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Xuesong Wang Department of Clinical Laboratory, Weifang People's Hospital, Weifang, Shandong, China

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Binglei Wang Department of ICU, Weifang People's Hospital, Weifang, Shandong, China

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Xiaohong Lu Department of Clinical Laboratory, Weifang People's Hospital, Weifang, Shandong, China

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Jie Ma Department of Clinical Laboratory, Weifang People's Hospital, Weifang, Shandong, China

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Zhanzhao Wang Department of Clinical Laboratory, Weifang People's Hospital, Weifang, Shandong, China

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https://orcid.org/0009-0007-7354-3160
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Yuhui Wang Department of Clinical Laboratory, Weifang People's Hospital, Weifang, Shandong, China

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https://orcid.org/0009-0002-8755-5035
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Abstract

This study examined the prevalence and antibiotic resistance pattern of blaCTX-M extended-spectrum β-lactamase positive Salmonella species isolated from a hospital in Weifang. Salmonella strains were isolated from hospitalized patients from January 2018 to April 2023. Whole-genome sequencing was performed by Illumina platform. CTX-M-producing Salmonella were identified by Comprehensive Antibiotic Research Database (CARD). Strain susceptibility to six antimicrobial agents was assessed by BD Phoenix™ M50 System. MLST analysis confirmed sequence types and additionally, serotypes were determined by SeqSero2. Genetic environments of blaCTX-M genes were analyzed by Isfinder and BLASTn. Single nucleotide polymorphisms were used to construct a phylogenetic tree to analyze homology. A total of 34 CTX-M-producing Salmonella were detected. The most prevalent serotype was Salmonella enterica subsp. enterica 1,4,[5],12:i:- (14/34, 41.18%), belonging to ST34, followed by Salmonella Enteritidis (10/34, 29.41%), belonging to ST11. The highest resistance rate was detected to ampicillin (97.06%), followed by ceftriaxone (94.12%) and ceftazidime (58.83%). In CTX-M-producing Salmonella five types of blaCTX-M genes were identified, the most prevalent was blaCTX-M-55 (47.06%, 16/34), followed by blaCTX-M-14, blaCTX-M-65, blaCTX-M-125, and blaCTX-M-27 at 26.47% (9/34), 11.77% (4/34), 8.82% (3/34), and 5.88% (2/34), respectively. Apart from blaCTX-M, 40 antibiotic resistance genes were also detected, conveying resistance to multiple drugs and the most frequent genes were namely, mcr-1.1, aph(6)-Id, aph(3″)-Ib, oqxAB, qnrB6, qnrS1. According to genetic environment analysis, the insertion sequence ISEcp1 was prevalent upstream of the blaCTX-M gene. Our study demonstrates that multiple resistance genes are carried by clinical isolates of Salmonella spp. however, the dominant ESBL genotype is CTX-M-55, that is associated with ISEcp1.

  • 1.

    Wegener HC, Hald T, Lo Fo Wong D, Madsen M, Korsgaard H, Bage F, et al. Salmonella control programs in Denmark. Emerg Infect Dis 2003; 9(7): 774780.

    • Search Google Scholar
    • Export Citation
  • 2.

    Sun T, Liu Y, Qin X, Aspridou Z, Zheng J, Wang X, et al. The prevalence and epidemiology of Salmonella in retail raw poultry meat in China: a systematic review and meta-analysis. Foods 2021; 10: 2757.

    • Search Google Scholar
    • Export Citation
  • 3.

    Chlebicz A, Śliżewska K. Campylobacteriosis, salmonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: a review. Int J Environ Res Public Health 2018; 15(5): 863.

    • Search Google Scholar
    • Export Citation
  • 4.

    Castro-Vargas RE, Herrera-Sánchez MP, Rodríguez-Hernández R, Rondón-Barragán IS. Antibiotic resistance in Salmonella spp. Isolated from poultry: a global overview. Vet World 2020; 13: 207084.

    • Search Google Scholar
    • Export Citation
  • 5.

    Scallan E, Mahon BE, Hoekstra RM, Griffin PM. Estimates of illnesses, hospitalizations and deaths caused by major bacterial enteric pathogens in young children in the United States. Pediatr Infect Dis J 2013; 32(3): 217221.

    • Search Google Scholar
    • Export Citation
  • 6.

    Mendes IF, Completo S, Vieira de Carvalho R, Jacinto S, Schäfer S, Correia P, et al. Salmonellosis in children at a Portuguese hospital: a retrospective dtudy. Acta Med Port 2023; 36(2): 96104.

    • Search Google Scholar
    • Export Citation
  • 7.

    Chen H, Qiu H, Zhong H, Cheng F, Wu Z, Shi T. Non-typhoidal Salmonella infections among children in Fuzhou, Fujian, China: a 10-year retrospective review from 2012 to 2021. Infect Drug Resist 2023; 16: 27372749.

    • Search Google Scholar
    • Export Citation
  • 8.

    Wu LJ, Luo Y, Shi GL, Li ZY. Prevalence, clinical characteristics and changes of antibiotic resistance in children with nontyphoidal Salmonella infections from 2009–2018 in Chongqing, China. Infect Drug Resist 2021; 14: 14031413.

    • Search Google Scholar
    • Export Citation
  • 9.

    Ngogo FA, Joachim A, Abade AM, Rumisha SF, Mizinduko MM, Majigo MV. Factors associated with Salmonella infection in patients with gastrointestinal complaints seeking health care at regional hospital in southern highland of Tanzania. BMC Infect Di 2020; 20(1): 135.

    • Search Google Scholar
    • Export Citation
  • 10.

    McDermott PF, Zhao S, Tate H. Antimicrobial resistance in nontyphoidal Salmonella. Microbiol Spectr 2018; 6(4). https://doi.org/10.1128/microbiolspec.

    • Search Google Scholar
    • Export Citation
  • 11.

    He Y, Wang J, Zhang R, Chen L, Zhang H, Qi X, et al. Epidemiology of foodborne diseases caused by Salmonella in Zhejiang Province, China, between 2010 and 2021. Front Public Health 2023; 11:1127925.

    • Search Google Scholar
    • Export Citation
  • 12.

    CDC. Antibiotic resistance threats in the United States, 2013; 2013. http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf#page=112.

    • Search Google Scholar
    • Export Citation
  • 13.

    Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, et al. 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): 244255.

    • Search Google Scholar
    • Export Citation
  • 14.

    Shi Q, Ye Y, Lan P, Han X, Quan J, Zhou M, et al. Prevalence and characteristics of ceftriaxone-resistant Salmonella in children’s hospital in Hangzhou, China. Front Microbiol 2021; 12: 764787.

    • Search Google Scholar
    • Export Citation
  • 15.

    D'Andrea MM, Arena F, Pallecchi L, Rossolini GM. CTX-M-type β-lactamases: a successful story of antibiotic resistance. Int J Med Microbiol 2013; 303(6–7): 305317.

    • Search Google Scholar
    • Export Citation
  • 16.

    Bauernfeind A, Grimm H, Schweighart S. A new plasmidic cefotaximase in a clinical isolate of Escherichia coli. Infection 1990; 18(5): 294298.

    • Search Google Scholar
    • Export Citation
  • 17.

    Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC Antimicrob Resist 2021; 3(3): dlab092.

    • Search Google Scholar
    • Export Citation
  • 18.

    Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 2017; 72(8): 21452155.

    • Search Google Scholar
    • Export Citation
  • 19.

    CLSI. Performance Standards for antimicrobial susceptibility testing, 31st ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2021. CLSI supplement M100.

    • Search Google Scholar
    • Export Citation
  • 20.

    Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. Plos Comput Biol 2017; 13(6): e1005595.

    • Search Google Scholar
    • Export Citation
  • 21.

    Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ, Tolstoy I, et al. Validating the AMRFinder tool and resistance gene Database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother 2019; 63(11).

    • Search Google Scholar
    • Export Citation
  • 22.

    Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50(4): 13551361.

    • Search Google Scholar
    • Export Citation
  • 23.

    Zhang S, den Bakker HC, Li S, Chen J, Dinsmore BA, Lane C, et al. SeqSero2: rapid and improved Salmonella serotype determination using whole-genome sequencing data. Appl Environ Microbiol 2019; 85(23): e01746-19.

    • Search Google Scholar
    • Export Citation
  • 24.

    Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics 2003. Chapter 10.

    • Search Google Scholar
    • Export Citation
  • 25.

    Kumar S, Stecher G, Li M, Knyaz C, Tamura K. Mega X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35(6): 15471549.

    • Search Google Scholar
    • Export Citation
  • 26.

    Letunic I, Bork P. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47(W1): W256W9.

  • 27.

    Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34(Database issue): D32-6.

    • Search Google Scholar
    • Export Citation
  • 28.

    Xu X, Chen Y, Pan H, Pang Z, Li F, Peng X, et al. Genomic characterization of Salmonella Uzaramo for human invasive infection. Microb Genom 2020; 6(7): mgen000401.

    • Search Google Scholar
    • Export Citation
  • 29.

    Seixas R, Santos TR, Machado J, Tavares L, Bernardo F, Semedo-Lemsaddek T, et al. Phenotypic and molecular characterization of Salmonella 1,4,[5],12:i:- R-type ASSuT isolates from humans, animals, and environment in Portugal, 2006–2011. Foodborne Pathog Dis 2016; 13(11): 633641.

    • Search Google Scholar
    • Export Citation
  • 30.

    Zheng D, Ma K, Du J, Zhou Y, Wu G, Qiao X, et al. Characterization of human origin Salmonella erovar 1,4,[5],12:i:- in astern China, 2014 to 2018. Foodborne Pathog Dis 2021; 18(11): 790797.

    • Search Google Scholar
    • Export Citation
  • 31.

    Kent RM, Fitzgerald GF, Hill C, Stanton C, Ross RP. Novel approaches to improve the intrinsic microbiological safety of powdered infant milk formula. Nutrients 2015; 7(2): 12171244.

    • Search Google Scholar
    • Export Citation
  • 32.

    Machado J, Bernardo F. Prevalence of Salmonella in chicken carcasses in Portugal. J Appl Bacteriol 1990; 69(4): 477480.

  • 33.

    European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 2019; 17(2): e05598.

    • Search Google Scholar
    • Export Citation
  • 34.

    Liang Z, Ke B, Deng X, Liang J, Ran L, Lu L, 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.

    • Search Google Scholar
    • Export Citation
  • 35.

    Sun H, Wan Y, Du P, Bai L. The epidemiology of monophasic Salmonella Typhimurium. Foodborne Pathog Dis 2020; 17(2): 8797.

  • 36.

    Takkinsatian P, Silpskulsuk C, Prommalikit O. Clinical features and antibiotic susceptibility of Salmonella gastroenteritis in children: a ten-year review. Med J Malaysia 2020; 75(6): 672676.

    • Search Google Scholar
    • Export Citation
  • 37.

    Song W, Shan Q, Qiu Y, Lin X, Zhu C, Zhuo Z, et al. Clinical profiles and antimicrobial resistance patterns of invasive Salmonella infections in children in China. Eur J Clin Microbiol Infect Dis 2022; 41(10): 12151225.

    • Search Google Scholar
    • Export Citation
  • 38.

    Cao C, Niu Q, Chen J, Xu X, Sheng H, Cui S, et al. Epidemiology and characterization of CTX-M-55-type extended-spectrum β-lactamase-producing Salmonella enterica Serovar Enteritidis isolated from patients in Shanghai, China. Microorganisms 2021; 9(2): 260.

    • Search Google Scholar
    • Export Citation
  • 39.

    Bonnet R. Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 2004; 48(1): 114.

  • 40.

    Sun Y, Zeng Z, Chen S, Ma J, He L, Liu Y, et al. High prevalence of bla(CTX-M) extended-spectrum β-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clin Microbiol Infect 2010; 16(9): 14751481.

    • Search Google Scholar
    • Export Citation
  • 41.

    Furlan JPR, Lopes R, Gonzalez IHL, Ramos PL, Stehling EG. Comparative analysis of multidrug resistance plasmids and genetic background of CTX-M-producing Escherichia coli recovered from captive wild animals. Appl Microbiol Biotechnol 2020; 104(15): 67076717.

    • Search Google Scholar
    • Export Citation
  • 42.

    Zhang J, Zheng B, Zhao L, Wei Z, Ji J, Li L, et al. Nationwide high prevalence of CTX-M and an increase of CTX-M-55 in Escherichia coli isolated from patients with community-onset infections in Chinese county hospitals. BMC Infect Dis 2014; 14: 659.

    • Search Google Scholar
    • Export Citation
  • 43.

    Zhang Y, Peng S, Xu J, Li Y, Pu L, Han X, et al. Genetic context diversity of plasmid-borne blaCTX-M-55 in Escherichia coli isolated from waterfowl. J Glob Antimicrob Resist 2022; 28: 185194.

    • Search Google Scholar
    • Export Citation
  • 44.

    Wyres KL, Hawkey J, Hetland MAK, Fostervold A, Wick RR, Judd LM, et al. Emergence and rapid global dissemination of CTX-M-15-associated Klebsiella pneumoniae strain ST307. J Antimicrob Chemother 2019; 74(3): 577581.

    • Search Google Scholar
    • Export Citation
  • 45.

    Poirel L, Decousser JW, Nordmann P. Insertion sequence ISEcp1B is involved in expression and mobilization of a bla(CTX-M) beta-lactamase gene. Antimicrob Agents Chemother 2003; 47(9): 29382945.

    • Search Google Scholar
    • Export Citation
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Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation
1954
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
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Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
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Publisher
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ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

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