Prevalence and Antimicrobial Resistance of Salmonella in Pork,Chicken,and Duck from Retail Markets of China

Abstract

Salmonella is one of the most important foodborne pathogens associated with animal and human diseases. In this study, 672 samples of fresh meat (pork, 347; chicken, 196; and duck, 129) were collected from retail markets in different provinces of China from 2010 to 2014. We identified 10 different serotypes among 80 Salmonella isolates, whereas 12 isolates were nonmotile precluding conventional identification of complete serotype. Among these 92 isolates, Salmonella enterica serovar Derby (n = 21) was the most prevalent serotype, followed by Salmonella Enteritidis (n = 17), Salmonella Typhimurium (n = 15), Salmonella Indiana (n = 9), Salmonella Agona (n = 7), and Salmonella Assinie (n = 5). Antimicrobial resistance testing for 18 antimicrobial agents revealed that all 92 isolates were resistant to at least 1 antimicrobial agent, and 39 different resistance profiles were identified. The highest resistance was to trimethoprim–sulfamethoxazole (n = 87), followed by tetracycline (n = 51), carbenicillin (n = 38), amoxicillin/A.clav (n = 30), and piperacillin (n = 24). Our results demonstrated that meats presented a potential public health risk, thereby underlining the necessity for local regulatory enforcement agencies in China to monitor salmonellosis.

Introduction

S almonella is one of the most important foodborne pathogens worldwide and causes severe public health problems and economic losses (Handeland et al., 2002). Meat products are the most commonly reported vehicles of foodborne pathogens, and the presence of Salmonella in these products is a significant food safety risk (Akbar et al., 2013). Pork, chicken, and duck meats are sold in public markets and are traditional staple food in China. Thus, understanding of the prevalence and antimicrobial resistance of Salmonella in markets can provide data used for guiding surveillance and controlling activities. One strategy is enhanced biosecurity to avoid food-to-human transmission.

The contamination and antimicrobial resistance of Salmonella isolated from food-producing animals are particularly severe in China (Yang et al., 2011; Li et al., 2013b; Kuang et al., 2015; Ren et al., 2016). Moreover, meats remain an important source of human Salmonella infections in Canada and the United States (Ray et al., 2007; Imanishi et al., 2014; Sanchez-Maldonado et al., 2017). Indeed, the emergence of multidrug-resistant (MDR) Salmonella strains is a new and great threat to public health (Ma et al., 2017). MDR between Salmonella strains is frequently isolated from food sources, and infections due to MDR Salmonella can increase instances of morbidity and mortality (Song et al., 2018).

In this study, we investigated the presence of Salmonella in pork, chicken, and duck samples from retail markets in the southern and northern areas of the Yangtze River (hereafter denoted as Yangtze). We then analyzed the antimicrobial resistance of Salmonella isolates and evaluated the risk of transmission of salmonellosis through food chains. Our findings can provide information on the prevalence and antimicrobial resistance of Salmonella in meat products and can thus help curb Salmonella contamination problems in China.

Materials and Methods

Sample collection

Between 2010 and 2014, meat samples were obtained from eight provinces. Three provinces (Guangdong, Jiangxi, and Hunan) were located south of the Yangtze, and five (Liaoning, Heilongjiang, Jilin, Gansu, and Ningxia) were located in the north. Based on the sampling plan, four to five cities were selected per province, two to three markets per city, three retail stalls per market, and two samples per stall. A total of 230 samples were collected north of the Yangtze and 442 samples were collected in the south. Samples of pork (n = 347), chicken (n = 196), and duck (n = 129) were randomly collected from retail markets using sterile gloves and transferred into sterile bags to avoid cross-contamination. Samples were stored in an icebox and immediately transferred to the laboratory for analysis.

Bacterial isolation

All samples were analyzed according to the National Standard GB/T 4789.4. In a typical procedure, 25 ± 0.5 g of each meat was aseptically weighed, transferred into 225 mL of buffered peptone water (Beijing Land Bridge, Beijing, China), and incubated at 37°C for 18 h. Then, 1 mL of the cultures was subcultured in 10 mL of selenite cystine broth (Beijing Land Bridge) at 37°C for 24 h. One loopful of each broth culture was streaked onto BS and Hektoen agar plates (Beijing Land Bridge) and incubated at 37°C for 24–48 h. Biochemical tests of suspected colonies were conducted using API ID 32E test kits following the manufacturer's recommendations (BioMérieux, Marcy-L'Étoile, France).

Serotyping

All Salmonella isolates were serotyped by slide agglutination using polyvalent O- and H- antisera (BD, Franklin Lakes) in accordance with the Kauffmann–White scheme (Issenhuth-Jeanjean et al., 2014).

Antimicrobial susceptibility testing

Antimicrobial susceptibility tests were performed on Mueller–Hinton agar plates according to the Clinical and Laboratory Standards Institute (CLSI) guidelines (CLSI, 2013) with 18 antimicrobial agents selected for ATB^® G-5 (BioMérieux, Marcy-L'Étoile, France) used in humans. The corresponding disk concentrations were as follows: meropenem (MER; 10 μg), streptomycin (STR;10 μg), gentamycin (10 μg), amikacin (10 μg), tobramycin (10 μg), trimethoprim–sulfamethoxazole (SXT; 23.75/1.25 μg), ciprofloxacin (CIP; 5 μg), amoxicillin–clavulanic acid (AMC; 20/10 μg), carbenicillin (CB; 100 μg), piperacillin (PIC; 100 μg), ticarcillin–clavulanate (TCC; 75/10 μg), tetracycline (TET; 30 μg), imipenem (IMI; 10 μg), cefuroxime (30 μg), ceftazidime (30 μg), cephalothin (30 μg), kanamycin (30 μg), and cefoxitin (30 μg). Resistance breakpoints were defined by the CLSI. Results were identified as susceptible (S), intermediate (I), or resistant (R). Escherichia coli ATCC 25922 was used as the quality control strain according to CLSI guidelines.

Results

Prevalence of Salmonella in China

Salmonella was recovered from 13.7% (92/672) of the tested samples. Overall, the prevalence of Salmonella in pork was 14.1% (49/347) with Salmonella recovered from 12.2% (10/82) of samples collected north of the Yangtze and 14.7% (39/265) of samples collected in the south. The overall prevalence of Salmonella in chicken and duck was 14.3% (28/196) and 11.6% (15/129), respectively. Salmonella was recovered from 14.9% (22/148) of chicken samples collected north of the Yangtze and 12.5% (6/48) of chicken samples collected in the south (Table 1).

Table 1.

Prevalence of Salmonella from Pork, Chicken, and Duck to the North and South of Yangtze River in China

Meat category	Northern (positive samples/total)	Southern (positive samples/total) ^a	Total (positive samples/total)
Pork	10/82	39/265	49/347
Chicken	22/148	6/48	28/196
Duck	—	15/129	15/129
Total	32/230	60/442	92/672

One Salmonella isolate was collected from each positive sample.

Distribution of Salmonella serotype

A total of 80 isolates were divided into 10 distinct serotypes, whereas 12 isolates were nonmotile precluding conventional identification of complete serotype (Table 2). The predominant serotypes were Salmonella enterica serovar Derby (n = 21), followed by Salmonella Enteritidis (n = 17) and Salmonella Typhimurium (n = 15). Salmonella Derby and Salmonella Typhimurium were isolated most frequently in pork, whereas Salmonella Enteritidis (n = 13) and Salmonella Indiana (n = 9) were the major serotypes in chicken. In duck, Salmonella Enteritidis (n = 4), Salmonella Agona (n = 5), and group C (n = 6) were identified. The detection rate of Salmonella Derby in pork was higher in areas south of the Yangtze (n = 20) than in areas to the north (n = 1). In chicken, 12 Salmonella Enteritidis strains were isolated from the areas north of the Yangtze, but none was isolated from the areas to the south.

Table 2.

Serotyping of Salmonella Isolates from Pork, Chicken, and Duck in Northern and Southern China

		No. in Pork		No. in Chicken
Group	Serotype	North	South	North	South	No. in Duck	Total no. (%)
C	NA	—	2	—	1	6	Total no. (%)	9 (9.8)
C1	Rissen	—	1	—	—	—	1 (1.1)
E1	NA	—	3		—	—	3 (3.3)
E1	Assinie	—	4	—	1	—	5 (5.4)
B	Agona	—	1	—	1	5	7 (7.6)
	Heidelberg	1	—	—	2	—	3 (3.3)
	Indiana	—	—	8	1	—	9 (9.8)
	Typhimurium	7	6	2	—	—	15 (16.3)
D	Enteritidis	1	—	12	—	4	17 (18.5)
	Derby	1	20	—	—	—	21 (22.8)
	London	—	1	—	—	—	1 (1.1)
	Newlands	—	1	—	—	—	1 (1.1)
	Total (%)	10	39	22	6	15	92

Antimicrobial susceptibility of isolated Salmonella

The antimicrobial susceptibility of all isolates is shown in Tables 3 and 4. All isolates showed resistance to one or more of the tested antimicrobials. Most isolates were resistant to SXT (n = 87), followed by TET (n = 51), CB (n = 38), AMC (n = 30), STR (n = 25), and PIC (n = 24). Resistance to cephem was observed in 60.1% (17/28) of isolates from chicken, 13.3% (2/15) from duck, and 2% (1/49) from pork. Resistance to CIP was also observed in 35.7% (10/28) of isolates from chicken, 0% (0/49) from pork, and 0% (0/15) from duck.

Table 3.

Antimicrobial Resistance Phenotypes of 92 Salmonella Isolates

	No. of resistant isolates
Antimicrobial agent	Pork (n = 49) ^a	Chicken (n = 28)	Duck (n = 15)	Total (n = 92)
Aminoglycosides
AMI	0	5	0	5
KAN	8	6	0	14
TOD	9	7	0	16
GEN	10	7	0	17
STR	11	12	2	25
β-lactams
TCC	1	1	2	4
AMC	11	14	5	30
Carbactams
MER	2	1	0	3
IMI	6	7	1	14
Cephems
CXT	0	0	1	1
CAZ	0	2	0	2
CFT	0	7	1	8
CXM	1	8	0	9
Folate pathway inhibitors
SXT	45	27	15	87
Penicillins
PIC	6	14	4	24
CB	14	19	5	38
Fluoroquinolones
CIP	0	10	0	10
TETs
TET	32	13	6	51

n, number of Salmonella-positive isolates tested.

AMI, amikacin; KAN, kanamycin; TOD, tobramycin; GEN, gentamycin; STR, streptomycin; TCC, ticarcillin–clavulanic acid; AMC, amoxicillin–clavulanic acid; MER, meropenem; IMI, imipenem; CXT, cefoxitin; CAZ, ceftazidime; CFT, cephalothin; CXM, cefuroxime; SXT, trimethoprim–sulfamethoxazole; PIC, piperacillin; CB, carbenicillin; CIP, ciprofloxacin; TET, tetracycline.

Table 4.

Diversity Profiles of Salmonella Isolates Based on Serotyping and Antimicrobial Resistance

	Serotype (no.)
Antimicrobial resistance profiles														No.	Pork (n = 49)	Chicken (n = 28)	Duck (n = 15)
GEN														1	Typhimurium (1)
SXT														30	Typhimurium (2), Enteritidis (1), Assinie (1), Derby(3), Heidelberg (1), Newlands (1), Rissen (1), Agona (1), group E1 (2)	Agona (1), Enteritidis (8)	Agona (5), group C (2), Enteritidis (1)
CB	SXT													1		Typhimurium (1)
IMI	SXT													1			Enteritidis (1)
IMI	TET													1	Group E1 (1)
SXT	TET													16	Assinie (3), Derby (13)
CB	PIC	SXT												1		Enteritidis (1)
CB	STR	TET												2		Assinie (1), group C (1)
IMI	MER	SXT
IMI	SXT	TET												1	Typhimurium (1)
STR	SXT	TET												1			Group C (1)
STR	SXT	TET												1	Group C (1)
AMC	CB	PIC	TET											1	Derby (1)
AMC	CB	PIC	SXT											1		Heidelberg (1)
AMC	CB	STR	TET											1	Typhimurium (1)
CB	IMI	SXT	TET											1	Derby (1)
CB	STR	SXT	TET											2	Derby (2)
CB	STR	SXT	TET											1	Typhimurium (1)
AMC	CB	PIC	SXT	TET										1			Group C (1)
AMC	CB	IMI	PIC	SXT										1		Enteritidis (1)
AMC	CB	CFT	CXT	SXT										1			Enteritidis (1)
AMC	CB	PIC	SXT	TCC										1		Heidelberg (1)
CB	CIP	STR	SXT	TET										1		Typhimurium (1)
IMI	MER	STR	SXT	TET										1	Derby (1)
AMC	CB	PIC	SXT	TCC	TET									2			Group C (2)
AMC	CB	IMI	PIC	STR	SXT									1		Enteritidis (1)
AMC	CB	GEN	KAN	SXT	TOD									2	Typhimurium (2)
AMC	PIC	PIC	STR	SXT	TET									1		Enteritidis (1)
AMC	PIC	PIC	STR	SXT	TET									1			Enteritidis (1)
AMC	CB	CIP	GEN	IMI	SXT	TOD								1		Indiana (1)
AMC	CB	GEN	KAN	SXT	TET	TOD								1	Typhimurium (1)
AMC	CB	GEN	PIC	STR	SXT	TET	TOD							1	London (1)
AMC	CB	GEN	KAN	PIC	STR	SXT	TET	TOD						4	Typhimurium (3), Derby (1)
AMC	CB	CIP	IMI	KAN	PIC	STR	SXT	TET						1		Indiana (1)
AMC	CB	CXM	GEN	IMI	KAN	STR	SXT	TET	TOD					1	Typhimurium (1)
AMC	CAZ	CB	CFT	CIP	CXM	KAN	PIC	STR	SXT	TET				1		Indiana (1)
AMC	CB	CIP	CXM	GEN	IMI	KAN	MER	PIC	STR	SXT	TOD			1		Indiana (1)
AMC	AMI	CB	CFT	CIP	CXM	GEN	KAN	PIC	STR	SXT	TET	TOD		3		Indiana (3)
AMC	AMI	CB	CFT	CIP	CXM	GEN	IMI	KAN	PIC	STR	SXT	TET	TOD	2		Indiana (2)

Antimicrobial susceptibility tests resulted in a total of 39 resistance profiles (Table 4). Salmonella Newlands, Salmonella Rissen, and Salmonella Agona were resistant to 1 antimicrobial agent; Salmonella Enteritidis (n = 7) to 2–6 antimicrobial agents; Salmonella Derby (n = 8) to 2–9 agents; Salmonella Typhimurium (n = 12) to 2–10 agents; and Salmonella Indiana (n = 9) to 7–14 agents. Among the three different meat species, the rate of isolates resistant to three or more antimicrobial agents was 64.3% (18/28) from chicken, 40.0% (6/15) from duck, and 36.7% (18/49) from pork.

Discussion

Monitoring the presence of foodborne pathogens in foods is the primary tool for implementing food safety systems. Our study revealed that the prevalence of Salmonella contamination had no significant difference among pork (14.1%), chicken (14.3%), and duck (11.6%), similar to the findings of a previous study conducted in the Jiangsu province (Li et al., 2014) but lower than those reported by a study in the Sichuan province (Ma et al., 2017) in China. The Salmonella serotypes identified in this study were diverse, that is, 80 isolates belonged to 10 different serotypes, whereas 12 isolates were nonmotile precluding conventional identification of complete serotype (Table 2). Salmonella Derby (n = 21) and Salmonella Typhimurium (n = 13) were the most prevalent serotypes isolated from pork, consistent with previous reports (Li et al., 2014; Lin et al., 2014; Bai et al., 2015; Terentjeva et al., 2017), Salmonella Rissen, Salmonella Assinie, Salmonella Agona, Salmonella London, Salmonella Newlands, group C, group C1, and group E1 were isolated from the south but not from the north. In chicken, Salmonella Enteritidis (n = 12) and Salmonella Indiana (n = 8) were the most popular serotypes, and the high isolation rates of Salmonella Enteritidis in chicken were consistent with previous studies (Bai et al., 2015; Li et al., 2017). Salmonella Assinie, Salmonella Agona, Salmonella Heidelberg, and group C were isolated from chicken in the south but not in the north. More serotypes were detected in pork and chicken south of the Yangtze, which indicated a wider diversity of serotypes in this area possibly due to the rapid animal product circulation. In duck, Salmonella Agona (n = 5), Salmonella Enteritidis (n = 4), and group C (n = 6) were isolated, and these results were inconsistent with previous reports (Tran et al., 2004; Tsai and Hsiang, 2005; Li et al., 2013a), possibly due to the regional variation of Salmonella.

The extensive use of antimicrobial in human and livestock leads to higher exposure to these compounds and consequently promotes the increase in antimicrobial resistance in Salmonella (Cruchaga et al., 2001; Antunes et al., 2003; Angkititrakul et al., 2005). In our study, 92 (100%) isolates were resistant to at least one antimicrobial agent, which was much higher than a previous report in Algeria, Senegal, and Vietnam (Stevens et al., 2006; Van et al., 2007; Elgroud et al., 2009). Higher degrees of resistance to SXT (87/92) and TET (51/92) were found, that is, the percentage of resistance to SXT in pork, chicken, and duck was 91.8% (45/49), 96.4% (27/28), and 100% (15/15), and the percentage of resistance to TET in pork, chicken, and duck was 65.3% (32/49), 64.4% (13/28), and 40% (6/15), respectively. These results indicated that farmers should reduce their use of SXT and TET to ensure their effectiveness in treating human infections and limit selective pressure, which drives resistance in an array of organisms.

The antimicrobial resistance profiles differed among serotypes. A total of 42 isolates were resistant to 3 or more antimicrobials, including 77.8% (7/9) in Salmonella Indiana, 66.7% (10/15) in Salmonella Typhimurium, 29.4% (5/17) in Salmonella Enteritidis, and 28.6% (6/21) in Salmonella Derby. Salmonella Indiana displayed resistance to the largest number of tested antimicrobials (including five isolates exhibiting resistance to IMI and/or MER). This degree of resistance is consistent with previous reports (Lu et al., 2011; Moe et al., 2017). In this study, resistance appeared to vary by serovar, and MDR Salmonella was isolated in higher numbers from chicken than from pork and duck. Apparently, serovars circulating in poultry environment were more resistant than serovars circulating in pig and duck farms, possibly due to differences in antimicrobial usage between chicken and pork farms. These findings highlighted the enormous challenges associated with the treatment of Salmonella infections in humans and animals and the importance of implementing legislation about antimicrobial use by authorities in China. Therefore, more investigations should be conducted and the antimicrobial resistance of foodborne pathogens from extensive sources should be continuously monitored.

Conclusion

We examined Salmonella contamination in fresh meat, provided data for foodborne pathogen risk assessment, and elucidated the differences in Salmonella distribution and antimicrobial susceptibility to control the significant threat of clinical Salmonella infection in humans and animals. Our results indicated a need to further investigate the prevalence and antimicrobial susceptibility pattern of Salmonella by considering it a potential foodborne pathogen from farm to table.

Footnotes

Acknowledgments

This work was supported by the Science and Technology Support Program of Jiangxi Province (Grant No. 20142BBF60019) and the Primary Research & Development Program of Jiangxi Province (Grant No. 20171BBF60053).

Disclosure Statement

No competing financial interests exist.

References

Akbar

, Anal

, Ansari

. Prevalence and antibiogram study of Salmonella and Staphylococcus aureus in poultry meat. Asian Pac J Trop Biomed, 2013; 3:163–168.

Angkititrakul

, Chomvarin

, Chaita

, Kanistanon

, Waethewutajarn

. Epidemiology of antimicrobial resistance in Salmonella isolated from pork, chicken meat and humans in Thailand. Southeast Asian J Trop Med Public Health, 2005; 36:1510–1515.

Antunes

, Reu

, Sousa

, Peixe

, Pestana

. Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. Int J Food Microbiol, 2003; 82:97–103.

Bai

, Lan

, Zhang

, et al. Prevalence of Salmonella isolates from chicken and pig slaughterhouses and emergence of ciprofloxacin and cefotaxime co-resistant S. enterica Serovar Indiana in Henan, China. PLoS One, 2015; 10:e0144532.

Cruchaga

, Echeita

, Aladuena

, Garcia-Pena

, Frias

, Usera

. Antimicrobial resistance in salmonellae from humans, food and animals in Spain in 1998. J Antimicrob Chemother, 2001; 47:315–321.

Elgroud

, Zerdoumi

, Benazzouz

, et al. Characteristics of Salmonella contamination of broilers and slaughterhouses in the region of Constantine (Algeria). Zoonoses Public Health, 2009; 56:84–93.

Handeland

, Refsum

, Johansen

, et al. Prevalence of Salmonella typhimurium infection in Norwegian hedgehog populations associated with two human disease outbreaks. Epidemiol Infect, 2002; 128:523–527.

Imanishi

, Rotstein

, Reimschuessel

, et al. Outbreak of Salmonella enterica serotype Infantis infection in humans linked to dry dog food in the United States and Canada, 2012. J Am Vet Med Assoc, 2014; 244:545–553.

Issenhuth-Jeanjean

, Roggentin

, Mikoleit

, et al. Supplement 2008–2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res Microbiol, 2014; 165:526–530.

10.

Kuang

, Hao

, Dai

, et al. Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front Microbiol, 2015; 6:602.

11.

, Lai

, Wang

, et al. Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China. Int J Food Microbiol, 2013a;163:14–18.

12.

, Zhou

, Miao

. Prevalence and antibiotic resistance of non-typhoidal Salmonella isolated from raw chicken carcasses of commercial broilers and spent hens in Tai'an, China. Front Microbiol, 2017; 8:2106.

13.

, Bai

, Zhang

, et al. [Prevalence and antibiogram distribution of Salmonella isolated from broiler production and processing course in four provinces, China]. Zhonghua Yu Fang Yi Xue Za Zhi, 2013b;47:435–438.

14.

, Pan

, Kang

, et al. Prevalence, characteristics, and antimicrobial resistance patterns of Salmonella in retail pork in Jiangsu province, eastern China. J Food Prot, 2014; 77:236–245.

15.

Lin

, Yan

, Lin

, Chen

. Increasing prevalence of hydrogen sulfide negative Salmonella in retail meats. Food Microbiol, 2014; 43:1–4.

16.

, Wu

, et al. Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China. Foodborne Pathog Dis, 2011; 8:45–53.

17.

, Lei

, Kong

, et al. Prevalence, antimicrobial resistance, and relatedness of Salmonella isolated from chickens and pigs on farms, abattoirs, and markets in Sichuan Province, China. Foodborne Pathog Dis, 2017; 14:667–677.

18.

Moe

, Paulsen

, Pichpol

, et al. Prevalence and antimicrobial resistance of Salmonella isolates from chicken carcasses in retail markets in Yangon, Myanmar. J Food Prot, 2017; 80:947–951.

19.

Ray

, Warnick

, Mitchell

, et al. Prevalence of antimicrobial resistance among Salmonella on midwest and northeast USA dairy farms. Prev Vet Med, 2007; 79:204–223.

20.

Ren

, Li

, Xu

, et al. Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China. Epidemiol Infect, 2016; 144:2989–2999.

21.

Sanchez-Maldonado

, Aslam

, Service

, et al. Prevalence and antimicrobial resistance of Salmonella isolated from two pork processing plants in Alberta, Canada. Int J Food Microbiol, 2017; 241:49–59.

22.

Song

, Xu

, Gao

, Zhang

. Overview of the development of quinolone resistance in Salmonella species in China, 2005–2016. Infection and drug resistance, 2018; 11:267–274.

23.

Stevens

, Kabore

, Perrier-Gros-Claude

, et al. Prevalence and antibiotic-resistance of Salmonella isolated from beef sampled from the slaughterhouse and from retailers in Dakar (Senegal). Int J Food Microbiol, 2006; 110:178–186.

24.

Terentjeva

, Avsejenko

, Streikisa

, Utinane

, Kovalenko

, Berzins

. Prevalence and antimicrobial resistance of Salmonella in meat and meat products in Latvia. Ann Agric Environ Med, 2017; 24:317–321.

25.

Tran

, Ly

, Nguyen

, et al. Prevalence of Salmonella spp. in pigs, chickens and ducks in the Mekong Delta, Vietnam. J Vet Med Sci, 2004; 66:1011–1014.

26.

Tsai

, Hsiang

. The prevalence and antimicrobial susceptibilities of Salmonella and Campylobacter in ducks in Taiwan. J Vet Med Sci, 2005; 67:7–12.

27.

Van

, Moutafis

, Tran

, Coloe

. Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Appl Environ Microbiol, 2007; 73:7906–7911.

28.

Yang

, Xi

, Wang

, et al. Prevalence of Salmonella on raw poultry at retail markets in China. J Food Prot, 2011; 74:1724–1728.