Skip to contents Skip to Global Navigation Menu
  • KDCA
  • Contact us
  • E-Submission

PHRP : Osong Public Health and Research Perspectives

OPEN ACCESS. pISSN: 2210-9099. eISSN: 2233-6052
Search
Advanced Search

Articles

Page Path

Original Article

Antibiotic Resistance Patterns and Serotypes of Salmonella spp. Isolated at Jeollanam-do in Korea

Ki-Bok Yoona, Byung-Joon Songa, Mi-Yeong Shina, Hyun-Cheol Lima, Yeon-Hee Yoona, Doo-Young Jeona, Hoon Haa, Soo-In Yanga, Jung-Beom Kimb
Osong Public Health and Research Perspectives 2017;8(3):211-219.
Published online: June 30, 2017

aDivision of Microbiology, Jeollanam-do Institute of Health and Environment, Muan, Korea

bDepartment of Food Science and Technology, Sunchon National University, Suncheon, Korea

Corresponding author: Jung-Beom Kim, E-mail: okjbkim@sunchon.ac.kr
• Received: March 9, 2017   • Revised: April 23, 2017   • Accepted: May 23, 2017

Copyright ©2017, Korea Centers for Disease Control and Prevention

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

  • 8,899 Views
  • 61 Download
  • 19 Crossref
  • 17 Scopus
prev next

Full Article

Download PDF Download PDF
  • Objectives
    Few long-term studies have been conducted on the serotype and antibiotic resistance patterns of Salmonella speices (spp.) The aim of this study was to determine the serotypes and antibiotic resistance patterns of Salmonella spp. isolated at Jeollanam-do in Korea from 2004 to 2014.
  • Methods
    A total of 276 Salmonella samples were evaluated. Serotyping was carried out according to the Kauffmann–White scheme. Antibiotic susceptibility was determined using the Vitek II system with an AST-N169 card.
  • Results
    A total of 22 different serotypes were identified, and the major serotypes were Salmonella Enteritidis (116 strains, 42.0%) and Salmonella Typhimurium (60 strains, 21.7%). The highest resistance was observed in response to nalidixic acid (43.4%), followed by ampicillin (40.5%) and tetracycline (31.6%). Resistance to nalidixic acid was detected in 81.0% of S. Enteritidis. Multidrug resistance was detected in 43.3% of Salmonella spp. S. Enteritidis and S. Typhimurium presented the highest resistance (98.3%) and multidrug resistance rate (73.3%), respectively. The most highly observed antibiotic resistance pattern among Salmonella spp. in this study was ampicillin-chloramphenicol (14 strains, 5.7%),
  • Conclusion
    Overall, S. Enteritidis and S. Typhimurium showed higher antibiotic resistance than the other Salmonella serotypes tested in this study. Our study will provide useful information for investigating the sources of Salmonella infections, as well as selecting effective antibiotics for treatment.
  • Keywords: Salmonella spp.; antibiotic susceptibility; serotype
Salmonella is a notorious pathogen that causes gastroenteritis in humans, and 94 million cases of salmonellosis are globally reported every year [1]. Salmonella infection is mainly caused by foods such as meat, eggs, fish, and shellfish, and the symptoms include nausea, vomiting, abdominal pain, diarrhea, and fever [2,3]. Salmonella infection is one of the most common diseases in developed countries, and Salmonella speices (spp.) are frequently isolated from diarrhea patients in Korea [4]. In the United States, about 26% of all foodborne infections are estimated to be due to Salmonella spp., and the socioeconomic cost reached over one billion US dollar in 1987 [3,5,6]. In Korea, the medical expenses and productivity loss associated with salmonellosis were estimated to cost approximately 5.9 billion Korean won in 1996 [2]. Approximately 2,500 different serotypes of Salmonella spp. have been reported [7]. Serotypes serve as epidemiological markers, and specific Salmonella spp. serotypes are associated with human disease [8]. In Korea, Salmonella Typhi, which is related to human infection, was frequently detected in the early 1990s [9], and Salmonella Enteritidis and Salmonella Typhimurium, which are also related to human infection, are observed frequently [10–12]. Kim et al. [13] reported that S. Enteritidis and S. Typhimurium were major serotypes among Salmonella spp. isolated from Gwangju in Korea during 2000–2009.
Antibiotics, which are metabolites produced by microorganisms, inhibit the growth of other pathogenic microorganisms at low concentrations. Since the first use of penicillin in 1940, more than 5,000 antibiotics have been developed, with a variety in current use [14,15]. Antibiotics play a decisive role in treatment by killing the causative organisms of infectious diseases, reducing the socioeconomic loss caused by infectious diseases [16]. However, antibiotic-resistant microorganisms are increasing due to indiscreet use of antibiotics [3]. Based on global surveillance results, the World Health Organization [17] reported that the antibiotic resistance of Salmonella spp. has increased in past years. Kim et al. [13] reported that the patterns of bacterial antibiotic resistance are constantly changing, and the emergence of multi-drug-resistant Salmonella threatens public health worldwide [18].
Thus, determination of the serotypes and changing antibiotic resistance patterns of Salmonella spp. is needed to investigate infection sources and select effective antibiotics. The Korea Centers for Disease Control and Prevention (KCDC) summarized and published the nationwide incidence of salmonellosis as a part of a national monitoring program for acute diarrheal disease. Short-term studies have published the serotypes and antibiotic resistance patterns of Salmonella spp. associated with gastroenteritis in humans [3,7,11,19]. However, long-term studies are lacking. Thus, the aim of this study was to determine the serotypes and antibiotic resistance patterns of Salmonella spp. isolated at Jeollanam-do in Korea from 2004 to 2014.
1. Bacterial strains
A total of 276 stocked Salmonella spp. were evaluated in this study. These strains were isolated from national surveillance “laboratory surveillance for diarrheal disease” at Jeollanam-do and were commissioned by a public health center at Jeollanam-do in Korea from 2004 to 2014. All strains were stored at −70°C in Tryptone soy broth (Oxoid, Basingstoke, UK) containing 0.6% yeast extract (Oxoid) with 20% glycerol (Difco, Detroit, MI, USA). All strains were inoculated into 5 mL of Selenite broth (Oxoid) for reactivation, followed by incubation at 37°C for 18 hours. The enrichment cultures were streaked onto Brilliance Salmonella agar (BSA; Oxoid) and then incubated at 37°C for 18 hours. Presumptive colonies exhibiting a purple color during culture on BSA were selected for biochemical testing. One colony from each BSA was identified to reconfirm Salmonella spp. strains using the Vitek II system with a GNI card (bioMerieux Inc., Marcy l’Etoile, France) and then sub-cultured on Tryptone soy agar (TSA; Oxoid) for serotyping and antibiotic susceptibility testing.
2. Serotyping
Serotyping of Salmonella spp. strains was carried out according to the Kauffmann–White scheme [20]. Somatic (O) antigens of each Salmonella spp. strain were determined using the slide agglutination method, with polyvalent and monovalent O antigens provided from the KCDC. Further serotyping was performed with flagella (H) antisera (Difco) using the tube agglutination method. The O and H antigen agglutination results for each Salmonella spp. were combined, and specific serotypes were determined according to the Antigenic Formulae of the Salmonella serovars [21].
3. Antimicrobial susceptibility
Antibiotic susceptibilities of the isolated and collected Salmonella spp. strains were determined using the Vitek II system with an AST-N169 card (bioMerieux Inc.) according to the manufacturer’s instructions. All strains, sub-cultured onto TSA plates at 37°C overnight, were suspended in saline solution and then adjusted to a McFarland standard of 0.6 with a Vitek II DensiCHEK instrument (bioMerieux Inc.). Each adjusted bacterial solution (145 μL) was injected into 3 mL of saline solution, mixed well, and used for antibiotic susceptibility testing. Antibiotic susceptibilities of the Salmonella spp. strains were interpreted according to the standards [22] issued by the Clinical and Laboratory Standards Institute (CLSI). The following antibiotics were tested: ampicillin, amoxicillin/clavulanic acid, ampicillin/sulbactam, cefalothin, cefazolin, cefotetan, cefoxitin, cefotaxime, ceftriaxone, imipenem, amikacin, gentamycin, nalidixic acid, ciprofloxacin, tetracycline, chloramphenicol, and trimethoprim/sulfamethoxazole.
1. Serotypes of Salmonella strains
As shown in Table 1, a total of 22 different serotypes were divided among 276 Salmonella spp. tested in this study. Somatic (O) antigen groups observed were D (53.5%), B (31.2%), C (12.4%), A (0.7%), and E (0.4%). The major serotype was S. Enteritidis (116 strains, 42.0%), followed by S. Typhimurium (60 strains, 21.7%), S. I 4,[5],12:i:- (25 strains, 9.1%), S. Typhi (24 strains, 8.7%), and S. Thompson (22 strains, 8.0%), accounting for 89.5% of Salmonella spp. The 17 other serotypes had a low detection rate (10.5% combined).
2. Antibiotic resistance of Salmonella strains
Antibiotic resistance patterns of Salmonella spp. strains isolated from Jeollanam-do in Korea during 2004–2014 are shown in Table 2. The antibiotic resistance test was performed on five major serotypes: S. Enteritidis, S. Typhimurium, S. I 4,[5],12:i:-, S. Typhi, and S. Thompson. The highest resistance was observed in response to nalidixic acid (43.4%), followed by ampicillin (40.5%), tetracycline (31.6%), chloramphenicol (19.8%), cefalothin (11.3%), cefazolin (10.1%), cefoxitin (8.9%), and trimethoprim/sulfame-thoxazole (8.1%). Lower resistance was observed in response to amoxicillin/clavulanic acid (4.9%), cefotaxime (4.0%), and ceftriaxone (4.0%). All strains in this study were susceptible to imipenem and amikacin. As shown in Table 3, the resistance rate of each antibiotic differed among Salmonella serotypes. Overall, S. Enteritidis and S. Typhimurium showed higher antibiotic resistance than the other tested serotypes. The resistance rates for ampicillin were 70.0, 40.5, and 36.0% in S. Typhimurium, S. Enteritidis, and S. I 4,[5],12:i:-, respectively. Nalidixic acid showed a resistance rate of 81.0% in S. Enteritidis. The highest resistance observed was to trimethoprim/sulfamethoxazole, in S. Typhimurium (85.0%).
3. Multidrug resistance of Salmonella serotypes
The multidrug resistance of Salmonella serotypes isolated at Jeollanam-do from 2004 to 2014 is presented in Table 4. Of the 247 Salmonella samples, 51 (20.6%) were susceptible to all of the antibiotics tested in this study. The highest antibiotic susceptibility was observed in S. Thompson (20 strains, 90.9%), followed by S. Typhi (18 strains, 75.0%), S. I 4,[5],12:i:- (six strains, 24.0%), S. Typhimurium (five strains, 8.3%), and S. Enteritidis (two strains, 1.7%). Resistance to one antibiotic was observed in 89 (36.0%) samples, while multidrug resistance, defined as resistance to two or more antibiotics, was detected in 107 (43.3%) Salmonella samples. Multidrug resistance was observed most frequently in S. Typhimurium (44 strains, 73.3%), followed by S. Enteritidis (49 strains, 42.2%), S. I 4,[5],12:i:- (nine strains, 36.0%), S. Typhi (three strains, 12.5%), and S. Thompson (two strains, 9.0%). S. Enteritidis and S. Typhimurium presented the highest resistance (98.3%) and multidrug resistance rates (73.3%), respectively. Tables 5–9 present the antibiotic resistance patterns of the Salmonella serotypes. The most highly observed antibiotic resistance patterns among Salmonella spp. in this study were against ampicillin-chloramphenicol (14 strains, 5.7%), ampicillin-tetracycline-trimethoprim/sulfamethoxazole (11 strains, 4.5%), and ampicillin-amoxicillin/clavulanic acid-ampicillin/sulbactam-cefalothin-cefazolin-cefoxitin-tetracycline (10 strains, 4.0%). The most frequent antibiotic resistance patterns of Salmonella serotypes were ampicillin-chloramphenicol (14 strains, 12.1%) in S. Enteritidis, ampicillin-tetracycline-trimethoprim/sulfamethoxazole (10 strains, 16.7%) in S. Typhimurium, ampicillin-tetracycline (six strains, 24.0%) in S. I 4,[5],12:i:-, cefalothin-cefoxitin-chloramphenicol (three strains, 12.5%) in S. Typhi, and ampicillin-cefalothin-cefazolin-nalidixic acid (one strain, 4.5%) in S. Thompson.
Serotyping can provide useful epidemiological information on salmonellosis [23]. S. Enteritidis and S. Typhimurium were major serotypes among Salmonella spp. tested in this study, consistent with previous domestic [3,11–13] and overseas studies [7,24]. S. Typhi was also frequently detected, which is highly abundant in South and East Asia but rarely detected in North America and Europe [25], and causes typhoid fever, one of the most notable infectious diseases in Korea. S. Typhi was highly recovered before 1973, but its detection rate has decreased due to improved sanitation conditions in Korea [9]. The 8.7% detection rate of S. Typhi observed in our study is similar to a previous result reporting that S. Typhi constituted 7.9% of Salmonella isolates in Korea during 2004–2005 [11], but higher than its 1.5% detection rate in the Gwangju area during 2000–2009 [13]. S. Typhi was the fourth most prevalent serotype in this study, suggesting that continuous investigation of serotyping is important. S. I 4,[5],12:i:- was first reported in Spain in 2009 [26] and is an unexpressed mutant of phase 2 S. Typhimurium [3,26,27]. The detection rate of S. I 4,[5],12:i:-, which causes diseases in humans and animals, has recently increased in Korea [28].
Resistance rates to nalidixic acid, ampicillin, tetracycline, and chloramphenicol in Salmonella spp. in this study were similar to previous results; indicating that resistance to these antibiotics is common in Salmonella spp. [23,29]. These antibiotics are frequently used to treat salmonellosis [30]. Salmonella spp. tested in this study showed higher resistance rates to antibiotics such as ampicillin/sulbactam, cefalothin, cefazolin, and nalidixic acid compared to the resistance rates of Salmonella spp. isolated from the Gwangju area during 2000–2009 [13]. Our results show higher resistances to cephalosporin group antibiotics compared to previous results suggesting that most Salmonella spp. are merely sensitive to cephalosporins [3,13,31]. Antibiotic resistance profiles were different among Salmonella serotypes. S. Enteritidis and S. Typhimurium are two of the most frequently isolated foodborne pathogens [32], and both had higher antibiotic resistance rates compared with other Salmonella serotypes tested in this study. These results are consistent with worldwide studies [3,33,34]. In S. Enteritidis, resistance rates for ampicillin (40.5%), chloramphenicol (29.3%), and nalidixic acid (81.0%) were similar to the KCDC national survey results in 2009 [4] but higher than previous results [3] presenting resistance rates of 13.5, 7.7, and 5.4% for ampicillin, chloramphenicol, and nalidixic acid, respectively. Furthermore, similar resistance to these antibiotics has been reported in Salmonella spp. isolated in Brazil [23] and Turkey [34]. S. Typhimurium presented the highest rate of resistance to tetracycline (85.0%) among the antibiotics tested in this study, consistent with S. Typhimurium isolated in Seoul from 1999 to 2002 [35]. The KCDC [4] reported in 2009 that S. Typhimurium was highly resistant to tetracycline (60.4%). This is concerning, as tetracycline, a useful antibiotic agent against a wide range of bacteria, is frequently used to treat salmonellosis [36].
Salmonella spp. tested in this study presented a lower multidrug resistance rate (43.3%) compared with samples (52.6%) from the Gwangju area from 2000–2009 [13]. Of the S. Typhimurium samples, 44 out of 60 (73.3%) displayed multidrug resistance, consistent with the 70.5% multidrug resistance observed for S. Typhimurium in the Gwangju study [13]. The multidrug resistance of S. Typhimurium phage type DT104 causes global health problems [37]. Multidrug resistant Salmonella spp. threatens public health worldwide [18], and the antibiotic resistance pattern of Salmonella spp. can be altered [38]. The most highly observed antibiotic resistance pattern among Salmonella spp. in this study was ampicillin-chloramphenicol. Ampicillin and chloramphenicol are used to treat bacterial diseases such as meningitis, salmonellosis, and endocarditis, and combined chloramphenicol and ampicillin treatment is a useful therapy for salmonellosis [29,30]. Thus, it is not surprising that the ampicillin-chloramphenicol resistance pattern is the most highly observed. This highlights the important of preventing the overuse of antibiotics to reduce the multidrug resistance of Salmonella spp.
In conclusion, this study found that S. Enteritidis and S. Typhimurium were major serotypes in Salmonella spp., and the highest resistance was observed in response to nalidixic acid, followed by ampicillin and tetracycline. Our study will provide useful information for investigating the source and selecting effective antibiotics for Salmonella infection.
Acknowledgements
This research was supported by the Public Health and Environment Institute of Jeollanam-do, Republic of Korea.

CONFLICTS OF INTEREST

No potential conflict of interest relevant to this article was reported.

  • 1. Majowicz SE, Musto J, Scallan E, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010;50:882−9. https://doi.org/10.1086/650733.
  • 2. Bahk GJ, Roh WS. Estimates of cases and social economic costs of foodborne Salmonellosis in Korea. J Food Hyg Saf 1998;13:299−304.
  • 3. Park SG, Park SK, Jung JH, et al. Antibiotic susceptibility of Salmonella spp. isolated from diarrhoea patients in Seoul from 1996 to 2001. J Food Hyg Saf 2002;17:61−70.
  • 4. Korean Center for Diseases Control and Prevention. The prevalence and characteristics of bacteria causing acute diarrhea in Korea, 2009. Public Health Wkly Rep 2010;3:545−52.
  • 5. Foley SL, Lynne AM. Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 2008;86(14 Suppl). E173−87. https://doi.org/10.2527/jas.2007-0447.
  • 6. Galanis E, Wong DMALF, Patrick ME, et al. Web-based surveillance and global Salmonella distribution, 2000–2002. Emerg Infect Dis 2006;12:381−8. https://doi.org/10.3201/eid1203.050854.
  • 7. Matheson N, Kingsley RA, Sturgess K, et al. Ten years experience of Salmonella infections in Cambridge, UK. J Infect 2010;60:21−5. https://doi.org/10.1016/j.jinf.2009.09.016.
  • 8. Schutze GE, Flick EL, Pope SK, Lofgren JP, Kirby RS. Epidemiology of salmonellosis in Arkansas. South Med J 1995;88:195−9. https://doi.org/10.1097/00007611-199502000-00006.
  • 9. Shin HB, Jeong SH, Kim M, et al. Isolation trend of enteropathogenic bacteria in 1969–1998. Korean J Clin Microbiol 2001;4:87−95.
  • 10. Cho SH, Kim JH, Kim JC, et al. Surveillance of bacterial pathogens associated with acute diarrheal disease in the Republic of Korea during one year, 2003. J Microbiol 2006;44:327−35.
  • 11. Kim S, Kim SH, Chun SG, et al. Prevalence of Salmonella serovars isolated from domestic residents and overseas travelers in Korea, 2004–2005. J Bacteriol Virol 2006;36:69−72. https://doi.org/10.4167/jbv.2006.36.2.69.
  • 12. Hwang KW, Oh BY, Kim JH, et al. Antimicrobial resistance and multidrug resistance patterns of Salmonella enteric serovar Enteritidis isolated from diarrhea patients, Incheon. Korean J Microbiol 2009;45:99−104.
  • 13. Kim TS, Kim MJ, Kim SH, et al. Serotypes of Salmonella isolated from faeces of patients with acute diarrhoea in Gwangju area, Korea, during 2000–2009. Zoonoses Public Health 2012;59:482−9. https://doi.org/10.1111/zph.12011.
  • 14. Kim JM, Kim JS, Jung HC, et al. Antibiotic resistance of Helicobacter pylori isolated from Korean patients in 2003. Korean J Gastroenterol 2004;44:126−35.
  • 15. Sefton AM. Mechanisms of antimicrobial resistance. Drugs 2002;62:557−66.
  • 16. Ha KS, Park SJ, Shim WB, et al. Screening of MRSA (methicilline resistant staphylococcus aureus) and seb gene in producing strains isolated from food service environment of elementary schools. J Food Hyg Saf 2003;18:79−86.
  • 17. World Health Organization. The medical impact of antimicrobial use in food animals. In: Report and proceedings of a WHO meeting; 1997 Oct 13–17; Berlin, Germany. Geneva, WHO. 1997. WHO document WHO/EMC/ZOO/97.4.
  • 18. Rayamajhi N, Kang SG, Kang ML, et al. Assessment of antibiotic resistance phenotype and integrons in Salmonella enterica serovar Typhimurium isolated from swine. J Vet Med Sci 2008;70:1133−7. https://doi.org/10.1292/jvms.70.1133.
  • 19. Kim KH, Ko JM, Jeong HY. A study on the isolation of Salmonella spp from patients with diarrhea in Incheon (1992–1997). Korean J Vet Serv 1999;22:213−20.
  • 20. Popff MY. WHO Collaborating Centre for Reference and Research on Salmonella. Antigenic formulas of the Salmonella serovars. 8th ed. Paris: WHO Collaborating Centre for Reference and Research on Salmonella; 2001.
  • 21. Grimont PAD, Weill F. Antigenic formulae of the Salmonella serovars. 9th ed. Paris: WHO Collaborating Centre for Reference and Research on Salmonella; 2007. p 166.
  • 22. Cockerill FR. Performance standards for antimicrobial susceptibility testing. 20th informational supplement. M100-S20-U. Wayne, PA: Clinical and Laboratory Standards Institute; 2011.
  • 23. Fernandes SA, Ghilardi AC, Tavechio AT, et al. Phenotypic and molecular characterization of Salmonella Enteritidis strains isolated in São Paulo, Brazil. Rev Inst Med Trop Sao Paulo 2003;45:59−63. https://doi.org/10.1590/S0036-46652003000200001.
  • 24. Ran L, Wu S, Gao Y, et al. Laboratory-based surveillance of non-typhoidal Salmonella infections in China. Foodborne Pathog Dis 2011;8:921−7. https://doi.org/10.1089/fpd.2010.0827.
  • 25. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ 2004;82:346−53.
  • 26. Soyer Y, Moreno Switt A, Davis MA, et al. Salmonella enterica serotype 4,5,12:i:-, an emerging Salmonella serotype that represents multiple distinct clones. J Clin Microbiol 2009;47:3546−56. https://doi.org/10.1128/JCM.00546-09.
  • 27. Hopkins KL, Kirchner M, Guerra B, et al. Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: a new pandemic strain? Euro Surveill 2010;15:19580.
  • 28. Lee DY, Lee E, Min JE, et al. Epidemic by Salmonella I 4,[5],12:i:- and characteristics of isolates in Korea. Infect Chemother 2011;43:186−90. https://doi.org/10.3947/ic.2011.43.2.186.
  • 29. de Castro FA Jr, dos Santos VR, Martins CH, et al. Prevalence and antimicrobial susceptibility of Salmonella serotypes in patients from Ribeirão Preto, São Paulo, Brazil, between 1985 and 1999. Braz J Infect Dis 2002;6:244−51. https://doi.org/10.1590/S1413-86702002000500005.
  • 30. Hur J, Choi YY, Park JH, et al. Antimicrobial resistance, virulence-associated genes, and pulsed-field gel electrophoresis profiles of Salmonella enterica subsp. enterica serovar Typhimurium isolated from piglets with diarrhea in Korea. Can J Vet Res 2011;75:49−56.
  • 31. Gordon MA, Graham SM, Walsh AL, et al. Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica Serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 2008;46:963−9. https://doi.org/10.1086/529146.
  • 32. Karatzas KA, Randall LP, Webber M, et al. Phenotypic and proteomic characterization of multiply antibiotic-resistant variants of Salmonella enterica serovar Typhimurium selected following exposure to disinfectants. Appl Environ Microbiol 2008;74:1508−16. https://doi.org/10.1128/AEM.01931-07.
  • 33. Erdem B, Ercis S, Hascelik G, et al. Antimicrobial resistance patterns and serotype distribution among Salmonella enterica strains in Turkey, 2000–2002. Eur J Clin Microbiol Infect Dis 2005;24:220−5. https://doi.org/10.1007/s10096-005-1293-y.
  • 34. Monno R, Rizzo C, De Vito D, et al. Prevalence, antimicrobial resistance, and extended-spectrum beta-lactamases characterization of Salmonella isolates in Apulia, southern Italy (2001–2005). Microb Drug Resist 2007;13:124−9. https://doi.org/10.1089/mdr.2007.683.
  • 35. Oh YH, Song MO, Kim MS, et al. Detection of antibiotic resistant genes in Salmonella enterica Serovar Typhimurium isolated from foodborne patients in Seoul using multiplex-PCR. J Bacteriol Virol 2005;35:183−90.
  • 36. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 2001;65:232−60. https://doi.org/10.1128/MMBR.65.2.232-260.2001.
  • 37. Cloeckaert A, Schwarz S. Molecular characterization, spread and evolution of multidrug resistance in Salmonella enterica typhimurium DT104. Vet Res 2001;32:301−10. https://doi.org/10.1051/vetres:2001126.
  • 38. Parry CM, Threlfall EJ. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis 2008;21:531−8. https://doi.org/10.1097/QCO.0b013e32830f453a.
Table 1
Serotypes of Salmonella spp. isolated at Jeollanam-do in Korea from 2004 to 2014
Table 1
Serotype No. of strains (%) Somatic antigen group
Salmonella Enteritidis 116 (42.0) D
Salmonella Typhimurium 60 (21.7) B
Salmonella I 4,[5],12:i:- 25 (9.1) B
Salmonella Typhi 24 (8.7) D
Salmonella Thompson 22 (8.0) C
Salmonella Hillingdon 6 (2.2) D
Salmonella Rissen 3 (1.1) C
Salmonella Paratyphi A 2 (0.7) A
Salmonella Stanley 2 (0.7) B
Salmonella Braenderup 2 (0.7) C
Salmonella Infantis 2 (0.7) C
Salmonella Ohio 2 (0.7) C
Salmonella Schwarzengrund 1 (0.4) B
Salmonella Fyris 1 (0.4) B
Salmonella Schleisshem 1 (0.4) B
Salmonella Budapest 1 (0.4) B
Salmonella Concord 1 (0.4) C
Salmonella Potsdam 1 (0.4) C
Salmonella Virchow 1 (0.4) C
Salmonella Emek 1 (0.4) C
Salmonella Kotu 1 (0.4) D
Salmonella Welterveden 1 (0.4) E
Total 276
Table 2
Antibiotic resistance of Salmonella spp. isolated at Jeollanam-do in Korea from 2004 to 2014
Table 2
Class of antibiotics Antimicrobials No. of resistance strains (%) (n = 247)a
Penicillins AM 100 (40.5)
AMC 12 (4.9)
β-Lactam combination SAM 34 (13.8)
Cephalosporins CF 28 (11.3)
CZ 25 (10.1)
CTT 1 (0.4)
FOX 22 (8.9)
CTX 10 (4.0)
CRO 10 (4.0)
Carbapenems IPM 0 (0)
Phenicols C 49 (19.8)
Aminoglycosides AN 0 (0)
GM 19 (7.7)
Quinolones NA 107 (43.3)
CIP 0 (0)
Tetracyclines TE 78 (31.6)
Sulfonamides SXT 20 (8.1)

AM, ampicillin; AMC, amoxicillin/clavulanic acid; SAM, ampicillin/ sulbactam; CF, cefalothin; CZ, cefazolin; CTT, cefotetan; FOX, cefoxitin; CTX, cefotaxime; CRO, ceftriaxone; IPM, imipenem; C, chloramphenicol; AN, amikacin; GM, gentamycin; NA, nalidixic acid; CIP, ciprofloxacin; TE, tetracycline; SXT, trimethoprim/sulfamethoxazole.

aS. Enteritidis, S. Typhimurium, S. I 4,[5],12:i:-, S. Typhi, S. Thompson were analyzed in this study.

Table 3
Antibiotic resistance of Salmonella spp. serotypes isolated at Jeollanam-do in Korea from 2004 to 2014
Table 3
Class of antibiotics Antimicrobials No. of resistance strains (%)
S. Enteritidis (n = 116) S. Typhimurium (n = 60) S. I 4,[5],12:i:- (n = 25) S. Typhi (n = 24) S. Thompson (n = 22)
Penicillins AM 47 (40.5) 42 (70) 9 (36.0) 0 (0) 2 (9.1)
AMC 1 (0.9) 11 (18.3) 0 (0) 0 (0) 0 (0)
β-Lactam combination SAM 11 (9.5) 22 (36.7) 1 (4.0) 0 (0) 0 (0)
Cephalosporins CF 11 (9.5) 12 (20) 1 (4.0) 3 (12.5) 1 (4.5)
CZ 12 (10.3) 12 (20) 0 (0) 0 (0) 1 (4.5)
CTT 1 (0.9) 0 (0) 0 (0) 0 (0) 0 (0)
FOX 8 (6.9) 11 (18.3) 0 (0) 3 (12.5) 0 (0)
CTX 10 (8.6) 0 (0) 0 (0) 0 (0) 0 (0)
CRO 10 (8.6) 0 (0) 0 (0) 0 (0) 0 (0)
Carbapenems IPM 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Phenicols C 34 (29.3) 12 (20) 0 (0) 3 (12.5) 0 (0)
Aminoglycosides AN 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
GM 8 (6.9) 11 (18.3) 0 (0) 0 (0) 0 (0)
Quinolones NA 94 (81.0) 9 (15.0) 0 (0) 3 (12.5) 1 (4.5)
CIP 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Tetracyclines TE 8 (6.9) 51 (85.0) 19 (76.0) 0 (0) 0 (0)
Sulfonamides SXT 1 (0.9) 17 (28.3) 1 (4.0) 0 (0) 1 (4.5)

AM, ampicillin; AMC, amoxicillin/clavulanic acid; SAM, ampicillin/sulbactam; CF, cefalothin; CZ, cefazolin; CTT, cefotetan; FOX, cefoxitin; CTX, cefotaxime; CRO, ceftriaxone; IPM, imipenem; C, chloramphenicol; AN, amikacin; GM, gentamycin; NA, nalidixic acid; CIP, ciprofloxacin; TE, tetracycline; SXT, trimethoprim/sulfamethoxazole.

Table 4
Multidrug resistance of Salmonella serotypes isolated at Jeollanam-do in Korea from 2004 to 2014
Table 4
No. of resistance antibiotics Total (n = 247) No. of resistance strains (%)
S. Enteritidis (n = 116) S. Typhimurium (n = 60) S. I 4,[5],12:i:- (n = 25) S. Typhi (n = 24) S. Thompson (n = 22)
0 51 (20.6) 2 (1.7) 5 (8.3) 6 (24.0) 18 (75.0) 20 (90.9)
1 89 (36.0) 65 (56.0) 11 (18.3) 10 (40) 3 (12.5) 0 (0)
2 30 (12.1) 20 (17.2) 3 (5.0) 6 (24.0) 0 (0) 1 (4.5)
3 27 (10.9) 10 (8.6) 11 (18.3) 3 (12.0) 3 (12.5) 0 (0)
4 23 (9.3) 7 (6.0) 15 (25.0) 0 (0) 0 (0) 1 (4.5)
5 4 (1.6) 1 (0.9) 3 (5.0) 0 (0) 0 (0) 0 (0)
6 1 (0.4) 0 (0) 1 (1.7) 0 (0) 0 (0) 0 (0)
7 14 (5.7) 4 (3.4) 10 (16.7) 0 (0) 0 (0) 0 (0)
8 5 (2.0) 5 (4.5) 0 (0) 0 (0) 0 (0) 0 (0)
9 2 (0.8) 1 (0.9) 1 (1.7) 0 (0) 0 (0) 0 (0)
11 1 (0.4) 1 (0.9) 0 (0) 0 (0) 0 (0) 0 (0)
Table 5
Antibiotic resistance patterns of Salmonella Enteritidis isolated at Jeollanam-do in Korea from 2004 to 2014
Table 5
No. of antibiotics Patterns Antimicrobials No. of strains (%) (n = 116)
1 A AM 5 (4.3)
B NA 60 (51.7)
2 F AM-C 14 (12.1)
G FOX-NA 5 (4.3)
H NA-C 1 (0.9)
3 J AM-NA-C 8 (6.9)
K AM-SAM-C 1 (0.9)
Q FOX-NA-C 1 (0.9)
4 S AM-CF-NA-C 1 (0.9)
X AM-SAM-NA-C 6 (5.2)
5 AD AM-SAM-FOX-NA-C 1 (0.9)
7 AH AM-CF-CZ-CTX-CRO-GM-NA 3 (2.6)
AI AM-CF-CZ-CTX-CRO-GM-NA 1 (0.9)
8 AJ AM-CF-CZ-CTX-CRO-GM-NA-TE 4 (3.4)
AK AM-SAM-CF-CZ-CTX-CRO-NA-TE 1 (0.9)
9 AM AM-SAM-CF-CZ-CTX-CRO-GM-NA-TE 1 (0.9)
11 AN AM-AMC-SAM-CF-CZ-CTT-FOX-NA-TE-C-SXT 1 (0.9)
Total 114 (98.3)

AM, ampicillin; NA, nalidixic acid; C, chloramphenicol; FOX, cefoxitin; SAM, ampicillin/sulbactam; CF, cefalothin; CZ, cefazolin; CTX, cefotaxime; CRO, ceftriaxone; GM, gentamycin; TE, tetracycline; AMC, amoxicillin/clavulanic acid; SXT, trimethoprim/sulfamethoxazole.

Table 6
Antibiotic resistance patterns of Salmonella Typhimurium isolated at Jeollanam-do in Korea from 2004 to 2014
Table 6
No. of antibiotics Patterns Antimicrobials No. of strains (%) (n = 60)
1 B NA 2 (3.3)
C TE 9 (15.0)
2 D AM-TE 2 (3.3)
I NA-TE 1 (1.7)
3 N AM-TE-SXT 10 (16.7)
O AM-CZ-TE 1 (1.7)
4 T AM-CF-TE-SXT 1 (1.7)
U AM-GM-NA-C 1 (1.7)
V AM-GM-TE-C 3 (5.0)
W AM-SAM-GM-TE 4 (6.7)
Y AM-SAM-TE-C 2 (3.3)
Z AM-SAM-TE-SXT 2 (3.3)
AA GM-NA-TE-SXT 1 (1.7)
AB AM-TE-C-SXT 1 (1.7)
5 AC AM-GM-NA-C-SXT 1 (1.7)
AE AM-SAM-NA-TE-C 2 (3.3)
6 AF AM-SAM-GM-TE-C-SXT 1 (1.7)
7 AG AM-AMC-SAM-CF-CZ-FOX-TE 10 (16.7)
9 AL AM-AMC-SAM-CF-CZ-FOX-NA-TE-C 1 (1.7)
Total 55 (91.7)

NA, nalidixic acid; TE, tetracycline; AM, ampicillin; SXT, trimethoprim/sulfamethoxazole; CZ, cefazolin; CF, cefalothin; GM, gentamycin; C, chloramphenicol; SAM, ampicillin/sulbactam; AMC, amoxicillin/clavulanic acid; FOX, cefoxitin.

Table 7
Antibiotic resistance patterns of Salmonella I 4,[5],12:i:- isolated at Jeollanam-do in Korea from 2004 to 2014
Table 7
No. of antibiotics Patterns Antimicrobials No. of strains (%) (n = 25)
1 C TE 10 (40.0)
2 D AM-TE 6 (24.0)
3 L AM-SAM-TE 1 (4.0)
M AM-CF-TE 1 (4.0)
N AM-TE-SXT 1 (4.0)
Total 19 (76.0)

TE, tetracycline; AM, ampicillin; SAM, ampicillin/sulbactam; CF, cefalothin; SXT, trimethoprim/sulfamethoxazole.

Table 8
Antibiotic resistance patterns of Salmonella Typhi isolated at Jeollanam-do in Korea from 2004 to 2014
Table 8
No. of antibiotics Patterns Antimicrobials No. of strains (%) (n = 24)
1 B NA 3 (12.5)
3 P CF-FOX-C 3 (12.5)
Total 6 (25.0)

NA, nalidixic acid; CF, cefalothin; FOX, cefoxitin; C, chloramphenicol.

Table 9
Antibiotic resistance patterns of Salmonella Thompson isolated at Jeollanam-do in Korea from 2004 to 2014
Table 9
No. of antibiotics Patterns Antimicrobials No. of strains (%) (n = 22)
2 E AM-SXT 1 (4.5)
4 R AM-CF-CZ-NA 1 (4.5)
Total 2 (9.0)

AM, ampicillin; SXT, trimethoprim/sulfamethoxazole; CF, cefalothin; CZ, cefazolin; NA, nalidixic acid.

Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

Format:

Include:

Antibiotic Resistance Patterns and Serotypes of Salmonella spp. Isolated at Jeollanam-do in Korea
Osong Public Health Res Perspect. 2017;8(3):211-219.   Published online June 30, 2017
DOI: https://doi.org/10.24171/j.phrp.2017.8.3.08
Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.
Format:
Include:
Antibiotic Resistance Patterns and Serotypes of Salmonella spp. Isolated at Jeollanam-do in Korea
Osong Public Health Res Perspect. 2017;8(3):211-219.   Published online June 30, 2017
DOI: https://doi.org/10.24171/j.phrp.2017.8.3.08
Close
PHRP : Osong Public Health and Research Perspectives

About

Browse articles 

Editorial policies

For authors  

phrp 사이트 QRCODE(URL : https://ophrp.org)
© Korea Disease Control and Prevention Agency.