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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: firstname.lastname@example.org.
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
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