Antimicrobial Resistance in Salmonella Serovars Isolated from Meat Shops at the Markets in North Vietnam

Abstract

A total of 97 out of 245 carcass, sewage effluent, and table surface samples in meat shops at the retail markets in North Vietnam showed Salmonella positive. Eleven Salmonella serovars, including Infantis, Anatum, Rissen, Reading, London, Typhimurium, Enteritidis, Agona, Newport, Emek, and Derby, were identified. The Salmonella isolates were tested for antimicrobial susceptibility and further investigated for antimicrobial resistance genes. Resistance to kanamycin, gentamicin, neomycin, nalidixic acid, chloramphenicol, trimethoprim, streptomycin, tetracycline, ampicillin, and sulphonamides was found in 28.9–56.7%. The isolates were neither resistant to ceftazidime nor norfloxacin. Sixty-four (66.0%) out of 97 isolates were resistant to at least one of 14 antimicrobials, and 55 (85.9%) out of the 64 isolates showed multidrug resistance. Thirteen resistance genes (bla _TEM , bla _OXA-1 , aadA1, sul1, tetA, tetB, tetG, cmlA1, floR, dfrA1, dfrA12, aac(3)-IV, and aphA1-1AB) were detected in the resistant isolates. This study indicates that Salmonella isolated from meat shops were resistant to multiple antimicrobials, and the resistance genes were widespread among the serovars isolated.

Introduction

F oodborne diseases caused by non-typhoid Salmonella represent an important public health concern and an economic burden in many parts of the world (Chen et al., 2004; Miko et al., 2005; Van et al., 2007). In recent years, an increase in the occurrence of antimicrobial resistance Salmonella spp. has been observed in several countries (Van et al., 2007; Yang et al., 2010). Antimicrobials are currently used for three main reasons in animal husbandry such as therapeutics, prophylaxis, and growth promotion. The routine practice of giving antimicrobials could be important factors in the emergence of antimicrobial-resistant bacteria that are subsequently transferred to humans via the food chain (Tollefson and Miller, 2000; Angulo et al., 2004). Several lines of evidence indicate that antimicrobial resistance among human Salmonella infections results from the use of antimicrobials in food animals (Angulo et al., 2000).

In Vietnam, as in most other developing countries, information about foodborne diseases and antimicrobial resistance among Salmonella has been limited. In addition, self-medication through retail pharmacies is a common practice, where antimicrobials for human and animal can be freely purchased over the counter without control (Ogasawara et al., 2008). To date, most studies have focused on the prevalence and molecular mechanisms of antimicrobial resistance of Salmonella spp. isolates from human medicine, whereas similar studies on Salmonella originating from foodstuffs are rare and limited (Van et al., 2007; Vo et al., 2010).

The aim of this study was to determine the level of antimicrobial resistance and to investigate the antimicrobial resistance genes in Salmonella serovars isolated from meat shops at retail markets in North Vietnam.

Materials and Methods

Sampling and Salmonella isolation

A total of 245 samples (116 from carcass, 84 from table surfaces, and 45 from sewage effluent) was collected in pork and chicken shops at 45 retail markets in North Vietnam between January 2008 and June 2009. Only one kind of sample from each meat shop was collected. Swabs of carcass and table surfaces were sampled by autoclaved cottons in an area approximately 20 cm² and placed in sterile bags with 90 mL of buffered peptone water. Approximately 100 mL of sewage effluent was placed in a 200-mL bottle, and then 10 mL was mixed with 90 mL of buffered peptone water for pre-enrichment. All samples were transported and analyzed in the laboratory of the Department of Microbiology, Infectious Disease and Pathology, Faculty of Veterinary Mmedicine, Hanoi University of Agriculture, Vietnam. The isolation methods of Salmonella were previously described (Vo et al., 2006; Van et al., 2007). Typical Salmonella isolates were serotyped by slide and microtiter agglutination for O and H antigens (Difco Laboratories, Detroit, MI) according to the Kauffmann and White scheme (Grimont and Weill, 2007) by the Department of Veterinary Hygiene, National Institute of Veterinary Research, Vietnam.

Antimicrobial susceptibility testing

The antimicrobial susceptibility of isolates was determined according to the guidelines of the Clinical and Laboratory Standards Institute (CLSI, 2006). Disk diffusion assays were performed on Muller-Hinton agar with disks containing 14 different antimicrobial agents (Oxoid, Basingstoke, Hampshire, UK). The following antimicrobials were tested: ampicillin (A), 10 μg; amoxicillin/clavulanic acid (Ac), 20/10 μg; ceftazidime (Cf), 30 μg; chloramphenicol (C), 30 μg; ciprofloxacin (Ci), 5 μg; gentamicin (G), 10 μg; kanamycin (K), 30 μg; nalidixic acid (Na), 30 μg; neomycin (Ne), 10 μg; norfloxacin (No), 10 μg; streptomycin (S), 10 μg; tetracycline (T), 30 μg; trimethoprim (Tp), 5 μg; and sulphonamides (Su), 300 μg. The interpretive categories—susceptible, intermediate, or resistant—were determined according to CLSI guidelines (CLSI, 2010), except for neomycin, where the zone criteria of ≤12 (resistant), 13–16 (intermediate), and ≥17 (susceptible) were determined (Haley and Prescott, 2002). Escherichia coli American Type Culture Collection (ATCC) 25922 was used as the control. An isolate was defined as “resistance” after confirmation of resistance to at least one antimicrobial tested, while “multiple resistances” was defined as resistance to three or more antimicrobials.

Detection of resistance genes

DNA templates used for polymerase chain reaction (PCR) were prepared by boiling bacterial cultures (Shahada et al., 2006). The following genes implicated with antimicrobials resistance were detected by PCR amplification: bla _PSE-1 , bla _OXA-1, and bla _TEM encoding β-lactam resistance; aadA1, aadA2, aac(3)-IV, aphA-1AB, and Kn encoding aminoglycoside resistance; catA1, cmlA1, and floR encoding chloramphenicol resistance; sul1 encoding sulphonamides resistance; tetA, tetB, tetG encoding tetracycline resistance; dfrA1, dfrA12 encoding trimethoprim resistance. The primer sets and the assay conditions used for amplification were previously described (Ng et al., 1999; Frana et al., 2001; Guerra et al., 2004).

PCR amplification reactions were performed in a 25-μL volume of reaction mixture containing 12.5 μL of GoTaq^® Green Master Mix, 2× (Promega, Madison, WI), 1 μL (10 ng/μL) of primers, 4 μL of DNA template, and nuclease-free water. The PCR program consisted of a hot start cycle of 94°C for 5 min, followed by 30 cycles of 94°C for 30 s, the corresponding temperature of each primer pair for 30 s and 72°C for 1 min, and a final extension step of 72°C for 5 min. The PCR products were analyzed by electrophoresis with 1.5% agarose in 1×Tris-boric acid ethylenediaminetetraacetic acid (TBE) buffer. The gels were stained with 1 μg/mL ethidium bromide, and visualized bands were photographed using a polaroid camera on an ultraviolet light transilluminator. A molecular weight standard ladder was included on each gel (Toyobo, Osaka, Japan).

Statistical analysis

Statistical comparison of the prevalence of Salmonella, the rate of antimicrobial resistance from different sources, was analyzed by the Chi-square test (Microsoft Excel, 2003).

Results

Distribution of Salmonella serovars

Approximately 39.6% (97/245) of the samples were contaminated with Salmonella, of which 44.0% (51/116) from carcass, 35.7% (30/84) from table surface, and 35.5% (16/45) from sewage effluent samples; and 11 serovars were identified (Table 1). The rate of Salmonella in three kinds of samples was not significantly different (p>0.05). Salmonella Infantis (33.0%) was the most common serovar, followed by Anatum (15.5%), Rissen (12.4%), and Reading (11.3%). Salmonella Typhimurium and Enteritidis were detected in 4.1% and 3.1% of the Salmonella isolates. Others serovars such as Emek, Derby, Newport, Agona, and London ranged from 3.1% to 6.2%.

Table 1.

Distribution of Salmonella Serovars Isolated from Meat Shops at Retail Markets

	Number (%) of each serovar isolated from meat shops in
Serovars	Carcass (116 samples)	Table surface (84 samples)	Sewage effluent 45 samples)	Total (245 samples)
Infantis	16	11	5	32 (33.0)
Anatum	8	5	2	15 (15.5)
Rissen	4	5	3	12 (12.4)
Reading	6	3	2	11 (11.3)
London	4	1	1	6 (6.2)
Agona	3	1	—	4 (4.1)
Emek	3	1	—	4 (4.1)
Typhimurium	2	1	1	4 (4.1)
Newport	1	1	1	3 (3.1)
Derby	2	1	—	3 (3.1)
Enteritidis	2	—	1	3 (3.1)
Total	51	30	16	97 (100)

Antimicrobial resistance

The prevalence of antimicrobial resistance of the Salmonella isolates was shown in Table 2. There was no significant difference between the resistance rates of 14 antimicrobials among three kinds of samples (p>0.05). The highest resistance was sulphonamides (56.7%), followed by ampicillin and tetracycline (48.5%), streptomycin (44.3%), trimethoprim (43.3%), chloramphenicol (42.3%), and nalidixic acid (40.2%). Resistance to gentamicin, neomycin, and kanamycin ranged from 28.9% to 38.1%. None of the isolates were resistant to ceftazidime and norfloxacin. Only four (4.1%) and six (6.2%) of the isolates were resistant to amoxicillin/clavunalic acid and ciprofloxacin, respectively.

Table 2.

Complete and Intermediate Resistance in Salmonella spp. Isolated from Meat Shops

	Carcass (51 isolates)		Table surface (30 isolates)		Sewage effluent (16 isolates)		Total (97 isolates)
Antimicrobials	I, No. (%)	R, No. (%)	I, No. (%)	R, No. (%)	I, No. (%)	R, No. (%)	I, No. (%)	R, No. (%)
A	4 (7.8)	26 (51.0)	0 (0.0)	14 (46.7)	0 (0.0)	7 (43.8)	4 (4.1)	47 (48.5)
Ac	7 (13.7)	3 (5.9)	2 (6.7)	1 (3.3)	1 (6.3)	0 (0.0)	10 (10.3)	4 (4.1)
Cf	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
C	3 (5.9)	21 (41.2)	2 (6.7)	15 (50.0)	1 (6.3)	5 (31.3)	6 (6.2)	41 (42.3)
Ci	5 (9.8)	4 (7.8)	4 (13.3)	2 (6.7)	2 (12.5)	0 (0.0)	11 (11.3)	6 (6.2)
G	2 (3.9)	17 (33.3)	0 (0.0)	7 (23.3)	0 (0.0)	4 (25.0)	2 (2.1)	28 (28.9)
K	4 (7.8)	20 (39.2)	0 (0.0)	14 (46.7)	0 (0.0)	3 (18.8)	4 (4.1)	37 (38.1)
Na	4 (7.8)	21 (41.2)	1 (3.3)	13 (43.3)	1 (6.3)	5 (31.3)	6 (6.2)	39 (40.2)
Ne	3 (5.9)	16 (31.4)	3 (10.0)	10 (33.3)	2 (12.5)	3 (18.8)	8 (8.2)	29 (29.9)
No	5 (9.8)	0 (0.0)	3 (10.0)	0 (0.0)	0 (0.0)	0 (0.0)	8 (8.2)	0 (0.0)
S	1 (2.0)	23 (45.1)	1 (3.3)	14 (46.7)	0 (0.0)	6 (37.5)	2 (2.1)	43 (44.3)
Su	3 (5.9)	31 (60.8)	0 (0.0)	19 (63.3)	0 (0.0)	5 (31.3)	3 (3.1)	55 (56.7)
T	3 (5.9)	30 (58.8)	0 (0.0)	13 (43.3)	0 (0.0)	4 (25.0)	3 (3.1)	47 (48.5)
Tp	2 (3.9)	24 (47.1)	1 (3.3)	15 (50.0)	0 (0.0)	3 (18.8)	3 (3.1)	42 (43.3)

A, ampicillin; Ac, amoxicillin/clavulanic acid; Cf, ceftazidime; C, chloramphenicol; Ci, ciprofloxacin; G, gentamicin; K, kanamycin; Na, nalidixic acid; Ne, neomycin; No, norfloxacin; S, streptomycin; Su, sulphonamides; T, tetracycline; Tp,trimethoprim; R, resistance; I, intermediate.

Resistance to at least one antimicrobial was found in 64 (66.0%) isolates (Table 3). Fifty-five (85.9%) out of the 64 antimicrobial-resistant isolates showed multidrug resistance (MDR). Of which, 20 isolates (31.3%) were resistant to 9–11 antimicrobials. MDR was widespread among the Salmonella serovars, and found frequently in the serovars Typhimurium, Infantis, Anatum, and Rissen.

Table 3.

Antimicrobial Resistance Phenotype of Salmonella Serovars Isolated from Meat Shops

Number of resistance patterns	Serovars	Resistance patterns	Number of resistant antimicrobials
1	Anatum (1), Emek (1), Infantis (2)	Su	1
2	Anatum (1), Infantis (1)	T	1
3	London (1), Reading (2)	AT	2
4	Enteritidis (2)	ASSu	3
5	Newport (1)	ACTG	4
6	Rissen (1)	CTTpNa	4
7	Rissen (2)	ACSuTTp	5
8	Derby (1)	ASuTGNa	5
9	Anatum (1)	ASuTKNe	5
10	Enteritidis (1), Infantis (1), Rissen (1)	ASuTKTp	5
11	Rissen (1)	ATGKNe	5
12	Infantis (1)	CSKNeNa	5
13	Infantis (2)	ASSuKNeTp	6
14	Infantis (1), Rissen (3)	CSSuTTpNa	6
15	Rissen (2)	SuTKNeTpNa	6
16	Anatum (2)	ACSSuGNeNa	7
17	Infantis (1)	ACSSuTGAc	7
18	Infantis (2)	ACSSuTTpNa	7
19	Infantis (1)	ASSuTKNeNa	7
20	Derby (1), Infantis (1)	CSSuKNeTpNa	7
21	Rissen (1)	ACSSuGKTpNa	8
22	Anatum (1), Emek (1)	ACSSuTGKNa	8
23	Anatum (1)	ACSuTGKNeTp	8
24	Infantis (1)	ASSuTKNeTpNa	8
25	Infantis (1)	CSSuTGKNeTp	8
26	Anatum (2)	ACSSuGKNeTpNa	9
27	Infantis (1)	ACSSuGKTpNaAc	9
28	Infantis (1)	ACSSuTGKNeTp	9
29	Agona (2), Reading (2), Typhimurium (1)	ACSSuTGKTpNa	9
30	Derby (1), Typhimurium (1)	ACSSuTGTpNaAc	9
31	Infantis (1), London (1), Typhimurium (1)	ACSSuTKNeTpNa	9
32	Emek (1), Infantis (4), Typhimurium (1)	ACSSuTGKNeTpCiNa	11

The abbreviations of antimicrobials are similar to those in Table 2.

Distribution and prevalence of resistance genes

The distribution and prevalence of resistance genes among the Salmonella serovars were shown in Table 4. Thirteen (bla _TEM , bla _OXA-1 , aadA1, sul1, tetA, tetB, tetG, cmlA1, floR, dfrA1, dfrA12, aac(3)-IV, and aphA1-1ab) out of 17 investigated resistance genes were detected. Among the 51 ampicillin-resistant isolates, the bla _TEM and bla _OXA-1 genes were detected in 38 (74.5%) and eight (15.7%) isolates, respectively. Of the 50 tetracycline-resistant isolates, 37 (74.0%) were positive for tetA, 13 (26.0%) for tetG, and three (6.0%) for tetB; of these, eight (16.0%) carried both the tetA and tetG genes. The sul1 gene was detected in 52 (89.7%) out of the 58 sulphonamides-resistant isolates. No aadA2 gene was found in the 45 streptomycin-resistant isolates; instead, aadA1 gene was found in 44 (97.8%) of the resistant isolates. Among the 41 kanamycin-resistant isolates, 39 (95.1%) were positive for the aphA1-Iab gene. Of the 30 gentamicin-resistant isolates, 27 (90.0%) carried the aac(3)-IV gene. The catA1 gene was not detected in the 47 chloramphenicol-resistant isolates, whereas the cmlA1 and floR genes were detected in 29 (61.7%) and 36 (76.6%) of the isolates, respectively. Among the 45 trimethoprim-resistant isolates, 39 (86.7%) and nine (20%) of the isolates were positive for dfrA1 and dfrA12, respectively.

Table 4.

Distribution and Prevalence of Resistance Genes Among the Salmonella Serovars

Antimicrobial resistance genes (number of isolates tested)	Number of positive isolates (%)	Antimicrobial resistance genes belong to serovars (number of positive isolates)
Ampicillin (51)
bla _TEM	38 (74.5)	Agona (2); Anatum (7); Derby (1), Emek (1); Enteritidis (1); Infantis (12); London (2); Newport (1); Reading (4); Rissen (4); Typhimurium (3)
bla _OXA-1	8 (15.7)	Emek (1); Enteritidis (2); Infantis (3); Reading (2)
bla _TEM + bla _OXA-1	2 (3.9)	Reading (2)
At least one gene	44 (86.3)
Chloramphenicol (47)
cmlA1	29 (61.7)	Agona (2); Anatum (5); Derby (2); Emek (1); Infantis (11); Newport (1); Reading (2); Rissen (2); Typhimurium (3)
floR	36 (76.6)	Agona (2); Anatum (6); Derby (1); Emek (2); Infantis (11), London (1), Newport (1), Reading (2), Rissen (6); Typhimurium (4)
cmlA1 + floR	24 (51.1)	Agona (2); Anatum (5); Derby (1); Emek (1); Infantis (8); Newport (1); Reading (2); Rissen (1); Typhimurium (3)
At least one gene	41 (87.2)
Gentamycin (30)
aac(3)-IV	27 (90.0)	Agona (2); Anatum (5); Derby (2); Emek (1); Infantis (9), Newport (1); Reading (2); Rissen (2); Typhimurium (3)
Kanamicin (41)
aphA1-1AB	39 (95.1)	Agona (2); Anatum (7); Derby (1); Infantis (15); London (1); Reading (4); Rissen (5); Typhimurium (4)
Steptomycin (45)
aadA1	44 (97.8)	Agona (2); Anatum (6); Derby (2); Emek (2); Enteritidis (2); Infantis (18); London (1); Reading (2); Rissen (5); Typhimurium (4)
Suphonamides (58)
sul 1	52 (89.7)	Agona (2); Anatum (7); Derby (3); Emek (3); Enteritidis (3); Infantis (20); Reading (2); Rissen (9); Typhimurium (4)
Tetracycline (50)
tetA	37 (74.0)	Agona (2); Anatum (3); Derby (2); Emek (2); Enteritidis (1); Infantis (11); London (1); Reading (4); Rissen (7); Typhimurium (4)
tetB	3 (6.0)	Infantis (2); Rissen (1)
tetG	13 (26.0)	Anatum (1) ; Infantis (3) ; London (1) ; Newport (1) ; Rissen (4) ; Typhimurium (3)
tetA + tetG	8 (16.0)	Infantis (2); Rissen (3); Typhimurium (3)
At least one gene	45 (90.0)
Trimethoprim (45)
dfrA1	39 (86.7)	Agona (2); Anatum (3); Derby (1); Emek (1); Enteritidis (1); Infantis (16); London (1); Reading (2); Rissen (8); Typhimurium (4)
dfrA12	9 (20.0)	Derby (1); Emek (1); Infantis (6); Rissen (1)
dfrA1 + dfrA12	7 (15.6)	Emek (1); Infantis (6)
At least one gene	41 (91.1)

Discussion

In this study, 11 Salmonella serovars were identified. Interestingly, although Salmonella Infantis was not reported in previous studies in Vietnam (Vo et al., 2006; Van et al., 2007), it was the most common serovar in this study. This serovar was detected in several European countries (Galanis et al., 2006; Miller et al., 2010), and the United States (Heithoff el al., 2008). This suggests that Salmonella Infantis may cause public health concerns worldwide. We observed that Salmonella Rissen and Anatum were frequently detected in pork and chicken meat shops. These serovars have been reported in both human and non-human sources in Asia (Bangtrakulnonth et al., 2004; Galanis et al., 2006) and in Vietnam (Vo et al., 2006; Van et al., 2007). In addition, the serovars Typhimurium, Enteritidis, Derby, and Newport, which were previously associated with human foodborne disease in Asian countries (Bangtrakulnonth et al., 2004; Galanis et al., 2006) and in the United States (CDC, 2008), were also detected in this study. Therefore, they may create public health concerns in Vietnam, as non-typhoidal Salmonella spp. is a zoonotic agent and could be transmitted through foods of animal origin.

This study demonstrated the high incidence of resistance to sulphonamides, tetracycline, ampicillin, chloramphenicol, streptomycin, and trimethoprim in Salmonella isolates. These findings were comparable to those in previous reports from Vietnam (Van et al., 2007; Vo et al., 2010), China (Yan et al., 2010; Yang et al., 2010), and Thailand (Wannaprasat et al., 2011). The high resistance to nalidixic acid in Salmonella isolates observed in this study was consistent with that in Thailand (Padungtod and Kaneene, 2006) and Vietnam (Van et al., 2007; Vo et al., 2010). This could suggest that these antimicrobials are widely used in animal husbandry in many countries. The resistance rate in the Salmonella isolates against gentamicin and kanamicin in this study was higher than those in other Asian countries (Benacer et al., 2010; Wannaprasat et al., 2011). The explanation may be that these antimicrobials were more frequently used in animal husbandry in recent years, after other antimicrobials were prohibited (MARD, 2009). In this study, there were no Salmonella isolates resistant to ceftazidime, similar to the previous report in South Vietnam (Vo et al., 2010). However, other reports described the reduction in susceptibility to this antimicrobial in Salmonella strains from food products in China (Yang et al., 2010), and from veterinary and human sources in Morocco (Bouchrif et al., 2009). Moreover, MDR Salmonella spp. was also found frequently in this study, similar to that in South Vietnam (Van et al., 2007; Vo et al., 2010), China (Yan et al., 2010; Yang et al., 2010), and Thailand (Wannaprasat et al., 2011). This may create challenges in the treatment of Salmonella infections in humans and animals.

In this study, the sul1 gene was commonly present in the sulphonamide-resistant isolates, which was also demonstrated in reports from Germany (Miko et al., 2005). The genes encoding for resistance to ampicillin (bla _TEM) and streptomycin (aadA1), frequently detected in the isolates, were observed in previous reports (Chen et al., 2004; Miko et al., 2005, Shahada et al., 2006). Similar to what was found in previous studies (Hamada et al., 2005; Miko et al., 2005), the mechanism for kanamycin resistance in Salmonella isolates was mainly encoded by aphA1-IAB gene. However, in Japan, the frequency of this gene was lower in resistant strains of Salmonella Infantis isolated from chicken (Shahara et al., 2006). Our results showed that resistance to gentamycin and trimethoprim was mainly mediated by the aac(3)-IV and dfrA1 genes. These genes may play important roles for resistance to these antimicrobials of Salmonella in Vietnam. The cmlA1 and floR genes were frequently detected in the chloramphenicol-resistant isolates. However, the molecular study of chloramphenicol resistance has received little attention so far, due to the limited usage in human and a ban on its use in animal husbandry (Fluit et al., 2001). In this study, resistance to tetracycline was mainly mediated by the tetA gene, consistent with results in previous reports (Asai et al., 2006; Chuanchuen and Padungtod., 2009). These findings are not surprising even though Salmonella isolates are often found to carry tetA, tetB, tetC, tetD, and tetE genes (Michael et al., 2006).

In summary, Salmonella contamination was common at retail meat shops in North Vietnam. The Salmonella isolates were resistant to multiple antimicrobials, and resistance genes were widespread among the serovars isolated. This problem should be closely monitored to minimize further health impacts in Vietnam.

Footnotes

Acknowledgments

We would like to thank the students, technicians, butchers, and other individuals who helped us in sampling and processing. We also thank the staff of the Department of Veterinary Hygiene, National Institute of Veterinary Research, Hanoi, Vietnam for their technical assistance with serovar identification. This study was supported by the TRIG project of Hanoi Agricultural University, Gia Lam, Hanoi, Vietnam.

Disclosure Statement

No competing financial interests exist.

References

Angulo

, Johnson

, Tauxe

, Cohen

. Origins and consequences of antimicrobial-resistant non-typhoidal Salmonella: Implications for the use of fluoroquinolones in food animals. Microb Drug Resist, 2000; 6:77–83.

Angulo

, Nargund

, Chiller

. Evidence of an association between use of antimicrobial agents in food animals and antimicrobial resistance among bacteria isolated from humans and the human health consequences of such resistance. J Vet Med B Infect Dis Vet Public Health, 2004; 51:374–379.

Asai

, Itagaki

, Shiroki

, Yamada

, Tokoro

, Kojima

, Ishihara

, Esaki

, Tamura

, Takahashi

. Antimicrobial resistance types and genes in Salmonella enterica Infantis isolates from retail raw chicken meat and broiler chickens on farms. J Food Prot, 2006; 69:214–216.

Bangtrakulnonth

, Pornreongwong

, Pulsrikarn

, Sawanpanyalert

, Hendriksen

, Lo-Fo-Wong

, Aarestrup

. Salmonella serovars from humans and other sources in Thailand, 1993–2002. Emerg Infect Dis, 2004; 10:131–136.

Benacer

, Thong

, Watanabe

, Puthucheary

. Characterization of drug resistant Salmonella enterica serotype Typhimurium by antibiograms, plasmids, integrons, resistance genes and PFGE. J Microbiol Biotech, 2010; 20:1042–1052.

Bouchrif

, Le

Hello S

, Pardos

, Karraouan

, Perrier-Gros-Claude

, Ennaji

, Timinouni

, Weill

. Ceftazidime-resistant Salmonella enterica, Morocco. Emerg Infect Dis, 2009; 15:1693–1695.

Chaslus-Dancla

, Pohl

, Meurisse

, Marin

, Lafont

. High genetic homology between plasmids of human and animal origins conferring resistance to the aminoglycosides gentamicin and apramycin. Antimicrob Agents Chemother, 1991; 35:590–593.

Chen

, Zhao

, White

, Schroeder

, Lu

, Yang

, McDermott

, Ayers

, Meng

. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol, 2004; 70:1–7.

Chuanchuen

, Padungtod

. Antimicrobial resistance genes in Salmonella enterica isolates from poultry and swine in Thailand. J Vet Med Sci, 2009; 71:1349–1355.

10.

[CDC] Centers for Disease Control Prevention. Salmonella Surveillance: Annual Summary, 2006. Atlanta: CDC, 2008.

11.

[CLSI] Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard, 10thCLSI Document M02-A9Wayne, PA: CLSI, 2006.

12.

[CLSI] Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twentieth Informational SupplementCLSI Document M100-S20Wayne, PA: CLSI, 2010.

13.

Fluit

, Visser

, Schmitz

. Molecular detection of antimicrobial resistance. Clin Microbiol Rev, 2001; 14:836–871.

14.

Frana

, Carlson

, Griffith

. Relative distribution and conservation of genes encoding aminoglycoside-modifying enzymes in Salmonella enterica serotype Typhimurium phage type DT104. Appl Environ Microbiol, 2001; 67:445–448.

15.

Galanis

, Lo Fo Wong

, Patrick

, Binsztein

, Cieslik

, Chalermchikit

, Aidara-Kane

, Ellis

, Angulo

, Wegener

. Web-based surveillance and global Salmonella distribution, 2000–2002. Emerg Infect Dis, 2006; 12:381–388.

16.

Grimont

PAD

, Weill

. Antigenic formulas of the Salmonella serovars, 9th. WHO Collaborating Center for Reference and Research on Salmonella: Paris, 2007.

17.

Guerra

, Junker

, Miko

, Helmuth

, Mendoza

. Characterization and localization of drug resistance determinants in multi-resistant, integron carrying Salmonella enterica serotype Typhimurium strains. Microb Drug Resist, 2004; 10:83–91.

18.

Harley

, Prescott

. Laboratory Exercises in Microbiology, 5th. New York: McGraw–Hill, 2002.

19.

Hamada

, Tsuji

, Oshima

. Identification and characterization of transferable integron-mediated antibiotic resistance among Salmonella serovar Typhimurium and Salmonella serovar Infantis isolates from 1991 to 2002. Jpn J Infect Dis, 2001; 55:135–138.

20.

Heithoff

, Shimp

, Lau

, Badi

, Enioutina

, Daynes

, Byrne

, House

, Mahan

. Human Salmonella clinical isolates distinct from those of animal origin. Appl Environ Microbiol, 2008; 74:1757–1766.

21.

[MARD] Ministry of Agriculture Rural Development. Circular: To promulgate the list of drugs, chemicals, antibiotics banned for uses, limited to use in veterinary and aquacultureNo. 15/2009/TT-BNNHanoi: Ministry of Agriculture and Rural Development, 2009(In Vietnamese.)

22.

Michael

, Butaye

, Cloeckaert

, Schwarz

. Genes and mutations conferring antimicrobial resistance in Salmonella: An update. Microbes Infect, 2006; 8:1898–1914.

23.

Miko

, Pries

, Schroeter

, Helmuth

. Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. J Antimicrob Chemother, 2005; 56:1025–1033.

24.

Miller

, Prager

, Rabsch

, Fehlhaber

, Voss

. Epidemiological relationship between Salmonella infantis isolates of human and broiler origin. Lohmann Information, 2010; 45:27–31.

25.

L-K

, Mulvey

, Martin

, Peters

, Johnson

. Genetic characterization of antimicrobial resistance in Canadian isolates of Salmonella serovar Typhimurium DT104. Antimicrob Agents Chemother, 1999; 43:3018–3021.

26.

Ogasawara

, Tran

, Ly

, Nguyen

, Iwata

, Okatani

, Watanabe

, Taniguchi

, Hirota

, Hayashidani

. Antimicrobial susceptibilities of Salmonella from domestic animals, food and human in the Mekong Delta, Vietnam. J Vet Med Sci, 2008; 70:1159–1164.

27.

Padungtod

, Kaneene

. Salmonella in food animals and humans in northern Thailand. Int J Food Microbiol, 2006; 108:346–354.

28.

Shahada

, Takehisa

, Takayuki

, Karoku

, Masuo

, Kozo

. Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovar Infantis from poultry in Kagoshima, Japan. Int J Antimicrob Agents, 2006; 28:302–307.

29.

Tollefson

, Miller

. Antibiotic use in food animals: Controlling the human health impact. J AOAC Int, 2000; 83:245–254.

30.

Van

TTH

, Moutafis

, Istivan

, Tran

, Coloe

. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl Environ Microbiol, 2007; 73:6885–6890.

31.

ATT

, van Duijkeren

, Fluit

, Heck

, Verbruggen

, Maas

, Gaastra

. Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella Typhimurium phage type 90. Vet Microbiol, 2006; 113:153–158.

32.

ATT

, van Duijkeren

, Gaastra

, Fluit

. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One, 2010; 5:e9440.

33.

Yan

, Li

, Alam

, Shinoda

, Miyoshi

, Shi

. Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol, 2010; 143:230–234.

34.

Yang

, Qu

, Zhang

, Shen

, Cui

, Shi

, Xi

, Sheng

, Zhi

, Meng

. Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. Int J Food Microbiol, 2010; 141:63–72.

35.

Wannaprasat

, Padungtod

, Chuanchuen

. Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans. Int J Antimicrob Agents, 2011; 37:457–461.