Veterinary Research Forum
Vet Res Forum

Antibiotic resistance patterns, characteristics of virulence and resistance genes and genotypic analysis of Salmonella serotypes recovered from different sources

Document Type : Original Article

Authors

Seyed Mahdi Hosseini 1
Rahem Khoshbakht 2
Hami Kaboosi 1
Fatemeh Peyravii Ghadikolaii 3

1 Department of Microbiology, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran

2 Department of Pathobiology, Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

3 Department of Biology, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran

https://doi.org/10.30466/vrf.2024.2019507.4123
Abstract
The present study evaluated the Salmonella isolates obtained from various origins in Iran. Salmonella strains previously recovered and stored in the veterinary microbiology laboratory were serotyped and subjected to antibiotic susceptibility test, detection of the virulence and resistance genes by polymerase chain reaction (PCR), and genotyping by enterobacterial repetitive intergenic consensus-polymerase chain reaction (ERIC-PCR). All Salmonella isolates showed resistance to erythromycin and the most resistance rates were detected for trimethoprim (86.66%), ampicillin (75.00%), and sulfamethoxazole-trimethoprim (63.33%), respectively. In total, 86.33% of the isolates were known as multi-drug resistant and none of the isolates showed resistance to cefepime, nalidixic acid, imipenem, ceftriaxone, and polymyxin B. The virulence genes, invA, sdiA, and hilA besides the tetA resistance gene were identified in all 60 Salmonella strains. The most prevalent resistance genes were respectively tetC (70.00%), sul2 (58.33%), and ereA (55.00%). Statistical analysis revealed a significant difference between Salmonella serotypes associated with the sul1 resistance gene. In ERIC-PCR analysis, 14 distinct clusters were obtained. Statistically, there were significant relationships between the source and ERIC’s genomic pattern and between the serotype of Salmonella isolates and genotypic pattern of ERIC. According to the results, Salmonella serotypes from non-human sources had considerable resistance to different antibiotics and carried significant virulence determinants and resistance genes. In addition, ERIC-PCR showed relevant results in discriminating Salmonella serotypes from other sources.

Keywords

Antibiotic susceptibility
ERIC-PCR
Salmonella serovars
Virulence determinants

Subjects

  1. Jajere SM. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World 2019; 12(4): 504-521.
  2. Mthembu TP, Zishiri OT, El Zowalaty ME. Detection and molecular identification of Salmonella virulence genes in livestock production systems in South Africa. Pathogens 2019; 8(3): 124. doi: 10.3390/pathogens 8030124.
  3. Zou W, Al-Khaldi SF, Branham WS, et al. Microarray analysis of virulence gene profiles in Salmonella serovars from food/food animal environment. J Infect Dev Ctries 2011; 5(2): 94-105.
  4. Keshmiri MA, Nemati A, Askari Badouei M, et al. Clonal relatedness and antimicrobial susceptibility of Salmonella serovars isolated from humans and domestic animals in Iran: a one health perspective. Iran J Vet Res 2022; 23(2): 104-110.
  5. Castro-Vargas RE, Herrera-Sánchez MP, Rodríguez-Hernández R, et al. Antibiotic resistance in Salmonella isolated from poultry: a global overview. Vet World 2020; 13(10): 2070-2084.
  6. Britto CD, John J, Verghese VP, et al. A systematic review of antimicrobial resistance of typhoidal Salmonella in India. Indian J Med Res 2019; 149(2): 151-163.
  7. Li Q, Yin J, Li Z, et al. Serotype distribution, anti-microbial susceptibility, antimicrobial resistance genes and virulence genes of Salmonella isolated from a pig slaughterhouse in Yangzhou, China. AMB Express 2019; 9(1): 210. doi: 10.1186/s13568-019-0936-9.
  8. Guibourdenche M, Roggentin P, Mikoleit M, et al. Supplement 2003-2007 (No. 47) to the white-Kauffmann-Le minor scheme. Res Microbiol 2010; 161(1): 26-29.
  9. Performance Standards for Antimicrobial Susceptibility Testing. 31st ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2021
  10. Chen Z, Bai J, Wang S, et al. Prevalence, antimicrobial resistance, virulence genes and genetic diversity of Salmonella isolated from retail duck meat in Southern China. Microorganisms 2020; 8(3): 444. doi: 10.3390/microorganisms8030444.
  11. Van TT, Chin J, Chapman T, et al. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol 2008; 124(3): 217-223.
  12. Saladin M, Cao VT, Lambert T, et al. Diversity of CTX-M beta-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett 2002; 209(2): 161-168.
  13. Eckert C, Gautier V, Arlet G. DNA sequence analysis of the genetic environment of various blaCTX-M J Antimicrob Chemother 2006; 57(1): 14-23.
  14. Naas T, Mikami Y, Imai T, et al. Characterization of In53, a class 1 plasmid-and composite transposon-located integron of Escherichia coli which carries an unusual array of gene cassettes. J Bacteriol 2001; 183(1): 235-249.
  15. Faldynova M, Pravcova M, Sisak F, et al. Evolution of antibiotic resistance in Salmonella enterica serovar typhimurium strains isolated in the Czech Republic between 1984 and 2002. Antimicrob Agents Chemother 2003; 47(6): 2002-2005.
  16. Levings RS, Partridge SR, Lightfoot D, et al. New integron-associated gene cassette encoding a 3-N-aminoglycoside acetyltransferase. Antimicrob Agents Chemother 2005; 49(3): 1238-1241.
  17. Sengeløv G, Agersø Y, Halling-Sørensen B, et al. Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int 2003; 28(7): 587-595.
  18. Maynard C, Fairbrother JM, Bekal S, et al. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149: K91 isolates obtained over a 23-year period from pigs. Antimicrob Agents Chemother 2003; 47(10): 3214-3221.
  19. Toro CS, Farfán M, Contreras I, et al. Genetic analysis of antibiotic-resistance determinants in multidrug-resistant Shigella strains isolated from Chilean children. Epidemiol Infect 2005; 133(1): 81-86.
  20. Shams E, Firoozeh F, Moniri R, et al. Prevalence of plasmid-mediated quinolone resistance genes among extended-spectrum β-Lactamase-producing Klebsiella pneumoniae human isolates in Iran. J Pathog 2015; 2015: 434391. doi: 10.1155/2015/434391.
  21. Wang YP, Li L, Shen JZ, et al. Quinolone-resistance in Salmonella is associated with decreased mRNA expression of virulence genes invA and avrA, growth and intracellular invasion and survival. Vet Microbiol 2009; 133(4): 328-334.
  22. Halatsi K, Oikonomou I, Lambiri M, et al. PCR detection of Salmonella using primers targeting the quorum sensing gene sdiA. FEMS Microbiol Lett 2006; 259(2): 201-207.
  23. Chiu CH, Ou JT. Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J Clin Microbiol 1996; 34(10): 2619-2622.
  24. Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991; 19(24): 6823-6831.
  25. Khakabimamaghani S, Najafi A, Ranjbar R, et al. GelClust: a software tool for gel electrophoresis images analysis and dendrogram generation. Comput Methods Programs Biomed 2013; 111(2): 512-518.
  26. Sharma J, Kumar D, Hussain S, et al. Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control 2019; 102: 104-111.
  27. Abatcha MG, Effarizah ME, Rusul G. Prevalence, antimicrobial resistance, resistance genes and class 1 integrons of Salmonella serovars in leafy vegetables, chicken carcasses and related processing environments in Malaysian fresh food markets. Food Control 2018; 91: 170-180.
  28. Waghamare RN, Paturkar AM, Zende RJ, et al. Studies on occurrence of invasive Salmonella from unorganised poultry farm to retail chicken meat shops in Mumbai city, India. Int J Current Microbiol Appl Sci 2017; 6(5): 630-641.
  29. Yang B, Xi M, Wang X, et al. Prevalence of Salmonella on raw poultry at retail markets in China. J Food Prot 2011; 74(10): 1724-1728.
  30. Hosseininezhad B, Berizi E, Nader M, et al. Prevalence of Salmonella contamination in consumed eggs in Iran: a systematic review and meta-analysis study on published studies from 1996 to 2018. Vet World 2020; 13(12): 2743-2751.
  31. Khademi F, Vaez H, Ghanbari F, et al. Prevalence of fluoroquinolone-resistant Salmonella serotypes in Iran: a meta-analysis. Pathog Glob Health 2020; 114 (1): 16-29.
  32. Michael GB, Schwarz S. Antimicrobial resistance in zoonotic nontyphoidal Salmonella: an alarming trend? Clin Microbiol Infect 2016; 22(12): 968-974.
  33. Iwu CJ, Iweriebor BC, Obi LC, et al. Multidrug-resistant Salmonella isolates from swine in the Eastern Cape Province, South Africa. J Food Prot 2016; 79(7): 1234-1239.
  34. Mohammadzadeh M, Montaseri M, Hosseinzadeh S, et al. Antibiotic residues in poultry tissues in Iran: a systematic review and meta-analysis. Environ Res 2022; 204(Pt B): 112038. doi: 10.1016/j.envres. 2021.112038.
  35. Shao Y, Wang Y, Yuan Y, et al. A systematic review on antibiotics misuse in livestock and aquaculture and regulation implications in China. Sci Total Environ 2021; 798: 149205. doi: 10.1016/j.scitotenv. 2021.149205.
  36. McMillan EA, Jackson CR, Frye JG. Transferable plasmids of Salmonella enterica associated with antibiotic resistance genes. Front Microbiol 2020; 11: 562181. doi: 10.3389/fmicb.2020.562181.
  37. Herrera-Sánchez MP, Rodríguez-Hernández R, Rondón-Barragán IS. Molecular characterization of antimicrobial resistance and enterobacterial repetitive intergenic consensus-PCR as a molecular typing tool for Salmonella isolated from poultry and humans. Vet World 2020; 13(9): 1771-1779.
  38. Borah P, Dutta R, Das L, et al. Prevalence, antimicrobial resistance and virulence genes of Salmonella serovars isolated from humans and animals. Vet Res Commun 2022; 46(3): 799-810.
  39. Long L, You L, Wang D, et al. Highly prevalent MDR, frequently carrying virulence genes and antimicrobial resistance genes in Salmonella enterica serovar 4,[5], 12: i:-isolates from Guizhou Province, China. PloS One 2022; 17(5): e0266443. doi: 10.1371/journal. pone.0266443.
  40. Zenati F, Barguigua A, Nayme K, et al. Characterization of uropathogenic ESBL-producing Escherichia coli isolated from hospitalized patients in western Algeria. J Infect Dev Ctries 2019; 13(4): 291-302.
  41. Telli AE, Biçer Y, Telli N, et al. Pathogenic Escherichia coli and Salmonella in chicken carcass rinses: isolation and genotyping by ERIC-PCR. Pak Vet J 2022; 42(4): 493-498.
  42. Tawfik RG, Gawish MF, Abotaleb MM, et al. Genetic relationship between Salmonella isolates recovered from calves and broilers chickens in Kafr El-Sheikh city using ERIC PCR. Animals (Basel) 2022; 12(23): 3428. doi: 10.3390/ani12233428.
  43. Nath G, Maurya P, Gulati AK. ERIC PCR and RAPD based fingerprinting of Salmonella Typhi strains isolated over a period of two decades. Infect Genet Evol 2010; 10(4): 530-536.
  44. Firouzi R, Derakhshandeh A, Khoshbakht R. Distribution of sdiA quorum sensing gene and its two regulon among Salmonella serotypes isolated from different origins. Comp Clin Pathol 2014; 23: 1435-1439.
Veterinary Research Forum
Volume 15, Issue 9
September 2024
Pages 499-508

  • Receive Date 04 January 2024
  • Revise Date 31 January 2024
  • Accept Date 04 March 2024

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