Phenotypic and molecular characterization of Salmonella Enteritidis isolates

This is a retraction to: Phenotypic and molecular characterization of Salmonella Enteritidis isolates https://dergipark.org.tr/en/pub/auvfd/article/691746

Retraction Note

After this article was published, the corresponding author contacted the journal to notify concerns to the editors about the presence of repetitive band patterns in the dendrogram in Figure 1. The corresponding author requested the retraction of this article because the repetitive band patterns raise concerns about the scientific accuracy of the dendrogram. We sincerely apologize for any impact on the scientific community. The Editorial Board of the Ankara University Faculty of Veterinary Medicine journal has retracted this article.

Abstract

Salmonella spp. is the most frequently isolated foodborne pathogens causing human and animal diseases. The aim of this study was to investigate antimicrobial susceptibility profiles and the molecular typing of 200 Salmonella Enteritidis strains isolated from the patients’ stools between 2016 and 2019 in Turkey. The isolates were examined for antibiotic susceptibility patterns (21 antimicrobial agents) by Kirby-Bauer disc diffusion method or molecular typing by Pulsed-field gel electrophoresis (PFGE) and plasmid profiling. Although all isolates were susceptible to four antibiotics (suphamethoxazole/trimethoprim, chloramphenicol, streptomycin and trimethoprim), all were resistant to 15 different antibiotics. In the PFGE study performed with XbaI enzyme, all isolates were found to be related to each other according to similarity rates of 85% and above. There were two major clones, clone A and B. Clone A was divided into 6 pulsotypes (A1-A2-A3-A4-A5-A6) and clone B was divided into 3 pulsotypes (B1-B2-B3). Clone A had 87% similarity and Clone B had 90% similarity. The clustering rate was 86% (172/200). All isolates harboured 1-4 plasmid ranging in size from 2.5 to 57 kb and showed 6 plasmid profiles (P1-P6). All isolates carried the 57 kb plasmid individually or in combination with other plasmids. Most of the isolates 136 (68%) had P2 profile. Our findings indicate that the majority of all isolates were clonally related and had cross contamination problems. In this study, the importance of molecular typing methods in order to take more effective protection and control measures against Salmonella has been demonstrated and proposed to use such methods.

Keywords

• Antimicrobial resistance
• PFGE
• plasmid profiling
• Salmonella Enteritidis

References

1. Aktas Z, Day M, Kayacan CB, et al (2007): Molecular characterization of Salmonella Typhimurium and Salmonella Enteritidis by plasmid analysis and pulsed-field gel electrophoresis. Int J Antimicrob Agents, 30, 541-545.
2. Alali WQ, Hofacre CL, Mathis GF, et al (2013): Effect of essential oil compound on shedding and colonization of Salmonella enterica serovar Heidelberg in broilers. Poult Sci, 92, 836-841.
3. Aysev AD, Güriz H, Erdem B (2001): Drug resistance of Salmonella strains isolated from community infections in Ankara, Turkey, 1993-99. Scand J Infect Dis, 33, 420-422.
4. Bhowmick PB, Srikumar S, Devegowda D, et al (2012): Serotyping and molecular characterization for study of genetic diversity among seafood associated non typhoidal Salmonella serovars. Indian J Med Res, 135, 371-381.
5. Brichta-Harhay DM, Arthur TM, Bosilevac JM, et al (2011): Diversity of multidrug-resistant Salmonella enterica strains associated with cattle at harvest in the United States. Appl Environ Microbiol, 77, 1783-1796.
6. CLSI (2012): M100-S25: Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Fifth Informational Supplement.
7. De Oliveira FA, Pasqualotto AP, Da Silva WP, et al (2012): Characterization of Salmonella Enteritidis isolated from human samples. Food Research International, 45, 1000-1003.
8. Durmaz R, Otlu B, Koksal F, et al (2009): The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis, 62, 372-377.

9. Eng SK, Pusparajah P, Ab Mutalib NS, et al (2015): Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci, 8, 284-293.
10. Erdem B, Ercis S, Hascelik G, et al (2005): Antimicrobial resistance patterns and serotype distribution among Salmonella enterica strains in Turkey, 2000-2002. Eur J Clin Microbiol Infect Dis, 24, 220-225.
11. Gantois I, Ducatelle R, Pasmans F, et al (2009): Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Lett, 33, 718-738.
12. Gülmez D, Gür D, Hasçelik G, et al (2012): Ulusal Enterik Patojenler Laboratuvar Sürveyans Ağına (UEPLA) dahil olan bir üniversite hastanesinin deneyimleri: Dört yıllık Salmonella, Shigella ve Campylobacter verileri. Türk Mikrobiyol Cem Derg, 42, 85-92.
13. Hadimli HH, Pinarkara Y, Sakmanoğlu A, et al (2017): Serotypes of Salmonella isolated from feces of cattle, buffalo, and camel and sensitivities to antibiotics in Turkey. Turk J Vet Anim Sci, 41, 193-198.
14. Hoffmann S, Scallan E (2017): Epidemiology, Cost, and Risk Analysis of Foodborne Disease. 31-63. In: Christine D, Tim A, Richard S (Eds). Foodborne Diseases. Academic Press, San Diego.
15. Kado CI, Liu ST (1981): Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol, 145, 1365-1373.
16. Kaldhone P, Nayak R, Lynne AM, et al (2008): Characterization of Salmonella enterica serovar Heidelberg from turkey-associated sources. Appl Environ Microbiol, 74, 5038-5046.
17. Karakecili F, Cikman A, Karagoz A (2017): A Salmonella typhimurium outbreak associated with food served at a wedding reception. KLIMIK Journal, 30, 131-136.
18. Kemal J (2014): A review on the public health importance of bovine salmonellosis. J Veterinar Sci Technol, 5, 1.
19. Kilic A, Bedir O, Kocak N, et al (2010): Analysis of an outbreak of Salmonella enteritidis by repetitive-sequencebased PCR and pulsed-field gel electrophoresis. Internal Medicine, 49, 31-36.
20. Klemm EJ, Shakoor S, Page AJ, et al (2018): Emergence of an extensively drug-resistant Salmonella enterica Serovar Typhi Clone Harboring a promiscuous plasmid encoding resistance to fluoroquinolones and thirdgeneration cephalosporins. MBio, 20, e00105-18.
21. Küçüker MA, Tolun V, Helmuth R, et al (2000): Phage types, antibiotic susceptibilities and plasmid profiles of SalmonellaTyphimurium and Salmonella Enteritidis strains isolated in Istanbul, Turkey. Clin Microbiol Infect, 6, 593-599.
22. Kwon YK, Kim A, Kang MS, et al (2010): Prevalence and characterization of Salmonella Gallinarum in the chicken in Korea during 2000 to 2008. Poultry Sci, 89, 236-242.
23. Le Minor L (1984): Salmonella lignieres. 427-458. In: Krieg NR (Ed), Bergey’s Manual of Systematic Bacteriology. Volume 1. Baltimore: Williams and Wilkins.
24. Le Minor L, Rohde R (1989): Guidelines for the preperation of Salmonella antisera. Paris: WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur.
25. Nair DVT, Venkitanarayanan K, Kollanoor JA (2018): Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods, 7, 167.
26. Ozdemir K, Acar S (2014): Plasmid profile and pulsedfield gel electrophoresis analysis of Salmonella enterica isolates from humans in Turkey. PloS one, 9, e95976.
27. Pal M, Merera O, Abera F, et al (2015): A major foodborne disease of Global significance. Beverage Food World, 42, 21-24.
28. Pallavi S, Foley SL, Nayak R, et al (2013): Massively parallel sequencing of enriched target amplicons for highresolution genotyping of Salmonella serovars. Mol Cell Probes, 27, 80-85.
29. Pang JC, Chiu TH, Chiou CS, et al (2005): Pulsed field gel electrophoresis, plasmid profiles and phage types for the human isolates of Salmonella enterica serovar Enteritidis obtained over 13 years in Taiwan. J Appl Microbiol, 99, 1472-1483.
30. Pang JC, Chiu TH, Helmuth R, et al (2007): A pulsed field gel electrophoresis (PFGE) study that suggests a major world-wide clone of Salmonella enterica serovar Enteritidis. Int J Food Microbiol, 116, 305-312.
31. Peters TM, Berghold C, Brown D, et al (2007): Relationship of pulsed-field profiles with key phage types of Salmonella enterica serotype Enteritidis in Europe: results of an international multi-centre study. Epidemiol Infect, 135, 1274-1281.
32. Rivoal K, Protais J, Quéguiner S, et al (2009): Use of pulsed-field gel electrophoresis to characterize the heterogeneity and clonality of Salmonella serotype Enteritidis, Typhimurium and Infantis isolates obtained from whole liquid eggs. Int J Food Microbiol, 129, 180-186.
33. Sahan Ö, Aral EM, Aden MMA, et al (2016): Türkiye'deki broyler tavuk işletmelerinden izole edilen Salmonella serovarlarının antimikrobiyel direnç durumu. Ankara Univ Vet Fak Derg, 63, 1-6.
34. Shah DH, Zhou X, Kim HY, et al (2012): Transposon mutagenesis of Salmonella enterica serovar Enteritidis identifies genes that contribute to invasiveness in human and chicken cells and survival in egg albumen. Infect Immun, 80, 4203-4215.
35. Stevens A, Kerouanton A, Marault M, et al (2008): Epidemiological analysis of Salmonella enterica from beef sampled in the slaughterhouse and retailers in Dakar (Senegal) using pulsed-field gel electrophoresis and antibiotic susceptibility testing. Int J Food Microbiol, 123, 191-197.
36. Sukhnanand S, Alcaine S, Warnick LD, et al (2005): DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes. J Clin Microbiol, 43, 3688-3698.
37. Tankouo-Sandjong B, Kinde H, Wallace I (2012): Development of a sequence typing scheme for differentiation of Salmonella Enteritidis strains. FEMS Microbiol Lett, 331, 165-175.
38. Tegegne FM (2019): Epidemiology of salmonella and its serotypes in human, food animals, foods of animal origin, animal feed and environment. J Food Nutr Health, 2, 7-14.
39. Telli AE, Biçer Y, Kahraman HA, et al (2018): Presence and antibiotic resistance of Salmonella spp. isolated from chicken meat and giblets consumed in Konya, Turkey. Eurasian J Vet Sci, 34, 164-170.
40. Tenover FC, Arbeit RD, Goering RV (1997): How to select and interpret molecular strain typing methods for epidemiological studies of bacterial infections: a review for healthcare epidemiologists. Infect Control Hosp Epidemiol, 18, 426-439.
41. Threlfall EJ, Rowe B, Ward LR (1989): Subdivision of Salmonella enteritidis phage types by plasmid profile typing. Epidemiol Infect, 102, 459-465.
42. Tural Kara T, Özdemir H, Kurt F, et al (2015): Prevalence of Salmonella and Shigella spp. and Antibiotic Resistance Status in Acute Childhood Gastroenteritis. J Pediatr Inf, 9, 102-107.
43. Us E, Erdem B, Tekeli A, et al (2011): Salmonella serotip enteritidis izolatlarının plazmid profil analizi ve “pulsed field” jel elektroforezi ile incelenmesi. Mikrobiyol Bül, 45, 210-227.
44. Yoon KB, Song BJ, Shin MY, et al (2017): Antibiotic resistance patterns and serotypes of Salmonella spp. isolated at Jeollanam-do in Korea. Osong Public Health Res Perspect, 8, 211.
45. Zou W, Chen HC, Hise KB, et al (2013): Meta-analysis of pulsed-field gel electrophoresis fingerprints based on a constructed Salmonella database. PLoS One, 8, e59224.