dogs but their role in canine diarrhoea is not yet well known. EIEC and EAggEC were not reported to occur in dogs or cats. Very little is known on diarrhoegenic E. coli in cats and further epidemiological investigations on this subject are needed. Besides its role in gastro-intestinal infections, E. coli can cause infections of the urogenital tract and systemic disease in dogs and cats. Extra-intestinal pathogenic E. coli strains from dogs and cats belong to a limited number of serotypes and clonal groups and are frequently found as a part of the normal gut flora of these animals. Many of these E. coli strains carry P-fimbriae and produce alpha-hacmolysin and a necrotizing cytotoxin (ChlF1 Some of the frequently isolated types of extra-intestinal pathogenic E. cnli from dogs, cats and humans were found to be highly genetically related but showed differences in their P-fimbrial adhesins which determine host specificity. Transmission of extra-intestinal and enteral pathogenic E. coli between dogs and humans was reported. Further research is needed, however, to determine the role of dogs and cats as transmission vectors of pathogenic E. coli strains to other animals and humans. © Inra/Elsevier, Paris.

Escherichia coli infections / dogs / cats / humans / diarrhoea / extra-intestinal diseases / virulence factors

Résumé Escherichia coli, un agent pathogène du chien et du chat. Certaines souches d’Esche- riclrio ioli sont pathogènes pour le chien et le chat, et provoquent des maladies gastro-intestinales et extru-intestinales. Parmi les cinq groupes d’E. coli responsables de diarrhée à savoir E. coli entéro- pathogène (EPEC), E. coli entérotoxinogènc (ETEC), E. culi entéroinvasive (EIEC), E. coli produi-

Tel.: (49) 30 4547 2484; fax: (49) 30 4547 2673; e-mail: [email protected] sant des toxines Shiga (STEC) et E. coli entéroaggrégatif (EAggEC), seules les EPEC et les ETEC ont été clairement associés à des maladies entériques chez les jeunes chiens. Des isolats d’ETEC issus de chiens diarrhéiques sont positifs en sonde nucléique pour des gènes d’entérotoxines thermostables Sta et Stb mais négatifs pour des gènes d’entérotoxines thermolabiles (LT). Les ETEC canins étaient différents des ETEC des autres animaux et des humains par leurs sérotypes, par la production de l’hémolysine alpha, de facteurs d’adhésions et par la production d’entérotoxines encore non-carac- térisées. Les EPEC canins peuvent être distingués des EPEC des humains ou d’autres animaux par leurs sérotypes et par l’intimine (Eae) qui permet l’adhésion intime des EPEC sur les cellules de la muqueuse intestinale. Les STEC, en revanche, ont parfois été isolés des fèces de chiens en bonne santé ainsi que de fèces de chiens diarrhéiques, mais leur rôle dans la diarrhée canine n’est pas encore bien connu. Les EIEC et EAggEC n’ont pas été signalés chez les chiens et les chats. On a peu de renseignements concernant la diarrhée due à l’E. coli chez les chats et des études épidémiologiques complémentaires sont nécessaires. E. coli peut provoquer également des infections de la voie urogénitale et des affec- tions systémiques chez le chien et le chat. Les souches pathogènes d’E. coli extra-intestinales de chiens et de chats appartiennent à un nombre limité de sérotypes et de clones et font fréquemment par- tie de la flore intestinale normale de ces animaux. Plusieurs de ces souches d’E. Coli produisent des fimbriae de type P, une hémolysine alpha et une cytotoxine nécrosante (CNFI). Les souches d’E. coli isolées d’infections extra-intestinales chez le chien, le chat et l’homme sont génétiquement très simi- laires, néanmoins les séquences de leurs adhésines de type P sont différentes et pourraient déterminer la spécificité d’hôte. La transmission d’E. coli pathogène à localisation extra-intestinale et entérique pathogène entre les chiens et les humains a été signalée. Toutefois, d’autres études sont nécessaires pour déterminer le rôle des chiens et chats en tant que vecteurs dans la transmission des souches d’E. coli pathogènes de l’homme et d’autres animaux. © Inra/Elsevier, Paris. infections dues à Escherichia coli / chiens / chats / humains / diarrhée / maladies extra- intestinales / facteurs de virulence

1. INTRODUCTION tic animals are present in industrialized countries. For example, the number of dogs Dogs and cats belong to those species of and cats living in Germany is estimated to be animals which have been living in a close 5 million and 6 million, respectively (pers. community with man for many thousands comm.). As a consequence, contacts of years. Large populations of these domes- between humans, dogs and cats are numer- ous and the possibility of transmission of 4) shiga-toxin producing E. coli (STEC) micro-organisms between these different expressing one or more different types host species is extremely high. of cytotoxins (Stxl and Stx2); The enterobacterium Escherichia coli is 5) enteroaggregative E. coli (EAggEC) a normal commensal inhabitant of the gut showing a distinct aggregative pattern of of humans and warm-blooded animals. As adherence to epithelial cells. other mammals, and cats are colonized dogs Strains belonging to either group of with E. coli the first of their life during days EPEC, ETEC or STEC are known to cause [74]. Among the E. coli some strains species, disease in humans and in some species of are known to cause enteric or extra-intesti- animals, whereas EIEC and were nal infections in humans and EAggEC animals. More- only isolated from infected humans. Besides over, some E. coli strains are pathogenic the recognized groups of diarrhoeagenic transmitted between different host species E. coli, certain E. coli strains were described and may cause disease in one host but not in which express other types of cyto- and the other. E. coli as a in and pathogen dogs enterotoxins, or adherence factors. The role cats was the of two earlier subject review of these E. coli strains and their virulence articles The aim of this review is to [15, 56]. factors in diarrhoeal disease is not well summarize the current state of knowledge known and requires further investigation. E. coli as a in regarding pathogen dogs and This chapter describes what is known about cats and to discuss findings on the relation- E. coli as an agent of diarrhoea in dogs and between E. coli strains which were ships cats. isolated from dogs, cats, other animals and humans. 2.1. Verocytotoxic E. coli and shiga-toxin-producing 2. INTESTINAL ESCHERICHIA E. coli (STEC) COLI INFECTIONS

Verocytotoxic E. coli were first described E. coli which were iso- Diarrhoeagenic in 1977 by their ability to cause damage to lated from animals and humans were shown cultured Vero cells [43]. Many, but not all to be heterogeneous for their virulence mark- verocytotoxic E. coli strains produce shiga- ers, their specificity for certain hosts and toxins (Stxl, Stx2 and Stx2 variants) [3 1] and for the diseases in age groups, caused and the latter strains are called shiga-toxin- human and animal patients. In regard to the producing E. coli (STEC) [17J.1. virulence markers which are associated with E. coli were isolated from fae- diarrhoea, five groups of enteral pathogenic Cytotoxic ces of and diarrhoeic and cats E. coli were established: healthy dogs in a number of different studies (table o. 1) enteropathogenic E. coli (EPEC) express- STEC, however, were only detected among ing colonization factors such as bundle isolates from dogs [11, 12, 26, 32] (table n. forming pili (bfp) and intimin (eae); Canine STEC were shown to produce different types of shiga-toxins and some of 2) enterotoxigenic E. coli (ETEC) express- these strains showed an ing heat-stable (ST) and heat-labile (LT) enterohaemolytic and were for the enterotoxins and different phenotype positive plas- host-specific mid encoded colonization antigens; haemolysin of enterohaemorrhagic E. coli (EHEC-haemolysin) [12]. 3) enteroinvasive E. coli (EIEC) carrying Other STEC strains from dogs carried both the genes for invasion of intestinal epithe- the genes for heat-stable enterotoxins STap lial cells; and STb together with stxl or stx2- sequences [32]. The combined expression lished where STEC 0157:H7 were isolated of shiga-toxins and enterotoxins was not from dogs [41,76]. The dog STEC 0157:H7 found in STEC from cattle or humans but strains belonged both to the same phage type was observed in some porcine STEC strains PT4 which was found associated with which are agents of post-weaning diarrhoea 21.0 % of STEC 0157:H7 isolates from in pigs [33]. The ST-producing STEC strains human patients in Canada [41]. In an out- were all isolated from diarrhoeic dogs and break investigation, epidemiologically were not found in the healthy control group related 0157:H7 strains were isolated from [32]. In contrast, other types of ST-produc- a dog, other farm animals and from a child ing ETEC from diarrhoeic dogs were found who developed bloody diarrhoea after infec- to be negative for shiga-toxins [60, 63]. tion [76]. Thus, asymptomatic dogs might function as vectors of transmission for STEC STEC carrier rates were not significantly 0157:H7 to humans and other animals. different between groups of asymptomatic (3.2-12.3% and with dogs positive) dogs Verocytotoxic E. coli were isolated at a diarrhoea (8.9 % positive) (table n. In one high frequency from healthy and diarrhoeic however, an association between diar- study, cats [ I, 11 ]. Stx-genes were not detected, rhoeal disease in and dogs Stx2-producing however, in these strains [12] or were not STEC strains was found [32]. Further inves- investigated [ 1 ]. STEC were not reported on numbers of and tigations larger healthy to occur in cats but it is noteworthy to diarrhoeic animals are needed in order to remark that these organisms were investi- learn more about the role of STEC strains as gated in only a small number of cats. The enteric in possible pathogens dogs. cytotoxins produced by some E. coli iso- Among STEC, strains of serotype lates from cats were not further characterized 0157:H7 are regarded as the most virulent for their pheno- and genotypes; however, for humans and these strains frequently heat-stable (ST) or heat-labile enterotoxins cause bloody diarrhoea and haemolytic ure- (LT) were not detected in these strains [1, mic syndrome [28[. Two cases were pub- 141. This finding and the observation that E. coli producing uncharacterized cytotox- E. coli is associated with diarrhoea in dogs ins were frequently isolated from faecal sam- and cats. In contrast, the production of CNFII ples of the healthy control group makes it is closely associated with E. coli strains unlikely that such E. coli strains are closely which cause extra-intestinal infections in associated with diarrhoea in cats. dogs and cats but the contribution of CNFl to extra-intestinal diseases is not well known and has to be further investigated. 2.2. toxin Cytotoxic necrotizing E. coli producing CNF2 were only rarely (CNF)-producing E. coli isolated from cats and were not detected in dogs [14, 58, 60]. In contrast, CNF2- E. coli inducing necrotizing lesions in producing E. coli were more associated with rabbit skin and morphological changes in bovines [58]. HeLa and Vero cell lines were first described in the mid 1980s [31]. Two types of cytotoxic necrotizing factors (CNF), 2.3. Enteropathogenic E. coli (EPEC) CNF1 and CNF2 were described and CNF- producing E. coli strains were isolated from Enteropathogenic E. coli (EPEC) belong healthy and diseased humans and from dif- to different serotypes and are known to be ferent species of animals [21, 31, 58]. Pro- agents of gastro-enteritis in young infants duction of CNFI was shown to be closely and in neonatal farm animals [24, 36, 56]. associated with alpha-haemolysin produc- According to their virulence markers, some tion and with certain serotypes of E. coli strains belonging to the EPEC group were strains isolated from dogs and cats [14, 21, later reclassified as enterotoxigenic E. coli 57, 58, 60]. Two lines of genetically closely (ETEC), shiga-toxin-producing E. coli related CNF1 producing E. coli 06 strains (STEC) and enteroaggregative E. coli could be established by analysing isolates (EAggEC). Classical EPEC strains are neg- from dogs, pigs, cows and humans [21 ]. ative for shiga-toxins and enterotoxins but Among CNFI strains from cats and dogs, carry the eae-gene which is located on the 04 and 06 serogroups were the most fre- chromosomal locus of enterocyte efface- quent [14, 21, 57, 58, 60]. In healthy cats, ment (LEE) [24]. Eae-positive EPEC strains CNF production was frequently associated can cause intimate adherence and attaching with E. coli 06:K53:H strains [14]. In an and effacing (AE) lesions in intestinal earlier study, strains belonging to the same epithelial cells of infected humans and ani- serotype were described as verocytotoxic mals. Besides eae, a second virulence E. coli and these were isolated from healthy marker is present in classical EPEC strains and from diarrhoeic cats [1]. Thus, it appears which is a plasmid-encoded (bfpA) bundle possible that some of the cytotoxic strains forming pilus mediating localized adher- which were not further characterized for ence of EPEC on epithelial cells. The eae- their toxin types might belong to the CNF- gene was also found inL. coli strains which producing group of E. coli (table o. do not belong to the EPEC serotypes and which are for These CNF1-producing E. coli were isolated negative shiga-toxins. from intestinal and extra-intestinal infec- strains are also called attaching and effacing tions in dogs and cats but also from faeces of E. coli (AEEC). asymptomatic animals [14, 58, 60]. The E. coli belonging to some of the classical CNF-producing strains were found to be human EPEC serogroups (026, 044, 055, negative for other virulence markers asso- 086, Olll, 0114, 0119, 0125, 0126, ciated with diarrhoeal disease such as shiga- 0127, 0128, 0142 and 0158) were occa- toxins and enterotoxins. In conclusion, these sionally isolated from diarrhoeic cats [85] data do not indicate that CNF production in and dogs [25, 70, 88!. Because there is only little data available on these strains, the sig- which stimulate intestinal fluid secretion. nificance of the classical EPEC types as pos- ETEC infections cause non-bloody, watery sible diarrhoeal agents in dogs and cats is diarrhoea in humans and in young farm ani- not known. mals [36, 51]. ETEC strains are serologi- diverse and different AE-lesions were detected in the intestine cally very express adhesion factors which determine their host of two cats with diarrhoea but the causative [51,54,91]. The toxins agent of the disease was not isolated [59]. specificity produced ETEC are divided into two Except in this study, EPEC were not asso- by major groups: heat-labile toxins and heat-stable tox- ciated with diarrhoea in cats. In contrast, (LT) ins Two of LT are known, LTI EPEC to different serotypes were (ST). types belonging in isolated from diarrhoeic [9, 15, 25, 38, and LTII which show partial homology dogs in their 78]. Some of the eae-positive E. coli strains their A-subunit, but no homology B-subunit. In a similar two biochemi- from dogs were also positive for the eaeB way, unrelated of heat-stable entero- gene (now termed espB), for plasmid-deter- cally types toxins were described which are mined EPEC-adherence factor sequences designated as STa and STb. The STa toxin is fur- (EAF) and the and thus resem- group bfpA-gene, called bled human EPEC strains. Enterotoxins, ther divided into two related subtypes (STIa) and ST-human (STh, shiga-toxins and haemolysins were not ST-porcine detected in canine EPEC strains [9, 25, 78]. STIb) [30, 51]. The serotypes of the few canine EPEC iso- ETEC were isolated as diarrhoeal lates were heterogeneous (045, 049:H 10, pathogens from neonatal calves, lambs, kids 0115, 0118:NM; 0119 and O-untypable) and pigs. An association between the ani- and most of these were different from those mal host and bacterial properties such as of human EPEC [25, 78]. In another study, serotypes, production of enterotoxins and the similarity between cloned eae genes from specific colonization factors was found [16, EPEC isolates originating from dogs, pigs 33, 35, 36, 56]. ETEC were also isolated and humans was investigated. An overall from diarrhoeic dogs and were character- homology between 81 and 84 % was found ized by a number of methods including between the different eae-protein sequences. bioassays, such as the infant mouse assay However, the eae-protein obtained from the and the ligated ileal loop assay, by serolog- dog strain was found to be serologically ical tests and by nucleic acid-based detection related to the eae of the human EPEC and methods. ETEC were found to be associ- not to that of the porcine EPEC strain [3]. ated with 2.7-31.1 % of cases of diarrhoea, in and were not iso- The data indicate that EPEC are potential particularly young dogs lated from control /7). diarrhoeic agents, particularly in young dogs healthy groups (table and that canine EPEC might be different Most canine ETEC strains were found to heat-stable enterotoxins which were from EPEC originating from other sources. express detected with the infant mouse 140, However, these findings need further con- assay firmation by examination of larger numbers 63 By the use of DNA-specific detection most canine ETEC of diarrhoeic and healthy dogs. At present, methods, ST-producing were shown to the for STa, and not much is known on the epidemiology of carry genes fewer strains were for STb, some- EPEC in dogs nor on their clinical signifi- positive times both toxin were in the cance for cats. types present same strain [25, 32, 60, 65, 80]. ETEC producing the heat-labile entero- 2.4. Enterotoxigenic E. coli (ETEC) toxin LT1 were not found in dogs (table 1!. Canine E. coli strains which stimulated Enterotoxigenic E. coli (ETEC) produce intestinal fluid secretion in the ligated ileal one or more different types of enterotoxins loop assay or exerted cytotonic effects on CHO cells in culture were, however, locations [60, 63, 80]. Some canine ETEC detected in different investigations [8, 52, were investigated for their fimbriae which 53, 81]. The biological activity of these serve in intestinal colonization. None of the strains resembled heat-labile enterotoxin ETEC isolates examined was positive for although they reacted negatively in other K88 (F4), K99 (F5) or CFAI (F2) and tests specific for LT [52, 53, 60 It is there- CFAII (F3) antigens except some ST-pro- fore possible that uncharacterized types of ducing 042:H37 ETEC strains from Nor- enterotoxins, which are different from those way which were positive for K99 fimbriae found in ETEC from humans and other ani- [25, 53, 63, 64, 80]. The fimbrial antigen mals, are produced by some canine E. coli. K99 is strongly associated with bovine In experimental infections, dogs were found ETEC but it is sporadically found in ETEC to be susceptible to LT produced by human strains originating from other animals [ 16]. ETEC strains were resistant to although they ETEC from human and animal sources colonization with these ETEC types [66!.j. carry their enterotoxin genes on plasmids In contrast to the moderate effect caused by of different sizes [91 ]. This was also found LT, the dogs were found to be more sus- with ST-producing ETEC strains from dogs ceptible and did not develop immunity to [60, 80 Like porcine ETEC, ETEC from ST [50, 66]. These could findings explain dogs were frequently found to produce strains in why ST-producing predominate alpha-haemolysin which is not found in natural infections of dogs with ETEC. human ETEC strains [12, 33, 60, 63, 80]. The genes were found to The ETEC isolated from were dif- alpha-haemolysin dogs be encoded on 48 MD size transferable ferent from ETEC isolated from other ani- plas- mids in canine ETEC 042:H37 and on mals or humans some traits. by phenotypical 52 MD size plasmids in ETEC 070:H- Canine ETEC were attributed to serotypes strains. The genes for ST and for alpha- which are or not found ETEC rarely among were located on different isolated from humans, and calves haemolysin plas- pigs [54, mids [60[. 91 ]. Among canine ETEC, ST-producing 042:H37 strains were most frequently found In contrast to dogs, there is only very lit- and were isolated at different geographical tle information available on ETEC in cats. ETEC were not found among 22 diarrhoeic lent metritis (pyometra). E. coli was iso- and 25 healthy cats which were investigated lated in 50-85 % of bitches suffering from for ST by the infant mouse assay and for pyometra [13, 29, 68, 79] and was also LT by the Y 1 adrenal cell test [ 1 In another detected as a cause of pyometra in cats [22].] . study, LT-positive E. coli were not found In dogs with pyometra, quantitative deter- among 159 bacterial isolates which origi- mination of live E. coli in the uterine con- nated from 23 healthy cats [ 14]. tents yielded high numbers (10&dquo;’-10&dquo;/mL) and the infective E. coli strain was gener- ally present in the pure culture [68, 79]. Fre- 3. EXTRA-INTESTINAL quently, bitches with pyometra were found INFECTIONS WITH to suffer simultaneously from UTI and in ESCHERICHIA COLI most of these cases the same E. coli strain type was isolated from urine and the uterine Certain strains of E. coli can behave as content [68, 71, 79].] . opportunistic pathogens causing extra- intestinal infections in humans and animals. In dogs and cats, facultative pathogenic 3.3. Systemic infections E. coli were shown to cause urinary tract infection (for reviews see [15, 56]), pro- Besides Staphylococcus aureus, E. coli statitis, vaginitis and pyometra J 13, 79, 84], is an important cause of perinatal death of perinatal infections and puppy death [13, puppies and kittens [49, 67, 94]. The infec- 67, 94], otitis externa [7], cardiovascular tive E. coli strains can be transmitted intra- infections [18[, cholecystititis [47J, septi- uterine or by the infected genital tract lead- caemia and endotoxaemia [37, 77] . ing frequently to abortion or to a septicaemic death of the puppies in the first days of life [ 13, 44, 67]. Furthermore, subclinical mas- 3.1. Urinary tract infections (UTI) titis of the bitch was found as another important source of bacterial infection in new- E. coli is the bacterium most commonly bom colibacillosis isolated from the urine of dogs and cats with puppies [67]. Septicaemic urinary tract infections (UTI) [4, 34, 42, 56, caused by E. coli strains of the normal 92]. The incidence of bladder infection in intestinal flora was observed as a frequently in with bitches was found to increase particularly occurring complication dogs parvoviral enteritis Bacterial endo- with their age. In most cases of UTI, the [37, 77]. carditis result from E. coli infecting E. coli strain was isolated in pure may systemic infection in and UTI was discussed as culture from urine and a level of 100 000 dogs a source of these blood-borne infections bacteiia/mL or more was proposed as a basis for distinguishing significant bacteriuria [18]. E. coli were also isolated from infected and shown to be a cause of from contamination 142, 56]. E. coli was organs septi- caemia in cats also found to be a cause of pyelonephritis [57, 58, 62]. in dogs and cats showing non-significant bacteriuria In contrast, E. coli [23, 45, 82J. 3.4. Characteristics of E. coli strains was not found to a role in canine or play from the normal faecal flora and feline urolithiasis [69, 83[. from extra-intestinal infections in dogs and cats 3.2. Genital infections E. coli strains causing extra-intestinal Besides its role in UTI, E. coli is the infections in dogs and cats were found to major pathogen in male dogs with prostati- be associated with a few 0-groups which tis [84 and in bitches with chronic puru- were also frequently found in the normal faecal flora of these animals. It was therefore haemolysin, CNFl, P-fimbriae and aer- suggested that the faecal flora serves as a obactin [14, 27, 60, 61, 62, 86!. Enterotox- major reservoir and a source of infection ins or shiga-toxins were not detected among with these strains [22, 29, 46, 89, 90]. Basi- faecal and uropathogenic E. coli isolates cally the same observations were made for from dogs or cats [14, 57, 60]. E. coli strains causing extra-intestinal infections in humans [39!. 3.5. between faecal and Serological typing of 0-, K- and H-anti- Relationships uropathogenic E. coli isolated from gens of faecal and extra-intestinal E. coli dogs, cats and humans from cats and dogs was performed in a number of different studies [1, 5, 10, 14, 21, 27, The E. coli strains isolated from the fae- 57, 60, 62, 88-90]. Strains belonging to a small number of 0-serogroups (02, 04, 06, cal flora and from extra-intestinal infections of cats and humans were found to have 08, 09, 022, 025, 075 and 083) were dogs, a similar of certain of found to dominate among faecal and extra- frequency 0-types, some K- and and of vir- intestinal isolates from dogs and cats [1, 14, H-antigens typical 22, 27, 60, 62, 73, 86]. Among these strains, ulence attributes such as alpha-haemolysin, of CNFI and aer- E. coli of serogroups 04 and 06 were most P-fimbriae, production obactin some E. coli frequently isolated. Some E. coli serotypes, [19,39,55]. Moreover, strains from cats and humans such as 04:H-, 04:H5, 06:K53:H1 and dogs, sharing identical such as 04:H5 and 06:H31 strains were isolated from extra- serotypes intestinal and faecal samples of both dogs 06:K13: H 1, were also found to have highly related P-fimbriae and cats [1, 10, 14, 21, 27, 60, 62]. serotypes (F12, F13). Uropathogenic E. coli strains from humans, Other faecal and extra-intestinal E. coli dogs and cats were shown to be highly isolates from dogs and cats were found to genetically related and could be assigned to be positive for the K1 or K5 capsular anti- six major E. coli clonal groups [87]. The gens. The E. coli K I strains belonged to predominating serotypes within different groups 02, 07, 018, 021 and 083 [I, 10, uropathogenic clones were 04:H-, 04:H5, 21, 27, 60, 73, 86]. The K5 antigen was 06:Hl; and 06:H31 [21, 87]. Dog and found in 06, 021 and 075 strains. Strains human E. coli 02, 04 and 06 strains were belonging to 02:K1:H6 and 06:K5:H1I also found to be similar for the chromosomal serotypes were isolated in different studies position and for the DNA sequences of from both dogs and cats [ 1, 21, 27, 73, 861. alpha-haemolysin determinants and P-fim- E. coli expressing K1 and K5 are also fre- briae [46, 61 It was, therefore, suggested quently occurring in the human faecal flora that the clonally related human and canine E. and are highly associated with neonatal coli strains might be transmitted as urinary meningitis, bacteremia and pyelonephritis pathogens between dogs and humans [46, in humans [39, 55]. 86]. Faecal and extra-intestinal E. coli iso- Other studies indicated, however, that lates from dogs and cats were also found to the genetically related canine and human be similar for the expression of different uropathogenic E. coli strains had different virulence attributes. Most of these strains adhesins (minor fimbrial subunit) which show haemolytic activity and further inves- determine the receptor specificity of P-(F12) tigations revealed that they carry chromo- fimbriae [27, 72, 73, 75]. Phenotypically, somally encoded alpha-haemolysin deter- most uropathogenic E. coli from dogs were minants [ 10, 60, 61 !. E. coli 04, 06 and found to agglutinate dog but not human ery- 075 strains from dogs and cats were found throcytes and to adhere to canine but not to to be similar for the production of alpha- human uroepithelial cells, whereas most human E. coli strains showed the opposite detection of diarrhoeal pathogens should be picture [27, 73]. It was therefore suggested based on the identification of virulence that the variation in the Galal-4Ga1 recep- markers which are associated with diarrhoeal tor specificity is a mechanism for shifting disease. In contrast, serotyping of clinical host specificity in E. coli from humans and isolates was not found to be suitable as a dogs and that this variation has evolved in screening method for diarrhoeagenic E. coli response to the topography of host cellular strains in dogs and cats [6, 88]. receptors [75]. The differences found in the Uropathogenic E. coli from dogs and cats fimbrial receptor specificity between were found to be similar to human E. coli from and humans uropathogenic dogs strains with to their could indicate that these strains are uropathogenic regard specific clonal and virulence for their their clonal related- serotypes, types host, despite attributes. The role of ness. alpha-haemolysin, P-fimbriae, capsular antigens and aerobactin in the pathogenicity of these strains is well known. However, further stud- 4. CONCLUSION already ies are needed on the role of CNF1 which is closely associated with normal faecal and There is little information available about extra-intestinal E. coli strains in dogs, cats E. coli causing disease in dogs and cats com- and humans. pared to the number of investigations which and cats also an were performed on E. coli as a pathogen of Dogs might play impor- humans, pigs and cattle. Among the five tant role as E. coli transmission vectors to or man. indi- groups of diarrhoeagenic E. coli, only ETEC other animals Several studies related and EPEC strains were clearly associated cate that transmission of clonally with gastro-intestinal disease in young dogs faecal and uropathogenic E. coli types and very little is known on the epidemiology between humans, dogs and cats has occurred of these strains, their adhesion mechanisms and might still happen [20, 81, 87]. How- and their host specificity. Although E. coli ever, the frequency of transmission of belonging to the STEC group were already uropathogenic E. coli between different isolated from dogs, it is not clear if these mammalian hosts is not known and the dif- are associated with disease in dogs or cats. ferences found between the P-fimbrial Further research on this subject is needed, adhesins of E. coli strains from dogs and particularly in view of a global health prob- humans indicate that these strains are host lem which is caused by STEC infections in specific. humans Further are also [93]. investigations Recent findings indicate that the trans- on those E. coli strains which necessary mission of diarrhoeagenic E. coli strains were isolated from diarrhoeic and dogs occurs between dogs and humans. Asymp- which were shown to ’unconven- produce tomatic dogs were identified as carriers of tional’ enterotoxins or cytotoxins. human pathogenic STEC including E. coli Very few data are available on E. coli as 0157:H7 strains and could thus play a role a possible agent of diarrhoea in cats. E. coli in outbreaks of STEC infections in humans strains belonging to one of the five different [41, 76]. Diarrhoeic dogs were identified as pathogroups associated with diarrhoeal dis- an important source of bacterial contami- ease were not found among clinical isolates nation of the environment in apartments of from cats. However, only a small number dog holders which might contribute to the of diarrhoeic and healthy cats were investi- spread and transmission of pathogenic E. gated, and epidemiological studies involving coli strains [48]. Thus, further research larger numbers of animals and appropriate should be directed towards detecting and detection methods are needed. Studies for characterizing diarrhoeagenic E. coli types in dogs and cats, their host specificity and [12] Beutin L., Geier D., Zimmermann S., Karch H., the possible of strains Virulence markers of Shiga-like toxin-producing exchange pathogenic Escherichia coli strains originating from healthy between animals and humans. domestic animals of different species, J. Clin. Microbiol. 33 (1995) 631-635. [13] Bjurstroem L., Aerobic bacteria occurring in the REFERENCES vagina of bitches with reproductive disorders, Acta Vet. Scand. 34 (1993) 29-34. [14] Blanco J., Blanco M., I., Blanco J.E., Abaas Franklin Wong [1] S., A., Kuehn I., Orskov F., Haemolytic Escherichia coli strains isolated from Orskov on Vero cells 1., Cytotoxin activity among stools of cats necro- Escherichia coli strains associated healthy produce cytotoxic with diarrhea tizing factor type 1 (CNF1),Vet. Microbiol. 38 in cats, Am. J. Vet. Res. 50 (1989) 1294-1296. (1993)157-165. [2] Adesiyun A.A., Campbell M., Kaminjolo J.S., [15] Broes A., Les Escherichia coli pathogènes du Prevalence of bacterial enteropathogens in pet chien et du chat, Ann. M6d. Vet. 137 (1993) dogs in Trinidad, Zentralbl. Veterinarmed. Reihe 377-384. B 44 (1997) 19-27. [ 16) Butler D.G., Clarke R.C., Diarrhoea and dysentery [3] An H., Fairbrother J.M., Dubreuil J.D., Harel J., in calves, in: Gyles C.L. (Ed.), Escherichia coli in Cloning and characterization of the eae gene from Domestic Animals and Humans, CAB Interna- a dog attaching and effacing Escherichia coli tional, Wallingford, 1994, pp. 91-1 16. strain 4221, FEMS Microbiol. Lett. 148 (1997) [17! Calderwood S.B., Acheson D.W.K., Keusch T., 239-245. Barrett T.J., Griffin P.M., Strockbine N.A., [4] Apel J., Hamann H.P., Weiss R., Zu Vorkom- Swaminathan B., Kaper J.B., Levine M.M., men und Antibiotika-Resistenz bakterieller Infek- Kaplan B.S., Karch H., O’Brien A.D., Obrig T.G., tionserreger in Urinproben von Katzen, Klein- Takeda Y., Tarr P.I., Wachsmuth LK., Proposed tierpraxis 34 (1989) 467-472. new nomenclature for SLT (VT) family, Am. Soc. Microbiol. News 62 I 18-I 19. [5] Askaa J., Jacobsen K.B., Sorensen M., Neonatal (ASM) (1996) infections in puppies caused by Escherichia coli [18] Calvert C.A., Greene C.E., Hardie E.M., Cardio- vascular infections in serogroups 04 and 025, Nord.Veterinarmed. 30 dogs: epizootiology, clini- (1978) 486-488. cal manifestations, and prognosis, J. Am. Vet. Med. Assoc. 187 (1985) 612-616. [6J Awad-Masalmeh M., Youssef U., Silber R., Zur Falbo E. coli [19] Caprioli A., V., Ruggeri F.R., Minelli F., Charakterisierung h!molysierender Orskov Donelli between Stamme aus an Diarrh6c bzw. Enteritis erkrank- I., G., Relationship cytotoxic factor and ten oder verendeten Hunden und Katzen, ihre necrotizing production serotype in Escherichia Viruienzfaktoren und hemolytic coli, J. Clin. Microbiol. Antibiotikaempfindlichkeit, 1 . Wien. Tier5rztl. Monatsschr. 77 (1990) 254-258. 27 ( 1989) 758-761. 120J D.A., Levin B.R., Selander R.K., Dis- Baba Fukata Saito Incidence of otitis Caugant [7] E., T., M., tribution of multilocus of Escherichia externa in and cats in Vet. Rec. 108 genotypes dogs Japan, coli within and between host families, J. Hyg. 92 () 981)393-395. (1984)377-384. [8] Baijer G., Saito M., Mayr A., Nachweis von !21 J Cherifi A., Contrepois M., Picard B., Goullel P., Enterotoxinbildenden E. coli St5iiimen (ETEC) Orskov 1., Orskov F., De Rycke J., Clonal rela- bei Hunden mit akuter Der Gastroenteritis, prak- tionships among Escherichia coli serogroup 06 tische Tierarzt 67 ( I 986) 472-476. isolates from human and animal infections, FEMS /9! Beaudry M., Zhu C., Fairbrother J.M., Harel J., Microbiol. Lett. 64 (1991) 225-230. Genotypic and phenotypic characterization of [22J Choi W.P., Kawata K., 0 group of Escherichia Escherichia coli isolates from dogs manifesting coli from canine and feline pyometra, Jap. J. Vet. attaching and effacing lesions, J. Clin. Microbiol. Res. 23 ( 1975) 141-143. 144-8. 34 (1996) 123] Christie B.A., The occurrence of vesicoureteral [ 10! Beutin L., Montenegro M., Orskov I., Orskov F., reflux and pyelonephritis in apparently normal Prada J., Zirnmermann S., Stephan R., Clone asso- dogs, Investig. Urol. 10 (1973) 359-366. ciation of verotoxin (shiga-like toxin) production [24! Donnenberg M.S., Enteropathogenic Escherichia with in strains of in: Blaser Ravdin enterohemolysin production coli, M.J., J.1., Greenberg H.B.,., E.scherichia coli, J. Clin. Microbiol. 27 (1989) Guerrant R.L. (Eds.), Infections of the Gastroin- 2559-2564. testinal Tract, Raven Press, New York, 1995, [ I I ! Beutin L., Geier D., Steinrucck H., Zimmermann pp.709-726. S., Scheutz F., Prevalence and some properties [25J Drolet R., Fairbrother J.M., Harel J., Helie P., of verotoxin (Shiga-like toxin)-producing Attaching and effacing and enterotoxigenic Escherichia cali in seven different species of Escherichia coli associated with enteric col- healthy domestic animals, J. Clin. Microbiol. 311 ibacillosis in the dog, Can. J. Vet. Res. 58 (1994) (1993) 2483-2488. 87-92. [26! Gallien P., Klie H., Lehmann S., Protz D., Hel- [40] Josse M., Jacquemin E., Kaeckenbeeck A., muth R., Schaefer R., Ehrler M., Nachweis vero- Presence chez le chien, d’ Escherichia coli pro- toxinbildender E. coli in Feldisolaten von Haus- ductrices d’une enterotoxine thermostable (Sta), und landwirtschaftlichen Nutztieren in Sachsen- Ann. M6d. V6t. 124 (1980) 211-214. Anhalt (Detection of verotoxin-producing E. coli !4)] ] Khakhria R., Duck D., Lior H., Extended phage- in field isolates from domestic and agricultural typing scheme for Escherichio cnli 0157:H7, animals in Suchsen-Anhalt), Berl. Muench. Tier- Epidemiol. Infect. 105 (1990) 51 I-520. arztl. Wochenschr. 107 ( 1994) 331-334. [421 Kivistoe A.K., Vasenius H., Sandholm M., Lab- 1271 Garcia E., Bergmans H.E., Van den Bosch J.F., oratory diagnosis of canine pyometra, Acta Vet. Orskov I., Van der Zeijst B.A., Gaastra W., Iso- Scand. 18 ( 1977) 308-315. lation and characterisation of dog uropathogenic 143] Konowalchuk J., J.L, Stavric S., Vero Escherichia coli strains and their fimbriae, Speirs to a of Escherichia coli, Infect. Antonie Leeuwenhoek 54 ( 1988) 149-163. response cytotoxin Immun.I8 (1977) 775-779. Griffin P.M.D., Escherichia coli 0157:H7 and [28] 1441 Linde C., Partial abortion associated with other enterohemorrhagic Escherichia coli, in: genital Escherichia coli infection in a bitch, Vet. Rec. Blaser M.J., Ravdin J.L, H.B., Guerrant Greenberg 112 ( 1983) 454-455. R.L. (Eds.), Infections of the Gastrointestinal Tract. Raven Press, New York, 1995, 145] Ling G.V., Cullen J.M., Kennedy P.C., Ruby pp. 739-761.1 . A.L., Brooks D.L., Relationship of upper and lower tract infection and bacterial invasion M., Renton J.P., D.H., urinary 1291 Grindlay Ramsay 0-groups of to bacteria test of Evcherichici coli associated with canine uroepithelium antibody-coated pyome- results in female Am. J. Vet. Res. 46 Res. Vet. Sci. 14 75-77. dogs, ( 1985) tra, ( 1973) 499-504. Escherichiti coli in: [30] Gyles C.L., enterotoxins, Low Braaten Johnson C.L. Escherichia coli in Domestic 146] D.A., B.A., Ling G.V., Gyles (Ed.), D.L., A.L., Isolation and of Animals and Humans, CAB Ruby comparison International, E.scherichia coli strains from canine and human Wallingford, 1994, pp. 337-364. patients with urinary tract infections, Infect. [311 Gyles CL., E.scherichia coli verotoxins and other Immun. 56 (1988) 2601-2609. in: C.L. (Ed.), E,scherichia coli cytotoxins, Gyles 147] Matthiesen D.T., J., Gallbladder in domestic animals and humans, CAB Interna- Lammerding rupture and bile peritonitis secondary to cholelithi- tional. Wallingford, 1994, pp. 365-398. asis and cholecystitis in a dog, J. Am. Vet. Med. !32! Hammermueller J., Kruth S., Prescott J., Gyles Assoc. 184 (1984) 1282-1283. C., Detection of toxin in Escherichin coli genes A., Goetz S., Schels H., isolated from normal and with diar- 148] Mayr Untersuchungen dogs dogs ueber die bei der von Hunden in rhea, Can. J. Vet. Res. 59 ( 1995) 265-270. Hygiene Haltung staedtischen Wohnungen (The hygiene of keeping [ 33 j Hampson D.J., Postweaning Escherichia coli diar- dogs in city apartments), Zentralbl. Baktcriol. rhoca in pigs, in: Gyles C.L. (Ed.), Escherichio Mikrobiol. Hyg. Ser. B, Umwelthyg. Kranken- coli in Domestic Animals and Humans, CAB haushyg. Arbeitshyg. Praev. Med. 183 (1986) International, Wallingford, 1994, pp. 171-191.1. 24(>-253. [341 Hirsh D.C.. Multiple antimicrobial resistance in 1491 Muennich A., Grucsscl T., Leopold T., Erfahrun- Eschericia coli isolated from the urine of dogs gen in der Diagnostik und Therapie von Welpen- and cats with cystitis, J. Am. Vet. Med. Assoc. erkrankungen in den ersten Lebenstagen (Expe- 162 885-887. (1973) riences in diagnosis and therapy of puppy diseases [35 Hodgson J.C., Diseases due to Escherichia cnli in in the first days of life), Ticraer!tliche Praxis 23 sheep, in: Gyles C.L. (Ed.). Escherichia coli in ( 1995) 497-501.1 . Domestic Animals and Humans, CAB Intcrna- 1501 Nalin D.R., Levine M.M., Young C.R., Bergquist tional, Wullingford, 1994, pp. 135-150. E.J., MeLaughlin J.C., Increased Escherichia cmli [36 ! Holland R.E., Some infectious causes of diarrhea enterotoxin detection after concentrating culture in young farm animals, Clin. Microbiol. Rev. 3 supernatants: possible new enterotoxin detectable (1990)34S-375. in dogs hut not in infant mice, J. Clin. Microbiol. [37! Isogai E., Isogai H., Onuma M., Mizukoshi N., 8 ( 1978) 700-703. Hayshi M., Namioka S., li.scherichia coli endo- 1511 Nataro J.P., Kaper J.B., Diarrheagenic Escherichin toxemia in dogs with parvovirus infection. Jpn. J. culi, Clin. Microhiol. Rev. 1 I ( 1998) 142-201.1. Vct. Sci. 51 (1989) 597-606. [52j Olson P., Hedhammar A.. Wadstrocm T., Entcro- 1381 Janke B.H., Francis D.H., Collins J.E., Libal M.C., toxigenic Eschericia coli infection in two dogs Zeman D.H., Johnson D.D.. Attaching and effac- with acute diarrhea, J. Am. Vet. Med. Assoc. 184 ing Escherichia coli infections in calves, pigs, ( 1984) 982-983. lambs, and dogs, J. Vet. Diagn. Invest. 1 ( 1989) !53 ! Olson P., Hedhammar A., Faris A., Krovacek K., 6-I1 . Wadstrocm T., Enterotoxigenic E.scherichia coli [39! Johnson J.R.. Virulence factors in lóscherichia (ETEC) and Klehsiella pneulI10lliae isolated from cnli urinary tract infection, Clin. Microbiol. Rev. dogs with diarrhoea, Vet. Microbiol. 10 ( 1985) 4F (l 1 9928. 1 ) 8( 577-589. [54J Orskov I, Orskov F., Significance of surface anti- with nonradioactive digoxigenin-labeled DNA gens in relation to enterotoxigenicity of E. cnli, in: probes, J. Clin. Microbiol. 28 (1990) 1465-1468. Ouchterlony 0., Holmgren J. (Eds.), Cholera and [66! Sack R.B., Johnson J., Pierce N.F., Keren D.F., Related Diarrheas. Molecular of a Global Aspects Yardley J.H., Challenge of dogs with live entero- Health Problem, Karger, Basel, 1978, toxigenic Escherichin coli and effects of repeated pp. 134-141. challenges on fluid secretion in jejunal Thiry- [55] Orskov I., Orskov F., Escherichia coli in extrain- Vella loops, J. Infect. Dis. 134 (1976) 15-24. testinal infections, J. Hygiene (Cambridge), 95 [67! Sager M., Remmers C., Ein Beitrag zur perina- (1985)551-575. talen Welpensterblichkeit beim Hund. Klinische, [56] Peeters J.E., Escherichia coli infections in rab- bakteriologische und pathologische Unter- bits, cats, dogs, goats and horses, in: Gyles C.L. suchungcn (Perinatal mortality in dogs. Clinical, (Ed.), Escherichia coli in Domestic Animals and bacteriological and pathological studies), Tier- Humans, CAB International, Wallingford, 1994, arztliche Praxis 18 (1990) 415-419. pp 261-283. [68 Sandholm M., Vasenius H., Kivistoe A.K., Patho- [57J Pohl P., Mainil J., Devriese L.A., Haesebrouck genesis of canine pyometra, J. Am. Vet. Med. F., Broes A., Lintermans P., Oswald E., Assoc. 167 (1975) 1006-1010. Escherichia coli productrices de la toxine cyto- [69] Schechter R.D., The significance of bacteria in toxique n6crosante de type I (CNF I) isolee a par- feline cystitis and urolithiasis, J. Am. Vet. Med. tir de processus pathologiques chez des chats et Assoc. 156 (1970) 1567-1573. des chiens, Ann. Med. Vet. 137 (1992) 21-25. 170] Schiff L.J., Barbera P.W., Port C.D., Yamashiroya [58] Pohl P., Oswald E., Van Muylem K., Jacquemin H.M., Shefner A.M., Poiley S.M., Entero- Escherichia coli infections: E., Lintermans P., Mainil J., E.scherichia coli pro- pathogenic increasing ducing CNFI and CNF2 cytotoxins in animals awareness of a problem in laboratory animals, with different disorders, Vet. Res. 24 (1993) Lab. Anim. Sci. 22 (1972) 705-708. 31 I-315. [7)] Schwarz J., Zur Beteiligung von E. coli an des [59] A., Mainil J.G., Moon H.W., Erkrankungen Urogenitaltraktes des Hundes. Pospischil Baljer G., 1. Attaching and effacing bacteria in the intestines of Mitteilung: Kulturelle Untersuchungen, Klein- 36 179-184. calves and cats with diarrhea, Vet. Pathol. 24 tierpraxis (1991) ( I 987) 330-334. [72] Senior D., Baker N., Cedergren B., Falk P., Lar- son G., Lindstedt R., Eden C.S., Globo-A-a new [60] Prada J., G., De J., Steinrueck H., Baljer Rycke for Escherichia coli, Zimmermann S., R., Beutin L., Charac- receptor specificity attaching Stephan FEBS Lett. 237 (1988) 123-127. teristics of alpha-hemolytic strains of Escherichin coli isolated from dogs with gastroenteritis, Vet. [73! Senior D.F., dcMan P., Svanborg C., Serotype, Microbiol. 29 (1991) 59-73. hcmolysin production, and adherence characteristics of strains of Escherichin coli causing urinary J., Zimmermann Beutin [61 / Prada S., Stephan R., L., tract infection in dogs, Am. J. Vet. Res. 53 (1992) Restriction fragment length polymorphisms asso- 494-498. ciated with determinants are alpha-hemolysin Smith The correlating with the expression of alpha-hemolysin 1741 H.W., development of the flora of the tract in in strains of Escherichia coli, Zentralbl. Bakte- alimentary young animals, J. Pathol. Bac- teriol. riol. 276 ( 1992) 152-164. 90 ( 1965) 495-5 13. 1751 N., Marklund B.I., Lund B., liver D., Rhoadcs H.E., Saxena Sero- Stroemberg !62! S.P., Meyer R.C., Hamers A., Gaastra W., Karlsson K.A., Nonnark identification of Escherichia coli isolated logical S., Host-specificity Escherichia from cats and Can. J. Med. 35 1) of uropathogenic dogs, Compo ( 1971 ) coli on differences in 2 I 8-223. depends binding specificity to Gal alpha I-4Gal-containing isoreceptors, [631 Richter T., Hellmunn E., Vorkommen und Eigen- EMBO J. 9 ( 1990) 2001-2010. schaftcn enterotoxinbildender Escherichia coli- 1761 Trevena W.B., Hooper R.S., Wray C., Willshaw Staemmc beim enteritiskranken Junghund (Occur- G.A., Cheasty T., Domingue G., Vero cytotoxin- rence and properties of enterotoxigenic producing Escherichia coli O 157 associated withh Escherichia coli strains from young dogs with companion animals, Vet. Rec. 138 (1996) 400. enteritis), Zentralbl. Vcterinanned. Reihe B 32 J., Miller Brown Fales Fischer (1985)446-453. ! 77 Turk M., T., W., J.,., Gosser H., Nelson S., Shaw D., Solorzano R., Richter Grund Hellmann Zum [64! T., S., E., Vorkom- Coliform septicemia and pulmonary disease asso- men von enterotoxischen E. coli beim Junghund. ciatcd with canine parvoviral enteritis: 88 cases Beschreibung mutmasslicher Pathogenitaetsfak- ( 1987-1988), J. Am. Vet. Med. Assoc. 196 (1990) toren (Occurrence of enterotoxic E. coli in the 771-773. of young dog. Description probable pathogenic- [78 Wada Y., Kondo H., Nakaoka Y., Kubo M., Gas- Bcrl. Muench. Tierarztl. Wochen- ity factors), tric and Escherichia coli lesions schr. 97 (1984)37-43. attaching effacing in a puppy with naturally occurring enteric col- !65 ] Riley L.K., Caffrey C.J., Identification of entero- ibacillosis and concument canine distemper virus toxigcnic Escherichia coLi by colony hybridization infection.Vet. Pathol. 33 (1996) 717-720. [791 Wadas B., Kuehn I., Lagerstedt A.S., Jonsson P., with canine urinary tract infections, Res. Vet. Sci. Biochemical phenotypes of Escherichia coli in 42(1987)404-406. dogs: comparison of isolates isolated from bitches ! 87] Whittam T.S., Wolfe M.L., Wilson R.A., Genetic from and tract infec- suffering pyometra urinary relationships among Escherichia coli isolates tion with isolates from faeces of healthy dogs, causing urinary tract infections in humans and Vet. Microbiol. 52 ( 1996) 293-300. animals, Epidemiol. Infect. 102 (1989) 37-46. Wasteson Olsvik Skancke [80] Y., 0., E., Bopp C.A., [881 Wilk S., G., Meier C., Serotypisierung Fossum K., Amtsberg Heat-stable-enterotoxin-pi-oducing und von Evcheri(!hici-(!oli- E.rcherichin coli strains isolated from Rcsistenzpruefung dogs, Staemmen aus und enteritiskranken J. Clin. Microbiol. 26 2564-2566. gesunden (1988) Hunden (Serotyping and drug resistance of [81] WastlhuberU.H., BaljerG., Daimon H., Huebert E.scherichia coli strains in healthy dogs and dogs P.H., Mayr A., Vergleichende Untersuchungen with enteritis), Berl. Muench. Tierarztl. Wochen- ueher die Plasmidverteilung bei E.scherichia coli schr. 95 (1982) 271-275. (E. coli)-Staemmen von und durchfal- gesunden Wilkinson G.T., of E. coli in the lkranken Hunden sowie von Hundehesitzern [89J 0-groups vagina and tract of the Vet. Rec. 94 studies of distribution in alimentary dog, (Comparative plasmid ( I 974) I O5. Escherichin cnli (E. coli) strains from healthy and diarrheic dogs and their owners), Zentralbl. [90] Wilson R.A., Keefe T.J., Davis M.A., Browning Veterinarmed. Reihe B 35 ( 1988) 218-229. M.T., Ondrusek K., Strains of Escherichia coli [82] Watson A.D., Culvenor J.A., Middleton D.J., associated with urogenital disease in dogs and cats, Am. J.Vet. Rcs. 49 Rothwell T.L., Distal renal tubular acidosis in a (1988) 743-746. cat with pyelonephritis, Vet. Rec. 119 ( 1986) [9)] ] Wolf K.W., Occurrence, distribution and associ- 65-68. ations of O and H- serogroups, colonization fac- !83J Weaver A.D.. Pillinger R., Relationship of bac- tor antigens, and toxins of enterotoxigenic terial infection in urine and calculi to canine Eschcrichia coli. Clin. Microbiol. Rev. 10 ( 1997) urolithiasis, Vet. Rec. 97 ( 1975) 48-50. 569-584. [84] Weaver A.D., Pillinger R., Lower urinary tract 1921 Wooley R.E., Blue J.L., Bacterial isolations from pathogens in the dog and their sensitivity to canine and feline urine, Mod. Vet. Pract. 57 chemotherapeutic agents, Vet. Rec. 101 ( 1977) ( 1976) 535-538. 77-79. !93! World Health Organization, Prevention and [851 Weber A., Wachowitz R., Roth M., Serotyp- control of enterohaemorrhagic Escherichia cnli isierung und Antibiotikacmpfindlichkcit von E. infections, Report of a WHO Consultation, co/i-Stammen, isoliert von enteritiskranken WHO/FSF/FOS/97.6 Geneva, Switzerland, 28 Katzen, VET 4 ( I 990) 17-19. April-I May. 1997. [861 Wcsterlund B., Pere A., Korhonen T.K., Jarvi- 194J Young C., Preweaning mortality in specific nen A.K., Siitonen A., Williams P.H., Charac- pathogen free kittens, J. Small Anim. Pract. 14 terisation of Escherichio cmli strains associated (1973)391-397.