Prevalence, serotypes, and antimicrobial resistance of Salmonella isolates from patients with diarrhea in Shenzhen, China

doi:10.21203/rs.2.19682/v2

Download PDF

Research

Prevalence, serotypes, and antimicrobial resistance of Salmonella isolates from patients with diarrhea in Shenzhen, China

https://doi.org/10.21203/rs.2.19682/v2

This work is licensed under a CC BY 4.0 License

Journal Publication

published 06 Jul, 2020

Read the published version in BMC Microbiology →

Version 2

posted

You are reading this latest preprint version

Background : Salmonella is one of the main causative agents of diarrhea which results in substantial disease burden. To determine the prevalence, serotype distribution, and antimicrobial resistance profiles of clinical Salmonella isolates in Shenzhen, a 6-year surveillance study was conducted. Methods: Three sentinel hospitals were chosen and patients who visited the gastroenteritis clinics with acute diarrhea were enrolled. Salmonella isolates from the stool samples were subjected to serotyping, antimicrobial susceptibility testing to 24 antibiotics, and detection of resistance genes. Results: A total of 297 (5.7%) Salmonella strains were isolated from stool samples from 5,239 patients. Among the 42 serovars identified, serovar Typhimurium was the most common serotype which represented 39.7% of the isolates (118), followed by serovar Enteritidis (71, 23.9%), London (12, 4.0%), 4, 5, 12: i: - (11, 3.7%), and Senftenberg (8, 2.7%). A high frequency of resistance was found in ampicillin (70.6%), piperacillin (64.5%), tetracycline (63.5%), and streptomycin (54.3%). Resistance to ampicillin and tetracycline was observed in 95.3% of S. Typhimurium isolates; and nalidixic acid in 93.1% of S. Enteritidis isolates. Resistance to 5 or more antimicrobial agents was found in 78.8% of S. Typhimurium and 69.0% of S. Enteritidis isolates. Conclusions: Salmonella is an important cause of acute gastroenteritis and a broad range of serotypes are prevalent in Shenzhen, with Enteritidis and Typhimurium being the most common serovars. The high level of antibiotic resistance is of public health significance and ongoing monitoring combined with rational use of antibiotics are recommended.

General Microbiology

Salmonella

prevalence

serotype

antimicrobial resistance

diarrhea.

Salmonella is a main foodborne pathogen worldwide which causes an annual death of 230,000 due to foodborne disease [1]. Salmonella is also a common cause of foodborne outbreaks and transmitted by contaminated food such as beef, pork, tomato, and cucumbers [2-5]. Salmonella is prevalent throughout the year, but it was reported the most commonly detected between April and October in China [6]. Children less than 5 years old accounted for the largest proportion of infections [7, 8].

Over 2500 serovars have been reported [9], with serovar Enteritidis and Typhimurium being the most common serotypes causing gastroenteritis [10]. Salmonella isolates with different serovars vary in the pathogenicity, prevalence, and sensitivity to antibiotics. Salmonella Typhi and Salmonella Paratyphi are usually associated with higher mortality [11]. Some serovars were reported in only one single region of the world, such as Salmonella Rissen and Salmonella Weltevreden were only identified in Asia [12, 13]. Multi-drug resistance was the most common in S. Typhimurium [14].

Salmonellosis is not a severe infection, but the emergence of third-generation cephalosporins and multi-drug resistant isolates has raised concerns [15, 16]. The wide use of antibiotics in poultry and for empirical treatment of salmonellosis has led to the rising of drug resistance rate of Salmonella. A high resistance rate to at least one clinically important antimicrobial was found in the clinical and animal-derived isolates [16, 17]. A wide range of mechanisms were associated with cephalosporins and quinolone resistance, including mutation in the quinolone-resistance determining regions (QRDRs), overexpression of an efflux pump and acquisition of drug resistance plasmids [18].

A one-year surveillance was conducted in our previous research and Salmonella was found one of the main causes (12.1%) of acute infectious diarrhea in Shenzhen [19]. Nevertheless, the long-term trend of serotype distribution and antimicrobial resistance pattern of the Salmonella isolates were not defined. To improve our understanding of the prevalence of Salmonella in this region and thus provide basis for designing prevention and control strategies, we investigated the serotypes and antibiotic resistance of the isolates obtained from the surveillance network during 2013 and 2018.

Stool samples collection. Peking University Shenzhen Hospital (PKUSZH), Shenzhen Children’s Hospital (SCH), and The Eighth Affiliated Hospital, Sun Yat-Sen University (SYSU8H) were selected as sentinel hospitals. Stool samples were collected from outpatients who visited gastroenteritis clinic due to acute infectious diarrhea and agreed to take part in this study. Acute diarrhea was defined as over3 passages of loose, mucus-, watery, or bloody-stools during 24-hour period. The stool samples were examined for Salmonella sp. using CHROM agars. The clinical signs and demographic information were collected from electronic medical records.

A total of 5,239 cases (2,749 of whom were male) were included during study period. Among these patients, 3,870, 425, and 944 cases were enrolled from PKUSZH, SCH, and SYSU8H, respectively. Patients ranged in age from 0 to 96 years (median 30 years). Local population accounted for 60.4% of the patients. Of all the patients, 310 (5.9%) had fever, 635 (12.1%) had vomiting, and 50 (1.0%) had blood in stools, respectively. Of the patients over 5 years old, 2,098 (54.1%) had abdominal pain (Table 1). Overall, Salmonella was isolated from 297 (5.7%) of all cases.

Serotyping and antimicrobial susceptibility testing. The Salmonella sp. isolates were identified using Vitek-2 compact system (bioMerieux, France) and serotyped with a commercial serotyping kit (S&A company, S&A Reagent Lab, Bangkok, Thailand).

A total of 197 Salmonella isolates representing 26 serotypes were selected for antimicrobial susceptibility testing. Twenty-four antimicrobials (Oxoid, UK) including amikacin (30 micrograms (mcg), AK), ampicillin/sulbactam (20 mcg, SAM), ampicillin (10 mcg, AMP), aztreonam (30 mcg, ATM), cefepime (30 mcg, FEP), cefotaxime (30 mcg, CTX), cefoxitin (30 mcg, FOX), ceftazidime (30 mcg, CAZ), ceftriaxone (30 mcg, CRO), cephazolin (30 mcg, KZ), chloramphenicol (30 mcg, C), ciprofloxacin (5 mcg, CIP), gentamicin (10 mcg, CN), imipenem (10 mcg, IPM), levofloxacin (5 mcg, LEV), meropenem (10 mcg, MEM), nalidixic acid (30 mcg, NA), nitrofurantoin (300 mcg, F), norfloxacin (10 mcg, NOR), piperacillin (100 mcg, PRL), streptomycin (10 mcg, S), sulphamethoxazole/trimethoprim (25 mcg, SXT), tetracycline (30 mcg, TE), and trimethoprim (5 mcg, W) were tested using disk diffusion method.

The MacFarland 0.5 inoculums were prepared and swabbed on the entire surface of Mueller-Hinton agar (Huankai, China) and left to dry for 3-5 min. Antimicrobial susceptibility test discs (Oxoid, UK) were placed on the inoculated agar plate with a disc dispenser (Oxoid, UK) and incubated at 37℃ for 24h. After incubation, the diameter of inhibition zone was measured and the results were interpreted as susceptible, intermediate, and resistant according to the Clinical and Laboratory Standards Institute guideline (CLSI, 2019)[20]. Escherichia coli strain ATCC 25922 was used as quality control.

The multiple antibiotic resistance (MAR) index was the ratio between the number of antibiotics to which the organism was resistant and the number of antibiotics tested. Multi-drug resistant (MDR) was defined as resistant to three or more different classes of antimicrobial agents.

Detection of target gene mutations. A total of 21 fluoroquinolone resistant isolates were chosen to screen for the mutations of the gyrA, gyrB, parC, and parE genes in the QRDRs. The bacterial nucleic acid was extracted using QIAamp DNA Mini Kit (Qiagen GmbH, Hilden, Germany) and subjected to PCR amplification using Taq PCR Master Mix Kit (Qiagen GmbH, Hilden, Germany), according to the manufacturer’s recommended protocols. The PCR products were sent to Sangon (Shanghai, China) for sequencing and the results were analyzed using BLAST (PubMed). The primers used for PCR amplification and sequencing were listed in Table 2.

Serotyping results. A total of 42 serovars were identified in the 285 Salmonella isolates and additional 12 strains were un-typable. Serovar Typhimurium (118, 39.7%) was the most common serotype, followed by serovar Enteritidis (71, 23.9%), London (12, 4.0%), 4, 5, 12: i: - (11, 3.7%), and Senftenberg (8, 2.7%). A total of 46 isolates with uncommon serotypes were found, including serovar Virchow, Corvallis, Vilvoorde, and Sarajane (Table 3).

Of the 118 S. Typhimurium isolates, 87 (73.7%) were recovered from children aged below 5 years old. Eight of 11 serovar 4, 5, 12: i: - strains were isolated from this age group, while similar detection rate of S. Enteritidis strains was observed in each age group. Of the 72 isolates with other serotypes, 51 (70.8%) were isolated from adults aged between 20 ~ 59 years old (Table 4).

Age and monthly distribution. The highest detection rate was observed in the age group of 5 ~ 9 years (15.1%), followed by <5 years (10.1%) and 30 ~ 39 years (4.9%). The age group of over 60 years showed the lowest prevalence (2.8%). A high prevalence of S. Typhimurium infection was seen in the young children aged less than 5 years (6.4%) and 5~9 years old (5.5%). In the age group of 5 ~ 9 years, serovar Enteritidis and 4, 5, 12: i: - were the other two common serotypes (Table 4).

The highest detection rate was seen in August (11.01%), followed by September (8.56%), June (8.49%), and October (7.88%). The detection rate between May and November (8.19%) was significantly higher than that between December and April (1.89%). Similar seasonal distribution was also observed in the serovar Typhimurium isolates (Figure 1).

Antimicrobial resistance profile. The highest rate of resistance was found in ampicillin (139, 70.6%), followed by piperacillin (127, 64.5%), tetracycline (125, 63.5%), streptomycin (107, 54.3%), cefazolin (87, 44.2%), and sulphamethoxazole/trimethoprim (75, 38.1%). The resistance to ampicillin and tetracycline was observed in 81 (95.3%) of S. Typhimurium isolates. Twenty-seven (93.1%) of S. Enteritidis isolates were resistant to nalidixic acid (Table 5). Five out of 8 S. Senftenberg isolates were susceptible to all the tested antibiotics. Among the 163 isolates resistant to three or more antimicrobial agents, 82 and 23 were found in S. Typhimurium and S. Enteritidis isolates, respectively. The MAR index of 123 isolates was over 0.21. The highest MAR index (0.71) was found in a serogroup B un-typable strain.

Mutations with QRDRs. The mutation of amino acids 87 in gyrA was seen in 14 isolates. Ten strains were identified with mutation in gyrB. A single base change in amino acids 67, 75, 77, 117, and 123 in parC were found in 5 of the tested strains. The mutation of codons 500 and 509 in parE was found in 3 and 7 isolates, respectively (Table 6).

Salmonella is an important causative microorganism of acute gastroenteritis, which was shown in the detection rate during 2013 and 2018 (4.2%~6.8%). The detection rate was lower compared with our previous study (12.1%) which incorporated PCR method [19], but it was comparable to another study (4.8%) conducted in Guangzhou using conventional assay [23]. A rate of 4.5% was observed in a large laboratory-based surveillance study in Guangdong province during 2009 and 2012, suggesting the continued prevalence in this region [17].

A broad distribution of serotypes was also reported in another study conducted in Shenzhen [24]. Apart from the detection rate, this study provided the trend of prevalence over a long period and antimicrobial resistance data, and identified some rare serotypes.

The detection rate between May and November was significantly higher compared with that in other months, which might be associated with high temperature. Hot weather contributed to bacterial growth and the chance of consumption of insufficiently heat-treated food or salad was higher. A linear association between temperature and the number of reported cases of salmonellosis was found and it was proven that higher temperature was associated with Salmonella infections [25]. As a result, the sporadic cases and salmonellosis outbreak were commonly found during this period [17].

The high incidence of Salmonella infection in children was consistent with another study where a recovery rate of 17.2% in children was reported [15]. The high frequency of infections in children could be attributed to the behavior such as frequent contact with contaminated limbs, consumption of contaminated food or water, or close contacts with an asymptomatic caretaker [23]. S. Typhimurium and S. Enteritidis were the most common serovars in children aged below 5 years old, which represented 75.4% (104/138) of the isolates, in accordance with other studies [15, 17]. The high frequency of multi-drug resistance in S. Typhimurium posed the difficulties in treating pediatric patients. Some measures such as good hygiene, proper hand washing, and education of their guardians were recommended to reduce the disease burden of salmonellosis in children.

Wide distribution of serotypes might be another reason of the continued prevalence of Salmonella infections. Apart from S. Typhimurium and S. Enteritidis, a broad range of uncommon serovars including Vilvoorde and Sarajane were identified, indicating the wide sources of Salmonella. As one of the major pathogenic bacteria in Chinese food commodities [26], Salmonella was commonly isolated from beef, pork, and poultry meat [27, 28]. Agona, Corvallis, and Kentucky were reported the dominant serotypes in chicken samples, while Typhimurium, Rissen, and Derby were the most common in pork samples [16]. Serovar Gallinarum-pullorum was isolated from a 24-year-old male patient with mild diarrhea. S. Gallinarum-pullorum was generally regarded as chicken-derived which causing little public health concern. However, occasional infections in human were reported following consumption of heavily contaminated food and low detection rate was found in humans between 1982 and 1992 [29]. Transient illness caused by large number of S. Gallinarum-pullorum was observed in both volunteers [30] and our case. Although the contaminated raw meat was not considered as a food safety risk due to the thorough cooking tradition, it was often associated with direct exposure to enteric pathogens and cross-contamination of ready-to-eat foods [31]. As a result, contamination from food handlers, or the consumption of contaminated or cross contaminated food may lead to the Salmonella infections.

Salmonella infections are normally associated with self-limiting diarrhea and antimicrobial therapy was not indicated, but appropriate antimicrobial treatment could be life-saving in severe cases. In addition, antibiotic treatment with ciprofloxacin or fluoroquinolones was recommended for Salmonella infections in infants less than 3 months of age due to the high risk of bacteremia and extraintestinal complications [32, 33]. The occurrence of multiple drug resistant strains raised the importance of antibiotics resistance surveillance. The high level of resistance to the first-line agents: ampicillin, sulphamethoxazole/trimethoprim, and chloramphenicol was also observed in other studies [23]. A similar profile was also found in the isolates from food-producing animals [34], suggesting the careful use of antibiotics in breeding industry was necessary.

The frequency of multiple drug resistance was common. Resistance to 5 or more antibiotics was commonly observed in S. Enteritidis (69.0%) and S. Typhimurium (78.8%). The occurrence of multidrug resistant (MDR) strains was reported to be associated with coexistence of resistance-related genes [14] and their transmission led to great difficulties in treatments. The resistance to first-line drugs of treating severe infections, such as third-generation cephalosporins and fluoroquinolones were of clinical concerns. The emergence of MDR isolates and increasing resistance to important antibiotics suggested the prevention measures and ongoing surveillance of antibiotic resistance were needed to control the infections.

The resistance to ciprofloxacin was mediated by multiple mechanisms [35], and the main mechanism of mutations in QRDRs were investigated in this study. A high frequency of mutations in the gyrA, gyrB, parC, and parE gene were found, indicating the need of long-term surveillance on QRDRs. In the isolates absence of chromosomal mutations, other mechanisms such as overexpression of efflux pump and mutations of other elements might contribute to the resistance [36, 37]. Due to the small sample size and complexity of resistance mechanisms, the association between the detected mutations and resistant phenotypes was difficult to identify. But it was investigated in other studies, such as isolates with a mutation in both gyrA and parC were more susceptible to ciprofloxacin than the isolates with a mutation in gyrA alone [38].

Salmonella was an important causative microorganism of acute diarrhea in this region. A total of 42 serovars and 12 un-typable strains were identified from the 297 isolates during 2013 and 2018. S. Typhimurium and S. Enteritidis were the most common serotypes. The highest detection rate was found in the age group of less than 9 years old and during June and October. The highest rate of resistance was found in ampicillin (70.6%), followed by piperacillin (64.5%), tetracycline (63.5%), streptomycin (54.3%), cefazolin (44.2%), and sulphamethoxazole/trimethoprim (38.1%). Resistant to 5 or more antibiotics was most common in serotype Typhimurium (78.8%) and Enteritidis (69.0%). An increasing trend of resistant rate to third-generation cephalosporins and multi-drug resistance, and a high frequency of mutations in QRDRs were observed, which raised the awareness of rational use of antibiotics and ongoing surveillance.

Ethical approval.

All aspects of the study were performed in accordance with national ethics regulations and approved by the Ethics Committees of the participated organizations, including Shenzhen Center for Disease Control and Prevention, Futian District Center for Disease Control and Prevention, and the sentinel hospitals. Participants received information regarding the purpose of this study and of their right to confidentiality. Written consent was obtained from the participants or the parents or guardians of the pediatric patients.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding authors on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

HS, JZ, and YO were involved in the collection of samples and detection of Salmonella isolates. TH detected the antibiotic resistant genes. HC collected the clinical data. WM, SC, and LZ helped analyzed data. QH and YZ designed this study. HS and YZ drafted and revised this manuscript.

Funding

This research was supported by Natural Science Foundation of Guangdong Province (NO.2018A0303130119), Sanming Project of Medicine in Shenzhen (NO. SZSM201811071 and SZSM201612023), Futian District Public Health Research Project (NO. FTWS2019067 and FTWS2019073), and Seeding Program of Shenzhen Hospital of Southern Medical University (NO.2016MM07 and 2018MM01).

Acknowledgements

We thank the staff from Peking University Shenzhen Hospital, Shenzhen Children’s Hospital, and The Eighth Affiliated Hospital, Sun Yat-Sen University who participated in the study.

Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, Praet N, Bellinger DC, de Silva NR, Gargouri N et al: World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Med 2015, 12(12):e1001923.
Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ: Outbreak-associated Salmonella enterica serotypes and food Commodities, United States, 1998-2008. Emerg Infect Dis 2013, 19(8):1239-1244.
Muller L, Kjelso C, Frank C, Jensen T, Torpdahl M, Soborg B, Dorleans F, Rabsch W, Prager R, Gossner CM et al: Outbreak of Salmonella Strathcona caused by datterino tomatoes, Denmark, 2011. Epidemiol Infect 2016, 144(13):2802-2811.
Marshall KEH, Tewell M, Tecle S, Leeper M, Sinatra J, Kissler B, Fung A, Brown K, Wagner D, Trees E et al: Protracted Outbreak of Salmonella Newport Infections Linked to Ground Beef: Possible Role of Dairy Cows - 21 States, 2016-2017. MMWR Morb Mortal Wkly Rep 2018, 67(15):443-446.
Laughlin M, Bottichio L, Weiss J, Higa J, McDonald E, Sowadsky R, Fejes D, Saupe A, Provo G, Seelman S et al: Multistate outbreak of Salmonella Poona infections associated with imported cucumbers, 2015-2016. Epidemiol Infect 2019, 147:e270.
Ran L, Wu S, Gao Y, Zhang X, Feng Z, Wang Z, Kan B, Klena JD, Lo Fo Wong DM, Angulo FJ et al: Laboratory-based surveillance of nontyphoidal Salmonella infections in China. Foodborne Pathog Dis 2011, 8(8):921-927.
Besser JM: Salmonella epidemiology: A whirlwind of change. Food Microbiol 2018, 71:55-59.
Chen C, Wang LP, Yu JX, Chen X, Wang RN, Yang XZ, Zheng SF, Yu F, Zhang ZK, Liu SJ et al: Prevalence of Enteropathogens in Outpatients with Acute Diarrhea from Urban and Rural Areas, Southeast China, 2010-2014. Am J Trop Med Hyg 2019, 101(2):310-318.
Su LH, Chiu CH: Salmonella: clinical importance and evolution of nomenclature. Chang Gung Med J 2007, 30(3):210-219.
Qi X, Li P, Xu X, Yuan Y, Bu S, Lin D: Epidemiological and Molecular Investigations on Salmonella Responsible for Gastrointestinal Infections in the Southwest of Shanghai From 1998 to 2017. Front Microbiol 2019, 10:2025.
Buckle GC, Walker CL, Black RE: Typhoid fever and paratyphoid fever: Systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2012, 2(1):010401.
Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM: Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 2011, 8(8):887-900.
Galanis E, Lo Fo Wong DM, Patrick ME, Binsztein N, Cieslik A, Chalermchikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC et al: Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg Infect Dis 2006, 12(3):381-388.
Wang J, Li Y, Xu X, Liang B, Wu F, Yang X, Ma Q, Yang C, Hu X, Liu H et al: Antimicrobial Resistance of Salmonella enterica Serovar Typhimurium in Shanghai, China. Front Microbiol 2017, 8:510.
Li Y, Xie X, Xu X, Wang X, Chang H, Wang C, Wang A, He Y, Yu H, Wang X et al: Nontyphoidal salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog Dis 2014, 11(3):200-206.
Zhang L, Fu Y, Xiong Z, Ma Y, Wei Y, Qu X, Zhang H, Zhang J, Liao M: Highly Prevalent Multidrug-Resistant Salmonella From Chicken and Pork Meat at Retail Markets in Guangdong, China. Front Microbiol 2018, 9:2104.
Liang Z, Ke B, Deng X, Liang J, Ran L, Lu L, He D, Huang Q, Ke C, Li Z et al: Serotypes, seasonal trends, and antibiotic resistance of non-typhoidal Salmonella from human patients in Guangdong Province, China, 2009-2012. BMC Infect Dis 2015, 15:53.
Eguale T, Birungi J, Asrat D, Njahira MN, Njuguna J, Gebreyes WA, Gunn JS, Djikeng A, Engidawork E: Genetic markers associated with resistance to beta-lactam and quinolone antimicrobials in non-typhoidal Salmonella isolates from humans and animals in central Ethiopia. Antimicrob Resist Infect Control 2017, 6:13.
Shen H, Zhang J, Li Y, Xie S, Jiang Y, Wu Y, Ye Y, Yang H, Mo H, Situ C et al: The 12 Gastrointestinal Pathogens Spectrum of Acute Infectious Diarrhea in a Sentinel Hospital, Shenzhen, China. Front Microbiol 2016, 7:1926.
Humphries RM, Abbott AN, Hindler JA: Understanding and Addressing CLSI Breakpoint Revisions: a Primer for Clinical Laboratories. J Clin Microbiol 2019, 57(6).
Fabrega A, du Merle L, Le Bouguenec C, Jimenez de Anta MT, Vila J: Repression of invasion genes and decreased invasion in a high-level fluoroquinolone-resistant Salmonella typhimurium mutant. PloS one 2009, 4(11):e8029.
Randall LP, Coldham NG, Woodward MJ: Detection of mutations in Salmonella enterica gyrA, gyrB, parC and parE genes by denaturing high performance liquid chromatography (DHPLC) using standard HPLC instrumentation. J Antimicrob Chemoth 2005, 56(4):619-623.
Liang B, Xie Y, He S, Mai J, Huang Y, Yang L, Zhong H, Deng Q, Yao S, Long Y et al: Prevalence, serotypes, and drug resistance of nontyphoidal Salmonella among paediatric patients in a tertiary hospital in Guangzhou, China, 2014-2016. J Infect Public Health 2019, 12(2):252-257.
Long LD, Wei HJ, WU SJ, Jiang PS, LI HJ, Zhuo F: Characteristics of drug resistance and molecular typing for Salmonella in diarrhea patients from four hospitals in Shenzhen. Chinese Journal of Zoonoses 2017, 33(10):897-902.
Kovats RS, Edwards SJ, Hajat S, Armstrong BG, Ebi KL, Menne B: The effect of temperature on food poisoning: a time-series analysis of salmonellosis in ten European countries. Epidemiol Infect 2004, 132(3):443-453.
Paudyal N, Pan H, Liao X, Zhang X, Li X, Fang W, Yue M: A Meta-Analysis of Major Foodborne Pathogens in Chinese Food Commodities Between 2006 and 2016. Foodborne Pathog Dis 2018, 15(4):187-197.
Yang X, Wu Q, Zhang J, Huang J, Chen L, Wu S, Zeng H, Wang J, Chen M, Wu H et al: Prevalence, Bacterial Load, and Antimicrobial Resistance of Salmonella Serovars Isolated From Retail Meat and Meat Products in China. Front Microbiol 2019, 10:2121.
Li Y, Pei XY, Zhang XL, Wu LL, Liu Y, Zhou HD, Ma GZ, Chen QX, Liang H, Yang DJ: A surveillance of microbiological contamination on raw poultry meat at retail markets in China. Food Control 2019, 104:99-104.
Shivaprasad HL: Fowl typhoid and pullorum disease. Rev Sci Tech 2000, 19(2):405-424.
Mc CN, Eisele CW: Experimental human salmonellosis. IV. Pathogenicity of strains of Salmonella pullorum obtained from spray-dried whole egg. J Infect Dis 1951, 89(3):259-265.
Yang B, Xi M, Wang X, Cui S, Yue T, Hao H, Wang Y, Cui Y, Alali WQ, Meng J et al: Prevalence of Salmonella on raw poultry at retail markets in China. J Food Prot 2011, 74(10):1724-1728.
Bula-Rudas FJ, Rathore MH, Maraqa NF: Salmonella Infections in Childhood. Adv Pediatr 2015, 62(1):29-58.
Haeusler GM, Curtis N: Non-typhoidal Salmonella in Children: Microbiology, Epidemiology and Treatment. Adv Exp Med Biol 2013, 764:13-26.
Lai J, Wu C, Wu C, Qi J, Wang Y, Wang H, Liu Y, Shen J: Serotype distribution and antibiotic resistance of Salmonella in food-producing animals in Shandong province of China, 2009 and 2012. Int J Food Microbiol 2014, 180:30-38.
Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, Zeng M: Salmonella Typhimurium and Salmonella Enteritidis Infections in Sporadic Diarrhea in Children: Source Tracing and Resistance to Third-Generation Cephalosporins and Ciprofloxacin. Foodborne Pathog Dis 2019, 16(4):244-255.
Lin D, Chen K, Wai-Chi Chan E, Chen S: Increasing prevalence of ciprofloxacin-resistant food-borne Salmonella strains harboring multiple PMQR elements but not target gene mutations. Sci Rep 2015, 5:14754.
Shen J, Yang B, Gu Q, Zhang G, Yang J, Xue F, Shao J, Yi X, Jiang Y: The Role of AcrAB-TolC Efflux Pump in Mediating Fluoroquinolone Resistance in Naturally Occurring Salmonella Isolates from China. Foodborne Pathog Dis 2017, 14(12):728-734.
Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ, White AP, Piddock LJ: Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother 2004, 48(10):4012-4015.

Download PDF

Journal Publication

published 06 Jul, 2020

Read the published version in BMC Microbiology →

Version 2

posted

You are reading this latest preprint version

Prevalence, serotypes, and antimicrobial resistance of Salmonella isolates from patients with diarrhea in Shenzhen, China

Status:

Journal Publication

Version 2

Abstract

Figures

Background

Materials And Methods

Results

Discussion

Conclusion

Declarations

References

Status:

Journal Publication

Version 2