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Article

Antimicrobial Resistance of Staphylococcus borealis Isolated from Pig Farms: High Prevalence of SCCmec Type V and Emergence of cfr-Positive Isolates

by
Ji Hyun Lim
1,
Ji Heon Park
1,
Gi Yong Lee
2,* and
Soo-Jin Yang
1,*
1
Department of Veterinary Microbiology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 08826, Republic of Korea
2
Department of Molecular Microbiology and Immunology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA
*
Authors to whom correspondence should be addressed.
Antibiotics 2025, 14(9), 910; https://doi.org/10.3390/antibiotics14090910
Submission received: 12 August 2025 / Revised: 5 September 2025 / Accepted: 8 September 2025 / Published: 9 September 2025
(This article belongs to the Special Issue Antimicrobial Resistance of Staphylococcus spp. in Animals: A One Health Perspective)
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Abstract

Background: The emergence of livestock-associated antimicrobial-resistant staphylococci, particularly non-aureus staphylococci, has become a major public health problem requiring immediate global attention. Methods: In this study, 92 Staphylococcus borealis isolates from 20 different pig farms in Korea were examined to determine the following: (1) antimicrobial-resistance (AMR) profiles of the isolates, (2) prevalence of methicillin resistance and staphylococcal cassette chromosome methicillin resistance gene (SCCmec) types, (3) occurrence of chloramphenicol–florfenicol resistance gene (cfr)-mediated oxazolidinone resistance, and (4) genomic characteristics of cfr-positive methicillin-resistant S. borealis (MRSB) via whole-genome sequence (WGS) analysis. Results: The overall rate of S. borealis isolation was 9.1% (92 isolates/1009 swabs), and 34.8% (32/92) of the isolates were MRSB. Surprisingly, all 32 MRSB isolates carried SCCmec V for methicillin resistance, and 31/32 MRSB isolates displayed multidrug-resistance phenotypes. Although 22 cfr-positive S. borealis isolates (20 MRSB and two methicillin-susceptible S. borealis) were identified, most of the isolates were susceptible to linezolid because they carried the 35-bp insertion sequence in the cfr promoter. Moreover, WGS analyses suggested horizontal transmission of SCCmec V and cfr-containing plasmids among different staphylococci species, including Staphylococcus aureus, S. epidermidis, and S. borealis. Conclusions: To the best of our knowledge, this study is the first to describe the AMR characteristics of livestock-associated S. borealis isolates, particularly the high prevalence of SCCmec V and cfr. Collectively, these results suggest that S. borealis is a crucial reservoir of AMR genes on pig farms in Korea.

1. Introduction

Coagulase-negative staphylococci are common commensal inhabitants of the skin and mucous membranes in humans and various animals. Although outbreaks of livestock-associated (LA) methicillin-resistant Staphylococcus aureus (MRSA) have been the main species of interest in veterinary research [1,2,3], antimicrobial-resistant non-aureus staphylococci (NAS), particularly methicillin-resistant NAS (MR-NAS), have also become a serious health issue in both humans and animals [4,5,6].
Frequent carriage of staphylococcal cassette chromosome mec type V (SCCmec V) has been observed in MRSA and MR-NAS isolates derived from livestock and farm environments, particularly in pigs and pig farm environments [7,8,9,10]. Moreover, the dissemination of SCCmec V elements between different species of staphylococci has been suggested [11,12]. Thus, NAS species are widely considered key reservoirs of various types of SCCmec elements [13,14]. In addition to SCCmec elements, NAS species can acquire diverse antimicrobial-resistance genes, leading to the emergence of multidrug-resistance (MDR) phenotypes against commonly used antimicrobial agents in livestock animals, such as β-lactams, phenicols, tetracyclines, and fluoroquinolones [15,16]. Notably, the number of reports of NAS isolates carrying the chloramphenicol–florfenicol resistance gene (cfr) have increased [17,18]. The cfr confers resistance to linezolid (LZD), which is a drug of last resort for treating infections caused by vancomycin-resistant enterococci and MRSA [19]. The first identification of cfr gene in a bovine-associated Staphylococcus sciuri isolate also suggests that NAS species acts as important reservoirs of critical AMR genes [20]. Therefore, putative transmission of AMR genes to and from staphylococci poses a significant threat to animal health by causing hard-to-treat infections that reduce productivity and welfare, while their zoonotic potential raises serious public health concerns.
Staphylococcus borealis is a recently recognized coagulase-negative NAS species that has frequently been misidentified as Staphylococcus haemolyticus owing to genotypic and phenotypic similarities [21,22]. Considering the initial reclassification of S. borealis isolates recovered from the human skin and blood in 2020 [21], its clinical significance has since been highlighted by reports of isolation from immunocompromised patients, suggesting its role as an opportunistic pathogen [22]. In addition, S. borealis has also been isolated from livestock, notably from bovine mastitis cases and from pigs, underscoring the importance of investigating livestock-derived isolates. In Spain, methicillin-resistant S. borealis (MRSB) carrying SCCmec V was isolated from healthy pigs [23] and was suggested as a potential zoonotic pathogen capable of spreading AMR genes among different NAS species. However, information regarding the AMR profiles and genetic factors associated with the AMR phenotypes of livestock-derived S. borealis isolates is limited.
Therefore, in this study, 92 S. borealis isolates were collected from 20 different pig farms (pigs, farm environments, and farmers) in South Korea to investigate: (i) their AMR profiles; (ii) the prevalence of MRSB and profiles of SCCmec types; (iii) the occurrence of cfr-mediated LZD resistance; and (iv) the genomic structure of a cfr-positive MRSB isolate via whole-genome sequence (WGS) analysis.

2. Results

2.1. Prevalence of S. borealis in Pig Farms in Korea

As presented in Table 1, 92 S. borealis isolates were obtained from pigs (n = 79), farm workers (n = 3), and farm environments (n = 10). Although the overall rate of methicillin-resistant S. borealis (MRSB) in 92 isolates was 34.8% (32/92 isolates), 81.3% (26/32 isolates) of the MRSB isolates were derived from healthy pigs (Figure 1). However, one MRSB isolate was identified in a pig farmer in Gyeonggi. The isolation rates of MRSB were 3.4%, 2.9%, and 2.3% in pigs, farm workers, and farm environments, respectively.
The overall prevalence of methicillin-susceptible S. borealis (MSSB) was higher than that of MRSB. The isolation rates of MSSB were 7.0%, 5.9%, and 2.3% in pigs, farm workers, and farm environments, respectively (Table 1).

2.2. AMR Profiles of S. borealis Isolates

As shown in Table 2, all 92 S. borealis isolates were susceptible to ciprofloxacin (CIP), mupirocin (MUP), rifampicin (RIF), and LZD except for one pig-associated CIP-resistant MSSB isolate. The MRSB isolates (96.9%) exhibited considerably higher levels of MDR phenotypes than those of the MSSB isolates (50.0%). Both MRSB and MSSB isolates showed >80% of resistance phenotypes to chloramphenicol (CHL) and clindamycin (CLI), both of which are classified as highly important antimicrobials for human and veterinary medicine. In addition, both MRSB and MSSB isolates showed similar resistance profiles regardless of the three different sample sites (pigs, farm workers, and farm environments).

2.3. High Prevalence of SCCmec V Among MRSB Isolates

All 32 MRSB isolates were mecA-positive and exhibited cefoxitin (FOX) resistance (Table 3). SCCmec type analysis of the MRSB isolates revealed that all 32 isolates carried SCCmec V for the methicillin-resistance phenotype. WGS analysis of the MRSB PCFA-123-1 isolate revealed that PCFA-123-1 possessed 30 kb-sized SCCmec V integrated into the orfX regions. SCCmec V in the PCFA-123-1 isolate were consisted of a single compartment divided by two direct repeats (Figure 2). Comparison of the SCCmec V sequences of the PCFA-123-1 isolate with those of five MRSA strains (three ST398 MRSA and two ST541 MRSA isolates) revealed that all six SCCmec elements contained the class C2 mec gene complex and type 5 ccrC gene complex, thereby suggesting a prototype of SCCmec V (5C2 in ST398 and 5C2 and 5 in ST541). Similar to those of the two ST541 MRSA strains (PCFA-221 and PCFH-226), PCFA-123-1 harbored two type 5 ccrC genes (ccrC2 and ccrC8), displaying the highest nucleotide sequence homology (99.3%) to that of the ST541 MRSA strain (PCFH-226). In contrast, three ST398 MRSA strains (PJFA-521M, PJFH-522M, and PJFE-503) strains carried a single type 5 ccrC gene (ccrC10) and class C2 mec gene complex, thus sharing 95.2% of nucleotide sequence identity with an ST541 MRSA (PCFA-221).

2.4. Identification of cfr-Positive Isolates and Comparative Analysis of cfr-Containing Regions

As shown in Table 3, 62.5% (20/32) of MRSB isolates and 3.3% (2/60) of MSSB isolates were cfr positive. None of the 22 cfr-positive S. borealis isolates showed resistance phenotype to LZD (Table 2 and Table 3).
WGS analysis of the cfr-positive but LZD-susceptible MRSB isolate (PCFA-123-1) revealed that cfr was carried on a 38 kb-plasmid. Comparative analysis of the cfr-containing genetic regions in the MRSB and the previously sequenced plasmids of ST398 MRSA strains [24,25] and S. epidermidis [26] revealed that all strains carried the florfenicol–chloramphenicol exporter gene (fexA) downstream of the cfr (Figure 3). Except for the PJFA-521M strain, all three cfr-positive strains carried two transposase genes (tnpA and tnpB), which are associated with the mobility of Tn558. The cfr-containing genetic regions of the S. borealis PCFA-123-1 isolate shared 100% sequence similarity with that of the ST398 MRSA strain (PJFA-521M).

3. Discussion

Although S. borealis is a relatively newly recognized coagulase-negative NAS, concerns regarding AMR of S. borealis isolates are increasing. Antimicrobial-resistant S. borealis has been identified in various hosts, including human patients, bovine mammary glands, and pigs [22,23,27]. However, data regarding the prevalence and AMR profiles of S. borealis isolates associated with livestock farms is limited.
This study describes the prevalence and AMR profiles of S. borealis isolates collected from pigs, farm workers, and farm environments in Korean pig farms. The overall isolation rate of S. borealis was 9.1% (92 isolates from 1009 swabs), and 34.8% (32/92) of S. borealis isolates were MRSB (Table 1). The rate of methicillin resistance (34.8%) in S. borealis isolates observed in this study was comparable with that of S. aureus isolates (40/81, 49.4%) and S. epidermidis isolates (22/89, 24.7%) obtained from pig farms in Korea in previous studies [28,29]. Although 79/92 S. borealis isolates were obtained from pigs in this study, three isolates (one MRSB and two MSSB) were obtained from nasal swabs of farm workers. Although only three isolates from farm workers were included in this study, this result indicates potential zoonotic transmission of pig-associated S. borealis to human workers, most likely facilitated by frequent contact with pigs or indirect exposure to contaminated aerosols or feeding areas in the pig farms.
Both the MRSB and MSSB isolates exhibited the highest resistance to chloramphenicol (CHL) and clindamycin (CLI), which correlated with the frequent and prolonged use of these antimicrobial agents in pig farms in Korea [30,31]. This result also indicates the risk of reduced treatment efficacy and zoonotic transmission of resistant strains. Moreover, the MRSB isolates showed higher levels of resistance to ampicillin (AMP), sulfamethoxazole-trimethoprim (SXT), and tetracycline (TET) than those of MSSB isolates. This contributed to the increased prevalence of the MDR phenotype in MRSB isolates (Table 2). Resistance to these antimicrobials is commonly associated with genes such as cfr/fexA (CHL), erm (CLI), blaZ/mecA (AMP), dfr/sul (SXT), and tet genes (TET), which are frequently carried on mobile genetic elements that facilitate horizontal transfer. The AMR profiles of the MRSB isolates observed in the current study were similar to those of MRSA [28] and methicillin-resistant S. epidermidis (MRSE) isolates [29] obtained from Korean pig farms in previous studies. These results suggest that S. borealis strains originating from pigs can also serve as reservoirs of AMR and consequently present as a critical public health concern.
Previous studies reported a high prevalence of SCCmec V among MRSA and methicillin-resistant NAS isolates derived from Korean livestock farms, particularly pig farms [11,28,29,32]. SCCmec V has been frequently identified in the clonal complex (CC) 398 lineages of LA-MRSA isolates, which is the most commonly reported LA-MRSA clone in many countries, including Korea [33,34]. Interestingly, all 32 MRSB isolates in this study carried SCCmec V for methicillin resistance (Table 3). In Spain, MDR S. borealis isolates carrying SCCmec V were also detected in healthy pigs. The co-occurrence of identical SCCmec V elements among the MRSA and MR-NAS isolates suggests the horizontal transmission of SCCmec V between different species of staphylococci in livestock farms, given that SCCmec is a mobile genetic element capable of interspecies transfer. As shown in Figure 2, WGS analysis of the MRSB isolate (PCFA-123-1) revealed two essential components of SCCmec V, a type 5 ccrC gene complex and a class C2 mec gene complex. Although the three ST398 MRSA strains carried one ccrC and a class C2 mec gene complex in SCCmec V, an additional ccrC gene was identified in the two ST541 MRSA and PCFA-123-1 isolates (Figure 2). Although structural variations were observed in the joining (J) regions of SCCmec V, the core regions comprising the class C2 mec gene complex and type 5 ccrC gene complexes in the MRSB strain showed >95% nucleotide sequence homology with the five MRSA strains isolated from pig farms. This provides molecular evidence that the highly conserved structure of SCCmec V has been transferred among S. aureus and S. borealis isolates from pig farms, which underscores the potential zoonotic risk and public health concerns.
As shown in Table 3, 22 of the 92 S. borealis isolates were cfr-positive. The cfr gene produces a ribosomal methyltransferase that leads to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A (PhLOPSA) resistance phenotype [35,36]. In addition to the SCCmec V, WGS analysis of the PCFA-123-1 isolate revealed that cfr was carried on a 38 kb-plasmid along with fexA gene (Figure 3). However, all 22 cfr-positive S. borealis isolates, including the PCFA-123-1 isolate, were susceptible to LZD (Table 2 and Table 3). A point mutation within the cfr open reading frame (ORF), Q148K, was identified in cfr-positive but LZD-susceptible S. aureus and NAS isolates from pig farms [25]. Thus, sequencing analyses of the cfr ORFs in the 22 cfr-positive S. borealis isolates were performed. However, no point mutations were identified in these isolates (Table S1). Furthermore, a 35-bp insertion sequence in the cfr promoter region was found to be responsible for the LZD-susceptible phenotype in cfr-positive S. aureus isolates [37]. Sequencing analyses of the cfr promoter region revealed that 19 of the 22 cfr-positive S. borealis isolates, including the PCFA-123-1 isolate, harbored the previously described 35-bp insertion sequences [37]. This indicated that the plasmids carrying the 35-bp insertion mutations were transmitted between S. aureus and NAS isolates in the pig farms. Interestingly, the remaining three isolates displayed a wild-type cfr ORFs and promoter sequences, but were still susceptible to LZD. In a previous study, it has also been reported that linezolid-susceptible phenotype may emerge even in the presence of the wild-type cfr gene in CoNS [23]. Comparative analysis of the plasmid regions containing cfr genes also confirmed carriage of cfr and fexA in the plasmids of S. borealis, S. aureus, and S. epidermidis, with >99.6% nucleotide sequence homology with the p14-01514 plasmid in a clinical strain of S. epidermidis (Figure 3). Taken together, the presence of antimicrobial resistance genes within mobile genetic elements highlights the role of S. borealis in horizontal transmission of AMR in livestock farms.

4. Materials and Methods

4.1. Swab Samples and Isolation of S. borealis

A total of 1009 swab samples were collected from 20 different pig farms located in five provinces of South Korea in 2017. Swab samples were collected from pigs (760 nasal swabs), farm environments (215 swabs from floors, sewage areas, ventilators, and fences), and farm workers (34 nasal swabs). Sampling was performed using sterile cotton swabs (Copan Italia Spa, Brescia, Italy). All swab samples were placed into sterile transport tubes, stored at 4 °C in ice-cooled containers, and transported to the laboratory for bacterial isolation within 24 h. The sampling procedure was reviewed and approved by the Institutional Review Board (NHIMC 2017-07-041) and Institutional Animal Care and Use Committee (2017-00112).
For NAS isolation, swab samples from pig farms were inoculated into 3.5 mL of tryptic soy broth (Difco Laboratories, Detroit, MI, USA) supplemented with 10% NaCl and incubated at 37 °C for 18–24 h. Thereafter, ~20-µL aliquots of the pre-enriched cultures were streaked onto Baird-Parker agar (Difco Laboratories) containing 5% egg yolk and potassium tellurite. The plates were then incubated at 37 °C for up to 48 h. Presumptive staphylococcal colonies were selected and re-streaked on tryptic soy agar for subsequent experiment. S. borealis was identified using matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF/MS; Bruker Daltonics GmbH, Bremen, Germany) with the MBT reference library v12.0 and 16S ribosomal RNA sequencing. Sequence analysis of hsp60 was performed to distinguish S. borealis from S. haemolyticus as previously described [21].

4.2. Antimicrobial Susceptibility Test

The AMR profiles of S. borealis isolates were analyzed using the standard disc diffusion method according to the Clinical and Laboratory Standards Institute’s (CLSI) guidelines [38]. Briefly, each isolate was suspended in 0.85% saline and evenly swabbed onto Mueller–Hinton agar (Difco Laboratories) plates. Antimicrobial discs were then placed on the agar surface, and plates were incubated at 37 °C. Following incubation, the diameters of inhibition zones were measured, and susceptibility or resistance was interpreted according to the CLSI breakpoints. The following 13 antimicrobial agents were used: ampicillin (AMP, 10 μg), cefoxitin (FOX, 30 μg), ciprofloxacin (CIP, 5 μg), clindamycin (CLI, 2 μg), chloramphenicol (CHL, 30 μg), erythromycin (ERY, 15 μg), gentamicin (GEN, 30 μg), linezolid (LZD), mupirocin (MUP, 200 μg), quinupristin–dalfopristin (SYN, 15 μg), rifampin (RIF, 5 μg), sulfamethoxazole-trimethoprim (SXT, 23.73–1.25 μg), and tetracycline (TET, 30 μg). All antimicrobial agents used for the disc diffusion assay, except MUP (Oxoid, Hampshire, UK), were obtained from BD BBLTM (Becton Dickinson, Franklin Lakes, NJ, USA). The S. aureus ATCC 29213 strain was used as a reference strain for the disc diffusion tests.

4.3. SCCmec Typing and Detection of cfr

S. borealis isolates showing FOX resistance phenotype were screened for the presence of mecA gene using polymerase chain reaction (PCR), as described previously [39]. For all mecA-positive S. borealis isolates, SCCmec types were determined by PCR amplification of mec regulatory elements (mec) and chromosomal cassette recombinase (ccr), and subsequent assignment of SCCmec types was performed as previously described [40].
The presence of cfr, which confers LZD resistance by encoding a 23S rRNA methyltransferase [41], was screened for all S. borealis isolates using the PCR method as described before [36].

4.4. WGS Analysis

A cfr-positive S. borealis PCFA-123-1 isolate carrying SCCmec V for methicillin resistance was subjected to WGS analysis using a TruSeq DNA PCR-free kit (Illumina Inc., San Diego, CA, USA). The concentration and purity of the DNA sample was assessed using a NanoDropTM 2000c spectrophotometer (Thermo Fisher Scientific, Wilmington, NC, USA) as previously described [42], and 1.0 μg of total DNA was used for the library construction. Genomic sequences of the S. borealis isolates were generated using a combination of the Illumina iSeq platform (Illumina) and Oxford Nanopore MinION (Oxford Nanopore Technologies, Oxford, UK). The raw reads generated via 150-bp paired-end sequencing on the Illumina platform were trimmed using Trimmomatic (v0.36) to eliminate low-quality adaptor sequences. Raw read sequencing data were de novo assembled using SPAdes (v3.13), and library preparation was carried out using MinION reads in Trycycler v.0.3.0 (https://github.com/rrwick/Trycycler (accessed on 2 June 2020)). Rapid Annotation was carried out using Subsystem Technology and functional annotation was performed using Prokka (v1.12).
SCCmecFinder v1.2 (https://cge.food.dtu.dk/services/SCCmecFinder/ (accessed on 13 July 2020)) of the Center for Genomic Epidemiology (CGE) (http://www.genomicepidemiology.org/ (accessed on 13 July 2020)) was used to analyze SCCmec elements by identifying the combination of mec and ccr gene complexes within assembled contigs and comparing them with reference SCCmec structures. The locations of the cfr gene and other AMR genes were analyzed using the Comprehensive Antibiotic Resistance Database (https://card.mcmaster.ca/ (accessed on 13 July 2020)) and ResFinder v4.1 of the CGE databases with resistance determinants assigned based on sequence identity (≥90%) relative to reference sequences.

4.5. Comparative Analysis of SCCmec V and cfr

For comparative analysis of the SCCmec V elements in the PCFA-123-1 isolate, raw sequence files of three ST398 MRSA isolates (ST398 PJFA-521M from a pig [GenBank accession no. SRKD00000000] [24], ST398 PJFH-522M from a pig farm worker [GenBank accession no. RKRI00000000], ST398 PJFE-503M from pig farm environment [GenBank accession no. CP049976-CP049977] [25]) and two ST541 isolates (ST541 PCFA-221 from a pig [GenBank accession no. CP035003-CP035004] and ST541 PCFH-226 from a pig farm worker [GenBank accession no. CP035005-CP035006]) carrying SCCmec V were included in the analyses. The conserved orfX site where insertion and excision of SCCmec occur, along with its flanking direct repeat regions, was used to identify SCCmec structures in each genome. The nucleotide sequences and gene organizations of the SCCmec elements were then compared using BLAST version 5 to assess structural similarity and homology across isolates.
To examine the cfr-containing genomic region in the S. borealis isolate, comparative sequence analysis of PCFA-123-1 and previously reported cfr-positive staphylococci was performed using BLAST to assess sequence conservation and gene organization. These strains included two ST398 LA-MRSA strains (PJFA-521M and PJFE-503M) [24,25] and the ST5 S. epidermidis p14-01514 (GenBank accession no. NZ_KX520649) [26].

4.6. Nucleotide Sequence Accession Number

The WGS data of S. borealis PCFA-123-1 were deposited in the NCBI database under the accession numbers of CP116211-CP116213.

4.7. Statistical Analysis

All quantitative data were analyzed using the Kruskal–Wallis test for multiple-group comparisons with Dunn’s post hoc test (IBM SPSS Statistics 25, Chicago, IL, USA). A p-value < 0.05 was considered statistically significant.

5. Conclusions

In conclusion, our results suggest that (i) S. borealis isolates with MDR phenotypes colonize healthy pigs, farm workers, and farm environments; (ii) SCCmec V is predominantly distributed in pig-associated MRSB isolates in Korea; (iii) the 35-bp insertion sequence in the cfr promoter region is responsible for LZD-susceptibility in most cfr-positive S. borealis isolates; and (iv) different species of staphylococci, including S. aureus and S. borealis, acquire SCCmec V- and cfr-containing plasmids through intra- and inter-species transmission in pig farms. It should be recognized that the present study has some limitations. First, only three isolates obtained from farm workers limits the representativeness of human-associated S. borealis. Second, the comparative analyses of SCCmec V- and cfr-containing plasmids were performed using a single representative S. borealis isolate (PCFA-123-1). However, our findings provide important insights into the AMR profiles and genetic determinants of livestock-associated S. borealis, underscoring their implications for both animal and human health. Therefore, continuous monitoring of AMR in livestock-associated staphylococci is essential to limit further spread and protect public health.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/antibiotics14090910/s1, Table S1: Genetic mutation of cfr and linezolid resistance phenotypes of cfr-carrying S. borealis.

Author Contributions

Conceptualization, G.Y.L. and S.-J.Y.; methodology, J.H.L., G.Y.L. and J.H.P.; formal analysis, J.H.L., G.Y.L. and J.H.P.; investigation, J.H.L. and S.-J.Y.; data curation, J.H.L. and S.-J.Y.; writing—original draft preparation, J.H.L., G.Y.L. and S.-J.Y.; writing—review and editing, J.H.L., G.Y.L., J.H.P. and S.-J.Y.; project administration, J.H.L. and G.Y.L.; funding acquisition, S.-J.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by grants from the Research of Korea Centers for Disease Control and Prevention (grants No. 2017NER54060 and 2024ER2209-00).

Institutional Review Board Statement

The collection of samples and study design were approved by the Institutional Animal Care and Use Committee (approval number: 2017-00112) and the Institutional Review Board (approval number: NHIMC 2017-07-041).

Informed Consent Statement

Permission for sample collection was granted by the farm owners, and all participating farm workers provided written informed consent.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Antibiotics 14 00910 g001
Figure 1. Distribution of MSSB and MRSB isolates from pigs, farm workers, and farm environments in Korea.
Figure 1. Distribution of MSSB and MRSB isolates from pigs, farm workers, and farm environments in Korea.
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Antibiotics 14 00910 g002
Figure 2. Comparative analysis of SCCmec V elements from MRSB isolated from pig farms. The SCCmec V sequences in the MRSB strain (PCFA-123-1) were compared with those of five MRSA strains available in the GenBank database: ST398 MRSA strain PJFA-521M (SRKD00000000), ST398 MRSA strain PJFH-522M (RKRI00000000), ST398 MRSA strain PJFE-503M (CP049976-CP049977), ST541 MRSA strain PCFA-221 (CP035003-CP035004), and ST541 MRSA strain PCFH-226 (CP035005-CP035006). SCCmec V, staphylococcal cassette chromosome methicillin resistance gene type V; MRSB, methicillin-resistant S. borealis; MRSA, methicillin-resistant S. aureus. Homologous regions are marked with colors corresponding to nucleotide sequence identities, and their percentages are indicated. The light green arrow indicates orfX. The methicillin resistance (mec) and chromosomal cassette recombinase (ccr) genes are shaded red and blue, respectively. The class C2 mec gene complex, composed of IS431-mecA-ΔmecR1::IS431, is specifically highlighted with a red box. The type I restriction-modification system composed of hydroxysteroid dehydrogenase genes (hsdR, hsdS, and hsdM) is shaded pink.
Figure 2. Comparative analysis of SCCmec V elements from MRSB isolated from pig farms. The SCCmec V sequences in the MRSB strain (PCFA-123-1) were compared with those of five MRSA strains available in the GenBank database: ST398 MRSA strain PJFA-521M (SRKD00000000), ST398 MRSA strain PJFH-522M (RKRI00000000), ST398 MRSA strain PJFE-503M (CP049976-CP049977), ST541 MRSA strain PCFA-221 (CP035003-CP035004), and ST541 MRSA strain PCFH-226 (CP035005-CP035006). SCCmec V, staphylococcal cassette chromosome methicillin resistance gene type V; MRSB, methicillin-resistant S. borealis; MRSA, methicillin-resistant S. aureus. Homologous regions are marked with colors corresponding to nucleotide sequence identities, and their percentages are indicated. The light green arrow indicates orfX. The methicillin resistance (mec) and chromosomal cassette recombinase (ccr) genes are shaded red and blue, respectively. The class C2 mec gene complex, composed of IS431-mecA-ΔmecR1::IS431, is specifically highlighted with a red box. The type I restriction-modification system composed of hydroxysteroid dehydrogenase genes (hsdR, hsdS, and hsdM) is shaded pink.
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Antibiotics 14 00910 g003
Figure 3. Comparative analysis of the cfr-containing regions from MRSB isolated from a pig farm. Arrows indicate the positions and orientations of the genes. Nucleotide sequences >95% of similarity are shown in yellow.
Figure 3. Comparative analysis of the cfr-containing regions from MRSB isolated from a pig farm. Arrows indicate the positions and orientations of the genes. Nucleotide sequences >95% of similarity are shown in yellow.
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Table 1. S. borealis isolates collected from pigs, farm workers, and farm environments.
Table 1. S. borealis isolates collected from pigs, farm workers, and farm environments.
No. of Isolates/No. of Samples (%)
S. borealis (n = 92)Pig Farms (n = 92/1009, 9.1%)
PigsFarmersEnviron. 1
MRSB 2 (n = 32/92)26/760 (3.4%)1/34 (2.9%)5/215 (2.3%)
MSSB 3 (n = 60/92)53/760 (7.0%)2/34 (5.9%)5/215 (2.3%)
Total79/760 (10.4%)3/34 (8.8%)10/215 (4.6%)
1 Environ., environments. 2 MRSB, methicillin-resistant S. borealis. 3 MSSB, methicillin-susceptible S. borealis.
Table 2. Antimicrobial resistance profiles of 92 S. borealis isolates recovered from pigs, farm workers, and farm environments.
Table 2. Antimicrobial resistance profiles of 92 S. borealis isolates recovered from pigs, farm workers, and farm environments.
Number (%) of Isolates Resistant to 1
AMPFOXCHLCIPCLIERYGENMUPRIFSXTSYNTETLZDMDR
MRSB 2
(n = 32)		Pigs
(n = 26)		26
(100)		26
(100)		25
(96.2)		026
(100)		05
(19.2)		0020
(76.9)		2
(7.7)		25
(96.2)		026
(100)
Farmers
(n = 1)		1
(100)		1
(100)		1
(100)		01
(100)		1
(100)		1
(100)		00001
(100)		01
(100)
Environ. 4
(n = 5)		4
(80)		5
(100)		4
(80)		04
(80)		00002
(40)		04
(80)		04
(80)
Total31
(96.9)		32
(100)		30
(93.8)		031
(96.9)		1
(3.1)		6
(18.8)		0022
(68.8)		2
(6.3)		30
(93.8)		031
(96.9)
MSSB 3
(n = 60)		Pigs
(n = 53)		2
(3.8)		041
(77.4)		1
(1.9)		44
(83)		26
(49.1)		1
(1.9)		0001
(1.9)		21
(39.6)		027
(50.9)
Farmers
(n = 2)		002
(100)		02
(100)		000000000
Environ.
(n = 5)		005
(100)		05
(100)		3
(60)		000003
(60)		03
(60)
Total2
(3.3)		048
(80)		1
(1.7)		51
(85)		29
(48.3)		1
(1.7)		0001
(1.7)		24
(40)		030
(50)
Total
(n = 92)		 33
(35.9)		32
(34.8)		78
(84.8)		1
(1.1)		82
(89.1)		30
(32.6)		7
(7.6)		0022
(23.9)		3
(3.3)		54
(58.7)		061
(66.3)
1 AMP, ampicillin; FOX, cefoxitin; CHL, chloramphenicol; CIP, ciprofloxacin; CLI, clindamycin; ERY, erythromycin; GEN, gentamicin; MUP, mupirocin; RIF, rifampicin; SXT, trimethoprim-sulfamethoxazole; SYN, quinupristin–dalfopristin; TET, tetracycline; LZD, linezolid; MDR, multidrug resistance. 2 MRSB, methicillin-resistant S. borealis. 3 MSSB, methicillin-susceptible S. borealis. 4 Environ., environment.
Table 3. Carriage of antimicrobial resistance genes in MRSB and MSSB isolates from pig farms in Korea.
Table 3. Carriage of antimicrobial resistance genes in MRSB and MSSB isolates from pig farms in Korea.
No. of S. borealis Isolates
Methicillin ResistanceCarriage of cfr
MR/MS mecASCCmec Type
MRSB 1
(n = 32)		Pigs
(n = 26)		26/26
(100%)		SCCmec V
(26/26, 100%)
SCCmec V
(1/1, 100%)
SCCmec V
(5/5, 100%)		17/26
(65.4%)
Farmers
(n = 1)		1/1
(100%)		1/1
(100%)
Environ. 3
(n = 5)		5/5
(100%)		2/5
(40.0%)
Total32/32
(100%)		32/32
(100%)		20/32
(62.5%)
MSSB 2
(n = 60)		Pigs
(n = 53)		--2/53
(3.8%)
Farmers
(n = 2)		---
Environ.
(n = 5)		---
Total--2/60
(3.3%)
Total
(n = 92)		 32/92
(34.8%)		 22/92
(23.9%)
1 MRSB, methicillin-resistant S. borealis; 2 MSSB, methicillin-susceptible S. borealis; 3 Environ., environment.
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Lim, J.H.; Park, J.H.; Lee, G.Y.; Yang, S.-J. Antimicrobial Resistance of Staphylococcus borealis Isolated from Pig Farms: High Prevalence of SCCmec Type V and Emergence of cfr-Positive Isolates. Antibiotics 2025, 14, 910. https://doi.org/10.3390/antibiotics14090910

AMA Style

Lim JH, Park JH, Lee GY, Yang S-J. Antimicrobial Resistance of Staphylococcus borealis Isolated from Pig Farms: High Prevalence of SCCmec Type V and Emergence of cfr-Positive Isolates. Antibiotics. 2025; 14(9):910. https://doi.org/10.3390/antibiotics14090910

Chicago/Turabian Style

Lim, Ji Hyun, Ji Heon Park, Gi Yong Lee, and Soo-Jin Yang. 2025. "Antimicrobial Resistance of Staphylococcus borealis Isolated from Pig Farms: High Prevalence of SCCmec Type V and Emergence of cfr-Positive Isolates" Antibiotics 14, no. 9: 910. https://doi.org/10.3390/antibiotics14090910

APA Style

Lim, J. H., Park, J. H., Lee, G. Y., & Yang, S.-J. (2025). Antimicrobial Resistance of Staphylococcus borealis Isolated from Pig Farms: High Prevalence of SCCmec Type V and Emergence of cfr-Positive Isolates. Antibiotics, 14(9), 910. https://doi.org/10.3390/antibiotics14090910

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