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Enterococcus Faecalis and Enterococcus Faecium Isolates from Milk,Beef, Andchicken Andtheir Antibiotic Resistance

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Enterococcus Faecalis and Enterococcus Faecium Isolates from Milk,Beef, Andchicken Andtheir Antibiotic Resistance 931 Journalof Food Protection, Vol. 66, No. 6, 2003, Pages 931– 936 Copyright q,InternationalAssociation for FoodProtection Enterococcus faecalis and Enterococcus faecium Isolates from Milk,Beef, andChicken andTheir Antibiotic Resistance W.CHINGWARU, S.F.MPUCHANE, AND B. A. GASHE* Departmentof Biological Sciences, University ofBotswana, Gaborone, Private Bag 0022, Gaborone, Botswana MS02-282:Received 28August 2002/ Accepted 2December 2002 ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/66/6/931/1674782/0362-028x-66_6_931.pdf by guest on 01 October 2021 Theoccurrence and antibiotic resistance of enterococci, especially Enterococcusfaecalis and Enterococcusfaecium, in milk,beef, and chicken in Gaborone, Botswana, were studied. Enterococci were isolated from these sources with the use of bileesculin agar and identi ed with API 20Strep kits. Antibiotic resistance was determined by the disk diffusion method. Theantibiotics tested were vancomycin, teicoplanin, ampicillin, tetracycline, and cephalothin. Among the 1,467 enterococci isolatedfrom the samples, E. faecalis (46.1%) and E. faecium (29.0%)were found to be the predominant species. Other enterococcalspecies made up 25% of the isolates. More than 96 and 97% ofthe E. faecalis and E. faecium isolates,respectively, werefound to be resistant to ampicillin. Almost 34, 27.3, and 22.4% of the E. faecalis isolatesfrom milk, beef, and chicken, respectively,were also resistant to cephalothin. The percentages of E. faecium isolatesthat were found to be resistant to cephalothinwere 32.8, 16.9, and 17.3% for milk, beef, and chicken, respectively. Resistance to vancomycin was widespread. Itwas found that 18.8, 7.8, and 13.1% of the E. faecalis isolatesfrom milk, beef, and chicken samples, respectively, were resistantto vancomycin. In contrast, 32.8, 24.7, and 30.7% of the E. faecium isolatesfrom milk, beef, and chicken samples, respectively,were resistant to vancomycin. Isolates that were resistant to multipledrugs were found in relativelylarge numbers. Enterococciare found in a varietyof environments. tion (3, 37). Someenterococci are resistant to commonly Theyfrequently occur in large numbers in dairy and food usedantibiotics such as ampicillin, tetracycline, and ceph- products (12, 13). Theyalso occur in humans and animals alothin.However ,suchenterococci can be signi cantly re- (16, 38). Enterococcihave been regarded as harmless com- ducedwith vancomycin and teicoplanin therapy. A problem mensalsand have been used as indicators of fecalcontam- ariseswhen these enterococci are also resistant to vanco- ination (14). Enterococcican survive for longperiods on mycinand teicoplanin. environmentalsurfaces and on the hands of health care Thereis little information available on the prevalence workers (23). Severalinvestigators have found enterococci, ofdrug-resistant enterococci in southern Africa. Asigni- particularlythose that are resistant to multiple drugs, on cantpercentage of peoplewho are immunocompromisedas variousobjects in ahospitalenvironment, including on bed aresultof acquired immunode ciency syndrome (AIDS) rails,night tables, curtains, bathroom sinks, toilet rings, andthose under intensive care in health care centers live in electronicthermometers, and other patient care equipment thisregion. In Botswana, unfortunately, no assessment of (24,25, 29). Enterococcihave recently been identi ed as theprevalence of antibiotic-resistant enterococci among hu- secondaryinvaders in hospital-acquired infections (27). manimmunode ciency virus– AIDS patientshas been car- Sincethe 1980s, numbers of infections in hospitalized pa- riedout, but there is a generallyhigh level of antibiotic- tientsdue to enterococcihave increased tremendously (17). resistantenterococci among hospitalized patients. When pa- Colonizationwith vancomycin-resistant enterococci tientsare infectedwith drug-resistant enterococci, there (VRE) innonhospitalized patients has been on the increase maybe a problemwith the availability of or the selection inthe United States and Europe (3). Inthe United King- ofan appropriate drug for treatment.The appearance and dom,VRE were isolatedfrom raw sewageand from farm increasein the incidence of vancomycin elsewhere has be- animals,including pigs, chickens, ducks, and turkeys, but comea causefor greatconcern. VRE couldbe comingpart- noVRE were recoveredfrom cattleand sheep (3). Some lyfrom foodanimals, and this possibility has prompted fermentedtraditional foods in Africa alsoharbor entero- muchresearch on microbial isolates, mainly in the devel- cocci,although their resistance patterns are not known (12). oped world. Thedevelopment of the resistance of enterococci to van- Reservoirsfor antibiotic-resistantenterococci have not comycinin animals is mainly attributed to the use of anti- beencompletely determined. Animals, human food, and the biotics,especially avoparcin (a glycopeptideantibiotic), in inanimateenvironmental components have been suspected animalfeeds as a growthpromoter (9). InEurope, evidence sourcesof some of the resistant clinical isolates (2, 4, 15, suggeststhat foodborne VRE maycause human coloniza- 18, 19). Muchinformation on the antibiotic resistance of enterococciisolated from clinicalsources has accumulated *Authorfor correspondence. Tel: 267-355-2599; Fax: 267-585097; (1), butthe levels of antibiotic resistance of enterococci E-mail: [email protected]. isolatedfrom foodshave not yet been thoroughly docu- 932 CHINGWARU ETAL. J.FoodProt., Vol. 66, No. 6 TABLE 1. Enterococcalspecies from different sources %ofpositivesamples (no.positive/ no.tested) Enterococcus species Milk Beef Chicken E. faecalis 42.8(411/ 970) 57.2(154/ 269) 46.9(107/ 228) E. faecium 28.2(278/ 970) 28.6(77/ 269) 32.9(75/ 228) E.gallinarum 7.9(77/ 970) 5.9(16/ 269) 7.0(16/ 228) E. avium 6.2(60/ 970) 3.0 (8/269) 5.3(12/ 228) E. durans 2.5(24/ 970) 2.6 (7/269) 0 (0/228) E. hirae 2.4(23/ 970) 2.6 (7/269) 0 (0/228) E.casseliavus 9.6(93/ 970) 0 (0/269) 7.9(18/ 228) E. mundtii 0.4 (4/970) 0 (0/269) 0 (0/228) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/66/6/931/1674782/0362-028x-66_6_931.pdf by guest on 01 October 2021 mented (13). Ithas been realized that there is a needto Chemicalsand media. Allof themedia and antibiotic disks assessthe occurrence of drugresistance in animal products usedin the study were obtained from Oxoid. widelyused for foodin Botswana. This paper reports on Antibioticsusceptibility testing. Eachof the characterized enterococci,especially Enterococcusfaecalis and Entero- Enterococcus specieswas inoculated in Mueller-Hinton broth coccusfaecium, isolatedfrom milk,beef, and chicken and (Oxoid).The askswere incubated at 25 8Cona Gallenkamp theirpatterns of susceptibilityto veof theantibiotics that shaker(200 rpm) for 24 h orslightly longer depending on the arecommonly directed against them. growthpattern for the Enterococcus speciesinvolved. Amodied version of the method of Steinberg and Lehrer MATERIALS AND METHODS (34) wasused to obtain an absorbance of 0.6 at 600 nm. One Samplingperiod. Thisstudy was conducted between May milliliterof the cell suspension was transferred into 15 to 20 ml ofmoltenMueller-Hinton agar ,mixedthoroughly, and poured into 1999and July 2000. plates.The mixture was then allowed to solidify in the plates. Milk. Milkwas either purchased from supermarkets or ob- Antibioticdisks (ampicillin [10 mg],vancomycin [30 mg], tainedfrom dair yfarmslocated around Gaborone. A totalof 227 teicoplanin[30 mg],tetracycline [10 mg],and cephalothin [30 milksamples (142 raw-milk samples and 84 pasteurized-milk mg])were then placed onto the medium with sterile forceps. Care samples)were obtained. Samples were transported to the labora- wastaken to ensurethat the disks were completely in contactwith toryin acoolbox in 20 to30min. From each milk sample, 1 ml theagar .Theplates were incubated at 37 8Cfor24 h. The diam- wasaseptically transferred into test tubes containing 9 mlof 0.1% etersof the zones of inhibition were measured with a ruleras sterilepeptone water (Mast Diagnostics, Merseyside, UK). Further recommendedby the NCCLS (28) andWilley et al. (40).Staph- dilutionwas carried out as deemed necessary. From the diluted ylococcusaureus ATCC 29213was used as a controlstrain for samples,0.1 ml was spread plated onto bile esculin agar (BEA; the test. CM888).Plates were incubated at 45 8C for 24 h (26). RESULTS AND DISCUSSION Beefand chicken. Fifty-sevenbeef samples and 58 chicken Enterococcaldiversity in the samples. A total of sampleswere purchased from supermarkets around Gaborone. 1,467enterococcal isolates were pickedfrom the342 sam- Portions(25 g each)of minced and unprocessed beef or chicken sampleswere transferred into stomacher bags containing 225 ml ples(227 milk, 57 beef, and 58 chicken samples). These ofsterile peptone water .Thesamples were homogenized with a isolatescomprised 970 isolates from milk,269 from beef, stomacher(Seaward Stomacher 400, T ekmar,Cincinnati,Ohio) for and228 from chicken. E. faecalis (46.1%) and E. faecium 1min.A 0.1-mlportion of the diluted sample was spread plated (29.0%)accounted for mostof theisolates from thediffer- ontoBEA andincubated at 45 8C for 24 h (20). entsamples (T able1). The remaining species identi ed were Enterococcuscasseli avus (7.6%), Enterococcusgal- Isolation. Aftermeat and milk samples had been incubated linarum (7.4%), Enterococcusavium (5.5%), Enterococcus on BEA at 458Cfor24 h, colonies showing brown halos were durans (2.1%), Enterococcushirae (2.0%), and Enterococ-
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