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Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep

Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep Ann Microbiol (2010) 60:489–494 DOI 10.1007/s13213-010-0074-8 ORIGINAL PAPERS Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep Muammer Goncuoglu & Fatma Seda Bilir Ormanci & Naim Deniz Ayaz & Irfan Erol Received: 29 March 2010 /Accepted: 13 May 2010 /Published online: 24 June 2010 Springer-Verlag and the University of Milan 2010 Abstract A total of 102 Escherichia coli O157:H7 Introduction colonies recovered from 11 cattle and 14 sheep were collected and tested for their antibiotic resistance profiles Escherichia coli O157:H7 is considered one of the most using a disc diffusion method, according to the Clinical and important food-borne pathogens among shiga toxin- Laboratory Standards Institute. Four (36.36 %) of the 11 producing E. coli (STEC) strains. It causes diarrhea that cattle E. coli O157:H7 isolates were resistant to cephalo- may result in life-threatening conditions ranging from thin, one (9.09 %) isolate was resistant to streptomycin, and hemorrhagic colitis (HC) to hemolytic-uremic syndrome one (9.09 %) to nalidixic acid. Two (14.28 %) of the 14 (HUS) (Mead et al. 1999; Meng et al. 2001). Gastrointes- sheep E. coli O157:H7 isolates were resistant to sulphame- tinal tracts of ruminants especially cattle and sheep have thoxazole, one (7.14 %) isolate was resistant to sulphona- been shown to act as a reservoir of E. coli O157:H7 (Kudva mide compounds, and one (7.14 %) to streptomycin. All et al. 1996, 1997; Shere et al. 1998). Epidemiological cattle and sheep isolates were found to be susceptible to investigations have clearly associated E. coli O157:H7 cephazolin, gentamicin, ciprofloxacin, imipenem, trimetho- human infections to the consumption of contaminated raw prim/ sulphamethoxazole, chloramphenicol, trimethoprim, or undercooked ground beef and products with feces during and ceftiofur. Six cattle isolates were susceptible at a ratio slaughterhouse processing (Beutin et al. 1993; Paiba et al. of 54.54 %, and 11 (78.57 %) isolates from sheep were 2002). susceptible to all 20 antibiotics tested. As an overall result, Antimicrobial resistance of food-borne bacteria should 68 % of the E. coli O157:H7 isolates belonging to cattle not necessarily be considered distinct from that in isolates and sheep were susceptible to all antibiotics tested. On the from humans, food animals, or other niches. When food other hand, most of the E. coli O157:H7 isolates were animals, as carriers of asymptomatic E. coli O157:H7, are intermediately resistant to streptomycin, cephalothin, sul- exposed to antimicrobial agents, they may become the phamethoxazole, ampicillin, and kanamycin. reservoir of this antimicrobial-resistant bacteria. So it becomes important to determine whether the bacteria . . . Keywords E. coli O157:H7 Antibiotic resistance Cattle develop resistance to antimicrobials during food animal Sheep production. Also, recent studies have reported that there has been a rise in the antimicrobial resistance patterns of E. coli O157:H7 (Galland et al. 2001; Schroeder et al. 2002, 2004). It is controversial to use antibiotic treatment in humans to prevent HUS due to lysis of the bacteria and increased releasing of the expression of the shiga toxins in the : : : M. Goncuoglu F. S. Bilir Ormanci N. D. Ayaz I. Erol (*) intestinal tract (Takahashi et al. 1997; Wong et al. 2000). Department of Food Hygiene and Technology, Ankara University, However, it is has been reported that using some anti- School of Veterinary Medicine, microbials in the early stage of infection may be protective 06110 Diskapi, against HUS progression (Fukushima et al. 1999; Ikeda et Ankara, Turkey al. 1999). e-mail: erol@veterinary.ankara.edu.tr 490 Ann Microbiol (2010) 60:489–494 The objective of this study was to evaluate the antibiotic tested for the O157 antigen by latex agglutination (Oxoid resistance profile to 20 different antibiotics of E. coli O157: DR0620), and up to five agglutination positive colonies H7 isolates collected from cattle and sheep at slaughter for were taken and stored at −80°C (Sanyo MDF-U5186S, at least a 1-year period. As this is the first comprehensive Japan) in cryovials for PCR analysis and antibiotic study to evaluate the antibiotic resistance profile of E. coli resistance determination. O157:H7 in Turkey, it was possible to acquire epidemio- logical data for the future analysis. DNA extraction and PCR analysis for detection of fliC gene h7 Materials and methods DNA extraction was performed using Chelex-100 (Bio- Rad, Hercules, CA, USA) resin-based technique as reported Bacterial strains previously (Goncuoglu et al. 2010). The PCR was performed with FLICH7-F and FLICH7-R Escherichia coli ATCC 25922 and Staphylococcus aureus primers in a final volume of 50 µl containing 1X Reaction ATCC 25923 were used for antibiotic susceptibility testing. Buffer (Promega, Madison, WI, USA), 1.5 mM MgCl E. coli O157:H7 ATCC 43895 was used as positive controls (Promega), 400 µM each of the four deoxynucleoside for the detection of fliC gene in PCR assay. triphosphates (Promega), 2.5 U Taq DNA polymerase h7 (Promega), 0.50 µM of primers (Promega) and 10 µl DNA. Isolates Thermal cycling (Biometra Personel Cycler, Göttingen, Germany) was carried out with the initial denaturation at A total of 102 E. coli O157:H7 isolates recovered from 25 94°C for 2 min and then 35 cycles of denaturation at 94°C for animals including 11 cattle and 14 sheep were analyzed. 20 s, annealing at 54°C for 1 min, and extension at 72°C for The 41 isolates from the 11 cattle were obtained from 282 1 min, with a final extension for 10 min at 72°C (Fratamico et cattle (207 beef and 75 dairy cattle) feces and/or colon al. 2000). A 10-µl aliquot of each PCR product was subjected tissue samples between April 2002 and December 2003, to 1.5 % agarose gel (SeaKem LE Agarose, Rockland, ME, and 61 isolates from 14 sheep were obtained from 218 USA) electrophoresis containing 0.1 µg/ml ethidium bromide sheep feces and/or colon tissue samples between November for 1 h at 100 V. Amplicon visualization and documentation 2007 and November 2008 (with a total of 500 animals) was performed using gel documentation and analysis system (Table 1). (Syngene Ingenius, Cambridge, UK). IMS based cultural technique for the isolation of E. coli Antibiotic susceptibility testing O157:H7 The antibiotic susceptibility test of E. coli O157:H7 isolates Immunomagnetic separation (IMS)-based selective enrich- was performed with the disc diffusion method as recom- ment technique was used for the isolation of E. coli O157 mended by the Clinical and Laboratory Standards Institute (Byrne et al. 2003). Briefly, 10 g of feces and/or colon (CLSI) (Anon 2006) in Mueller-Hinton agar (Oxoid tissue samples of cattle and sheep were weighed in a sterile CM0337) with 20 different antibiotics and antibiotic bag and enriched with 90 ml EC broth (Oxoid CM0853, combinations at given concentrations (Oxoid) as shown in Hampshire, UK) containing novobiocin (20 µg/l; Sigma N- Table 2. 1628, St. Louis, MO, USA) and incubated at 37°C at Escherichia coli O157:H7 isolates were transferred to 100 rpm for 18 h in a shaking incubator (Bellco Shel Lab BHI broth (Oxoid CM0225) and incubated at 37°C for Shaking Incubator S16R, Oregon, USA). After the incuba- 24 h. A loopfull of growth was transferred into 5 ml tion period, IMS was performed according to the manu- containing Tryptone Soya Broth (Oxoid CM0129). The facturer’s protocol. Then, 20 µl of magnetic beads coated culture was incubated at 37°C until it achieved the with specific antibody against E. coli O157 (Dynabeads turbidity of the 0.5 McFarland standard. The correct anti E. coli O157, Prod. No. 710.04; Dynal, Oslo, Norway) density of the turbidity standard was measured by Nano- were used. Following the IMS procedure, 100 μl of PBS- Drop Spectrophotometer (NanoDrop ND-100, Delaware, Tween 20 was added to resuspend the bead and E. coli USA). The absorbance of the broth cultures at 625 nm was O157 complex. fixedto0.08–0.10. The suspension was inoculated Resuspended IMS mixture was plated on Sorbitol uniformly to Mueller Hinton agar (uniform depth of MacConkey Agar (Oxoid CM0813) plates containing 4 mm) with a sterile cotton swab. Then, antibiotic discs Cefixime-tellurite supplement (Oxoid SR0172). After over- were placed onto the plate and incubated at 37°C for 18 h. night incubation at 42°C, sorbitol negative colonies were According to the sizes of the inhibition zones, interpreta- Ann Microbiol (2010) 60:489–494 491 Table 1 Sampling design and Sampling date Source of isolates No. of isolates Code of isolates Resistance to: antibiotic resistance profiles of E. coli O157:H7 isolates from 16.05.2002 Cattle (male/enteritis) 5 1001–1005 KF cattle and sheep samples 01.10.2002 Catlle (female/healthy) 5 1005–1010 S 01.10.2002 Catlle (female/healthy) 5 1011–1015 01.10.2002 Catlle (female/healthy) 4 1016–1019 KF 01.10.2002 Catlle (female/healthy) 2 1020–1021 24.07.2003 Cattle (male/healthy) 5 1022–1026 24.07.2003 Catlle (male/healthy-colon tissue) 5 1027–1031 24.07.2003 Cattle (male/healthy) 5 1032–1036 24.07.2003 Cattle (male/healthy) 1 1037 a a 24.07.2003 Cattle (male/healthy) 1 1038 KF ,NA 24.07.2003 Cattle (male/healthy) 3 1039–1041 KF 10.12.2007 Sheep (healthy) 5 1042–1046 18.04.2008 Sheep (healthy) 5 1047–1051 18.04.2008 Sheep (healthy) 5 1052–1056 16.05.2008 Sheep (healthy) 5 1057–1061 17.07.2008 Sheep (healthy) 2 1062–1063 17.07.2008 Sheep (healthy) 4 1064–1067 RL 23.07.2008 Sheep (healthy) 5 1068–1072 29.08.2008 Sheep (healthy) 5 1073–1077 29.08.2008 Sheep (healthy) 4 1078–1081 29.08.2008 Sheep (healthy) 4 1082–1085 S3 29.08.2008 Sheep (healthy) 4 1086–1089 a 29.08.2008 Sheep (healthy) 5 1090–1094 KF Cephalothin, S3 Sulphona- a a mide compounds, S Streptomycin, 29.08.2008 Sheep (healthy) 5 1095–1099 S ,RL NA Nalidixic acid, RL 29.08.2008 Sheep (healthy) 3 1100–1102 Sulphamethoxazole tion of the strains as susceptible, intermediate, or resistant streptomycin, eight (72.72 %) were intermediately resistant was made according to the CLSI (Anon 2006). to kanamycin, seven (63.63 %) were intermediately resistant to sulphamethoxazole, cephalothin, and ampicillin. In addi- tion, five (45.45 %) isolates were intermediately resistant to Results and discussion amikacin, three (27.27 %) were intermediately resistant to sulphonamide compounds, and two different isolates (9.09 %) All the E. coli O157:H7 colonies (up to five colonies were intermediately resistant to amoxicillin/clavulanic acid belonging to a positive sample) isolated from the same and cefoxitin, respectively. positive animals showed the same antibiotic resistance/ Among those isolates recovered from sheep, two (14.28 %) susceptible profiles (Tables 1 and 2). Therefore, the results were resistant to sulphamethoxazole, one (7.14 %) to are given according to the number of the positive animals, streptomycin, and one (7.14 %) to sulphonomide compounds. e.g., 11 cattle and 14 sheep, instead of the total number In one (7.14 %) E. coli O157:H7 sheep isolate, multiple drug (102) of the isolates tested in this study (Table 2). All resistance was shown to streptomycin and sulphonomide compounds. From total sheep isolates, eleven (78.57 %) of isolates except one were recovered from healthy animals. Four of the 11 cattle isolates were recovered from cows. them were intermediately resistant to streptomycin, ten Nevertheless, no antibiotic resistance profile differences (71.42 %) were intermediately resistant to cephalothin, seven were seen between male and female host samples, one of (50.00 %) were intermediately resistant to sulphamethox- the animals even showed enteritis. azole, and five (35.71 %) were intermediately resistant to Overall, among the cattle isolates, 36.36 % (4/11) of them ampicillin. For all that, three (21.42 %) isolates were were resistant to cephalothin, 9.09 % (1/11) were resistant to intermediately resistant to tetracycline and nalidixic acid, streptomycin and 9.09 % (1/11) were resistant to nalidixic acid. respectively. In addition, two (14.28 %) isolates were In one (9.09 %) E. coli O157:H7 cattle isolate, multiple drug intermediately resistant to amikacin and kanamycin, respec- resistance was shown to cephalothin and nalidixic acid. Also, tively, and one (7.14 %) was intermediately resistant to ten isolates (90.90 %) were intermediately resistant to ceftriaxone. 492 Ann Microbiol (2010) 60:489–494 Table 2 Antibiotic resistance profiles of E. coli O157:H7 isolates from cattle and sheep feces and/or colon tissue samples Number of E. coli O157:H7 isolates (%) Cattle (n = 11) Sheep (n = 14) −1 a a a a a a Antibiotic (μg disc)R I S R I S Ampicillin (AMP-10) 7 (63.63) 4 (36.36) 5 (35.71) 9 (64.28) Cephazolin (KZ-30) 11 (100) 14 (100) Cephalothin (KF-30) 4 (36.36) 7 (63.63) 10 (71.42) 4 (28.57) Gentamicin (CN-120) 11(100) 14 (100) Amikacin (AK-30) 5 (45.45) 6 (54.54) 2 (14.28) 12 (85.71) Amoxicillin/clavulanic acid (AMC-30) 1 (9.09) 10 (90.90) 14 (100) Cefoxitin (FOX-30) 1 (9.09) 10 (90.90) 14 (100) Ceftriaxone (CRO-30) 11 (100) 1 (7.14) 13 (92.85) Ciprofloxacin (CIP-5) 11 (100) 14 (100) Imipenem (IPM-10) 11 (100) 14 (100) Trimethoprim/sulphamethoxazole (SXT-25) 11 (100) 14 (100) Chloramphenicol (C-30) 11 (100) 14 (100) Kanamycin (K-30) 8 (72.72) 3 (27.27) 2 (14.28) 12 (85.71) Tetracycline (TE-30) 11 (100) 3 (21.42) 11 (78.57) Trimethoprim (W-5) 11 (100) 14 (100) Sulphonamide compounds (S3-300) 3 (27.27) 8 (72.72) 1 (7.14) 13 (92.85) Ceftiofur (EFT-30) 11 (100) 14 (100) Streptomycin (S-10) 1 (9.09) 10 (90.90) 1 (7.14) 11 (78.57) 2 (14.28) Nalidixic acid (NA-30) 1 (9.09) 10 (90.90) 3 (21.42) 11 (78.57) Sulphamethoxazole (RL-25) 7 (63.63) 4 (36.36) 2 (14.28) 7 (50.00) 5 (35.71) R Resistant, I Intermediately resistant, S Susceptible All isolates from cattle and sheep were susceptible to commonly on cattle and sheep feedlots as well as to cephazolin, gentamicin, ciprofloxacin, imipenem, trimeth- chloramphenicol. Scott et al. (2006) showed that E. coli oprim/sulphamethoxazole, chloramphenicol, trimetho- O157:H7 strains isolated from cattle feedlots were suscep- prim, and ceftiofur. Among those isolates recovered tible to 13 tested antibiotics. In particular, different studies from cattle, six (54.54 %) were susceptible to all 20 (Kim et al. 1994; Galland et al. 2001; Schroeder et al. 2002; antibiotics tested. On the other hand, these susceptible Wilkerson et al. 2004) have evidenced that only from 6.63 isolates were all intermediately resistant to cephalothin to 38.46% of E. coli O157:H7 isolates from bovines were and streptomycin. Regarding sheep isolates, eleven resistant to tetracycline. Various countries including Turkey (78.57 %) isolates were susceptible to all tested antibiotics. have banned the usage of chloramphenicol for food- Similar to the cattle isolates, most of the susceptible sheep producing animals, so this result is good data for chloram- isolates (ten, 71.42 %) were intermediately resistant to phenicol resistance. Sheep isolates were more susceptible to streptomycin. antibiotics than cattle isolates. This difference may be Similar to the previous studies, in this study, suscepti- explained by the slaughtering age of the animals that reach bility was amore common character instead of showing up to 1 year old for sheep and more than 1 year old for cattle. resistance to tested antibiotics (Meng et al. 1998; Zhao et Moreover, since intensive sheep breeding does not occur al. 2001; Schroeder et al. 2002; Walsh et al. 2006). In fact, generally in Turkey, the antibiotics are not widely used on no multiresistant character was observed in all the isolates farms for animal prophylaxis, particularly for sheep. tested but, in agreement with Vali et al. (2004), a low Although ciprofloxacin, aminoglycosides and trimetho- prevalence of resistance to cephalothin, sulphamethoxazole, prim/sulphamethoxazole are used as therapeutics in human streptomycin, sulphonamide compounds, and nalidixic medicine, our isolates showed high susceptibility rates, acid, was detected. Also, cephalothin and nalidixic acid except streptomycin and kanamycin with high intermediate resistance ratios were similar to Khan et al.'s (2002) resistant patterns. This variation in results may be due to findings. All isolates were susceptible to tetracycline used attaining resistance from other organisms by genetic Ann Microbiol (2010) 60:489–494 493 ByrneC,Erol I, CallJ,Buege D, Kaspar CW,HiemkeC,Fedorka-CrayP, linkage of genetic factors, or by being from different origin, Hermosillo J, Ball T, Wallace M, Handy M, Luchansky JB (2003) or these resistance patterns are the natural characteristic of Characterization of Escherichia coli O157:H7 from downer and the bacteria. healthy dairy cattle in the upper Midwest region of the United States. Although some of the isolates were recovered on the Appl Environ Microbiol 69:4683–4688 Fratamico PM, Bagi LK, Pepe T (2000) A multiplex polymerase chain same slaughter day, the antibiotic resistance patterns of the reaction assay for rapid detection and identification of Escher- isolates from different animals were quite distinct (Table 1). ichia coli O157:H7 in foods and bovine feces. J Food Prot The antibiotic resistance profiles of four cattle isolates, 63:1032–1037 which were coded as 1005 to 1021, were all different from Fukushima H, Hashizume T, Morita Y, Tanaka J, Azuma K, Mizumoto Y, Kaneno M, Matsuura M, Konma K, Kitani T each other. One of the isolates was resistant to streptomycin (1999) Clinical experiences in Sakai City Hospital during the and another to cephalothin. On the other hand, two isolates massive outbreak of enterohemorrhagic Escherichia coli O157 showed no resistance to any antibiotic tested; also, all the infections in Sakai City. Pediatr Int 41:213–217 four isolates were intermediately resistant to different Galland JC, Hyatt DR, Crupper SS, Acheson DW (2001) Prevalence, antibiotic susceptibility and diversity of Escherichia coli O157: antibiotics. Similarly, among the sheep isolates coded as H7 isolates from a longitudinal study of beef cattle feedlots. Appl 1073–1102, the antibiotic resistance profiles did not have Environ Microbiol 67:1619–1627 the same pattern. Also, the intermediate resistance profiles Goncuoglu M, Erol I, Ayaz ND, Bilir Ormanci FS, Kaspar CW (2010) of the isolates were all different from each other; in isolates Isolation and genomic characterization of Escherichia coli O157: H7 in bile of cattle. Ann Microbiol 60:293–297 1078–1081, the only intermediate resistance was to strep- Ikeda K, Ida O, Kimoto K, Takatorige T, Nakanishi N, Tatara K tomycin, but isolates 1100 to 1102 were intermediately (1999) Effect of early fosfomycin treatment on prevention of resistant to nine different antibiotics. hemolytic uremic syndrome accompanying Escherichia coli According to the previous studies conducted worldwide O157:H7 infection. Clin Nephrol 52:357–362 Khan A, Das SC, Ramamurthy T, Sikdar A, Khanam J, Yamasaki S, on this subject, most isolates that are resistant to antibiotics Takeda Y, Nair GB (2002) Antibiotic resistance, virulence gene, are widely used on farms in food animals, more commonly and molecular profiles of shiga toxin-producing Escherichia coli used as prophylactics and therapeutics, but our results were isolates from diverse sources in Calcutta. India J Clin Microbiol unforeseeable. In the present study, most of the isolates 40:2009–2015 Kim H, Samadpour M, Grimm L, Clausen C, Besser T, Baylor M, showed an intermediate resistant profile which is a clue for Kobayashi J, Neill ML, Schoenknecht F, Tarr P (1994) potential resistance risk that may occur in the future. Characteristics of antibiotic-resistance Escherichia coli O157: Therefore, attention has to be paid to high intermediate H7 in Washington State, 1984–1991. J Infect Dis 170:1606– resistant profiles of these antibiotics. 1609 Kudva IT, Hatfield PG, Hovde CJ (1996) Escherichia coli O157:H7 in This is the first report of antibiotic resistance patterns of microbial flora of sheep. J Clin Microbiol 34:431–433 E. coli O157:H7 strains isolated from cattle and sheep in Kudva IT, Hatfield PG, Hovde CJ (1997) Characterization of Turkey. It is concluded that the overall prevalence of Escherichia coli O157:H7 and other shiga-toxin producing E. antibiotic resistance of E. coli O157:H7 isolates recovered coli serotypes isolated from sheep. J Clin Microbiol 35:892–899 Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, from cattle and sheep tested in this study is very low. Griffin PM, Tauxe RV (1999) Food-related illness and death in However, longitudinal studies should be performed to the United States. 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Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep

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Copyright © 2010 by Springer-Verlag and the University of Milan
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Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
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Ann Microbiol (2010) 60:489–494 DOI 10.1007/s13213-010-0074-8 ORIGINAL PAPERS Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep Muammer Goncuoglu & Fatma Seda Bilir Ormanci & Naim Deniz Ayaz & Irfan Erol Received: 29 March 2010 /Accepted: 13 May 2010 /Published online: 24 June 2010 Springer-Verlag and the University of Milan 2010 Abstract A total of 102 Escherichia coli O157:H7 Introduction colonies recovered from 11 cattle and 14 sheep were collected and tested for their antibiotic resistance profiles Escherichia coli O157:H7 is considered one of the most using a disc diffusion method, according to the Clinical and important food-borne pathogens among shiga toxin- Laboratory Standards Institute. Four (36.36 %) of the 11 producing E. coli (STEC) strains. It causes diarrhea that cattle E. coli O157:H7 isolates were resistant to cephalo- may result in life-threatening conditions ranging from thin, one (9.09 %) isolate was resistant to streptomycin, and hemorrhagic colitis (HC) to hemolytic-uremic syndrome one (9.09 %) to nalidixic acid. Two (14.28 %) of the 14 (HUS) (Mead et al. 1999; Meng et al. 2001). Gastrointes- sheep E. coli O157:H7 isolates were resistant to sulphame- tinal tracts of ruminants especially cattle and sheep have thoxazole, one (7.14 %) isolate was resistant to sulphona- been shown to act as a reservoir of E. coli O157:H7 (Kudva mide compounds, and one (7.14 %) to streptomycin. All et al. 1996, 1997; Shere et al. 1998). Epidemiological cattle and sheep isolates were found to be susceptible to investigations have clearly associated E. coli O157:H7 cephazolin, gentamicin, ciprofloxacin, imipenem, trimetho- human infections to the consumption of contaminated raw prim/ sulphamethoxazole, chloramphenicol, trimethoprim, or undercooked ground beef and products with feces during and ceftiofur. Six cattle isolates were susceptible at a ratio slaughterhouse processing (Beutin et al. 1993; Paiba et al. of 54.54 %, and 11 (78.57 %) isolates from sheep were 2002). susceptible to all 20 antibiotics tested. As an overall result, Antimicrobial resistance of food-borne bacteria should 68 % of the E. coli O157:H7 isolates belonging to cattle not necessarily be considered distinct from that in isolates and sheep were susceptible to all antibiotics tested. On the from humans, food animals, or other niches. When food other hand, most of the E. coli O157:H7 isolates were animals, as carriers of asymptomatic E. coli O157:H7, are intermediately resistant to streptomycin, cephalothin, sul- exposed to antimicrobial agents, they may become the phamethoxazole, ampicillin, and kanamycin. reservoir of this antimicrobial-resistant bacteria. So it becomes important to determine whether the bacteria . . . Keywords E. coli O157:H7 Antibiotic resistance Cattle develop resistance to antimicrobials during food animal Sheep production. Also, recent studies have reported that there has been a rise in the antimicrobial resistance patterns of E. coli O157:H7 (Galland et al. 2001; Schroeder et al. 2002, 2004). It is controversial to use antibiotic treatment in humans to prevent HUS due to lysis of the bacteria and increased releasing of the expression of the shiga toxins in the : : : M. Goncuoglu F. S. Bilir Ormanci N. D. Ayaz I. Erol (*) intestinal tract (Takahashi et al. 1997; Wong et al. 2000). Department of Food Hygiene and Technology, Ankara University, However, it is has been reported that using some anti- School of Veterinary Medicine, microbials in the early stage of infection may be protective 06110 Diskapi, against HUS progression (Fukushima et al. 1999; Ikeda et Ankara, Turkey al. 1999). e-mail: erol@veterinary.ankara.edu.tr 490 Ann Microbiol (2010) 60:489–494 The objective of this study was to evaluate the antibiotic tested for the O157 antigen by latex agglutination (Oxoid resistance profile to 20 different antibiotics of E. coli O157: DR0620), and up to five agglutination positive colonies H7 isolates collected from cattle and sheep at slaughter for were taken and stored at −80°C (Sanyo MDF-U5186S, at least a 1-year period. As this is the first comprehensive Japan) in cryovials for PCR analysis and antibiotic study to evaluate the antibiotic resistance profile of E. coli resistance determination. O157:H7 in Turkey, it was possible to acquire epidemio- logical data for the future analysis. DNA extraction and PCR analysis for detection of fliC gene h7 Materials and methods DNA extraction was performed using Chelex-100 (Bio- Rad, Hercules, CA, USA) resin-based technique as reported Bacterial strains previously (Goncuoglu et al. 2010). The PCR was performed with FLICH7-F and FLICH7-R Escherichia coli ATCC 25922 and Staphylococcus aureus primers in a final volume of 50 µl containing 1X Reaction ATCC 25923 were used for antibiotic susceptibility testing. Buffer (Promega, Madison, WI, USA), 1.5 mM MgCl E. coli O157:H7 ATCC 43895 was used as positive controls (Promega), 400 µM each of the four deoxynucleoside for the detection of fliC gene in PCR assay. triphosphates (Promega), 2.5 U Taq DNA polymerase h7 (Promega), 0.50 µM of primers (Promega) and 10 µl DNA. Isolates Thermal cycling (Biometra Personel Cycler, Göttingen, Germany) was carried out with the initial denaturation at A total of 102 E. coli O157:H7 isolates recovered from 25 94°C for 2 min and then 35 cycles of denaturation at 94°C for animals including 11 cattle and 14 sheep were analyzed. 20 s, annealing at 54°C for 1 min, and extension at 72°C for The 41 isolates from the 11 cattle were obtained from 282 1 min, with a final extension for 10 min at 72°C (Fratamico et cattle (207 beef and 75 dairy cattle) feces and/or colon al. 2000). A 10-µl aliquot of each PCR product was subjected tissue samples between April 2002 and December 2003, to 1.5 % agarose gel (SeaKem LE Agarose, Rockland, ME, and 61 isolates from 14 sheep were obtained from 218 USA) electrophoresis containing 0.1 µg/ml ethidium bromide sheep feces and/or colon tissue samples between November for 1 h at 100 V. Amplicon visualization and documentation 2007 and November 2008 (with a total of 500 animals) was performed using gel documentation and analysis system (Table 1). (Syngene Ingenius, Cambridge, UK). IMS based cultural technique for the isolation of E. coli Antibiotic susceptibility testing O157:H7 The antibiotic susceptibility test of E. coli O157:H7 isolates Immunomagnetic separation (IMS)-based selective enrich- was performed with the disc diffusion method as recom- ment technique was used for the isolation of E. coli O157 mended by the Clinical and Laboratory Standards Institute (Byrne et al. 2003). Briefly, 10 g of feces and/or colon (CLSI) (Anon 2006) in Mueller-Hinton agar (Oxoid tissue samples of cattle and sheep were weighed in a sterile CM0337) with 20 different antibiotics and antibiotic bag and enriched with 90 ml EC broth (Oxoid CM0853, combinations at given concentrations (Oxoid) as shown in Hampshire, UK) containing novobiocin (20 µg/l; Sigma N- Table 2. 1628, St. Louis, MO, USA) and incubated at 37°C at Escherichia coli O157:H7 isolates were transferred to 100 rpm for 18 h in a shaking incubator (Bellco Shel Lab BHI broth (Oxoid CM0225) and incubated at 37°C for Shaking Incubator S16R, Oregon, USA). After the incuba- 24 h. A loopfull of growth was transferred into 5 ml tion period, IMS was performed according to the manu- containing Tryptone Soya Broth (Oxoid CM0129). The facturer’s protocol. Then, 20 µl of magnetic beads coated culture was incubated at 37°C until it achieved the with specific antibody against E. coli O157 (Dynabeads turbidity of the 0.5 McFarland standard. The correct anti E. coli O157, Prod. No. 710.04; Dynal, Oslo, Norway) density of the turbidity standard was measured by Nano- were used. Following the IMS procedure, 100 μl of PBS- Drop Spectrophotometer (NanoDrop ND-100, Delaware, Tween 20 was added to resuspend the bead and E. coli USA). The absorbance of the broth cultures at 625 nm was O157 complex. fixedto0.08–0.10. The suspension was inoculated Resuspended IMS mixture was plated on Sorbitol uniformly to Mueller Hinton agar (uniform depth of MacConkey Agar (Oxoid CM0813) plates containing 4 mm) with a sterile cotton swab. Then, antibiotic discs Cefixime-tellurite supplement (Oxoid SR0172). After over- were placed onto the plate and incubated at 37°C for 18 h. night incubation at 42°C, sorbitol negative colonies were According to the sizes of the inhibition zones, interpreta- Ann Microbiol (2010) 60:489–494 491 Table 1 Sampling design and Sampling date Source of isolates No. of isolates Code of isolates Resistance to: antibiotic resistance profiles of E. coli O157:H7 isolates from 16.05.2002 Cattle (male/enteritis) 5 1001–1005 KF cattle and sheep samples 01.10.2002 Catlle (female/healthy) 5 1005–1010 S 01.10.2002 Catlle (female/healthy) 5 1011–1015 01.10.2002 Catlle (female/healthy) 4 1016–1019 KF 01.10.2002 Catlle (female/healthy) 2 1020–1021 24.07.2003 Cattle (male/healthy) 5 1022–1026 24.07.2003 Catlle (male/healthy-colon tissue) 5 1027–1031 24.07.2003 Cattle (male/healthy) 5 1032–1036 24.07.2003 Cattle (male/healthy) 1 1037 a a 24.07.2003 Cattle (male/healthy) 1 1038 KF ,NA 24.07.2003 Cattle (male/healthy) 3 1039–1041 KF 10.12.2007 Sheep (healthy) 5 1042–1046 18.04.2008 Sheep (healthy) 5 1047–1051 18.04.2008 Sheep (healthy) 5 1052–1056 16.05.2008 Sheep (healthy) 5 1057–1061 17.07.2008 Sheep (healthy) 2 1062–1063 17.07.2008 Sheep (healthy) 4 1064–1067 RL 23.07.2008 Sheep (healthy) 5 1068–1072 29.08.2008 Sheep (healthy) 5 1073–1077 29.08.2008 Sheep (healthy) 4 1078–1081 29.08.2008 Sheep (healthy) 4 1082–1085 S3 29.08.2008 Sheep (healthy) 4 1086–1089 a 29.08.2008 Sheep (healthy) 5 1090–1094 KF Cephalothin, S3 Sulphona- a a mide compounds, S Streptomycin, 29.08.2008 Sheep (healthy) 5 1095–1099 S ,RL NA Nalidixic acid, RL 29.08.2008 Sheep (healthy) 3 1100–1102 Sulphamethoxazole tion of the strains as susceptible, intermediate, or resistant streptomycin, eight (72.72 %) were intermediately resistant was made according to the CLSI (Anon 2006). to kanamycin, seven (63.63 %) were intermediately resistant to sulphamethoxazole, cephalothin, and ampicillin. In addi- tion, five (45.45 %) isolates were intermediately resistant to Results and discussion amikacin, three (27.27 %) were intermediately resistant to sulphonamide compounds, and two different isolates (9.09 %) All the E. coli O157:H7 colonies (up to five colonies were intermediately resistant to amoxicillin/clavulanic acid belonging to a positive sample) isolated from the same and cefoxitin, respectively. positive animals showed the same antibiotic resistance/ Among those isolates recovered from sheep, two (14.28 %) susceptible profiles (Tables 1 and 2). Therefore, the results were resistant to sulphamethoxazole, one (7.14 %) to are given according to the number of the positive animals, streptomycin, and one (7.14 %) to sulphonomide compounds. e.g., 11 cattle and 14 sheep, instead of the total number In one (7.14 %) E. coli O157:H7 sheep isolate, multiple drug (102) of the isolates tested in this study (Table 2). All resistance was shown to streptomycin and sulphonomide compounds. From total sheep isolates, eleven (78.57 %) of isolates except one were recovered from healthy animals. Four of the 11 cattle isolates were recovered from cows. them were intermediately resistant to streptomycin, ten Nevertheless, no antibiotic resistance profile differences (71.42 %) were intermediately resistant to cephalothin, seven were seen between male and female host samples, one of (50.00 %) were intermediately resistant to sulphamethox- the animals even showed enteritis. azole, and five (35.71 %) were intermediately resistant to Overall, among the cattle isolates, 36.36 % (4/11) of them ampicillin. For all that, three (21.42 %) isolates were were resistant to cephalothin, 9.09 % (1/11) were resistant to intermediately resistant to tetracycline and nalidixic acid, streptomycin and 9.09 % (1/11) were resistant to nalidixic acid. respectively. In addition, two (14.28 %) isolates were In one (9.09 %) E. coli O157:H7 cattle isolate, multiple drug intermediately resistant to amikacin and kanamycin, respec- resistance was shown to cephalothin and nalidixic acid. Also, tively, and one (7.14 %) was intermediately resistant to ten isolates (90.90 %) were intermediately resistant to ceftriaxone. 492 Ann Microbiol (2010) 60:489–494 Table 2 Antibiotic resistance profiles of E. coli O157:H7 isolates from cattle and sheep feces and/or colon tissue samples Number of E. coli O157:H7 isolates (%) Cattle (n = 11) Sheep (n = 14) −1 a a a a a a Antibiotic (μg disc)R I S R I S Ampicillin (AMP-10) 7 (63.63) 4 (36.36) 5 (35.71) 9 (64.28) Cephazolin (KZ-30) 11 (100) 14 (100) Cephalothin (KF-30) 4 (36.36) 7 (63.63) 10 (71.42) 4 (28.57) Gentamicin (CN-120) 11(100) 14 (100) Amikacin (AK-30) 5 (45.45) 6 (54.54) 2 (14.28) 12 (85.71) Amoxicillin/clavulanic acid (AMC-30) 1 (9.09) 10 (90.90) 14 (100) Cefoxitin (FOX-30) 1 (9.09) 10 (90.90) 14 (100) Ceftriaxone (CRO-30) 11 (100) 1 (7.14) 13 (92.85) Ciprofloxacin (CIP-5) 11 (100) 14 (100) Imipenem (IPM-10) 11 (100) 14 (100) Trimethoprim/sulphamethoxazole (SXT-25) 11 (100) 14 (100) Chloramphenicol (C-30) 11 (100) 14 (100) Kanamycin (K-30) 8 (72.72) 3 (27.27) 2 (14.28) 12 (85.71) Tetracycline (TE-30) 11 (100) 3 (21.42) 11 (78.57) Trimethoprim (W-5) 11 (100) 14 (100) Sulphonamide compounds (S3-300) 3 (27.27) 8 (72.72) 1 (7.14) 13 (92.85) Ceftiofur (EFT-30) 11 (100) 14 (100) Streptomycin (S-10) 1 (9.09) 10 (90.90) 1 (7.14) 11 (78.57) 2 (14.28) Nalidixic acid (NA-30) 1 (9.09) 10 (90.90) 3 (21.42) 11 (78.57) Sulphamethoxazole (RL-25) 7 (63.63) 4 (36.36) 2 (14.28) 7 (50.00) 5 (35.71) R Resistant, I Intermediately resistant, S Susceptible All isolates from cattle and sheep were susceptible to commonly on cattle and sheep feedlots as well as to cephazolin, gentamicin, ciprofloxacin, imipenem, trimeth- chloramphenicol. Scott et al. (2006) showed that E. coli oprim/sulphamethoxazole, chloramphenicol, trimetho- O157:H7 strains isolated from cattle feedlots were suscep- prim, and ceftiofur. Among those isolates recovered tible to 13 tested antibiotics. In particular, different studies from cattle, six (54.54 %) were susceptible to all 20 (Kim et al. 1994; Galland et al. 2001; Schroeder et al. 2002; antibiotics tested. On the other hand, these susceptible Wilkerson et al. 2004) have evidenced that only from 6.63 isolates were all intermediately resistant to cephalothin to 38.46% of E. coli O157:H7 isolates from bovines were and streptomycin. Regarding sheep isolates, eleven resistant to tetracycline. Various countries including Turkey (78.57 %) isolates were susceptible to all tested antibiotics. have banned the usage of chloramphenicol for food- Similar to the cattle isolates, most of the susceptible sheep producing animals, so this result is good data for chloram- isolates (ten, 71.42 %) were intermediately resistant to phenicol resistance. Sheep isolates were more susceptible to streptomycin. antibiotics than cattle isolates. This difference may be Similar to the previous studies, in this study, suscepti- explained by the slaughtering age of the animals that reach bility was amore common character instead of showing up to 1 year old for sheep and more than 1 year old for cattle. resistance to tested antibiotics (Meng et al. 1998; Zhao et Moreover, since intensive sheep breeding does not occur al. 2001; Schroeder et al. 2002; Walsh et al. 2006). In fact, generally in Turkey, the antibiotics are not widely used on no multiresistant character was observed in all the isolates farms for animal prophylaxis, particularly for sheep. tested but, in agreement with Vali et al. (2004), a low Although ciprofloxacin, aminoglycosides and trimetho- prevalence of resistance to cephalothin, sulphamethoxazole, prim/sulphamethoxazole are used as therapeutics in human streptomycin, sulphonamide compounds, and nalidixic medicine, our isolates showed high susceptibility rates, acid, was detected. Also, cephalothin and nalidixic acid except streptomycin and kanamycin with high intermediate resistance ratios were similar to Khan et al.'s (2002) resistant patterns. This variation in results may be due to findings. 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Annals of Microbiology – Springer Journals

Published: Jun 24, 2010

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