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.

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.