Skip to main content
PMC home page
Food Science & Nutrition logoLink to Food Science & Nutrition
. 2021 Jul 16;9(9):4701–4710. doi: 10.1002/fsn3.2266

Occurrence and antimicrobial resistance of Salmonella isolated from retail meats in Anhui, China

Wu Wang 1,2, Jing Chen 1,2, Xuefei Shao 1,2, Pan Huang 1,2, Jing Zha 1,2, Yingwang Ye 1,2,✉
PMCID: PMC8441314  PMID: 34531984

Abstract

Salmonella is considered one of the major foodborne pathogens associated with severe infections. Little attempt has been focused on the distribution of Salmonella in retail meats and the analysis of its phenotypic characteristics in Anhui Province. The aim of this study was to characterize the prevalence of Salmonella serovars, antimicrobial susceptibility, antimicrobial resistance genes, and virulence genes in Salmonella recovered from retail meats in Anhui, China. Out of the 120 samples collected from supermarket chains and open‐air markets, 16 samples (13.3%) were positive for Salmonella, of which Salmonella enterica serovars Enteritidis and Typhimurium were the common serotypes. Significant differences in incidence were found between supermarket chains and open‐air markets (p < 0.05). Overall, all 16 isolates were resistant to at least two tested antimicrobials, while 12 isolates showed multiple antimicrobial resistant phenotypes. High resistance was observed for ampicillin (87.5%), doxycycline (75.0%), and tetracycline (62.5%). The sul2 was detected in all isolates, and the aac(6′)‐Ib‐cr (93.8%) and the tetA (81.3%) were predominant in 10 resistance genes conferring five classes of antimicrobials. In addition, the correlation between resistance phenotypes and genes of tetracyclines and aminoglycosides was more than 80%. Interestingly, all the Salmonella isolates contained the genes mogA, mgtC, sopB, and spvB, whereas the siiE was variably represented. The findings in this study showed high prevalence, antimicrobial resistance, and the existence of virulence genes, suggesting that effective measures are required to ensure microbial safety from retail meats.

Keywords: antimicrobial resistance, resistance genes, retail meat, Salmonella, virulence genes

The study was to investigate the prevalence of Salmonella serovars, antimicrobial susceptibility, antimicrobial resistance genes and virulence genes in Salmonella recovered from retail meats in Anhui to analyze the relationship between antimicrobial resistance genes and antimicrobial susceptibility. The findings in this study showed high prevalence, antimicrobial resistance, and the existence of virulence genes, suggesting that effective measures are required to ensure microbial safety from retail meats.

graphic file with name FSN3-9-4701-g001.jpg

1. INTRODUCTION

Salmonella is the most common and representative pathogen isolated from confirmed cases of global foodborne diseases, which poses serious risks to human health (Cunha‐Neto et al., 2017). In most cases, the transmission to humans is associated with the consumption of contaminated foods or water, the treatment of contaminated raw meat, cross‐contamination, and the consumption of uncooked foods containing Salmonella (Yang et al., 2014). Salmonella is considered the main cause of outbreaks of foodborne infections reported in the European Union, and the number of cases has not shown any statistically significant decrease over the past 5 years from 2013 to 2017 (EFSA, 2018). An estimated 23% of bacterial foodborne poisoning is caused by Salmonella in Korea (Kim et al., 2016). Similarly in China, Salmonella is responsible for 19% of foodborne illnesses (Li et al., 2020).

Meats are likely to be contaminated with Salmonella at any stage during the slaughtering process and cross‐contaminated during subsequent processing, distribution, marketing, and handling (Jiang et al., 2021), that is why meat samples are more frequently involved in food infection cases caused by Salmonella. Therefore, the detection of Salmonella in retail meats is an indispensable part of food microbial inspection. In France, undercooked beef accounts for 35% of foodborne Salmonella infections, and consumption of contaminated poultry products is also a significant food safety risk in the USA (Velasquez et al., 2018). Mathole et al. (2017) indicated that 19% of poultry were infected with Salmonella in South Africa. Based on the surveillance of Salmonella contamination on raw poultry in 20 provinces of China, it is worth noting that the detection rate of Salmonella was 15.83% in retail markets (Li, Pei, et al., 2019). Despite this, however, attention on Salmonella is not limited to its global existence, but the major focus of food safety is the emergence of multiple antimicrobial resistant (MDR) Salmonella.

Recently, the widespread overuse and abuse of antimicrobial agents in food animal production and human medicine have contributed to the increasing incidence of antimicrobial resistance, particularly MDR (Arslan & Eyi, 2010). Antimicrobial resistance is recognized as one of the major challenges of public health worldwide in the twenty‐first century (Doménech et al., 2015). Notably, according to available data, China experienced the fastest growth rate worldwide in antimicrobial resistance of pathogens (Ren et al., 2016). With the widespread use of antimicrobials in livestock production, resistant isolates of Salmonella and their antimicrobial resistance can spread quickly to the human population by the consumption of products from contaminated meat (Zhu et al., 2019). The intensity of resistance varies globally, but the resistance rate is on the rise (Ifeanyichukwu et al., 2017; Louden et al., 2012; Mąka et al., 2015; Velasquez et al., 2018). To better understand the resistance mechanisms, it is necessary to detect antimicrobial resistance genes in Salmonella isolated from retail meats. In particular, genes active against β‐lactams and fluoroquinolones, which are first‐line antimicrobials, have been analyzed.

The pathogenicity of Salmonella is mediated by the interaction of numerous virulence genes, located in the Salmonella pathogenicity islands (SPIs), plasmids, lipopolysaccharides, and enterotoxins (Farahani et al., 2018). SPIs are clusters of virulence genes on chromosomes containing most of the virulence genes of Salmonella (Chaudhary et al., 2015). To date, 23 SPIs have been identified in Salmonella, of which SPI‐1 to SPI‐5 have been well studied (Ben Salem et al., 2017). In addition, plasmid‐borne virulence genes, such as spvB and spvC, have been reported to promote the survival and growth of Salmonella in host cells, aggravating the severity of enteritis (Oueslati et al., 2016). Although the prevalence of Salmonella in retail meats in China has been reported, there are few studies on virulence genes carried by Salmonella.

China has a high incidence of salmonellosis, with animal‐derived foods recognized as the major reservoirs of Salmonella dissemination, especially chicken, pork, and duck (Yang et al., 2019). Most investigations of prevalence and resistance of Salmonella in Anhui Province, a major province of livestock production and consumption in China, have focused on clinical and veterinary strains (Wang et al., 2013). However, little information on the incidence and antimicrobial resistant of Salmonella in retail meats exposed to consumers in Anhui is available, and there is a lack of epidemiological data for risk assessment. The study targeted chicken, pork, and duck that are collected by supermarket chains and open‐air markets.

The purpose of the present study was to investigate the prevalence of Salmonella and to further examine antimicrobial resistance, antimicrobial resistance genes, and virulence genes of Salmonella isolated from retail meats in Anhui, China.

2. MATERIALS AND METHODS

2.1. Sample collection

A total of 120 retail meat samples, including pork (n = 45), chicken (n = 45), and duck (n = 30), were collected randomly from different supermarket chains and open‐air markets in Hefei, Anhui Province. Immediately following purchase, the samples were aseptically packed into polyethylene bags containing ice and transferred to the laboratory for testing within 3 h.

2.2. Isolation and identification of isolates based on invA sequencing

From each meat sample, Salmonella isolates were searched and purified according to methods described by Yang et al. (2016). Salmonella genomic DNA was extracted using a Bacterial DNA Extraction kit (Tiangen, Beijing, China) and stored at −20°C until further use. Isolates with typical Salmonella phenotypes were further identified using polymerase chain reaction (PCR) amplification of the invasion gene invA (Bülte & Jakob, 1995) synthesized by GENEWIZ. The concentrations of the amplification reagents and the PCR cycling conditions are described in section 2.4.

2.3. Antimicrobial susceptibility testing

Antimicrobial susceptibility testing was determined using the broth microdilution method in accordance with the recommendations of the Clinical and Laboratory Standards Institute (CLSI) (CLSI, 2017). Eleven antimicrobial agents belonging to six different antimicrobial classes were applied: ampicillin, ceftiofur, ciprofloxacin, doxycycline, enrofloxacin, florfenicol, gentamicin, ofloxacin, spectinomycin, sulfisoxazole, and tetracycline. For the various types of antimicrobials, the isolates were classified as sensitive (S), intermediate (I), or resistant (R) according to the CLSI guidelines (CLSI, 2017). The multiple antimicrobial resistance (MAR) index was determined as described previously (Krumperman, 1983). Escherichia coli ATCC 25922 was used as a quality control strain.

2.4. Detection of antimicrobial resistance and virulence genes

Collected Salmonella isolates were tested for the presence of resistance and virulence genes using PCR. The following genes associated with antimicrobial resistance for fluoroquinolones (qnrS, aac(6′)‐Ib‐cr), aminoglycosides (aadA1, aadA2), tetracyclines (tetA, tetG), sulfonamides (sul1, sul2), and β‐lactams (bla TEM, bla CMY) were detected. Furthermore, seven genes that contribute to virulence were screened. Two target genes (spvB and spvC) were located on virulence plasmids, and five (mogA, sseL, mgtC, siiE, and sopB) were located on SPI‐1 to SPI‐5. All the primer sequences and predicted sizes of the amplified products are listed in Table S1.

The PCR protocol for amplification was previously described by Hai et al. (2020). PCR was performed in a final volume of 25 μl consisting of 12.5 μl DreamTaq Green PCR Master Mix, 1 μl each of forward and reverse primers (0.4 μM), 2 μl template DNA, and 8.5 μl dH2O. After completion of the PCR reaction cycles, the products were run on 2.0% agarose gel for 30 min at 110 V using electrophoresis. For confirmation of the amplified genes, all of the PCR products were sequenced by Sangon Biotech Co., Ltd (Shanghai, China) using an ABI3730 sequencer. The sequences obtained were compared with the previously published genes in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) using BLAST (https://blast.ncbi.nlm.nih.gov/Blast.cgi).

3. RESULTS

3.1. Prevalence of Salmonella in retail meats in Anhui

A total of 16 (13.3%) Salmonella isolates were identified from 120 retail meats of different animal origin analyzed in Anhui (Table 1). All the 16 isolates were positive for PCR based on invA sequencing. Of these isolates, 4 (14.3%) and 2 (9.5%) samples were obtained from chicken and duck samples in supermarket chains, respectively; 3 (13.6%), 6 (35.3%), and 1 (11.1%) were obtained from pork, chicken, and duck samples in open‐air markets, respectively. Overall, the prevalence of Salmonella in retail meats obtained from open‐air markets was significantly higher (p < 0.05) than that in supermarket chains.

TABLE 1.

Distribution of Salmonella obtained from supermarket chains and open‐air markets in different retail meats

Location Pork (%) Chicken (%) Duck (%) Total (%)
Supermarket chain 0.0a (0/23) 14.3a (4/28) 9.5a (2/21) 8.3b (6/72)
Open‐air market 13.6a (3/22) 35.3a (6/17) 11.1a (1/9) 20.8a (10/48)
Total 6.7 (3/45) 22.2 (10/45) 10.0 (3/30) 13.3 (16/120)
Open in a new tab

Values with different superscript letters (a‐b) indicate statistical significant differences between supermarket chains and open‐air markets (p < 0 .05).

Compared to the prevalence in pork (6.7%) and duck samples (10.0%), the prevalence of Salmonella was the highest in chicken (22.2%) among the retail meats tested. No Salmonella isolates were detected in the pork samples from supermarket chains. Further analysis revealed no significant difference (p > 0.05) in the overall contamination of Salmonella isolated from different retail meats.

The 16 isolates tested belonged to six serovars (Table 2). Salmonella enterica serovars Enteritidis and Typhimurium, both accounting for 31.3%, were the most frequently detected serotypes in the present study. The other four unusual serovars identified were S. Typhi, S. Paratyphi, S. Ouakam, and S. Goldcoast with an incidence of 18.8%, 6.3%, 6.3%, and 6.3%, respectively. It should be noted that S. Typhimurium was present in all three retail meats, while S. Enteritidis, S. Paratyphi, and S. Ouakam were found only in chicken.

TABLE 2.

Salmonella serotypes collected from pork, chicken, and duck samples

Serotype Pork Chicken Duck No. of isolates (%)
Salmonella Enteritidis 0 5 0 31.3 (5/16)
Salmonella Typhimurium 2 1 2 31.3 (5/16)
Salmonella Typhi 0 2 1 18.8 (3/16)
Salmonella Goldcoast 1 0 0 6.3 (1/16)
Salmonella Ouakam 0 1 0 6.3 (1/16)
Salmonella Paratyphi 0 1 0 6.3 (1/16)
Open in a new tab

3.2. Antimicrobial resistance

Antimicrobial susceptibility tests of the 16 Salmonella isolates against 11 antimicrobial agents are presented in Table 3. The prevalence of resistance was 87.5% for ampicillin, 75.0% for doxycycline, 62.5% for tetracycline, 50.0% for sulfisoxazole, and 50.0% for florfenicol. For spectinomycin, the percentage of Salmonella resistance was 43.8%, followed by gentamicin, 25.0%. In comparison, enrofloxacin resistance (18.8%) was observed less frequently, and most of the isolates were sensitive to ciprofloxacin (87.5%). Only one isolate was resistant to ceftiofur (6.3%) and ofloxacin (6.3%). These results indicate that high resistance rates were detected against ampicillin, oxytetracycline, and tetracycline. Except for enrofloxacin and sulfisoxazole, there was no significant difference (p > 0.05) between resistance phenotypes and sampling place. Additionally, the results showed complete resistance to doxycycline from supermarket chains (100.0%) and ampicillin from open‐air markets (100.0%).

TABLE 3.

Antimicrobial resistance of Salmonella among different supermarket chains and open‐air markets

Antimicrobial class Antimicrobial agent No. of resistant isolates (%)
Overall Supermarket chain Open‐air market
Tetracyclines DOX 75.0 (12/16) 100.0 (6/6) 60.0 (6/10)
TET 62.5 (10/16) 66.7 (4/6) 60.0 (6/10)
β‐Lactams AMP 87.5 (14/16) 66.7 (4/6) 100.0 (10/10)
CEF 6.3 (1/16) 16.7 (1/6) 0.0 (0/10)
Aminoglycosides GEN 25.0 (4/16) 33.3 (2/6) 20.0 (2/10)
SPT 43.8 (7/16) 33.3 (2/6) 50.0 (5/10)
Fluoroquinolones CIP 12.5 (2/16) 16.7 (1/6) 10.0 (1/10)
ENR 18.8 (3/16) 50.0 (3/6) 0.0 (0/10)
OFL 6.3 (1/16) 16.7 (1/6) 0.0 (0/10)
Amphenicols FFC 50.0 (8/16) 50.0 (3/6) 50.0 (5/10)
Sulfonamides SUL 50.0 (8/16) 0.0 (0/6) 80.0 (8/10)
Open in a new tab

Abbreviations: AMP, ampicillin; CEF, ceftiofur; CIP, ciprofloxacin; DOX, doxycycline; ENR, enrofloxacin; FFC, florfenicol; GEN, gentamicin; OFL, ofloxacin; SPT, spectinomycin; SUL, sulfisoxazole; TET, tetracycline.

Table 4 shows 11 different patterns of antimicrobial resistance in Salmonella. Among the multiple resistance patterns displayed, resistance to doxycycline, tetracycline, ampicillin, and spectinomycin simultaneously existed in 43.8% (7/16) of the isolates. Ampicillin (87.5%) was present in almost all the multi‐resistance patterns. A single isolate of S. Goldcoast from pork was observed to display resistance to seven antimicrobial agents with antimicrobial resistance phenotype of DOX + TET + AMP + SPT + CIP + FFC + SUL and had the highest MAR index of 0.64. The other one and three isolates were resistant to seven and six antimicrobial agents with MAR indices of 0.64 and 0.55, respectively. Therefore, it could be concluded that MDR was increasingly serious in the food hygiene environment of open‐air markets.

TABLE 4.

Antimicrobial resistance phenotype patterns and MAR indices of Salmonella from this study

Antimicrobial resistance phenotype pattern No. of antimicrobials No. of isolates MAR index
DOX + AMP 2 1 0.18
AMP + SUL 2 3 0.18
AMP + FFC + SUL 3 1 0.27
DOX + TET + GEN + FFC 4 2 0.36
DOX + TET + AMP + SUL 4 1 0.36
DOX + TET + AMP + SPT + ENR 5 2 0.45
DOX + TET + AMP + SPT + SUL 5 1 0.45
DOX + TET + AMP + GEN + SPT + FFC 6 2 0.55
DOX + TET + AMP + SPT + FFC + SUL 6 1 0.55
DOX + AMP + CEF + CIP + ENR + OFL + FFC 7 1 0.64
DOX + TET + AMP + SPT + CIP + FFC + SUL 7 1 0.64
Open in a new tab

As shown in Table 4, all the 16 Salmonella isolates showed resistance to at least two antimicrobials, and 12 of them exhibited an MDR phenotype. Serovars Typhimurium and Enteritidis were found most often in the MDR isolates. It should be highlighted that two Salmonella isolates that displayed resistance to up to 5 of the antimicrobials tested were all purchased from pork in the open‐air markets.

3.3. Detection of antimicrobial resistance genes

The antimicrobial resistance genes (tetA, tetG, bla TEM, bla CMY, aadA1, aadA2, qnrS, aac(6′)‐Ib‐cr, sul1, and sul2) conferring resistance to five classes of antimicrobials are shown in Table 5. All but three (81.3%) isolates contained tetA, while none of the isolates were positive for tetG. Ten out of the fourteen β‐lactam‐resistant isolates carried bla TEM, and no isolates carried bla CMY. aadA1 and aadA2 were observed in 10 (62.5%) and 6 (37.5%) of the 16 isolates, respectively. qnrS was present in a single isolate (6.3%), while aac(6′)‐Ib‐cr was detected in 93.8% of the isolates. sul2 was detected in all the 16 Salmonella isolates, while only 4 (25%) harbored sul1.

TABLE 5.

Distribution of antimicrobial resistance genes among Salmonella from this study

Antimicrobial Resistance genes No. of positive isolates (%)
Tetracyclines tetA 81.3 (13/16)
tetG 0.0 (0/16)
β‐Lactams bla TEM 62.5 (10/16)
bla CMY 0.0 (0/16)
Spectinomycin aadA1 62.5 (10/16)
aadA2 37.5 (6/16)
Fluoroquinolones qnrS 6.3 (1/16)
aac(6′)‐Ib‐cr 93.8 (15/16)
Sulfonamides sul1 25.0 (4/16)
sul2 100.0 (16/16)
Open in a new tab

3.4. Relationship between antimicrobial resistance genes and antimicrobial susceptibility

The coincidence rates of the antimicrobial resistance genes and the antimicrobial resistance phenotypes of the 16 Salmonella isolates ranged from 26.7% to 92.3% (Table 6). Almost all isolates (12/13) carrying tetA or tetB were resistant to tetracyclines, with similar results for aminoglycosides (9/11). In addition, 4 of the 15 isolates harboring qnrS or aac(6′)‐Ib‐cr were resistance to fluoroquinolones. Eight isolates with sul1 or sul2 were susceptible to sulfonamides.

TABLE 6.

Coincidence rates of antimicrobial resistance genes and antimicrobial susceptibility of Salmonella

Antimicrobial classes No. of resistant isolates No. of isolates carrying resistant genes Coincidence rate (%)
Tetracyclines 12 13 92.3
β‐Lactams 14 10 71.4
Aminoglycosides 9 11 81.8
Fluoroquinolones 4 15 26.7
Sulfonamides 8 16 50
Open in a new tab

3.5. Detection of virulence genes

In the present study, different serotypes of Salmonella carried different virulence genes, and the same virulence genes had different effects on the pathogenicity of Salmonella from different sources. The presence or absence of seven virulence genes is shown in Table 7. The size of the detected target band was consistent with the expected sizes. The mogA, mgtC, and sopB present in SPIs and spvB present in the virulent plasmids were detected in all 16 isolates, and almost all the isolates were positive for spvC (93.8%). Of the other virulence genes, the majority of the isolates carried sseL with the exception of four isolates. However, siiE was detected in 5 of the 16 isolates tested (31.3%). Overall, all the Salmonella isolates showed at least five virulence genes.

TABLE 7.

Percentage of virulence genes in Salmonella isolated from pork, chicken, and duck

Virulence genes Over all (%) Pork (%) Chicken (%) Duck (%)
invA 100.0 (16/16) 100.0 (3/3) 100.0 (10/10) 100.0 (3/3)
mogA 100.0 (16/16) 100.0 (3/3) 100.0 (10/10) 100.0 (3/3)
sseL 75.0 (12/16) 100.0 (3/3) 70.0 (7/10) 66.7 (2/3)
mgtC 100.0 (16/16) 100.0 (3/3) 100.0 (10/10) 100.0 (3/3)
siiE 31.3 (5/16) 33.3 (1/3) 30.0 (3/10) 33.3 (1/3)
sopB 100.0 (16/16) 100.0 (3/3) 100.0 (10/10) 100.0 (3/3)
spvB 100.0 (16/16) 100.0 (3/3) 100.0 (10/10) 100.0 (3/3)
spvC 93.8 (15/16) 100.0 (3/3) 90.0 (9/10) 100.0 (3/3)
Open in a new tab

4. DISCUSSION

Salmonella is often found in foods of meat origin and is implicated in many cases of human illness. In previous studies, the prevalence of Salmonella among retail meats in China varied widely (Chen et al., 2020; Yang et al., 2020; Zhang et al., 2018). In our study, the results for the proportion of Salmonella‐positive meat (13.3%) were similar to those reported by Sodagari et al. (2015), who found 19.8% in retail chicken meat and giblets in Iran, and Yu et al. (2014), who reported 46 positive samples from 367 raw meat samples, collected from supermarkets and open‐air markets in Henan (12.5%). This variation in the prevalence rates in different regions might be biased because of the types of meat samples, slaughterhouse sanitation, sampling season, and detection methods (Ou et al., 2020; Oueslati et al., 2016; Sallam et al., 2014).

Our study revealed that more chicken samples were positive for Salmonella than duck and pork samples, with no significant difference (p > 0.05), which was in agreement with the results reported by Yang et al. (2010) and Ou et al. (2020). This indicated that Salmonella contamination in retail meats in Anhui Province was serious, especially in chicken. This may be because of poor hygiene practices at the stage of product preparation and selling. In addition, the isolation rate of Salmonella collected from open‐air markets was remarkably higher than that from supermarket chains (p < 0.05), which was in concordance with the report of Zwe et al. (2018). Poor sanitary practices, such as cleaning knives and cutting boards untimely and not wearing masks and gloves could likely bring about cross‐contamination events. Regarding this issue, the supervision of open‐air markets should be strengthened to ensure high standards of environmental hygiene and reduce the risk of human infection.

Six Salmonella serovars were identified in the present study, dominated by S. Enteritidis, S. Typhimurium, and S. Typhi. Of note, all five S. Enteritidis isolates were present in chicken samples, and S. Enteritidis was also the dominant serovar from retail chicken in other survey studies (Ren et al., 2016; Yang et al., 2010), but another study from Singapore reported S. Saintpaul as the most common serotype in retail fresh chicken meat, followed by S. Brancaster (Zwe et al., 2018). A previous study by Furukawa et al. (2016) reported that S. Infantis was the most frequent in retail poultry meat in Japan. In Nigeria, S. Amoutive, the serotype isolated most frequently from retail beef, chicken, goat, and pork samples (Smith et al., 2016), was not detected in our study. The prevalence of Salmonella serovars in retail meats may vary greatly by geographic region, temporal changes, and different breeds of meat.

As reported in the USA (82%) (Chen et al., 2004), Singapore (80.8%) (Zwe et al., 2018), and northern India (100%) (Sharma et al., 2019), we noted a high prevalence of antimicrobial resistance of Salmonella isolates from retail meats. Similarly, all Salmonella isolates were resistant to the 11 antimicrobial agents in this study. For each antimicrobial agent, the antimicrobial with the highest resistance rate in this study was ampicillin, which was consistent with the results of reports from Wuhan (Zhu et al., 2020) and Yangzhou (Li, Yin, et al., 2019). The resistance of Salmonella to ampicillin has become commonplace in Africa and the USA owing to its extensive clinical use (Ke et al., 2014). Our findings also showed that the frequency of ampicillin resistance among isolates from supermarket chains was lower than that from open‐air markets. Further studies with larger sample sizes are needed to more accurately determine whether there are differences in antimicrobial resistance between Salmonella isolates from different locations.

Notably, resistance was frequently observed in tetracyclines, and active efflux systems are one of the main mechanisms of tetracyclines resistance. Our results were comparable to those of Yang et al. (2019), in which 65.6% of Salmonella isolates from retail meat and meat products in China were resistant to tetracycline. In northern Vietnam, resistance to tetracycline was also commonly observed in isolates from beef in retail markets (Thai et al., 2012). However, low‐level tetracycline resistance in Salmonella has previously been reported in most developed countries and regions (Kim et al., 2012; Nisar et al., 2017). These results could be related to the unsuitable or unrestricted use of corresponding antimicrobials in livestock farming, particularly in developing countries (Chen et al., 2020).

A relatively high resistance rate to enrofloxacin and ciprofloxacin was observed in this study. Fortunately, only one isolate was resistant to ofloxacin, whereas fluoroquinolone‐resistant isolates have emerged and are at high levels of resistance (Ou et al., 2020). These isolates should be of great concern, as second‐generation cephalosporins and third‐generation quinolones are the main antimicrobials of choice for Salmonella infections (Yang et al., 2016). A report by Smith et al. (2016) in 2013 from Lagos, Nigeria, stated that all of the tested isolates were susceptible to ofloxacin and ciprofloxacin; however, in the present study, 18.8% of the isolates were resistant to enrofloxacin, 12.5% were resistant to ciprofloxacin, and 6.3% were resistant to ofloxacin.

Our results of antimicrobial resistance of Salmonella were similar to those from the study by Zhang et al. (2018), who assayed for antimicrobial susceptibility of 615 Salmonella isolates obtained from chicken and pork in retail markets in Guangdong, China. The study showed that resistance to tetracycline, gentamicin, ciprofloxacin, florfenicol, and sulfisoxazole reached 75.3%, 16.3%, 12%, 38.7%, and 76.1%, respectively. However, in Canada, the percentage of resistance to ciprofloxacin, ampicillin, gentamicin, sulfisoxazole, and tetracycline was lower than in our study, except for ceftiofur (Aslam et al., 2012), which may indicate a better control of such antimicrobials in retail meats in Canada.

By analyzing total antibiotic resistance profiles, 12 isolates tested were resistant to three or more antimicrobial agents, accounting for 75% of the total number of isolates, which caused difficulties in the clinical treatment of Salmonella. The spread of MDR isolates was potentially severe: 60.7% in Korea (Seo et al., 2019), 88.1% in southern China (Chen et al., 2020), and 100% in Egypt (Sallam et al., 2014). The high level of antimicrobial resistance was directly related to the unscientific use of broad‐spectrum and cheap antimicrobials in the rearing of livestock and poultry, resulting in an increasing number of antimicrobial‐resistant and MDR bacteria. It is noteworthy that two isolates obtained from open‐air markets were resistant to seven different antimicrobials. The spread of MDR animal bacteria to humans threatens human health worldwide and could lead to some diseases with no remedy. Thus, it is necessary to strengthen the monitoring of the trends in the resistance spectrum of Salmonella to control MDR isolates.

The results of the detection of antimicrobial resistance genes showed that all five classes of antimicrobial resistance genes were detected at different degrees, among which the superior resistance genes were tetA (81.3%), bla TEM (62.5%), aadA1 (62.5%), aac(6′)‐Ib‐cr (93.8%), and sul2 (100.0%) (Table 5). The results showed that the coincidence rate of antimicrobial‐resistant phenotypes and antimicrobial‐resistant genes of the five classes of antimicrobials was over 60%. The coincidence rate of sulfonamides was the highest, up to 100.0%. sul2, located on non‐conjugative plasmids or a transmissible multi‐resistance plasmid (Nghiem et al., 2017), was the main sulfonamide resistance gene, which was consistent with the report by Zhu et al. (2017). However, Chen et al. (2020) found that sul1 was the main sulfonamide resistance gene detected in Salmonella recovered from retail duck meat in Southern China. This may be because of the different types of Salmonella among various regions, resulting in distinct resistance genes.

Recently, fluoroquinolones have been the most commonly used antimicrobials in the clinical control of Salmonella infection. Plasmid‐mediated quinolone resistance (PMQR) has emerged in Salmonella spp. and in other Enterobacteriaceae with increasing prevalence (Pribul et al., 2016). PMQR determinants generally generate only low‐level resistance, but nonetheless can complement the mechanisms of chromosomal resistance to reach clinical resistance levels (Wang et al., 2020). The recent discovery of PMQR could result in horizontal transfer of fluoroquinolone resistance between strains (Hopkins et al., 2005). qnrS mediates low levels of fluoroquinolone resistance by altering the role of the antimicrobial target site and then binding to the target enzyme, while the cr variant of aac(6′)‐Ib encodes an aminoglycoside acetyltransferase that confers reduced susceptibility to ciprofloxacin by N‐acetylation of its piperazinyl amine. aac(6′)‐Ib‐cr has two amino acid changes, Trp102Arg and Asp179Try, which together are necessary and sufficient for the enzyme's ability to acetylate ciprofloxacin (Park et al., 2006). The results of this study revealed that most isolates carried aac(6′)‐Ib‐cr (93.8%), which was similar (79.17%) to the data reported previously in Changchun (Ren et al., 2016). However, the detection rate of aac(6′)‐Ib‐cr was relatively low in Tunisia (1.7%) and Brazil (17.8%), depending on the location (Al‐Gallas et al., 2013). Since PMQR is probably the primary mechanism of quinolone resistance in animal‐derived foods, we conjecture that it was also the cause of fluoroquinolone resistance in this study.

Tetracycline resistance was mainly encoded by tetA, and in our study, a high prevalence of tetA was detected in the examined isolates. The superiority of tetA in Salmonella played an outstanding role in tetracycline resistance. However, no isolates were found to harbor tetG, and a similar phenomenon that did not find tetG among the three genes screened (tetA, tetB, tetG) has been suggested previously in Northern India (Sharma et al., 2019).

In Gram‐negative bacteria, resistance β‐lactams is mediated by different strategies such as production of β‐lactamases, efflux pumps, and alteration of penicillin binding proteins (Ma et al., 2017). The results of the detection of β‐lactam resistance genes showed that bla TEM was the most frequent gene; however, bla CMY was not detected in any Salmonella isolates. The β‐lactam resistance genes were of concern because the utilization of β‐lactam antimicrobials among patients reached 70% in China (Ren et al., 2016). Fortunately, bla CMY‐positive Salmonella has been found in China at a low rate and has only been reported in Shanxi and Sichuan (Zhao et al., 2017).

The data on antimicrobial resistance genes and phenotypes indicate that the Salmonella isolates had a high correlation between the phenotypes and genotypes of tetracyclines, β‐lactams, and aminoglycosides, while the coincidence rate of phenotypes and genotypes of fluoroquinolones and sulfonamides was relatively lower. This discrepancy indicates that the resistance phenotype was associated with the existence of resistance genes, but it did not rigidly follow a one‐to‐one correspondence, which was in connection with the complex mechanisms of antimicrobial resistance of Salmonella isolates (Chen et al., 2020). Factors, such as the expression of resistance genes, the interaction between different resistance genes, gene mutation, and biofilm formation affected the resistance to antimicrobials, or the resistance phenotypes encoded by the detected resistance genes did not match with the antimicrobials in this study, which resulted in the deviation between the genotypes and the resistance phenotypes (Ren et al., 2016). Comparisons of sequencing results of antimicrobial resistance genes showed that the sequences of antimicrobial resistance genes were remarkably similar to the reference sequences, which were all above 99%.

Pathogenicity in Salmonella is complex and multifactorial (Carvalho et al., 2017). Bacterial infections of the host usually adhere to the host cell, and then successfully invade the host cell through its virulence factors, resulting in the disease and even death of the host (Tang & Holden, 1999). This is due to the presence of the genetic determinants of virulence in Salmonella. High frequencies were reported for mogA (100%), mgtC (100%), sopB (100%), spvB (100%), and spvC (93.8%), with the exception of sseL (75.0%) and siiE (31.3%), which provided further evidence that these virulence genes were widespread in Salmonella. Based on virulence profiles, more than 68.8% of isolates harbored over six virulence genes, and 31.3% were positive for all the virulence genes tested. The more virulence genes the isolates harbored, the more likely they were to show pathogenicity and the stronger the virulence. Several studies have shown that the virulence and pathogenicity of Salmonella decrease when sseL (SPI‐2) is mutated, and pathogenicity is mainly related to SPI‐1 and SPI‐2 (Ochman et al., 1996). In this study, we found a high prevalence of spvB and spvC in Salmonella. Virulence plasmid genes are conducive to the adhesion and settlement of bacteria in host cells and improve the viability of host cells, which may be the reason why virulence plasmid genes enhance the pathogenicity of Salmonella (Haneda et al., 2001). In general, the high detection rate of virulence genes highlighted the pathogenic potential of these isolates, playing an important role in human disease.

5. CONCLUSION

In conclusion, the present study investigated the occurrence, antimicrobial resistance, antimicrobial resistance genes, and virulence genes of Salmonella among retail meats in Anhui, which demonstrated that retail meats, especially chicken, showed a high incidence of Salmonella exhibiting MDR phenotypes. The high rate of sul2 and aac(6′)‐Ib‐cr‐positive isolates suggested that the Salmonella surveillance system and the reasonable use of antimicrobials in livestock and poultry production would help combat and control Salmonella infection. Moreover, the genes mogA, mgtC, sopB, and spvB were found in all the Salmonella isolates. Further studies with large numbers of Salmonella isolates along the food chain are the required need to explore the epidemiological situation and to track and prevent salmonellosis.

CONFLICT OF INTEREST

The authors declare no conflicts of interest.

Supporting information

Supplementary Material

Click here for additional data file. (28KB, docx)

ACKNOWLEDGMENTS

This study was supported by the National Key R&D Program of China [grant no. 2018YFD0400801] and the Major Research and Development Program of Anhui, China [grant no. 1804a07020132].

Wang W, Chen J, Shao X, Huang P, Zha J, Ye Y. Occurrence and antimicrobial resistance of Salmonella isolated from retail meats in Anhui, China. Food Sci Nutr. 2021;9:4701–4710. 10.1002/fsn3.2266

REFERENCES

  1. Al‐Gallas, N., Abbassi, M. S., Gharbi, B., Manai, M., Ben Fayala, M. N., Bichihi, R., Al‐Gallas, A., & Ben Aissa, R. (2013). Occurrence of plasmid‐mediated quinolone resistance determinants and rmtB gene in Salmonella enterica serovar Enteritidis and Typhimurium isolated from food‐animal products in Tunisia. Foodborne Pathogens and Disease, 10(9), 813–819. 10.1089/fpd.2012.1466 [DOI] [PubMed] [Google Scholar]
  2. Arslan, S., & Eyi, A. (2010). Occurrence and antimicrobial resistance profiles of Salmonella species in retail meat products. Journal of Food Protection, 73(9), 1613–1617. 10.4315/0362-028x-73.9.1613 [DOI] [PubMed] [Google Scholar]
  3. Aslam, M., Checkley, S., Avery, B., Chalmers, G., Bohaychuk, V., Gensler, G., Reid‐Smith, R., & Boerlin, P. (2012). Phenotypic and genetic characterization of antimicrobial resistance in Salmonella serovars isolated from retail meats in Alberta, Canada. Food Microbiology, 32(1), 110–117. 10.1016/j.fm.2012.04.017 [DOI] [PubMed] [Google Scholar]
  4. Ben Salem, R., Abbassi, M. S., García, V., García‐Fierro, R., Fernández, J., Kilani, H., Jaouani, I., Khayeche, M., Messadi, L., & Rodicio, M. R. (2017). Antimicrobial drug resistance and genetic properties of Salmonella enterica serotype Enteritidis circulating in chicken farms in Tunisia. Journal of Infection & Public Health, 10(6), 855–860. 10.1016/j.jiph.2017.01.012 [DOI] [PubMed] [Google Scholar]
  5. Bülte, M., & Jakob, P. (1995). The use of a PCR‐generated invA probe for the detection of Salmonella spp. in artificially and naturally contaminated foods. International Journal of Food Microbiology, 26(3), 335–344. 10.1016/0168-1605(94)00139-W [DOI] [PubMed] [Google Scholar]
  6. Carvalho, F. C. T. D., Rodriguez, M. T. T., Menezes, F. G. R. D., Sousa, O. V. D., & Vieira, R. H. S. D. F. (2017). Ecotypes and virulence factors of Salmonella spp. detected in shrimp farms in State of Ceara, Brazil. Acta Scientiarum Biological Sciences, 39(4), 469–474. 10.4025/actascibiolsci.v39i4.34607 [DOI] [Google Scholar]
  7. Chaudhary, J. H., Nayak, J. B., Brahmbhatt, M. N., & Makwana, P. P. (2015). Virulence genes detection of Salmonella serovars isolated from pork and slaughterhouse environment in Ahmedabad, Gujarat. Veterinary World, 8(1), 121–124. 10.14202/vetworld.2015.121-124 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chen, S., Zhao, S., White, D. G., Schroeder, C. M., Lu, R., Yang, H., McDermott, P. F., Ayers, S., & Meng, J. (2004). Characterization of multiple‐antimicrobial‐resistant Salmonella serovars isolated from retail meats. Applied & Environmental Microbiology, 70(1), 1–7. 10.1128/AEM.70.1.1-7.2004 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen, Z., Bai, J., Wang, S., Zhang, X., Zhan, Z., Shen, H., Zhang, H., Wen, J., Gao, Y., Liao, M., & Zhang, J. (2020). Prevalence, antimicrobial resistance, virulence genes and genetic diversity of Salmonella isolated from retail duck meat in Southern China. Microorganisms, 8(3), 444–455. 10.3390/microorganisms8030444 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. CLSI (Clinical and Laboratory Standards Institute) (2017). Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute. [Google Scholar]
  11. Cunha‐Neto, A. D., Castro, V. S., Carvalho, L. A., Rodrigues, D. D. P., Mano, S. B., Figueiredo, E. E. D. S., & Conte‐Junior, C. A. (2017). Serotypes and antimicrobial resistance profiles of Salmonella isolated from fresh beef processing and chilled fresh beef samples produced and marketed in the metropolitan region of Cuiabá, in the State of Mato Grosso, Brazil. African Journal of Microbiology Research, 11(45), 1626–1631. 10.5897/AJMR2017.8665 [DOI] [Google Scholar]
  12. Doménech, E., Jiménez‐Belenguer, A., Pérez, R., Ferrús, M. A., & Escriche, I. (2015). Risk characterization of antimicrobial resistance of Salmonella in meat products. Food Control, 57, 18–23. 10.1016/j.foodcont.2015.04.001 [DOI] [Google Scholar]
  13. EFSA (European Food Safety Authority and European Centre for Disease Prevention and Control) (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2017. European Food Safety Authority Journal, 16(12), 22–67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Farahani, R. K., Ehsani, P., Rad, M. E., & Khaledi, A. (2018). Molecular detection, virulence genes, biofilm formation, and antibiotic resistance of Salmonella enterica serotype Enteritidis isolated from poultry and clinical samples. Jundishapur Journal of Microbiology, 11(10), e69504. 10.5812/jjm.69504 [DOI] [Google Scholar]
  15. Furukawa, I., Ishihara, T., Teranishi, H., Saito, S., Yatsuyanagi, J., Wada, E., Kumagai, Y., Takahashi, S., Konno, T., Kashio, H., Kobayashi, A., Kato, N., Hayashi, K., Fukushima, K., Ishikawa, K., Horikawa, K., Oishi, A., Izumiya, H., Ohnishi, T., … Kuroki, T. (2016). Prevalence and characteristics of Salmonella and Campylobacter in retail poultry meat in Japan. Japanese Journal of Infectious Diseases, 70(3), 239–247. 10.7883/yoken.JJID.2016.164 [DOI] [PubMed] [Google Scholar]
  16. Hai, D., Yin, X., Lu, Z., Lv, F., Zhao, H., & Bie, X. (2020). Occurrence, drug resistance, and virulence genes of Salmonella isolated from chicken and eggs. Food Control, 113, 107109. 10.1016/j.foodcont.2020.107109 [DOI] [Google Scholar]
  17. Haneda, T., Okada, N., Nakazawa, N., Kawakami, T., & Danbara, H. (2001). Complete DNA sequence and comparative analysis of the 50‐Kilobase virulence plasmid of Salmonella enterica serovar choleraesuis. Infection and Immunity, 69(4), 2612–2620. 10.1128/IAI.69.4.2612-2620.2001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hopkins, K. L., Davies, R. H., & Threlfall, E. J. (2005). Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. International Journal of Antimicrobial Agents, 25(5), 358–373. 10.1016/j.ijantimicag.2005.02.006 [DOI] [PubMed] [Google Scholar]
  19. Ifeanyichukwu, I., Chika, E., Ogonna, A., Chidinma, I., Monique, A., Ikechukwu, M., Stanley, E., Emmanuel, N., Ngozi, A., & Agabus, N. (2017). Prevalence and antibiogram of Salmonella species isolated from poultry products in Ebonyi State, Nigeria. Journal of Advanced Veterinary and Animal Research, 3(4), 353–359. 10.5455/javar.2016.c-172 [DOI] [Google Scholar]
  20. Jiang, Z., Anwar, T. M., Peng, X., Biswas, S., Elbediwi, M., Li, Y., Fang, W., & Yue, M. (2021). Prevalence and antimicrobial resistance of Salmonella recovered from pig‐borne food products in Henan, China. Food Control, 121, 107535. 10.1016/j.foodcont.2020.107535 [DOI] [Google Scholar]
  21. Ke, B., Sun, J., He, D., Li, X., Liang, Z., & Ke, C. (2014). Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007–2012 in Guangdong, China. BMC Infectious Diseases, 14(1), 338. 10.1186/1471-2334-14-338 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kim, H., Lee, J., Jang, Y., Chang, B., Kim, A., & Choe, N. (2016). Prevalence and antimicrobial resistance of Salmonella spp. and Escherichia coli isolated from ducks in Korea. Korean Journal of Veterinary Research, 56(2), 91–95. 10.14405/kjvr.2016.56.2.91 [DOI] [Google Scholar]
  23. Kim, M. S., Lim, T. H., Jang, J. H., Lee, D. H., Kim, B. Y., Kwon, J. H., Choi, S. W., Noh, J. Y., Hong, Y. H., Lee, S. B., Yang, S. Y., Lee, H. J., Lee, J. B., Park, S. Y., Choi, L. S., & Song, C. S. (2012). Prevalence and antimicrobial resistance of Salmonella species isolated from chicken meats produced by different integrated broiler operations in Korea. Poultry Science, 91(9), 2370–2375. 10.3382/ps.2012-02357 [DOI] [PubMed] [Google Scholar]
  24. Krumperman, P. H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high‐risk sources of fecal contamination of foods. Applied & Environmental Microbiology, 46(1), 165–170. 10.1128/AEM.46.1.165-170.1983 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Li, Q., Yin, J., Li, Z., Li, Z., Du, Y., Guo, W., Bellefleur, M., Wang, S., & Shi, H. (2019). Serotype distribution, antimicrobial susceptibility, antimicrobial resistance genes and virulence genes of Salmonella isolated from a pig slaughterhouse in Yangzhou, China. AMB Express, 9(1), 210. 10.1186/s13568-019-0936-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Li, W., Pires, S. M., Liu, Z., Ma, X., Liang, J., Jiang, Y., Chen, J., Liang, J., Wang, S., Wang, L., Wang, Y., Meng, C., Huo, X., Lan, Z., Lai, S., Liu, C., Han, H., Liu, J., Fu, P., & Guo, Y. (2020). Surveillance of foodborne disease outbreaks in China, 2003–2017. Food Control, 118, 107359. 10.1016/j.foodcont.2020.107359 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Li, Y., Pei, X., Zhang, X., Wu, L., Liu, Y., Zhou, H., Ma, G., Chen, Q., Liang, H., & Yang, D. (2019). A surveillance of microbiological contamination on raw poultry meat at retail markets in China. Food Control, 104, 99–104. 10.1016/j.foodcont.2019.04.037 [DOI] [Google Scholar]
  28. Louden, B. C., Haarmann, D., Han, J., Foley, S. L., & Lynne, A. M. (2012). Characterization of antimicrobial resistance in Salmonella enterica serovar Typhimurium isolates from food animals in the U.S. Food Research International, 45(2), 968–972. 10.1016/j.foodres.2011.03.055 [DOI] [Google Scholar]
  29. Ma, S., Lei, C., Kong, L., Jiang, W., Liu, B., Men, S., Yang, Y., Cheng, G., Chen, Y., & Wang, H. (2017). Prevalence, antimicrobial resistance, and relatedness of Salmonella isolated from chickens and pigs on farms, abattoirs, and markets in Sichuan Province, China. Foodborne Pathogens and Disease, 14(11), 667–677. 10.1089/fpd.2016.2264 [DOI] [PubMed] [Google Scholar]
  30. Mąka, Ł., Maćkiw, E., Ścieżyńska, H., & Popowska, M. (2015). Occurrence and antimicrobial resistance of Salmonella spp. isolated from food other than meat in Poland. Annals of Agricultural and Environmental Medicine: AAEM, 22(3), 403–408. 10.5604/12321966.1167701 [DOI] [PubMed] [Google Scholar]
  31. Mathole, M. A., Muchadeyi, F. C., Mdladla, K., Malatji, D. P., Dzomba, E. F., & Madoroba, E. (2017). Presence, distribution, serotypes and antimicrobial resistance profiles of Salmonella among pigs, chickens and goats in South Africa. Food Control, 72, 219–224. 10.1016/j.foodcont.2016.05.006 [DOI] [Google Scholar]
  32. Nghiem, M. N., Nguyen, V. T., Nguyen, T. T. H., Nguyen, T. D., & Vo, T. T. B. (2017). Antimicrobial resistance gene expression associated with multidrug resistant Salmonella spp. isolated from retail meat in Hanoi, Vietnam. International Microbiology, 20(2), 85–94. 10.2436/20.1501.01.288 [DOI] [PubMed] [Google Scholar]
  33. Nisar, M., Kassem, I. I., Rajashekara, G., Goyal, S. M., Lauer, D., Voss, S., & Nagaraja, K. V. (2017). Genotypic relatedness and antimicrobial resistance of Salmonella Heidelberg isolated from chickens and turkeys in the midwestern United States. Journal of Veterinary Diagnostic Investigation, 29(3), 370–375. 10.1177/1040638717690784 [DOI] [PubMed] [Google Scholar]
  34. Ochman, H., Soncini, F. C., Solomon, F., & Groisman, E. A. (1996). Identification of a pathogenicity island required for Salmonella survival in host cells. Proceedings of the National Academy of Sciences of the United States of America, 93(15), 7800–7804. 10.1073/pnas.93.15.7800 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ou, C., Shang, D., Yang, J., Chen, B., Chang, J., Jin, F., & Shi, C. (2020). Prevalence of multidrug‐resistant Staphylococcus aureus isolates with strong biofilm formation ability among animal‐based food in Shanghai. Food Control, 112, 107106. 10.1016/j.foodcont.2020.107106 [DOI] [Google Scholar]
  36. Oueslati, W., Rjeibi, M. R., Mhadhbi, M., Jbeli, M., Zrelli, S., & Ettriqui, A. (2016). Prevalence, virulence and antibiotic susceptibility of Salmonella spp. strains, isolated from beef in Greater Tunis (Tunisia). Meat Science, 119, 154–159. 10.1016/j.meatsci.2016.04.037 [DOI] [PubMed] [Google Scholar]
  37. Park, C. H., Robicsek, A., Jacoby, G. A., Sahm, D., & Hooper, D. C. (2006). Prevalence in the United States of aac( 6′)‐Ib‐cr encoding a ciprofloxacin‐modifying enzyme. Antimicrobial Agents and Chemotherapy, 50(11), 3953–3955. 10.1128/AAC.00915-06 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pribul, B. R., Festivo, M. L., Souza, M. M. S. D., & Rodrigues, D. D. P. (2016). Characterization of quinolone resistance in Salmonella spp. isolates from food products and human samples in Brazil. Brazilian Journal of Microbiology, 47(1), 196–201. 10.1016/j.bjm.2015.04.001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ren, D., Chen, P., Wang, Y., Wang, J., Liu, H., & Liu, H. (2016). Phenotypes and antimicrobial resistance genes in Salmonella isolated from retail chicken and pork in Changchun, China. Journal of Food Safety, 37(2), e12314. 10.1111/jfs.12314 [DOI] [Google Scholar]
  40. Sallam, K. I., Mohammed, M. A., Hassan, M. A., & Tamura, T. (2014). Prevalence, molecular identification and antimicrobial resistance profile of Salmonella serovars isolated from retail beef products in Mansoura, Egypt. Food Control, 38, 209–214. 10.1016/j.foodcont.2013.10.027 [DOI] [Google Scholar]
  41. Seo, K. W., Kim, J. J., Mo, I. P., & Lee, Y. J. (2019). Molecular characteristic of antimicrobial resistance of Salmonella Gallinarum isolates from chickens in Korea, 2014 to 2018. Poultry Science, 98(11), 5416–5423. 10.3382/ps/pez376 [DOI] [PubMed] [Google Scholar]
  42. Sharma, J., Kumar, D., Hussain, S., Pathak, A., Shukla, M., Prasanna Kumar, V., Anisha, P. N., Rautela, R., Upadhyay, A. K., & Singh, S. P. (2019). Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control, 102, 104–111. 10.1016/j.foodcont.2019.01.021 [DOI] [Google Scholar]
  43. Smith, S., Braun, S., Akintimehin, F., Fesobi, T., Bamidele, M., Coker, A., Monecke, S., & Ehricht, R. (2016). Serogenotyping and antimicrobial susceptibility testing of Salmonella spp. isolated from retail meat samples in Lagos, Nigeria. Molecular & Cellular Probes, 30(4), 189–194. 10.1016/j.mcp.2016.04.001 [DOI] [PubMed] [Google Scholar]
  44. Sodagari, H. R., Mashak, Z., & Ghadimianazar, A. (2015). Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran. Journal of Infection in Developing Countries, 9(5), 463–469. 10.3855/jidc.5945 [DOI] [PubMed] [Google Scholar]
  45. Tang, C., & Holden, D. (1999). Pathogen virulence genes ‐ Implications for vaccines and drug therapy. British Medical Bulletin, 55(2), 387–400. 10.1258/0007142991902448 [DOI] [PubMed] [Google Scholar]
  46. Thai, T. H., Hirai, T., Lan, N. T., Shimada, A., Ngoc, P. T., & Yamaguchi, R. (2012). Antimicrobial resistance of Salmonella serovars isolated from beef at retail markets in the north Vietnam. Journal of Veterinary Medical Science, 74(9), 1163–1169. 10.1292/jvms.12-0053 [DOI] [PubMed] [Google Scholar]
  47. Velasquez, C. G., Macklin, K. S., Kumar, S., Bailey, M., Ebner, P. E., Oliver, H. F., Martin‐Gonzalez, F. S., & Singh, M. (2018). Prevalence and antimicrobial resistance patterns of Salmonella isolated from poultry farms in southeastern United States. Poultry Science, 97(6), 2144–2152. 10.3382/ps/pex449 [DOI] [PubMed] [Google Scholar]
  48. Wang, H., Ye, K., Wei, X., Cao, J., Xu, X., & Zhou, G. (2013). Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control, 33(2), 378–384. 10.1016/j.foodcont.2013.03.030 [DOI] [Google Scholar]
  49. Wang, P., Hu, L., & Hao, Z. (2020). Palmatine is a plasmid‐mediated quinolone resistance (PMQR) inhibitor that restores the activity of ciprofloxacin against qnrS and aac( 6′)‐Ib‐cr‐producing Escherichia coli . Infection and Drug Resistance, 13, 749–759. 10.2147/IDR.S242304 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yang, B., Cui, Y., Shi, C., Wang, J., Xia, X., Xi, M., Wang, X., Meng, J., Alali, W. Q., Walls, I., & Doyle, M. P. (2014). Counts, serotypes, and antimicrobial resistance of Salmonella isolates on retail raw poultry in the People's Republic of China. Journal of Food Protection, 77(6), 894–902. 10.4315/0362-028X.JFP-13-439 [DOI] [PubMed] [Google Scholar]
  51. Yang, B., Qu, D., Zhang, X., Shen, J., Cui, S., Shi, Y., Xi, M., Sheng, M., Zhi, S., & Meng, J. (2010). Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. International Journal of Food Microbiology, 141(1–2), 63–72. 10.1016/j.ijfoodmicro.2010.04.015 [DOI] [PubMed] [Google Scholar]
  52. Yang, X., Huang, J., Wu, Q., Zhang, J., Liu, S., Guo, W., Cai, S., & Yu, S. (2016). Prevalence, antimicrobial resistance and genetic diversity of Salmonella isolated from retail ready‐to‐eat foods in China. Food Control, 60, 50–56. 10.1016/j.foodcont.2015.07.019 [DOI] [Google Scholar]
  53. Yang, X., Huang, J., Zhang, Y., Liu, S., Chen, L., Xiao, C., Zeng, H., Wei, X., Gu, Q., Li, Y., Wang, J., Ding, Y., Zhang, J., & Wu, Q. (2020). Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Science of the Total Environment, 713, 136385. 10.1016/j.scitotenv.2019.136385 [DOI] [PubMed] [Google Scholar]
  54. Yang, X., Wu, Q., Zhang, J., Huang, J., Chen, L., Wu, S., Zeng, H., Wang, J., Chen, M., Wu, H., Gu, Q., & Wei, X. (2019). Prevalence, bacterial load, and antimicrobial resistance of Salmonella serovars isolated from retail meat and meat products in China. Frontiers in Microbiology, 10, 2121–2129. 10.3389/fmicb.2019.02121 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yu, T., Jiang, X., Zhou, Q., Wu, J., & Wu, Z. (2014). Antimicrobial resistance, class 1 integrons, and horizontal transfer in Salmonella isolated from retail food in Henan, China. Journal of Infection in Developing Countries, 8(6), 705–711. 10.3855/jidc.4190 [DOI] [PubMed] [Google Scholar]
  56. Zhang, L., Fu, Y., Xiong, Z., Ma, Y., Wei, Y., Qu, X., Zhang, H., Zhang, J., & Liao, M. (2018). Highly prevalent multidrug‐resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China. Frontiers in Microbiology, 9, 2104. 10.3389/fmicb.2018.02104 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Zhao, X., Ye, C., Chang, W., & Sun, S. (2017). Serotype distribution, antimicrobial resistance, and Class 1 integrons profiles of Salmonella from animals in slaughterhouses in Shandong Province, China. Frontiers in Microbiology, 8, 1049. 10.3389/fmicb.2017.01049 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Zhu, A., Zhi, W., Qiu, Y., Wei, L., Tian, J., Pan, Z., Kang, X., Gu, W., & Duan, L. (2019). Surveillance study of the prevalence and antimicrobial resistance of Salmonella in pork from open markets in Xuzhou, China. Food Control, 98, 474–480. 10.1016/j.foodcont.2018.07.035 [DOI] [Google Scholar]
  59. Zhu, Y., Lai, H., Zou, L., Yin, S., Wang, C., Han, X., Xia, X., Hu, K., He, L., Zhou, K., Chen, S., Ao, X., & Liu, S. (2017). Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. International Journal of Food Microbiology, 259, 43–51. 10.1016/j.ijfoodmicro.2017.07.023 [DOI] [PubMed] [Google Scholar]
  60. Zhu, Z., Huang, Q., Hong, X., Chen, X., Lu, Y., Chen, Z., Wang, C., Meng, X., Xu, Q., & Li, S. (2020). Isolation and characterization of Salmonella in pork samples collected from retail and wholesale markets in each season from 2016 to 2018 in Wuhan, China. Journal of Applied Microbiology, 128(3), 875–883. 10.1111/jam.14515 [DOI] [PubMed] [Google Scholar]
  61. Zwe, Y. H., Yen Tang, V. C., Aung, K. T., Gutiérrez, R. A., Ng, L. C., & Yuk, H. G. (2018). Prevalence, sequence types, antibiotic resistance and gyrA mutations of Salmonella isolated from retail fresh chicken meat in Singapore. Food Control, 90, 233–240. 10.1016/j.foodcont.2018.03.004 [DOI] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material

Click here for additional data file. (28KB, docx)

Articles from Food Science & Nutrition are provided here courtesy of Wiley

RESOURCES