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Rev. Elev. Méd. vét. Pays trop., 1985, 38 (4) : 416-422.

Colonial, biochemical and serological characteristics of species isolated from animals in Nigeria

by D. E. AGBONLAHOR (l>, A. A. ADESIYUN (2), J. K. PS. KWAGA and L. H. LOMBIN

(1) Bendel State University, Department of Biological Sciences, PmB 14, Ekpoma, Nigeria. (2) Faculty of Veterinary Medicine, Ahmadu Bello University, Zaria, Nigeria.

RÉSUMÉ SUMMARY

AGBONLAHOR (D. E.), ADESIYUN (A. A.), KWAGA AGBONLAHOR (D. E.), ADESIYUN (A. A.), KWAGA (J. K. P.), LOMBIN (L. H.). - Caractéristiques sérologi- (J. K. P.), LOMBIN (L. H.). - Colonial, biochemical ques, biochimiques et culturales de certaines espèces de and serological characteristics of Yersiniu species isolated Yersiniu isolées sur des animaux au Nigeria. Rev. Elev. from animals in Nigeria. Rev. Elev. Méd. vét. Pays trop., Méd. vét.,Puys trop., 1985, 38 (4) : 416-422. 1985, 38 (4) : 416-422. Les auteurs ont étudié les caractéristiques culturales, The colonial, biochemical and serological characteristics biochimiques et sérologiques de 14 souches de Yersinia, of 14 strains of Yersinia isolated from 2,029 samples isolées à partir de 2 029 prélèvements obtenus sur des obtained from apparently healthy cattle, pigs, goats, and bovins, des porcs, des moutons et des chèvres apparem- sheep in Nigeria were studied. ment sains, au Nigeria. Nine strains of Yersinia enterotocolitica, 4 of Yersinia Neuf souches de Y. enterocoliticu, 4 de Y. intermedia et intermedia, and 1 of Yersimiu frederiksenii were isolated 1 de Y. frederiksenii ont été isolées de bovins et de porcs. from cattle and pigs. No isolations were made from sheep Il n’y a eu aucun isolement sur moutons et sur chèvres. and goasts. Les 3 espèces de Yersinia rencontrées ont toutes révélé Al1 3 species of Yersinia encountered ‘exhibited’ iden- les mêmes caractéristiques de culture sur milieux au citrate tical colonial characteristics on desoxycholate citrate, désoxycholate, de MacConkey et S.S. Le sérotype prédomi- MacConkey and Salmonella-Shigella media. nant isolé était le 0 : 12, 26, trouvé dans 5 (38 p. 100) des The predominant serotype isolated was 0:121 26 found in 13 souches typables de Yersinia. 5 (38.5 p. 100) of 13 typable strains of Yersinia. Al1 5 strains Les 5 souches (0 : 12, 26) ont toutes été isolées sur (0:12, 26) were isolated from cattle and were confirmed bovins, et leur identification a été confirmée par la biochi- biochemically to be Yersiniu enterocoliticu. mie comme étant Y. enterocolitica. Three strains of Y. enterocolitica were serotype O:s, 2 Trois souches de Y. enterocolitica répondaient au isolated from cattle and 1 from a pig. sérotype. 0 :8 ; 2 ont été isolées de bovins, 1 de porc. Deux Two strains of Y. intermediu were serotype 0:52, 53 souches de Y. intermedia répondaient au sérotype 0 ~52, while 1 strain each was of serotype 0:36, 0:16 and 0:3. 53, tandis que les 3 dernières répondaient respectivement The only Y. enterocolitica, serotype 0:3 isolated was aux sérotypes 0:36, 0:16 et 0:3. classified as biotype 4 while the other 8 strains of Le seul sérotypc 0:3 isolé (Y. enterocoliticu) a été classé Y. enterotocolitica were biotype 1. comme biotype 4, tandis que les 8 autres appartenaient au The isolation of Y. enterocolitica serotype 0:8 from pigs biotype 1. and cattle in Nigeria is of significance because this L’isolement du sérotype 0:8 de Y. enterocoliticu, à partir serotype has not been reported in animals outside the de porcs et de bovins au Nigeria, revêt une importance United States of America. Furthermore, the isolation of significative, parce que ce sérotype n’avait encore jamais serotypes 0:3 and 0:8, known as human pathogens, from été signalé sur des animaux en dehors des Etats-Unis. food animals in Nigeria suggests that cattle and pigs may De plus, l’isolement des sérotypes 0:3 et 0:8 (dont le play some role in Y. enterocolitica in human pouvoir pathogène est connu pour l’homme), à partir beings in this environment. d’animaux destinés à la consommation humaine au Nige- ria, semble indiquer que les bovins et les porcs pourraient jouer un certain rôle dans les infections à Y. enterocoliticu chez l’homme, dans cet environnement. Mots clés : Bovin Porc - - Key words : Cattle - Pig Yersiniu interocolitica - Yersinia intermedia - Yersinia frederiksenii - Nigeria. Yersinia intermedia - Yersinia frederiksenii - Nigeria.

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INTRODUCTION Live pigs : rectal and tongue swabs of each of 309 apparently healthy pigs kept at institu- Isolations of Yersinia enterocolitica have tional and private (backyard) farms were been reported from farm animals like pigs (28), studied. A total of 618 samples from pigs were cattle (14, 23), chickens (4), goats (20), sheep tested. (21), and horses (23) in several countries, par- Overall, 2,029 samples were processed for ticularly in Europe and North America. 1s is Yersinia isolation. also believed that these animals may serve as reservoir of human infections by Y. entero- Sample collection cofitica (13, 15, 16). This is because the serotypes associated with human diseases have Rectal swabs were obtained from dairy cows been isolated from animals in the same and pigs by the use of sterile swabs inserted environment (12, 24). into the rectum of each animal beyond the anal For sometime, it was believed that Y. entero- sphincter and gently rotated several times to colitica infections in humans and animals were obtain adequate faeces. restricted to temperate countries since the TO obtain tongue swabs, the ,dorsum and micro-organism has an affinity for low tem- ventrum of the tongue of each pig was peratures (25). Furthermore, most reports of sampled with a sterile swab. isolations of any of the 4 recognised species of Caecal contents of slaughtered cattle, sheep Yersinia, namely, Y. enterocolitica sensu and goats were sampled using sterile swabs, stricto, Y, inter-media, Y. fredericksenii, and Y. after an incision was made into each caecum. kristensenii (6, 7, 9, 30) have corne from tem- Each swab taken from the animals was perate countries. immediately returned into 5 ml of,sterile M/l5 However, of recent, human infections by phosphate buffered saline (PBS), pH 7.6 and species of Yersinia have been reported in refrigerated in the laboratory. tropical and subtropical countries specifically, Nigeria and Bangladesh (2, 10). TO date, infor- Enrichment of swab samples mation is not available on the prevalence and Al1 samples in PBS were cold-enriched at characteristics of Yersinia spp. infections in 4 “C for 3 weeks. Subcultures were made onto livestock in Nigeria. desoxycholate citrate agar (DCA) and Mac- This paper reports the colonial, biochemical Conkey agar (Mac) after 1 week and 3 weeks, and serological characteristics of strains of respectively. Yersinia spp. isolated from livestock in Nigeria. Isolation and identification of Yersinia MATERIALS AND METHOD Tiny to medium lactose non-fermenting colonies growing after 48 h at 25 “C on DCA Source of animais and Mac plates were inoculated into triple sugar iron (TSI) agar slants. Cultures that Dairy cows : a total of 46 dairy cows at produced acid slant over acid butt without HLS 2 institutional and governmental farms were but with or without gas production were rectally swabbed fortnightly for a period of inoculated into urea agar slants. Al1 urease- 3 months. A total of 276 samples were collected. positive suspect cultures were further Slaughter cattle : caecal samples from biochemically characterized (seetable no II) by 287 bulls slaughted at the National Animal standard methods (11, 22). Speciation of the Production Research Institute (NAPRI) abat- isolates was as earlier recommended (6, 7, 9, toir were collected. In addition, 237 and 30). 93 caecal contents of cattle from Zaria and Sabon Cari abattoirs, respectively, were taken. Determination of colonial morphology A total of 617 caecal contents from cattle were processed. Slaughter sheep and goats : caecal Cultures that were biochemically demonstra- contents of 294 sheep and 66 goats slaughtered ted to be Yersinia were streaked ‘for isolation at the Zaria abattoir, 26 sheep and 132 goats on DCA, Mac and Salmonella-Shigella (SS) slaughtered at Sabon Gari abattoir were sam- agar. Inoculated plates were incubated at both pled. Three hundred and twenty sheep caecal 25 “C and 37 “C for 24-48 h. The color and contents and 198 from goats were tested. size of each culture on these media under the

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TABLE No 1 - Colonial characteristics of Yersinio spp. from Nigerian cattle and pigs on 3 commonly used enteric media

Colonial characteristics*

Medium Colour 24 hours 48 hours

25W (mm) 37OC (mm) 25% (mm) 37OC (mm) I Salmonella- Shigella (SS) Colourless Pinpoint ‘Pinpoint 0.5-2.0 1.0-2.0 MacConkey Pale Pinpoint 1.5-2.0 1.0-1.5 2.0-2.5 Desoxycholate citrate agar Colourless Pinpoint 0.5-1.0 1.5-2.0 2’. o-2. 5 (DCA)

* 3 species of Yersinia encountered and studied i.e. Y. intermedia, Y. enterocolitica and Y. frederiksenii exhibited identical colonial characteristics.

TABLE No II - Biochemical characteristics of 14 Yersinia spp. isolated from animals in Nigeria

Number of isolates positive* C:haracteristic Y. enterocolitica Y. in termedia Y. frederiksenii (Il=91 (n=4) (n=l) Mobility at 25% 9 4 1 at 37% 0 0 ‘0 Indole 8 4 ‘1 Voges-Prouskauer at 25OC 9 4 1 at 37% 0 0 0 Urease** at 25OC 9 4 1 at 37% 9 4 1 Citrate (Simmon’s) 0 4 0 Phenylalanine deaminase 0 0 0 Hydrogen sulphide. (SIM) 0 0 0 Nitrate reduction 9 4 1 Lysine decarboxylase 0 0 0 Arglnine dihydrolase 0 P 0 Ornithine decarboxylase 9 4 1 Oxidase 0 0 0 B-Calactosidase (ONPG) 9 4 1 Acid from glucose 9 4 1 Sucrose 9 4 1 D-Cellobiose 9 4 1 L-Arabinose 9 4 1 D-Trehalose 9 4 + L-Rhamnose 0 4 1 D-Raffinose 0 4 0 D-Melibiose 0 4 0 a-methyl-D-glucoside 0 4 0 Maltose 9 4 1 Dulcitol 0 0 0

* Positive reactions were recorded generally after 48 heurs incubation at 25OC except where 37% ,is indicated. ** Urease detection was generally quicker at 37W.

- 418 - Retour au menu growth conditions mentioned earlier were The serotypes and biotypes of Yersinia determined. isolates are shown in table no III. The predominant serotype was 0:12,26 which cons- Determination of serotypes of Yersinia isolates tituted 5 (38.5 p. 100) of the 13 typable strains of Yersinia isolated. Al1 5 isolates The slide agglutination test described by (0:12,26) were Y. enterocolitica and were a11 WAUTERS (31) was employed to determine obtained from cattle. the serotypes, using 0-antisera 1 to 49 kindly Three strains of Y. enterocpfitica were provided by WAUTERS and S. WINBLAD. serotype 0:8, 2 of these isolated from cattle while 1 was from a pig. Biotype determination of isolates Only 1 strain of Y. enterocolitica isolated was serotype 0:3 (biotype 4) and it came from The Yersinia isolates were classified into a pig. Al1 other Y. enterocolitica strains were biotypes as described by WAUTERS (31). classified as biotype 1. Serotype 0:52,53 was detected in 2 of the Y. intermedia strains while the only Y. fre- RESULTS deriksenii strain was serotype 0:16. Overall, of 2,029 samples from’ 4 species of The colonial characteristics of Yersinia spp. animals tested, 14 (0.69 p. 100) Yersinia strains isolated from pigs and cattle in Nigeria species were isolated. Out of 893 and on SS, DCA and Mac are shown in table no 1. 618 samples examined for cattle and pigs The 3 species of Yersinia isolated, namely, respectively, the frequency of isolation of Yersinia enterocolitica, Yersinia inter-media species of Yersinia were 9 (1 .Ol R. 100) and 5 and Yersinia frederiksenii exhibited identical (0.81 p. 100). Yersiqia was not isolated from characteristics. sheep and goats. Table no II shows the biochemical charac- teristics of 9 strains of Y. enterocolitica, 4 of Y. intermedia and 1 of Y. frederiksenii isola- DISCUSSION ted in Nigerian livestock. Al1 9 strains of Y. enterocolifica isolated gave typical reactions This is considered the first comprehensive except a strain that was indole-negative. None study on Yersinia spp. infections in livestock of the 9 strains was rhamnose-positive. Yersi- in a tropical country. The frequency of isola- nia intermedia, and Y. frederiksenii strains tion (0.69 p. 100) appears low when compared also gave typical biochemical reactions. to studies in temperate countries (21, 23,

TABLE No III- Serotypes and biotypes of Yersinia spp. isolated from pigs and cattle in Nigeria

Strain No Source Species Serotype Biotype

YFR 175 Pi$ Y. int&media 0 : 52,53 NA YFR 168 Pi$ Y. intermedia 0 : 52,53 NA YFT 86 Pi$ Y. intermedia 0 : 36 NA YFT 12 Pigb Y. enterocolitica 0: 3 4 YFT 283 Pigb Y. enterocolitica 0:8 1 B23 Cattlec Y. intermedia NT NA B94 Cattle Y. ~nteracolitica 0 : 12,26 1 B95 Cattle Y. enterocolitica 0 : 12.26 1 B17 (1) A Cattle Y. en teracali tica 0 : 12,26 1 Bl? (1) B Cattle Y. en terocolotica 0 : 12.26 1 B282 Cattle Y. en teracoli tica 0 : 12,26 1 B262 A Cattle Y. en teracoli tica 0 : 8 1 B262 B Cattle Y. entenxolitica 0 : 8 1 BSG 31 Cattle Y. frederiksenii 0 : 16 NA

a = Pig rectum; b q Pig tongue; c = All isolations made from cattle came from caecal contents; NT = not typable with 49 antisera available; NA = not applicable.

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28). The finding in the present study is lopathy patients, over serotypes 0:3 and 0:9. however in agreement with the relatively low Pigs have been demonstrated to be reservoirs of isolation frequency for Yersinia spp. of 1.3 p. Y. enterocolitica serotype 0:3 in 100 from human ‘acute gastroenteritis cases in humans in some countries (23, 29). Deer have Southern Nigeria (2). been suspected as a reservoir of serotype 0:8 Yersinia spp. infections were not until infections in humans in the United States of recently first confirmed in Bangladesh, a America (18). Therefore’ cattle and pigs may subtropical country, despite several earlier serve as reservoirs of human infections by attempts to demonstrate the presence of the Y. enterocolitica serotypes 0:3 and 0:8. organism in that country (25). Earlier failures Of relevance to the debate on the unsolved to isolate Yersinia spp. from tropical and mystery of the geographical distribution of subtropical countries have been attributed to Yersinia spp. serotypes was the isolation of high temperatures in these areas (25). serotype 0:8 from cattle and pigs in Nigeria. Three of the 4 recognized species of The occurrence and distribution of the seroty- Yersinia, namely, Y. enterocolitica, Y. inter- pes of Yersinia have been reported to differ not media and Y. frederiksenii were isolated only between continents but also between geo- from livestock in Nigeria. These 3 species have graphically adjacent countries (8). Except for a earlier been isolated from human cases in short report (1) on our first isolate of Y. Southern Nigeria (2). Although the patho- enterocolitica, serotype 0:8 recovered from an genicity of strains of Y. enterocolitica have apparently healthy piglet, this serotype had been ascertained, it is not established yet what never been reported in animals outside the role other species of Yersinia play in infection United States of America. ‘The isolation of this despite reported isolation in diarrheal cases, serotype from cattle agrees with the report of either as only pathogen present or in asso- SHAYEGANI et af. (26) where apart from ciation with other pathogens (2, 10, 17). It is some other serotypes, 2 strains of Y. enteroco- therefore presently impossible to assess the risk litica serotype 0:8 were isolated from 352 cows to human beings, of isolation of Y. intermedia examined in the United States of America. and Y. frederiksenii from food animals in Nigeria. SHAYEGANI et a/. (27) had earlier reported The finding that 5 strains of Y. enterocoli- that occasionally, serotypes 0:8 recovered from tica isolated from cattle were serotype 0:12, animal and environmental sources, were bio- 26, representing 38.5 p. 100 of typable strains chemically atypical from human strains of the isolated is of significance. It conflicts with a serotype. Al1 our 3 isolates typed as 0:8 recent impression given by ALEKSIC and appeared to be biochemically typical for BOCKEMUHL (3) that serotype 0:12,26 exclu- Y. enterocolitica although it might be necess- sively belongs to Y. kristensenii and did ary to further characterize these isolates as to not occur in any other species. Al1 our 5 their virulence, pathogenicity and enterotoxi- strains which were serotype 0:12,26 did not genicity before making any comparison to belong to Y. kristensenii as they repeatedly isolates from humans. fermented sucrose, a feature not exhibited by In view of the fact that no specific animal Y. kristensenii (7). Contrary to their findings, reservoirs for human infections by Y. entero- all our 5 strains were Y. enterocolitica colitica have been identified, it is imperative to biotype 1 (table no II). further study the predominant serotype (0:12, Of public health significance was the 26) isolated from cattle. The risk of beefborne isolation of Y. enterocolitica serotypes 0:3 and amongst abattoir workers and 0:8, 2 known human pathogens, from appar- consumers of beef products in Northern ently healthy cattle and pigs. In an earlier study Nigeria, should they be pathogenic, cari then be in human cases in Southern Nigeria, 4 of 6 assessed. serotyped strains of Y. enterocolitica confirmed It was of interest to observe that no Yersinia to cause acute gastroenteritis were serotype spp. was isolated from a11the 320 sheep and 198 0:3’ (2). In the same environment where the goats sampled. Yersinia enterocolitica strains present study was conducted, AWUNOR- have been isolated from these animal species in RENNER and LAWANDE (5) serologically other countries (20, 21). KROGSTAD (19) in detected a predominance of Y. enterocolitica Norway also failed to isolate, Y. entebocofitica serotype 0:8 infection in chronic glumeru- from 190 goats, although 16.3 p. 100 of these

- 420 - Retour au menu animals were found to be seropositive for Y. spp. infections in livestock in Nigeria is an enterocolitica. There is a need to conduct a evidence that infection by members of this serological investigation of sheep and goats to genus occurs in livestock in the tropics. several serotypes of Yersinia in Nigeria. This However, before the health hazard to human Will reveal the infection status of these animals beings by these strains of Yersinh in livestock to the micro-organism. cari be assessed, it is imperative to determine In conclusion, the demonstration of Yersinia their virulence and pathogenicity. ~

RESUMEN

AGBONLAHOR (D. E.), ADESIYUN (A. A.), KWAGA Tres cepas de Y. enterocolitica correspondian a1 sero- (J. K. P.), LOMBIN (L. H.). - Caracteristicas serologicas, tipo 0:8 ; de las cuales 2 provenian de bovinos y l’de cer- bioquimicas y de cultiva de algunas especies de Yersiniu dos. 2 cepas de Y. intermedia correspondian a1 serotipo aisladas en animales de Nigeria. Rev. Elev. Méd. vét. Pays 0:52,53 mientras que las 3 ultimas correspondian respecti- trop., 1985, 38 (4) : 416-422. vamente a 10s serotipos 0:36, 0:16 y 0:3. El solo serotipo 0:3 aislado (Y. enterocolitica) fué clasifi- Los autores estudiaron las caracteristicas serologicas, cado como biotipo 4, mientras que 10s 8 demas pertenecian bioquiminas y de cultiva de 14 cepas de Yersinia, aisladas a a1 biotipo 1. partir de 2 029 muestras sacadas de bovinos, cerdos, carne- El aislamiento del serotipo 0:8 de Y. enterocolitica, a ros y cabras aparentemente sanos, en Nigeria. partir de cerdos y de bovinos en Nigeria, tiene una impor- Aislaron 9 cepas de Y. enterocolitica, 4 de Y. intermedia tancia significativa, porque no se habia nunca notado y 1 de Y. frederiksenii de bovinos y cerdos. dicho serotipo en animales fuera de 10s Estados-Unidos. Ademas, el aislamiento de 10s serotipos 0:3 y 0:8 (cuyo No se hiz6 ningun aislamiento en carneros y cabras. poder patogeno para el hombre es conocido a partir de ani- Las 3 especies de Yersinia observadas mostraron las mis- males para el consuma humano en Nigeria, narece indicar mas caracteristicas de cultiva sobre medios de citrato que 10s bovinos y 10s cerdos podrian desempefiar un pape1 desoxilato, de MacConkey y Salmonella-Shigella. 0: 12,26 cierto en las enfermedades con Y. enterocohtica en el hom- era el serotipo predominante encontrado en 5 (38 p. 100) de las cepas tipables de Yersinia. Todas estas fueron aisladas de bovinos, y se confirma bioquimicamente su identilïca- Palabras claves : Bovino - Cerdo - Yersinia enterocolitica - cion como Y. enterocolitica. Yersinia intermedia - Yersinia frederiksenii - Nigeria.

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