Meta-analysis on the susceptibility of Salmonella to carbapenem antibiotics
QIU Tian1, TIAN Ting2, QIN Si1,2, HUO Xiang1,2
1. School of Public Health, Nanjing Medical University, Nanjing, Jiangsu 211166, China; 2. Jiangsu Provincial Center for Disease Control and Prevention, Nanjing, Jiangsu 210009, China
Abstract:Objective The multiple drug resistance of Salmonella is becoming more and more serious. Carbapenems are among the most potent antimicrobial agents that are available to treat multidrug resistance (MDR) bacteria. The purpose of this study was to perform a meta-analysis on the sensitivity of Salmonella to carbapenem antibiotics. Methods The relevant research data were retrieved from international and domestic databases, such as PubMed, Medrix and CNKI. R software was used to perform a meta-analysis on the sensitive rates of Salmonella to three commonly-used carbapenems, imipenem, ertapenem and meropenem, and then subgroup analyses were conducted. Results The overall sensitive rates of Salmonella to imipenem, ertapenem and meropenem were 0.997 (95%CI:0.995-1.000), 0.990 (95%CI:0.978-1.000) and 0.993 (95%CI:0.988-0.999), respectively. The sensitive rate for imipenem was 0.999 (95%CI: 0.998-1.000) for samples from clinical sources and 0.992 (95%CI: 0.984-1.000) for samples from non-clinical sources. No statistically significant difference was found in the sensitive rates in samples from different sources (P=0.168). The sensitive rate for ertapenem was 0.999 (95%CI: 0.997-1.000) for samples from clinical sources and 0.884 (95%CI: 0.809-0.965) for samples from non-clinical sources, showing a statistically significant difference in the sensitive rates in samples from different sources (P=0.006). The sensitive rate for meropenem was 0.997 (95%CI: 0.992-1.000) for samples from clinical sources and 0.972 (95%CI: 0.954-0.991) for samples from non-clinical sources, with a statistically significant difference in the sensitive rates in samples from different sources (P=0.033). Conclusion The overall sensitivity of Salmonella to carbapenems is high. Samples from clinical sources are more sensitive to ertapenem and meropenem than those from non-clinical sources.
[1] Havelaar AH,Kirk MD,Torgerson PR,et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010[J].PLoS Med,2015,12(12):e1001923. [2] Sodagari HR,Wang P,Robertson I,et al. Non-typhoidal Salmonella at the human-food-of-animal-origin interface in Australia[J]. Animals (Basel),2020,10(7):1192. [3] McDermott PF,Zhao S,Tate H. Antimicrobial resistance in-nontyphoidal Salmonella[J].Microbiol Spectr,2018,6(4). [4] 郝运, 周沁怡, 李锐, 等. 四川省动物源常见细菌耐药性现状[J].动物医学进展,2021,42(8):107-111. [5] Michael GB,Schwarz S. Antimicrobial resistance in zoonotic non-typhoidal Salmonella: an alarming trend?[J].Clin Microbiol Infect, 2016, 22(12):968-974. [6] 苏良,杨柳青,宋迎春,等.2015—2019年长沙市食源性疾病沙门菌血清分型和耐药情况分析[J].实用预防医学,2022,29(1):82-84. [7] 徐红红, 王艳, 张小荣, 等. 不同来源沙门菌的分子分型及耐药性研究[J].中国病原生物学杂志,2020,15(10):1131-1136,1143. [8] 郑之北, 郑伟, 汪皓秋, 等. 杭州地区多重耐药沙门氏菌的耐药特征[J].微生物学通报,2021,48(2):536-544. [9] Peruzy MF,Capuano F,Proroga YTR,et al. Antimicrobial susceptibility testing for Salmonella serovars isolated from food samples: five-year monitoring (2015-2019)[J].Antibiotics (Basel),2020,9(7):365. [10] 喻华, 徐雪松, 李敏, 等. 肠杆菌目细菌碳青霉烯酶的实验室检测和临床报告规范专家共识[J].中国感染与化疗杂志,2020, 20(6):671-680. [11] 国家卫生健康委员会. 碳青霉烯类抗菌药物临床应用专家共识(国卫办医函〔2018〕822号)[EB/OL]. (2018-09-21)[2021-10-14]. http://www.nhc.gov.cn/cms-search/xxgk/getManuscriptXxgk.htm?id=95f65ca473b44746b24590e94468b8ff. [12] 胡继华, 梁振刚, 郭主声,等. 耐碳青霉烯类肠杆菌科细菌的现状研究[J].中华医院感染学杂志, 2017, 27(4):725-728. [13] 中国碳青霉烯耐药肠杆菌科细菌感染诊治与防控专家共识编写组, 中国医药教育协会感染疾病专业委员会, 中华医学会细菌感染与耐药防控专业委员会. 中国碳青霉烯耐药肠杆菌科细菌感染诊治与防控专家共识[J].中华医学杂志, 2021, 101(36):2850-2860. [14] 王中新, 黄颖, 卢敏,等. 2000—2009年血流感染革兰阴性杆菌的构成及耐药性[J].中国抗生素杂志,2011,36(9):708-711. [15] 郭宝俊, 曹小燕, 何昱苇. 135株鼠伤寒沙门菌耐药酶检测及药物敏感性分析[J].中华医院感染学杂志,2011,21(20):4396-4398. [16] 崔恩博, 陈素明, 张成龙,等. 2009—2013年我国16省市社区获得性细菌性腹泻病原菌分布及临床耐药分析[J].传染病信息,2014,27(3):143-147. [17] 林爱红, 夏俊杰, 梁焯南,等. 2011-2017年深圳市食源性沙门菌血清分型及耐药分析[J].实用预防医学,2019,26(4):495-496. [18] 于宝东, 申红霞, 刘畅,等. 2014年青岛地区儿童腹泻患儿致病菌流行特点及耐药性分析[J].儿科药学杂志,2015,21(11):41-43. [19] 马志平, 陈瑶. 2017—2018年汕头中心医院50例腹泻儿童鼠伤寒沙门菌临床分析[J].广州医药,2020,51(1):66-69. [20] 郭辉, 李杰, 彭荣臻,等. 蚌埠地区沙门氏菌菌型分布及其药敏分析[J].中华全科医学,2013,11(3):475-476. [21] 谭丽丽. 儿童沙门菌感染44例流行病学特征和耐药分析[J].中国医药科学,2014,4(10):120-121,197. [22] 高智群, 林菁, 朱炜春,等. 儿童鼠伤寒沙门菌感染54例临床分析[J].当代医学,2020,26(16):147-149. [23] 沈丽珍, 陈素菜, 张爱鸣,等. 感染性腹泻患者病原菌分布与耐药性研究[J].中华医院感染学杂志,2015,25(23):5338-5340. [24] 王惠姣, 应华永, 陈小平. 七起食物中毒的病原菌分析[J]. 上海预防医学,2015,27(2):64-65. [25] 吴平芳, 贺连华, 石晓路,等. 深圳市食源性疾病监测中沙门菌的耐药性分析[J]. 中国卫生检验杂志,2012,22(3):581-583. [26] 肖幸华, 陈先来. 亚胺培南对医院内革兰阴性菌的抗菌活性分析[J].国际病理科学与临床杂志,2012,32(4):281-286. [27] 王向辉. 郑州儿童医院5岁以下腹泻儿童病原学检测分析[J].江苏预防医学,2018,29(6):679-680. [28] Aslam A,Ahmed Kharal S,Aslam M,et al. Trends of antimicrobial resistance in typhoidal strains of Salmonella in a tertiary care hospital in Pakistan[J].Cureus,2021,13(1):e12664. [29] Tawyabur M,Islam MS,Sobur MA,et al. Isolation and characterization of multidrug-resistant Escherichia coli and Salmonella spp. from healthy and diseased turkeys[J].Antibiotics (Basel), 2020,9(11):770-774. [30] Umair M,Siddiqui SA. Antibiotic susceptibility patterns of Salmonella typhi and Salmonella paratyphi in a tertiary care hospital in Islamabad[J].Cureus,2020,12(9):e10228. [31] Wang X, Wang H, Li T, et al. Characterization of Salmonella spp. isolated from chickens in central China[J].BMC Vet Res, 2020,16(1):299. [32] Li Y,Yang X,Zhang H,et al. Prevalence and antimicrobial susceptibility of Salmonella in the commercial eggs in China[J].Int J Food Microbiol, 2020,325:108623. [33] Rush EM,Amadi VA,Johnson R,et al. Salmonella serovars associated with grenadian tree boa (Corallus grenadensis) and their antimicrobial susceptibility[J].Vet Med Sci, 2020,6(3):565-569. [34] Kapena MS, Muma JB, Mubita CM, et al. Antimicrobial resistance of Escherichia coli and Salmonella in raw retail table eggs in Lusaka, Zambia[J].Vet World, 2020,13(11):2528-2533. [35] Elhariri M,Elhelw R,Selim S,et al. Virulence and antibiotic resistance patterns of extended-spectrum beta-lactamase-producing Salmonella enterica serovar Heidelberg isolated from broiler chickens and poultry workers: a potential hazard[J].Foodborne Pathog Dis, 2020,17(6):373-381. [36] Perin AP,Martins B,Barreiros M,et al. Occurrence, quantification, pulse types, and antimicrobial susceptibility of Salmonella spp. isolated from chicken meat in the state of Paraná, Brazil[J].Braz J Microbiol,2020,51(1):335-345. [37] Wang Z,He J,Li Q,et al. First detection of NDM-5-positive Salmonella enterica serovar Typhimurium isolated from retail pork in China[J].Microb Drug Resist, 2020,26(5):434-437. [38] Rasschaert G, Elst DV, Colson L, et al. Antibiotic residues and antibiotic-resistant bacteria in pig slurry used to fertilize agricultural fields[J].Antibiotics (Basel), 2020,9(1):34. [39] Qiu Y,Yang J,Chen Y,et al. Microbiological profiles and antimicrobial resistance patterns of pediatric bloodstream pathogens in China, 2016-2018[J].Eur J Clin Microbiol Infect Dis, 2021,40(4):739-749. [40] Ohanu ME, Iroezindu MO, Maduakor U, et al. Typhoid fever among febrile Nigerian patients: prevalence, diagnostic performance of the Widal test and antibiotic multi-drug resistance[J].Malawi Med J, 2019,31(3):184-192. [41] Lee YL,Lu MC,Shao PL,et al. Nationwide surveillance of antimicrobial resistance among clinically important Gram-negative bacteria, with an emphasis on carbapenems and colistin: results from the Surveillance of Multicenter Antimicrobial Resistance in Taiwan (SMART) in 2018[J].Int J Antimicrob Agents, 2019,54(3):318-328. [42] Sobur MA,Sabuj A,Sarker R,et al. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance[J].Vet World, 2019,12(7):984-993. [43] Wajid M, Awan AB, Saleemi MK, et al. Multiple drug resistance and virulence profiling of Salmonella enterica serovars typhimurium and enteritidis from poultry farms of Faisalabad, Pakistan[J].Microb Drug Resist, 2019,25(1):133-142. [44] Hussain A, Satti L, Hanif F, et al. Typhoidal Salmonella strains in Pakistan: an impending threat of extensively drug-resistant Salmonella typhi[J].Eur J Clin Microbiol Infect Dis, 2019,38(11):2145-2149. [45] Wajid M,Saleemi MK,Sarwar Y,et al. Detection and characterization of multidrug-resistant Salmonella enterica serovar Infantis as an emerging threat in poultry farms of Faisalabad, Pakistan[J].J Appl Microbiol, 2019,127(1):248-261. [46] Elkenany R,Elsayed MM,Zakaria AI,et al. Antimicrobial resistance profiles and virulence genotyping of Salmonella enterica serovars recovered from broiler chickens and chicken carcasses in Egypt[J].BMC Vet Res, 2019,15(1):124. [47] Fall-Niang NK,Sambe-Ba B,Seck A,et al. Antimicrobial resistance profile of Salmonella isolates in chicken carcasses in Dakar, Senegal[J].Foodborne Pathog Dis,2019,16(2):130-136. [48] Viana C,Sereno MJ,Pegoraro K,et al. Distribution, diversity, virulence genotypes and antibiotic resistance forSalmonella isolated from a Brazilian pork production chain[J].Int J Food Microbiol,2019,310:108310. [49] Yang X,Wu Q,Zhang J,et al. Prevalence, bacterial load, and antimicrobial resistance of Salmonella serovars isolated from retail meat and meat products in China[J].Front Microbiol, 2019,10:2121. [50] Garcia C, Hinostroza N, Astocondor L, et al. Characterization of ESBL-producing Salmonella enterica serovar infantis infection in humans, Lima, Peru[J].Am J Trop Med Hyg, 2019,101(4):746-748. [51] Zhang L,Fu Y,Xiong Z,et al. Highly prevalent multidrug-resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China[J].Front Microbiol, 2018,9:2104. [52] Aziz S, Malik L. Emergence of multi-resistant enteric infection in a paediatric unit of Karachi, Pakistan[J].J Pak Med Assoc, 2018,68(12):1848-1850. [53] Hosseinzadeh S, Saei HD, Ahmadi M, et al. Antimicrobial effect of licochalcone A and epigallocatechin-3-gallate against Salmonella typhimurium isolated from poultry flocks[J].Iran J Microbiol, 2018,10(1):51-58. [54] Liu XJ, Lyu Y, Li Y, et al. Trends in antimicrobial resistance against Enterobacteriaceae strains isolated from blood: a 10-year epidemiological study in mainland China (2004-2014)[J].Chin Med J (Engl), 2017,130(17):2050-2055. [55] Fardsanei F,Nikkhahi F,Bakhshi B,et al. Molecular characterization of Salmonella enterica serotype enteritidis isolates from food and human samples by serotyping, antimicrobial resistance, plasmid profiling, (GTG)5-PCR and ERIC-PCR[J]. New Microbes New Infect, 2016,14:24-30. [56] Bonardi S, Alpigiani I, Bruini I, et al. Detection of Salmonella enterica in pigs at slaughter and comparison with human isolates in Italy[J]. Int J Food Microbiol, 2016,218:44-50. [57] Singh L, Cariappa MP. Blood culture isolates and antibiogram of Salmonella: experience of a tertiary care hospital[J].Med J Armed Forces India, 2016,72(3):281-284. [58] Qi XL,Wang HX,Bu SR,et al. Incidence rates and clinical symptoms of Salmonella, Vibrio parahaemolyticus, and Shigella infections in China, 1998-2013[J].J Infect Dev Ctries, 2016,10(2):127-133. [59] Obeng-Nkrumah N,Labi AK,Addison NO,et al. Trends in paediatric and adult bloodstream infections at a Ghanaian referral hospital: a retrospective study[J].Ann Clin Microbiol Antimicrob, 2016,15(1):49. [60] Naik VK,Shakya S,Patyal A,et al. Isolation and molecular characterization of Salmonella spp. from chevon and chicken meat collected from different districts of Chhattisgarh, India[J].Vet World, 2015,8(6):702-706. [61] Morar A,Sala C,Imre K. Occurrence and antimicrobial susceptibility of Salmonella isolates recovered from the pig slaughter process in Romania[J]. J Infect Dev Ctries, 2015,9(1):99-104. [62] Sodagari HR,Mashak Z,Ghadimianazar A. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran[J]. J Infect Dev Ctries, 2015,9(5):463-469. [63] Yaxian J,Hui Z,Hua N,et al. Antimicrobial resistance surveillance of Salmonella isolates from the First People's Hospital of Yunnan Province, China[J]. J Infect Dev Ctries, 2015,9(4):333-337. [64] Salimian Rizi K, Najar Peerayeh S, Bakhshi B, et al. Prevalence of the bla CTX-M-1 group and their transferability in resistant clinical isolates of Salmonella serogroups from several hospitals of Tehran[J]. Iran J Microbiol, 2015,7(4):203-207. [65] Xiao Y,Wei Z,Shen P,et al. Bacterial-resistance among outpatients of county hospitals in China: significant geographic distinctions and minor differences between central cities[J]. Microbes Infect, 2015,17(6):417-425. [66] Rowlands RE, Ristori CA, Ikuno AA, et al. Prevalence of drug resistance and virulence features in Salmonella spp. isolated from foods associated or not with salmonellosis in Brazil[J]. Rev Inst Med Trop Sao Paulo, 2014,56(6):461-467. [67] Tang HJ, Chen CC, Zhang CC, et al. Use of Carbapenems against clinical, nontyphoid Salmonella isolates: results from in vitro and in vivo animal studies[J]. Antimicrob Agents Chemother, 2012,56(6):2916-2922. [68] Singh S,Agarwal RK,Tiwari SC,et al. Antibiotic resistance pattern among the Salmonella isolated from human, animal and meat in India[J]. Trop Anim Health Prod, 2012,44(3):665-674. [69] Pathak A,Marothi Y,Kekre V,et al. High prevalence of extended-spectrum β-lactamase-producing pathogens: results of a surveillance study in two hospitals in Ujjain, India[J]. Infect Drug Resist, 2012,5:65-73. [70] Alghoribi MF, Doumith M, Alrodayyan M, et al. S.enteritidis and S.typhimurium harboring SPI-1 and SPI-2are the predominant serotypes associated with human salmonellosis in Saudi Arabia[J]. Front Cell Infect Microbiol, 2019,9:187. [71] Okanda T, Haque A, Ehara T, et al. Characteristics of resistance mechanisms and molecular epidemiology of fluoroquinolone-nonsusceptible Salmonella enterica serovar typhi and paratyphi A isolates from a tertiary hospital in Dhaka, Bangladesh[J]. Microb Drug Resist, 2018,24(10):1460-1465. [72] Ali Shah SA, Nadeem M, Syed SA, et al. Antimicrobial sensitivity pattern of Salmonella typhi: emergence of resistant strains[J]. Cureus, 2020,12(11):e11778. [73] Viana C, Grossi JL, Sereno MJ, et al. Phenotypic and genotypic characterization of non-typhoidal Salmonella isolated from a Brazilian pork production Chain[J]. Food Res Int, 2020,137:109406. [74] Cummings KJ, Perkins GA, Khatibzadeh SM, et al. Antimicrobial resistance trends among Salmonella isolates obtained from horses in the northeastern United States (2001-2013)[J]. Am J Vet Res, 2016,77(5):505-513. [75] Suleyman G,Perri M,Vager D,et al. Characterization of Salmonella isangi possessing a CTX-M15 ESBL associated with an outbreak in a US hospital[J]. Diagn Microbiol Infect Dis, 2016,85(3):386-390. [76] Noda T, Murakami K, Etoh Y, et al. Increase in resistance to extended-spectrum cephalosporins in Salmonella isolated from retail chicken products in Japan[J]. PLoS One, 2015,10(2):e0116927. [77] Miller S, Amadi V, Stone D, et al. Prevalence and antimicrobial susceptibility of Salmonella spp. in small Indian mongooses (Herpestes auropunctatus) in Grenada, West Indies[J]. Comp Immunol Microbiol Infect Dis, 2014,37(4):205-210. [78] Liu C, Yoon EJ, Kim D, et al. Antimicrobial resistance in South Korea: a report from the Korean global antimicrobial resistance surveillance system (Kor-GLASS) for 2017[J]. J Infect Chemother, 2019,25(11):845-859. [79] 徐红红. 沙门氏菌的分子流行病学和耐药性状研究[D].扬州:扬州大学, 2021. [80] 颜卫, 赵莎莎, 丁丽军, 等. 江苏地区沙门氏菌流行现状调查及耐药性分析[J].江苏农业科学, 2019, 47(2):157-159. [81] Vaez H,Ghanbari F,Sahebkar A,et al. Antibiotic resistance profiles of Salmonella serotypes isolated from animals in Iran: a meta-analysis[J]. Iran J Vet Res,2020,21(3):188-197. [82] 郑林, 祝令伟, 郭学军, 等. 沙门氏菌主要流行血清型耐药性的研究进展[J].江苏农业科学, 2020, 48(6):8-12. [83] 付盼, 何磊燕, 王传清, 等. 中国儿童细菌耐药监测组2019年儿童细菌耐药监测[J].中国循证儿科杂志, 2021, 16(1):43-49. [84] 付盼, 王传清, 俞蕙, 等. 中国儿童细菌耐药监测组2018年儿童细菌感染及耐药监测[J].中国循证儿科杂志, 2019, 14(5):321-326. [85] Bengtsson-Palme J,Kristiansson E,Larsson D. Environmental factors influencing the development and spread of antibiotic resistance[J]. FEMS Microbiol Rev, 2018, 42(1):fux053. [86] Ford L, Haywood P, Kirk MD, et al. Cost of Salmonella infections in Australia, 2015[J].J Food Prot, 2019, 82(9):1607-1614. [87] O’Brien SJ,Larose TL,Adak GK,et al. Modelling study to estimate the health burden of foodborne diseases: cases, general practice consultations and hospitalisations in the UK, 2009[J].BMJ Open, 2016, 6(9):e011119. [88] Esan OB, Perera R, McCarthy N, et al. Incidence, risk factors, and health service burden of sequelae of campylobacter and non-typhoidal Salmonella infections in England, 2000-2015: a retrospective cohort study using linked electronic health records[J].J Infect,2020, 81(2):221-230. [89] Antonelli P,Belluco S,Mancin M,et al. Genes conferring resistance to critically important antimicrobials in Salmonella enterica isolated from animals and food: a systematic review of the literature, 2013-2017[J]. Res Vet Sci, 2019, 126:59-67. [90] 胡付品, 郭燕, 朱德妹, 等. 2020年CHINET中国细菌耐药监测[J].中国感染与化疗杂志, 2021, 21(4):377-387. [91] Tack B, Vanaenrode J, Verbakel JY, et al. Invasive non-typhoidal Salmonella infections in sub-Saharan Africa: a systematic review on antimicrobial resistance and treatment[J]. BMC Med, 2020, 18(1):212. [92] Fernández J, Guerra B, Rodicio MR. Resistance to carbapenems in non-typhoidal Salmonella enterica serovars from humans, animals and food[J].Vet Sci, 2018, 5(2):40. [93] McEwen SA,Collignon PJ. Antimicrobial resistance: a one health perspective[J]. Microbiol Spectr, 2018, 6(2):10.