Antimicrobial use and resistance among commensal Escherichia coli and Salmonella enterica in rural Jordan small ruminant herds

Small Ruminant Research 149 (2017) 99–104

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Antimicrobial use and resistance among commensal Escherichia coli and Salmonella enterica in rural Jordan small ruminant herds M.M. Obaidat a,∗ , A.A. Al-Zyoud a , A.E. Bani Salman a , M.A. Davis b a b

Faculty of Veterinary Medicine, Jordan University of Science and Technology, Irbid 22110, Jordan Paul G Allen School for Global Animal Health, College of Veterinary Medicine, Washington State University, Pullman, WA, USA

a r t i c l e

i n f o

Article history: Received 27 November 2016 Received in revised form 26 January 2017 Accepted 29 January 2017 Available online 1 February 2017 Keywords: Antimicrobials Ruminants Rural Pastoralist Middle East

a b s t r a c t Small-scale small ruminants’ farming is the major system in poor resources settings, yet their farming practices largely unknown. This paper assessed the husbandry practices, antimicrobial use and antimicrobial resistance of commensal Escherichia coli and Salmonella enterica in sheep and goat pastoralists in rural Jordan. Fifty-two sheep and goat farmers were interviewed concerning disease incidence, antimicrobial use and knowledge of antimicrobials. E. coli and Salmonella were isolated from freshly passed fecal pellets by standard methods, confirmed by molecular methods, and tested for resistance against 12 antimicrobial by the disc diffusion method. Interview results indicated that a limited variety of antimicrobial drugs (oxytetracycline, penicillin and tylosin) are used by small ruminant farmers in Jordan. Moreover, farmers store the antimicrobials at improper temperatures and frequently obtain antimicrobials without prescription; veterinary consultation prior to antimicrobial use is infrequent. Higher antimicrobial resistance than most worldwide similar studies was exhibited by the isolates: 67.7% and 76.9% of the E. coli and Salmonella isolates, respectively, exhibited resistance to at least one antimicrobial and 33.3% and 38.5% exhibited resistance to at least three classes of antimicrobials. Among all bacterial isolates, the most frequent resistance was to tetracycline and cephalothin; resistance to ceftriaxone, gentamicin, and ciprofloxacin was rare. In general, E. coli exhibited higher resistance percentages than Salmonella for the tested antimicrobials. This study shows that upgrading the role of veterinarian and improving antimicrobial use practices at the grassroots level through educating farmers on proper handling and judicious use of antimicrobials are essential, as many antimicrobials are critically important for treating human infections. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Antimicrobial resistant pathogens significantly impact both human and animal health because they are difficult to treat and they have been associated with higher virulence than susceptible pathogens (Da Silva and Mendonca, 2012). Human infections with antimicrobial-resistant zoonotic pathogens have been attributed to use of antimicrobials in the animal reservoir (Smet et al., 2010; Landers et al., 2012; Robinson et al., 2016). Inappropriate or overuse of antimicrobials probably contributes to the emergence and dissemination of antimicrobial resistance in bacteria (Witte, 1998; McEwen and Fedorka-Cray, 2002). This risk might be augmented in the future due to the anticipated increase in antimicrobials use in livestock production (Garcia-Migura et al., 2014; Van Boeckel

∗ Corresponding author. E-mail address: [email protected] (M.M. Obaidat). http://dx.doi.org/10.1016/j.smallrumres.2017.01.014 0921-4488/© 2017 Elsevier B.V. All rights reserved.

et al., 2015). This likely to happen as the level of antimicrobials used strongly and positively correlates to the resistance levels these antimicrobials agents in commensal E. coli (Chantziaras et al., 2014). Data on the epidemiology of antimicrobial resistance in humans and animals in Jordan are sparse. Data from the Antimicrobial Resistance Surveillance & Control in the Mediterranean Region (ARMed) Project collected between 2003 and 2008 revealed high levels of resistance to four classes of antimicrobials among invasive strains of E. coli collected from blood cultures and cerebrospinal fluid in five Jordanian hospitals (Borg et al., 2008). In addition, there is a scarcity of literature to document antimicrobial usage in small ruminant husbandry, particularly in pastoralist husbandry. Publications describing the prevalence of resistance in E. coli or other bacteria isolated from animals in Jordan, or describing the prevalence of non-prescription antimicrobial treatment of livestock, are also lacking. A reported high burden of disease in humans from potentially zoonotic pathogens such as non-typhoid Salmonella enterica

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and Brucella spp. (Gargouri et al., 2009) suggests that zoonotic transmission of antimicrobial resistant bacteria may be important. Anecdotal evidence suggests that the existence of using antimicrobials without a prescription in livestock in rural Jordan (Dr. Dayyat, personal communication). Because of the potential zoonotic transmission of antimicrobial resistant pathogens, the extent of antimicrobial use in livestock, particularly in the absence of veterinary supervision, the development of antimicrobial resistance may be of concern.We interviewed small ruminant herd owners in rural Jordan to determine the prevalence of this practice, and obtained fecal samples to determine whether antimicrobial use without a veterinary prescription may be associated with antimicrobial resistance in small ruminant fecal E. coli and Salmonella enterica isolates. 2. Materials and methods 2.1. Farms selection This study was conducted to cover all regions and governorates of Jordan by visiting herdsmen randomly while grazing their animals or at their farms. The studied farms included 15 farm in Southern Jordan (Tafela, Maan, and Karak), 18 farm in Northern Jordan (Irbid and Jarash), 13 farm in the Badia (Mafrqa) and 6 farms in the Jordan Valley. The approached herdsmen were informed that the purpose of the study is for scientific research, their participation is completely voluntary and their decision to participate or not will not affect their right of future veterinary services. All approached herdsmen agreed to participate in the study. Interviews were performed in fifty-two farms and fecal sampling was obtained from fourteen farm. The questionnaires were administered in Arabic by a trained veterinarian whose original dialect is Bedouin. The questionnaire was divided into four sections: 1) information on the farms and animals, 2) farm management and animal care, and 3) disease incidence, antimicrobial use and knowledge of antimicrobials. Questions included numbers of animals, animal feeding and housing management systems, frequency of diseases (diarrhea, respiratory diseases, abortion, abscesses, mastitis, and mortalities), whether veterinary care was ever used and reasons for seeking veterinary care, sources and access to antimicrobials and when they used antimicrobials. When possible, photographs of antimicrobial drug vials, including the expiration date, were obtained to supplement the interview information. 2.2. Bacterial isolation and identification Freshly passed fecal samples (approximately 10 fecal pellets/sample) were randomly collected off the ground and placed into sterile containers which were labeled and stored on ice until return to the laboratory at the Jordan University of Science and Technology (JUST) for bacterial isolation, identification and antimicrobial agent susceptibility testing. Fecal samples were cultured for E. coli and Salmonella enterica using standard protocols as follows (Wang et al., 2011). All incubations were conducted at 35 ◦ C for 24 h and all media were manufactured by Oxoid Ltd. (Hampshire, England) and purchased through a local supplier (Al-Sami Tech Supplies Company, Amman, Jordan). Feces (5 g) were mixed with 45 ml of 0.1% buffered peptone water and mashed completely using sterile wooden spatulas. Fecal suspension (20 ml) was added to 20 ml of double-strength MacConkey broth and incubated. The resulting broth culture (100 ␮l) was streaked onto MacConkey agar. After incubation, pink to red colonies (one per sample) were transferred to eosin methylene blue plates and incubated. Presumptive E. coli colonies (dark center with

a green metallic sheen; five per sample) on eosin methylene blue agar were subcultured on Trypticase soy agar (TSA Indole-positive and oxidase-negative isolates were maintained in Trypticase soy broth (TSB) with 20% glycerol at − 20 ◦ C. Suspect E. coli isolates were confirmed by PCR targeting the E. coli translation elongation factor EF-Tu (tuf) gene. Genomic DNA was extracted by the boiling method (Kawasaki et al., 2005). The chosen E. coli-specific PCR primers were TEcol553 (5 -TGG GAG CGA AAA TCC TG-3 ) and TEcol754 (5 -CAG TAC AGG TAG ACT TCT G-3 ) (Integrated DNA Technologies, Coralville, IA, USA) (Maheux et al., 2009). Confirmed E. coli isolates were stored in TSB with 20% glycerol at − 20 ◦ C. Salmonella was isolated following a previously described method (Lestari et al., 2009) with some modifications. All incubations were conducted at 35 ◦ C for 24 h unless otherwise specified. Briefly, 20 ml of the fecal suspension described above was preenriched for 6 h under shaking at 100 rpm. Enriched broth culture (10 ml) was transferred to 100 ml of tetrathionate broth and incubated at 42 ◦ C. The tetrathionate broth culture was then streaked onto xylose lysine Tergitol 4 (XLT4) plates. Suspect Salmonella colonies (entirely black or pink to red with black centers; 3 per sample) were transferred to lysine iron agar, triple sugar iron and urea agar slants. Isolates with typical Salmonella phenotypes on the slants were confirmed by PCR to test for the invA gene using invA139 5 -GTG AAA TTA TCG CCA CGT TCG GGC AA-3 and invA-1341 5 -TCA TCG CAC CGT CAA AGG AAC C-3 (Rahn et al., 1992). Confirmed Salmonella isolates were stored in TSB with 20% glycerol at − 20 ◦ C. 2.3. Antimicrobial agent susceptibility testing Isolates were screened for susceptibility to a panel of 12 antimicrobials on Mueller-Hinton agar (Oxoid Ltd.) by the disk diffusion method (Clinical and Laboratory Standards Institute, 2012). The following disks (Oxoid) were used: Am (ampicillin; 10 ␮g), Amc (amoxicillin–clavulanic acid; 30 ␮g), Cef (cephalothin; 30 ␮g), Cro (ceftriaxone, 30 ␮g), C (chloramphenicol; 30 ␮g), Cip (ciprofloxacin; 5 ␮g), Nal (nalidixic acid; 30 ␮g), Gm (gentamicin; 10 ␮g), S (streptomycin; 10 ␮g), Sxt (sulfamethoxazole–trimethoprim; 25 ␮g), Te (tetracycline; 30 ␮g), and K (kanamycin; 30 ␮g). To avoid zones overlap, four antimicrobials were tested for each Muller Hinton agar plate. The zones of inhibition around each disc was measured after 18 h of incubation at 35 ± 2 ◦ C. Isolates with intermediate susceptibility to the tested antimicrobials were considered “susceptible” for analysis purposes. Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 29213 were used as reference strains for antimicrobial disk control. An isolate was defined as resistant if it was resistant to one or more of the agents tested, whereas isolates resistant to three or more antimicrobial classes were classified as MDR (Magiorakos et al., 2012). 2.4. Data analysis Data were entered, stored and analyzed using Microsoft Excel (Redmond, WA, USA). Proportion of antimicrobial resistant among E. coli and Salmonella enterica isolates were compared using the Chisquare test or Fisher’s exact test when appropriate. These statistics were calculated using WINPEPI (Abramson, 2011). 3. Results 3.1. Antimicrobial use The majority of farmers reported that they understood the definition and use of antimicrobials. The majority of farmers also

M.M. Obaidat et al. / Small Ruminant Research 149 (2017) 99–104 Table 1 Animal husbandry in 52 sheep and goat farms in rural Jordan. Data shown as numbers of farms and in parenthesis as percentages.

Table 2 Responses of 52 herdsmen questionnaire regarding use of veterinary services and antimicrobial s in rural Jordan.

Farms (N = 52) Can you define what an antimicrobial is? respondents provided correct definition 46 (86) 6 (14) respondents provided wrong definition Did you experience no response to antimicrobial treatment in your animals? 43 (79) Yes 9 (21) No Can you define what a zoonotic disease is? Respondents provided correct definition 48 (93) respondents provided wrong definition 4 (7) Average number of goats (mean ± standard deviation) 63 ± 80 Average number of sheep goats (mean ± standard deviation) 310.5 ± 488.7 Are sheep and goats mixed togethera Yes 20 (74.1) No 7 (30.4) b For what you raise goats? Milk 24 (96) Meat 24 (96) Fiber 11 (44) For what you raise sheep?b Milk 32 (100) Meat 31 (97) Wool 17 (53) Do your herds mingle with other herds? Never 28 (53) Sometimes 24 (47) Are your animals fenced or separated from other herds?b Yes 37 (80) 9 (20) No Do your animals move for distances >10 km? Yes 4 (8) 48 (92) No What do you feed your animals? 52 (100) Hay Barley 52 (100) Olive by-products 2 (14) Do your animals graze? Yes 52(100) How many months/year do they graze? All year 32 (62) 6 months/year 20 (38) What is the water source for your animals? Spring water 15 (28.8) Well 20 (38.5) Municipal water 17 (32.7) How often animals housed in a barn? 11 (21.2) Nightly 36 (69.2) Sometimes 5 (9.6) Never Do you clean and disinfect the animal housing areas? 48 (92.3 Sometimes 4 (7.7) Never Do you clean and disinfect feeding and treating equipment? 36 (69.2) Sometimes 16 (30.8) Never a b

Only 27 farm has both sheep and goats. some farmers did not respond to these questions.

reported experiencing antimicrobials resistance in diseased animals. Most small ruminant flocks in rural Jordan did not mingle with other flocks and were kept fenced during the night. Yearround, the flocks grazed during the day and were fed supplemental barley and hay. Spring water and wells were the major water sources (Table 1). Farmers reported oxytetracycline and tylosin as the most commonly used antimicrobials and fewer farmers reported using penicillin. However, some farmers reported that penicillin was not effective for treating their animals. Most farmers reported respiratory diseases and mastitis as the major health problems in their flocks, followed by diarrhea, abortion and dystocia. All interviewed farmers reported that antimicrobials are readily available for use without having prescriptions or examination by veteri-

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Farms (N = 52) Do you ever use a veterinarian? 49 (94.2 Yes 3 (6.8) No What diseases require a veterinarian? 7 (13.5) Complicated cases 21 (40.4) Gastroenteritis Respiratory Diseases 19 (36.5) Dystocia 21 (40.4) Abortion 13 (25) Mastitis 15 (28.8) In the last month, did any animals have Diarrhea 37 (71.1) Respiratory Diseases 42 (76.9) Abscess 17 (32.7 Mastitis 40 (76.9) Abortion 30 (57.7) Dystocia 30 (57.7) Mortalities 23 (44.2) Are antimicrobials easily purchased? Yes 52 (100) Where do you purchase antimicrobials? Government 8 (15.4) Private clinic 52 (100) What do you use antimicrobials for? Treatment 52 (100) 11 (21.2) Prevention 0 Growth Do you get a prescription? 39 (75) Never Rarely 13 (25) Does your veterinarian see your animal before prescribing antimicrobials? Never 8 (16) 39 (78 Sometimes Always 3 (6) What is the most common antimicrobial used? 52 (100) Oxytetracycline Tylosin 38 (73.1) Penicillin 15 (30.1 Gentamicin 4 (7.7) Enrofloxacin 2 (3.8)

narians. The farmers reported keeping and using antimicrobials without veterinary advice, but they consulted with veterinarians in emergency cases such as dystocia and diseases that did not improve with treatment. A large percent (75%) of the farmers reported that they never obtained prescriptions for antimicrobials. All farmers reported using antimicrobials for disease treatment and 21.2% of them reported also using antimicrobials for preventing diseases (Table 2). 3.2. Antimicrobial resistance of commensal E. coli and Salmonella In total, 189 E. coli and 26 Salmonella enterica isolates from 215 fecal samples on 14 farms were tested for antimicrobial resistance. The percentage of E. coli resistant to at least one antimicrobial was 67.7% and percentage of E. coli resistant to three or more antimicrobial classes were 33.3%. For Salmonella enterica, 76.9% of the isolates were resistance to at least one antimicrobial and 38.5% were r resistant to three or more antimicrobial classes (Table 3). The percent of E. coli isolates with resistance to tetracycline, ampicillin, streptomycin, cephalothin, sulfamethoxazole–trimethoprim or nalidixic acid ranged from 20.1% for nalidixic acid to 45.5% for tetracycline. Resistance among E.coli to ceftriaxone, gentamicin, ciprofloxacin, amoxicillinclavulanic acid, kanamycin or chloramphenicol was less frequent and ranged from 1% to 9%. For Salmonella, the total antimicrobial resistance percentages for tetracycline (46.2%), ampicillin (42.3%),

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Table 3 Antimicrobial resistant of E. coli and Salmonella isolated from fecal samples of 14 sheep and goat farms in rural Jordan (n, %). Total (N = 189) E. coli

Salmonella

Resistant to at least one antimicrobial Resistant to ≥3 classes of antimicrobial s Resistant to at least one antimicrobial Resistant to ≥3 classes of antimicrobial s

128 (67.7%) 63 (33.3%) Total (N = 26) 17 (76.9%) 8 (38.5%)

Table 4 Resistance percentages (in descending order) to individual antimicrobial s among E. coli isolated from fecal samples of sheep and goat farms in rural Jordan.

Antimicrobial (Breakpoints mm) Tetracycline (≤11) Ampicillin (≤13) Streptomycin (≤11) Cefalothin (≤14) Sulfamethoxazole– trimethoprim (≤10) Nalidixic acid (≤13) Chloramphenicol (≤12) Kanamycin (≤13) Amoxicillin-clavulanic acid (≤13) Ciprofloxacin (≤15) Gentamicin (≤12) Ceftriaxone (≤19)

E. coli Total (N = 189) Number%)

Salmonella Total (N = 26) Number%)

86 (45.5) 67 (35.4) 61 (32.3) 52 (27.5) 40 (21.1)

12 (46.2) 11 (42.3) 8 (30.8) 5 (19.2) 7 (26.9)

38 (20.1) 17 (9.0) 1 (7.4) 13 (6.9)

6 (23.1) 1 (3.8) 2 (7.7) 2 (7.7)

7 (3.7) 6 (3.2) 2 (1.1)

1 (3.8) 0 0

streptomycin (30.8%), sulfamethoxazole–trimethoprim (26.9%) and nalidixic acid (23.1) were higher than resistance to cephalothin (19.2%), kanamycin (7.7%), amoxicillin-clavulanic acid (7.7%) and ciprofloxacin (3.8%). No resistance to gentamicin or ceftriaxone was found (Table 4). Several antimicrobial resistance profiles were exhibited by the E. coli isolates. The most frequent profiles included pan-susceptibility (32.3%), resistance to the single antimicrobials tetracycline (6.3%), cephalothin (5.8%), and resistance to tetracycline and streptomycin (3.7%). The resistance profiles AmCefNalSTe, AmCefSSxtTe, AmCefSTe, AmNalSTe, AmSSxtTe, AmTe, and CefTe each included 3 isolates and the remaining 58 profiles were each carried by two or one isolates (Table 5). Several antimicrobial resistance profiles were also exhibited by Salmonella isolates, but AmSSxtTe was the most common (7.7%) MDR profile (Table 6). 4. Discussion In general, small ruminant farmers in rural Jordan use limited types of antimicrobials in their flocks, primarily oxytetracycline, tylosin and penicillin. The choice of these antimicrobials may be due to their low cost and their familiarity to farmers. A similar study in rural areas of Peru found that antimicrobials used in small dairy farms were limited to oxytetracycline, penicillin, cloxacillin, and trimethoprim-sulfamethoxazole (Redding et al., 2014). Other studies in other countries reported similarly limited numbers of antimicrobials for treating animals in Sudan, Costa Rica and Kenya (Roderick et al., 2000; Luna-Tortos et al., 2006; Eltayb et al., 2012). All farmers reported that they understood what antimicrobials were for but the majority reported they had experience of antimicrobials not working. Our study revealed that the majority of rural Jordanian farmers could readily afford and obtain antimicrobials without a prescription. Most of the farmers interviewed for our

study only consulted a veterinarian for cases that were severe or refractory to normal treatments, suggesting that there are fewer opportunities for veterinary-client education than would be optimal (Tables 5 and 6). Resistance patterns shared by E. coli and Salmonella in this study primarily included pansusceptibility and single resistances to tetracycline, ampicillin and streptomycin. The only MDR profile found in both bacterial species included resistance to ampicillin, streptomycin, sulfamethoxazole-trimethoprim and tetracycline. Plasmid transfer between two bacterial genera is rare but has been documented (Daniels et al., 2007). In general, E. coli exhibited higher resistance to the tested antimicrobials than Salmonella. This finding is similar to a previous finding in Ontario, Canada, where 13% and 0% of resistance was exhibited by commensal E. coli and Salmonella, respectively, in sheep flocks (Scott et al., 2012). Our findings are also consistent with previous findings (Varga et al., 2008) who compared the antimicrobial resistance of E. coli and Salmonella isolates from finishing swine and found that generic E. coli isolates were more likely than Salmonella to have single or multidrug resistance phenotypes, and that there was no significant association between E. coli and Salmonella resistance phenotypes within sample. This also supports the notion that E. coli is more susceptible to antimicrobial selection pressures than Salmonella for several antimicrobials. Moreover, previous studies indicated that antimicrobial resistance acquisition is more frequent among E. coli than Salmonella (Mathew et al., 2002). The high proportions of Salmonella and E. coli that were resistant to tetracycline which might be attributed to the frequent use of oxytetracycline as reported by the farmers interviewed for this study. A previous report showed the resistance of E. coli was highest toward tetracycline, which was associated with excessive tetracycline use (Scott et al., 2012). In addition, the resistance profiles of most multidrug-resistant E. coli and Salmonella isolates included resistance to tetracycline. Selection for co-resistance by oxytetracycline use may play a role in maintenance of MDR bacteria; however, fitness costs of resistance plasmids that are not carrying tetracycline resistance genes may counteract that effect (Subbiah et al., 2011). This study indicates that the most frequent resistance in E. coli was to tetracycline and cephalothin, with relatively lower resistance to ceftriaxone, gentamicin, and ciprofloxacin. This observation is consistent with other studies of the antimicrobial resistance of E. coli from different sources worldwide (Erskine et al., 2002; Schlegelova et al., 2002; Schroeder et al., 2002; Klein and Bülte, 2003; Sayah et al., 2005). The high prevalence of resistance among E. coli and Salmonella suggests a continuous source of sheep and goat colonization and infection with resistant strains, especially as E. coli has the ability to survive, and sometimes to grow, in fecal pellets in pastures (Weaver et al., 2005; Moriarty et al., 2011). To our knowledge, this is the first study to document antimicrobial resistance of enteric bacteria and antimicrobial use in sheep and goats among flocks in rural Jordan. Therefore, this study fills a critical knowledge gap and emphasizes the need for education of small rural herd owners regarding proper handling and judicious use of antimicrobials to preserve their efficacy. Additionally, epidemiologic surveillance to determine the prevalence and antimicrobial resistance of enteric pathogens in sheep and goats and their food products is needed. We have detected multidrugresistance in approximately one-third of both E. coli and Salmonella enterica in the sampled small ruminant herds of rural Jordan, in the context of limited classes of antimicrobials in use. This finding has public health significance as most of these antimicrobials (ampicillin, streptomycin, nalidixic acid, kanamycin, ciprofloxacin, gentamycin and ceftriaxone) are critically important for treating

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Table 5 Resistance patterns of Escherichia coli isolates from fecal samples of sheep and goat farms in Jordan. Resistance patterna

Number of isolates

% of isolates

Susceptible to all antimicrobials Am Te Cef STe AmCefNalSTe, AmCefSSxtTe AmCefSTe AmCefCSSxtTe AmCefNalSSxt AmCipNalSSxtTe AmCNalSSxtTe AmAmc AmAmcCef AmAmcCefCSSxtTe AmAmcCefCSxtTeK AmAmcCefK AmAmcCefNalSSxtTeK AmAmcNal AmAmcNalSTe AmcCef AmcCefNalTe AmcCefTe AmCefCipCNalSSxtTe AmCefCipCNalSSxtTeK AmCefCipNalSSxtTe AmCefCSSxt

61 7 12 11 7 3 (each profile)

32.3 3.7 6.3 5.8 3.7 1.6 (each profile)

2 (each profile)

1.1 (each profile)

1 (each profile)

0.5 (each profile)

AmNalSTe AmSSxtTe

AmTe CefTe

AmCSSxtTe AmCTe AmSTe AmSxtTe AmCefCSTe AmCefGmK AmCefGmSTeK AmCefNalSSxtTe AmCefNalSTeK AmCefSSxt AmCefSSxtK AmCefSSxtTeK AmCefSxtTe AmCefTe AmcNalTe AmCroCNalSxtTeK AmcSTe AmGmNalSSxtTe AmNalSSxtTe

CipNal CNalTe NalSSxtK NalTe AmS CefCro CefGm CefNalSTe Gm GmTe K Nal NalS NalSSxtTe NalSSxtTeK NalSTe S SSxtTe SxtTe

a Am, ampicillin; Amc, amoxicillin–clavulanic acid; Cef, cephalothin; Cro, ceftriaxone; C, chloramphenicol; Cip, ciprofloxacin; Nal, nalidixic acid; Gm, gentamicin; S, streptomycin; Sxt, sulfamethoxazole–trimethoprim; Te, tetracycline; and K, kanamycin.

Table 6 Resistance patterns of Salmonella isolates from fecal samples of sheep and goat farms in Jordan. Resistance patterna Susceptible to all antimicrobials Cef Am AmS AmAmcCefNalSSxtTe NalSSxtK SxtTeK a

AmSSxtTe

Te

CipCNalSxtTe AmcCefTe AmNalSTe AmNalTe

AmTe AmNalSSxt Nal AmCefSSxtTe

Number of isolates

% of isolates

6 2

23.1 7.7

1

3.8

See Table 7 for antimicrobial abbreviations.

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