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Journal of Food Protection, Vol. 73, No. 2, 2010, Pages 376–379Copyright G, International Association for Food Protection Antibiotic Resistance in Salmonella Isolates from Imported Chicken Carcasses in Bhutan and from Pig Carcasses in Vietnam L. ELLERBROEK,1* D. NARAPATI,2 N. PHU TAI,3 N. POOSARAN,4 R. PINTHONG,4 A. SIRIMALAISUWAN,4 P. TSHERING,2 R. FRIES,5 K.-H. ZESSIN,5 M. BAUMANN,5 AND A. SCHROETER1 1Federal Institute for Risk Assessment (BfR), Diedersdorfer Weg 1, D-12277 Berlin, Germany; 2National Centre for Animal Health, P.O. Box 155, Serbithang, Thimphu, Bhutan; 3Department of Animal Health, Ministry of Agriculture and Rural Development, 15/78 Giai Phong Road, Hanoi, Viet Nam;4Faculty of Agro Industry, Chiang Mai University (CMU), Chiang Mai, 50100 Thailand; and 5Free University, Berlin, Department of Veterinary Medicine, International Animal Health, Ko¨nigsweg 67, D-14163 Berlin, Germany MS 09-088: Received 25 February 2009/Accepted 6 July 2009 The antibiotic resistance in Salmonella isolates from 400 imported chicken carcasses in Bhutan and from 178 pig carcasses in Vietnam were analyzed on a random basis against 14 antimicrobial agents. Among the poultry samples tested, 13% werepositive for Salmonella. Salmonella Enteritidis dominated with a prevalence of 80.7%, and 40 of the 42 isolates harbored two ormore resistance determinants. For the 178 pigs investigated, 49.4% of the swabs and 34.8% of the lymph nodes were Salmonellapositive. The most prevalent serotypes in lymph nodes were Salmonella Derby (50.0%) and Salmonella Typhimurium (27.4%).
From the Salmonella isolates from pigs, only 6% were sensitive to the antimicrobial agents tested. The high resistance level ofSalmonella isolates from pigs and chicken carcasses to different classes of antimicrobials should be emphasized and encourage aprudent use of these agents in animal farming, especially in pig production.
It is recognized that the prevalence of foodborne patients between 1990 and 1991 were resistant to chloram- illnesses in developing countries is considerable (26). But phenicol, ampicillin, and trimethoprim-sulfamethoxazole.
in most of these countries limited data are available to allow Approximately 81% of the Salmonella enterica subsp.
the incidence of particular diseases and trends to be assessed enterica serovar Typhi isolates from northern India were over time. Furthermore, the emergency of new or antibiotic- resistant pathogens may contribute to increasing food safetyrisks (9, 19). Thus, food safety regulations and standards are increasingly influencing the ability of developing countries Sample collection, bacterial isolation, and identification.
to produce food with high quality and to access different Salmonella isolation and detection from skin samples from 400 markets in the world, particularly in industrialized countries.
poultry breasts and necks as well as from surface swabs and lymph A main source of food of animal origin in Bhutan is nodes from 178 pigs in Vietnam were performed according to chicken meat. Although poultry rearing has been an integral International Organization for Standardization (ISO) 6579:2002.
part of the Bhutanese farming system, the demand for Ninety-seven pigs slaughtered in Hanoi came from intensive chicken meat in the Bhutanese market is essentially met by farming, and 81 pigs came from backyard farming. The equipmentand facilities of animal slaughterhouses examined in Hanoi are imports, mainly from India. The annual import of poultry from six complex slaughterhouses, consisting of 8 to 12 lines for meat is approximately 1,300 metric tons, valued at US$2.4 million in 2005 (3). For Vietnam, pork meat production is ofhigh importance. It represents 81% of the total livestock in Antimicrobial susceptibility. The antimicrobial susceptibil- 2005 (11). There are only few reports of salmonellosis in ity of the Salmonella isolates was tested against 14 antimicrobial humans in Vietnam (8). For nontyphoid Salmonella agents by using the broth microdilution method Clinical and infections in humans, Salmonella Typhimurium is the most Laboratory Standards Institute (CLSI) M31-A3 (7, 23) and common causative agent in South Vietnam (30). In India an epidemiological cutoff values according to the European Commit- increased proportion of drugs used as noncontrolled tee on Antimicrobial Susceptibility Testing (http://www.eucast.
org). If cutoff values were not available, breakpoints for medication rather than by prescription results in impending sulfamethoxazole and streptomycin as well as colistin were taken health problems and antimicrobial resistance. Approximate- from the CLSI 18th Informational Supplement M100-S18 of 2008 ly 78% of Salmonella Typhi isolates collected from infected and DANMAP 2001 (2). The antimicrobial susceptibility of theSalmonella isolates to 14 antimicrobial agents (ampicillin, * Author for correspondence. Tel: z49-30-8412-2121; Fax: z49-30- chloramphenicol, ciprofloxacin, colistin, florfenicol, cefotaxime, 8412-2966; E-mail: l.ellerbroek@bfr.bund.de.
ceftazidime, gentamicin, kanamycin, nalidixic acid, sulfamethox- RESISTANCE OF SALMONELLA TO ANTIMICROBIAL AGENTS TABLE 1. Resistance pattern of the 135 antibiotic-resistant Salmonella isolates from the studied broiler chicken (51 isolates) and pig (84isolates) carcasses a AMP, ampicillin; NAL, nalidixic acid; TET, tetracycline; CIP, ciprofloxacin; GEN, gentamicin; STR, streptomycin; TMP, trimethoprim; SMX, sulfamethoxazole; CHL, chloramphenicol; FFN, florfenicol; KAN, kanamycin.
azole, streptomycin, tetracycline, and trimethoprim) was tested. For isolates) and PT21 (1 isolate) (Table 2). Of the eight further differentiation, phage typing was done for Salmonella Salmonella Typhimurium strains, seven belonged to RDNC Enteritidis and Salmonella Typhimurium according to the methods and one belonged to phage type PT22 (Table 2).
of Ward et al. (31) and Anderson et al. (1).
Among the 178 Vietnamese carcasses sampled, 87 (48.9%) carcass swabs and 62 (34.8%) lymph nodes were positive for Salmonella. The prevalence of Salmonella from Among the 400 samples from imported chicken to lymph nodes of animals raised in intensive farms was Bhutan, 13% were found to be positive for Salmonella.
different from that of animals from backyard farms. Twenty- Moreover, two different serotypes and one rough form were nine percent of samples from intensive production were detected. Salmonella Enteritidis dominated with a preva- Salmonella positive, while 43% of all samples from lence of 80.7%, and 40 of the 42 isolates harbored two or backyard production were Salmonella positive. The same more resistance determinants. In addition, all of the eight serovar was isolated from 24 pigs (swabs and lymph nodes).
Salmonella Typhimurium strains and the two rough isolates Four different serotypes were detected in lymph nodes.
were multiresistant. All isolates from chicken (except the Most prevalent in all samples were Salmonella Derby (50%) two sensitive ones) were resistant to nalidixic acid and and Salmonella Typhimurium (27.4%). Of 89 Salmonella ciprofloxacin, and eight of these strains were additionally isolates from pigs, only 6% were sensitive to the resistant to tetracycline and ampicillin (Table 1). Three antimicrobial agents tested. Over 11% (11.2%) of the different phage types and seven RDNC (reacts but does not isolates were resistant to one antimicrobial, 16.8% to two, conform) strains could be differentiated among Salmonella 15.7% to three, and 56.2% to more than three antimicrobials Enteritidis organisms. Phage type 1 (PT1) was the most (Table 1). About 92.2% of the Salmonella organisms prevalent one with 79.2% (32 isolates) followed by PT6a (2 isolated were found to be resistant to tetracycline, 56.7% TABLE 2. Resistance patterns and phage types of Salmonella Typhimurium and Salmonella Enteritidis strains isolated from chickenimported to Bhutan and from pig carcasses in Vietnama a NAL, nalidixic acid; CIP, ciprofloxacin; RDNC, reacts but did not conform; AMP, ampicillin; GEN, gentamicin; KAN, kanamycin; STR, streptomycin; TET, tetracycline; TMP, trimethoprim; SMX, sulfamethoxazole; NT, not typeable.
to trimethoprim, 57.3% to sulfamethoxazole, 41.5% to Europe since the end of the 1980s (12). In contrast, phage chloramphenicol, 49.4% to ciprofloxacin, 40.7% to ampi- type 1 could be frequently isolated in the Baltic countries cillin, 27.0% to kanamycin, 34.8% to gentamicin, 4.5% to and Russia in the 1990s of the last century (16). In florfenicol, 36.0% to streptomycin, and 28% to nalidixic Germany, this phage type is in the top five of nonhuman isolates and could be detected worldwide from human and A high proportion of Salmonella Typhimurium strains (24) isolated from pig carcasses in Vietnam were assigned to The overall prevalence of Salmonella at pig slaughter- phage type DT22 (48%), while the remaining strains were houses in Hanoi, Vietnam, in this study was lower than that in previous research (96%) reported by Ce´dric et al. (5).
Chantong found that prevalence levels of Salmonella from lymph nodes, swabs before spraying, and swabs after The Salmonella detection rate of 13% in poultry imported chilling were 64, 33, and 13%, respectively (6). This is in into Bhutan, harboring two major serotypes, Salmonella contrast to the present study, where Salmonella from swab Enteritidis (85%) and Salmonella Typhimurium (15%), is samples were more frequently isolated than those from consistent with the recent literature reporting 15% prevalence lymph nodes. Such findings are mostly associated with for Nepal (16), 19% for South Africa (29), and 12% for inappropriate slaughter hygiene procedures.
Turkey (21). Although a prevalence of 15% for Salmonella in A high portion of the Salmonella isolates from pigs were live poultry birds (18) was earlier reported from India, some found to be antibiotic resistant; only 6% were sensitive to the reports indicate negligible prevalence in poultry carcasses antimicrobial agents tested. Tran et al. (27) noticed a (28). The present observation of 94.2% Salmonella Enteritidis difference in antibiotic resistance with respect to the origin isolates resistant to nalidixic acid could be the result of mass of sampling. In contrast, Ce´dric et al. (5) reported a higher use of quinolones in the broiler farms in India.
prevalence (50%) for samples from an urban slaughterhouse According to previous reports all Salmonella strains in Hanoi than from pigs slaughtered in the rural Mekong Delta isolated were sensitive to chloramphenicol like the pattern (5%). All the Salmonella Typhimurium isolates were resistant found in Indian Salmonella isolates from 1996 to 1999 and to at least two and up to nine antimicrobial agents. The most 2001. These isolates were reported to be 100% chloram- prevalent phage type was DT22, which is rarely isolated in phenicol sensitive, with sensitivity as high as 79% in 2000 Germany from pigs or products thereof, while the remaining (17). The current resistance pattern of chloramphenicol isolates were not typeable with the phages used (22, 25).
could be attributed to the limited use of this drug during thelast decade in India (13).
Eight isolates of Salmonella Enteritidis were found to We thank C. Fester, M. Jaber, and K. Thomas for their skilled be resistant to four drugs: ampicillin, nalidixic acid, tetracycline, and ciprofloxacin. A higher proportion ofantibiotic resistance in Salmonella Enteritidis has been reported from southern Brazil (20). Salmonella Enteritidis Anderson, E. S., L. R. Ward, M. J. De Saxe, and J. D. H. De Sa.
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