Next Article in Journal
Long-Term Pulmonary Dysfunction by Hyperoxia Exposure during Severe Viral Lower Respiratory Tract Infection in Mice
Previous Article in Journal
Prevalence and Implications of Shiga Toxin-Producing E. coli in Farm and Wild Ruminants
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 11
Issue 11
10.3390/pathogens11111333
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Molecular Characteristics and Antibiotic Resistance of Staphylococcus aureus Isolated from Patient and Food Samples in Shijiazhuang, China

by
Han Zhang
1,†,
Liyun Qin
2,3,†,
Caiping Jin
1,
Huidong Ju
4,
Ruiping Jiang
2,3,
Lijie Li
2,3,
Hong Zhang
2,3,
Weili Gao
2,3,
Xiuping Wei
2,
Hongyan Dong
1,
Fei Lu
2,3,* and
Guoping Lv
1,*
1
Basic Medicine College, Hebei University of Chinese Medicine, Shijiazhuang 050200, China
2
Shijiazhuang Center for Disease Control and Prevention, Shijiazhuang 050011, China
3
Hebei Key Laboratory of Unidentifiable Bacteria, Shijiazhuang 050011, China
4
College of Chemical Technology, Shijiazhuang University, Shijiazhuang 050035, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Pathogens 2022, 11(11), 1333; https://doi.org/10.3390/pathogens11111333
Submission received: 12 October 2022 / Revised: 7 November 2022 / Accepted: 9 November 2022 / Published: 11 November 2022
Browse Figures
Review Reports Versions Notes

Abstract

:
Staphylococcus aureus (S. aureus) is a common opportunistic and zoonotic pathogen in the world and could easily cause human infections and food contaminations. This study investigated the sequence typing and resistance profiles of S. aureus isolates from patient and food samples in Shijiazhuang, China. A total of 101 S. aureus isolates were distributed into six clonal complexes (CCs) and 16 singletons. A total of 86 patient isolates were distributed into six clonal CCs and 12 singletons, including a new ST. CC59, CC5, CC22, and CC398 were the predominant CCs of patient isolates. A total of 15 foodborne S. aureus isolates were distributed into 3 CCs and 4 STs, and CC1 was the most prevalent CC. Moreover, 101 S. aureus isolates had high resistance to penicillin and low resistance to chloramphenicol and rifampicin. A total of 39 strains of methicillin-resistant Staphylococcus aureus (MRSA) were detected in this study, including thirty-eight strains of patient isolates (44.2%, 38/86) and one strain of food isolates (6.7%, 1/15). MRSA-ST5, MRSA-ST59, and MRSA-ST239 were the predominant MRSA isolates in hospitals. The present study explained the relationship between S. aureus isolated from patient and food samples and indicated the risks of S. aureus in infectious diseases.

1. Introduction

As a common zoonotic pathogen, S. aureus can cause serious diseases in humans [1,2]. S. aureus is one of the main pathogenic bacteria of infectious diseases, and can cause food poisoning outbreaks [1,3]. S. aureus from patient samples mainly comes from infectious diseases and is responsible for a wide variety of community-acquired or hospital-acquired infections [4,5,6]. It often contaminates foods and produces a wide variety of toxins, and contamination increases the risk of infectious diseases and food poisoning outbreaks [2,7]. S. aureus can cause poultry myelitis, sepsis, mastitis in cows and other animals, and contamination dairy products [8,9,10]. S. aureus transmission could contaminate environments and food, and endanger human and animal health [8,11]. S. aureus isolated from patient and food samples are closely related to human health.
S. aureus is prone to antimicrobial resistance and poses a great challenge in the treatment of related infectious diseases [12,13,14]. It presents high resistance to penicillin [15,16], and many S. aureus isolates can be resistant to multiple antibiotics. Methicillin-resistant S. aureus (MRSA) strains are resistant to most semisynthetic penicillin, and have various resistance to other antibiotics [6,14,16,17]. Compared with methicillin-susceptible S. aureus (MSSA), MRSA causes longer length of hospital stay, higher infection rates and higher mortality [6,18]. MRSA is distributed all over the world and poses a great threat to global public health.
The epidemic characteristics of S. aureus are important for understanding the transmissions and pathogenicity in different parts of the world. Multilocus sequence typing (MLST) is a general analytical tool that is used for molecular traceability analysis of bacteria worldwide. It is used at a global scale to compare and analyze a pathogen in different countries and different periods. The molecular characteristics of S. aureus vary with different regions and sources. In Shijiazhuang, China, the epidemic sequence types (STs) of S. aureus in foods are ST1, ST5, ST59, ST398, ST7, and ST9 [3]. Those STs are also prevalent in Chinese retail meat products [19]. ST59, ST9, ST1, and ST398 are the main STs of food-related MRSA in China [20]. However, the prevalent STs of clinical S. aureus are different from foodborne S. aureus in China.
The predominant STs of clinical S. aureus are ST5, ST188, ST239, ST59, ST7, and ST398 in teaching hospitals [21]. ST5, ST239, and ST59 are the prevalent clinical MRSA isolates in China [17,21]. ST9, ST398, and ST5 were predominant genotypes in USA [22], and ST93 was the most common MRSA of clinical isolates in Australia [23]. S. aureus isolates have different epidemic molecular types at different times, even if they come from the same source [21]. Among clinical S. aureus in Hainan, ST45, ST188, ST59, and ST88 were the prevalent STs from 2013 to 2014, but ST398, ST188, and ST59 were prevalent from 2019 to 2020 [16]. Therefore, MLST can help to monitor the molecular characteristics of S. aureus in food contaminations and bacterial infections.
The aim of this study was to characterize S. aureus isolated from patients and food samples in Shijiazhuang, China. A total of 101 S. aureus isolates were collected from hospitals and foods in 2019. In particular, MLST genotypes and resistance profiles were determined. In addition, the MRSA isolates were detected.

2. Methods

2.1. Bacterial Isolates

This study examined 101 S. aureus isolates from different tertiary hospitals and foods in 2019 from Shijiazhuang, China. There were 15 foodborne isolates from 192 food samples under surveillance for microbiological risk, including raw meat, raw poultry, aquatic products, cooked food, milk powder, and nutritious rice flour. Among them, there were seven isolates of S. aureus detected in raw meat, three isolates in raw poultry and five isolates in cooked meat. The 86 patient isolates included sputum sputa (n = 34, 39.5%), pus and secretion (n = 13, 15.1%), blood (n = 4, 4.7%), swabs (n = 11, 12.8%), and others (n = 24, 27.9%). Routine identification methods for S. aureus were conducted, including Gram staining, catalase tests, coagulase tests, and Matrix-Assisted Laser Desorption Ionization Time of Flight Mass Spectrometry (MALDI-TOF MS) System (Bruker, Berlin, Germany). The S. aureus strain ATCC25923 was used as a control. All isolates were then frozen and maintained in a Brain Heart Infusion (BHI) medium with 40% glycerol at −80 °C for further experiments.

2.2. Extraction DNA and Detection of Antibiotic Resistance Genes

Bacterial DNA was extracted by a bacterial genomic DNA extraction kit (DNeasy Blood and Tissue Kit, Qiagen Inc, Redwood City, CA, United States), and the blaZ, mec and nucA genes were detected using PCR assays. The nucA gene was used as an internal reference gene. All of the primers (TaKaRa, Beijing, China) were listed in our previous study [3]. A multiplex PCR assay was used to evaluate the reference gene nucA and to detect whether isolates carried antimicrobial resistance genes blaZ and mec. The PCR mixture contained 0.6 µL mec-F (10 µM), 0.6 µL mec-R (10 µM), 0.5 µL blaZ-F (10 µM), 0.5 µL blaZ-R (10 µM), 0.4 µL nucA-F (10 µM), 0.4 µL nucA-R (10 µM), 4 µL genome DNA template, 12.5 µL of premixTap TaKaRa (TaKaRA, China), and double-distilled water added to obtain a volume 25 µL. The PCR conditions were as follows: initial denaturation at 95 °C for 4 min, followed by 35 cycles of denaturation at 95 °C for 30 s, annealing at 54 °C for 30 s, extension at 72 °C for 1 min 40 s, and a final extension at 72 °C for 7 min. The PCR isolation method and the interpretation of the results come from our previous studies [3].

2.3. Antimicrobial Susceptibility Test

The Kirby-Bauer paper dispersion method was used for an antimicrobial susceptibility test. A total of 14 antibiotics were tested, including cefoxitin (FOX, 30 μg), penicillin G (PEN, 10U), oxacillin (OXA, 1 μg), tetracycline (TET, 30 μg), doxycycline (DOX, 30 μg), chloramphenicol (CAP, 30 μg), rifampicin (RFP, 5 μg), erythromycin (ERY, 15 μg), clarithromycin (CLR, 15 μg), sulfamethoxazole (SMZ, 1.25/23.75 μg), gentamicin (GM, 10 μg), clindamycin (CLI, 2 μg), ciprofloxacin (CIP, 5 μg), levofloxacin (LEV, 5 μg). S. aureus ATCC 25923 was used as a quality control strain, and results were interpreted according to the guidelines of the Clinical and Laboratory Standards Institute (CLSI M100-S30) [24]. The mec-positive or cefoxitin-resistant isolates (cefoxitin minimum zone diameter ≤ 21 mm) were identified as MRSA.

2.4. MLST

The base sequence of housekeeping genes of S. aureus, (arcC, aroE, glpF, gmkF, pta, tpi, and yqiL) were adapted for MLST, which was carried out according to a previous protocol [25]. PCR assays were used to amplify these seven housekeeping genes. The housekeeper genes were sequenced by Sanger dideoxy DNA sequencing (Sangon Biotech, Shanghai, China). The resulting alleles were input into the MLST website (http://saureus.mlst.net accessed on 26 July 2022) and compared with a known sequences search and by locus combinations to determine the allele number, STs, and CCs. The strains that did not match with known STs were named as new STs after submitting them to the database. The clustering of related STs was defined as CCs, and the STs that did not correlate with any clone groups were defined as singletons, which were defined by eBurst.

2.5. Statistical Analysis

Statistical analysis was performed using IBM SPSS Statistics 26.0. Pearson’s Chi-square tests or Fisher’s exact tests were used to analyze the data. A phylogenetic tree was constructed using BioNumerics 7.6.2 (Applied Maths, Sint-Martens-Latem, Belgium).

3. Results

3.1. Antibiotic Resistance Profiles of S. aureus

The 101 S. aureus isolates had lower resistance rate to CAP (4.0%, 4/101) and RFP (5.0%, 5/101). The other resistance rates were 97.0% (98/101) for PEN, 68.3% (69/101) for ERY, 68.3% (69/101) for CLR, 67.3% (68/101) for SMZ, 56.4% (57/101) for CLI, 39.6% (40/101) for TET, 38.6% (39/101) for FOX, 37.6% (38/101) for OXA, 26.7% (27/101) for CIP, 21.8% (22/101) for LEV, 17.8% (18/101) for GM, and 14.9% (15/101) for DOX. The difference in resistance rates between patients and food isolates to the same antibiotic is shown in Figure 1.The resistance rates of patient isolates to CAP, RFP, and LEV were 3.5%, 5.8%, and 25.6%, respectively, but the resistance rate of food isolates to CAP was 6.7%, and they were completely sensitive to RFP and LEV.
The patient isolates had significantly higher resistance rates to FOX than the food isolates (44.2% vs. 6.7%, p = 0.008), OXA (43.0% vs. 6.7%, p = 0.008), ERY (75.6% vs. 26.7%, p = 0.001), CLR (75.6% vs. 26.7%, p = 0.000), SMZ (74.4% vs. 26.7%, p = 0.001), and CLI (61.6% vs. 26.7%, p = 0.022). However, there was no significant statistical difference between patient and food isolates to other antibiotics. The resistance rates of patient isolates were 39.5% for TET, 29.1% for CIP, 25.6% for LEV, 19.8% for GM, 5.8% for RFP, and 3.5% for CAP. In food isolates, the resistance rates to these antibiotics were 40.0%, 13.3%, 0%, 6.7%, 0%, and 6.7%, respectively.
The 101 S. aureus isolates were examined for the mec and blaZ gene. A total of 38.6% (39/101) of isolates were positive for mec gene, and 76.2% (77/101) were positive for the blaZ gene. The detection rate of the mec gene was 44.2% (38/86) in patient isolates and 6.7% (1/15) in food isolates. The detection rates of the blaZ gene were 74.4% (64/86) and 86.7% (13/15), respectively.
The 62 MSSA isolates had low resistance rates to DOX (1.6%, 1/62), RFP (1.6%, 1/62), LEV (3.2%, 2/62), and CAP (4.8%, 3/62). However, the resistance rates to PEN, SMZ, ERY, and CLR were higher, at 95.2%, 66.1%, 64.5%, and 64.5%, respectively. The MSSA isolates included 48 patient isolates and 14 food isolates. The patient MSSA isolates were resistant to PEN (95.8%, 46/48), SMZ (79.2%, 38/48), ERY (77.1%, 37/48), and CLR (77.1%, 37/48), but no S. aureus isolate was resistant to DOX. The food MSSA isolates had the highest resistance rate to PEN (92.9%, 13/14) and were completely sensitive to RFP and LEV. 80.4% (37/46) of the PEN-resistant patient MSSA isolates were blaZ-positive strains, while 84.6% (11/13) of the PEN-resistant foodborne MSSA isolates were blaZ-positive.
Among the 101 S. aureus isolates, 39 isolates were MRSA, and 62 isolates were MSSA. Among the 39 MRSA isolates, thirty-eight were isolated from patient isolates and one was from food isolates. Patients MRSA isolates had higher frequencies than the food MRSA isolates (44.2% vs. 6.7%, p < 0.05). The patient MRSA isolates had significantly higher resistance rates to TET (68.4% vs. 16.7%, p = 0.000), DOX (36.8% vs. 0.0%, p = 0.000), CIP (55.3% vs. 8.3%, p = 0.000), LEV (52.6% vs. 4.2%, p = 0.000) and CLI (73.7% vs. 52.1%) than the MSSA isolates. (Table 1).

3.2. STs and CCs of S. aureus Isolates

A total of 26 STs were detected in the 101 S. aureus isolates and were divided into six CCs and 14 STs were singletons. The CCs and singletons included CC1, CC5, CC15, CC22, CC8, CC121, ST59, ST398, ST7, ST3069, ST4845, ST88, ST1281, ST3068, ST20, ST25, ST3355, ST522, ST2472, and a new type. The allelic profile of newly discovered sequence is 7-6-1-5-8-8-1. As shown in Table 2, there were different distribution characteristics between patient isolates and food isolates.
A total of 22 STs were obtained from 86 patient isolates. ST59 was the predominant ST (25.5%, n = 22), followed by ST5 (24.4%, n = 21), ST22 (11.6%, n = 10), ST398 (8.1%, n = 7), ST239 (5.8%, n = 5), ST15 (3.4%, n = 3), ST20 (2.3%, n = 2), and ST7 (2.3%, n = 2). The other 14 STs (ST121, ST1281, ST2315, ST25, ST306, ST3068, ST3069, ST3355, ST4845, ST6, ST6769, ST72, ST88, and a new ST), each accounted for 1.1% (n = 1). These STs belonged to six CCs and 12 singletons. The minimum spanning tree was built from the MLST allelic profiles of 86 S. aureus isolates with CCs and singletons (Figure 2). The cladogram was highly diverse. The most prevalent clinical S. aureus isolates were CC59, CC5, CC22, and CC398. The other CCs or singletons were isolated sporadically (Figure 2).
A total of 15 food isolates of S. aureus from eight STs were assigned to three CCs and four singletons STs, (ST7, ST522, ST59, ST2472, ST1, ST6, ST15, and ST9). CC1, CC5, CC7, and CC59 were the dominant CCs. The predominant CCs or singletons were CC1 (40%, n = 6), followed by ST59 (13.3%, n = 2), CC5 (13.3%, n = 2), and ST7 (13.3%, n = 2). The other CCs or singletons were CC15, ST522, and ST2472, which each accounted for 6.7% (n = 1).

3.3. STs in MRSA and MSSA Isolates

Among the 39 MRSA isolates, thirty-eight strains were from patient isolates, and one strain (MRSA-ST59) was from foodborne isolates. The predominant STs of MRSA isolates in patients were ST5 (15/38, 39.5%), ST59 (12/38, 31.6%), ST239 (4/38, 10.5%), and ST398 (3/38, 7.9%). The other MRSA isolates included ST15, ST25, ST72, and ST3355, which each accounted for 2.6% (1/38). ST59 (19.4%, 12/62) and ST22 (17.7%, 11/62) were the most common in MSSA isolates, followed by ST5 (9.7%, 6/62), ST1 (6.5%, 4/62), ST398 (4.8%, 3/62), ST239 (3.2%, 2/62), ST15 (3.2%, 2/62), ST20 (3.2%, 2/62), ST6 (3.2%, 2/62), ST7 (3.2%, 2/62), and ST9 (3.2%, 2/62). ST121, ST1281, ST2135, ST306, ST3068, ST3355, ST15, ST522, and ST2472 each accounted for 1.6% (1/62).

4. Discussion

S. aureus isolates were collected from hospitals and food samples for investigation of their antibiotic resistance profiles and molecular characteristics. The isolates had low resistance rate to CAP (4.0%) and RFP (5.0%), while they had high resistance rates to PEN (93.3% for food isolates and 97.7% for patient isolates). The PEN resistance results are consistent with those reported in Hainan hospitals and in food animals in Sichuan, China [16,26]. S. aureus isolates are widely resistant to penicillin in China. The antibiotic resistance rate was reported as 84.6% in meat samples, and 85.1% in blood isolates in Shandong [19,27].
The patient isolates were more resistant to ERY, CLR, SMZ, and CLI than the food isolates. The patient isolates had high resistance to ERY (75.6%), CLR (75.6%), SMZ (74.4%), and CLI (61.6%). The resistance was 81.2% for ERY and 78.2% for CLI in Shandong [27]. 95.62% of MRSA isolates and 73.66% of MSSA isolates were resistant to ERY in Shenzhen [28], whereas in Hainan, the resistance rate was 75.0% for ERY and 64.5% for CLI for MRSA isolates, and 35.8% for ERY and 29.8% for CLI in MSSA isolates [16].
In this study, 95.2% (59/62) MSSA isolates were resistant to PEN and 81.4% (48/59) of them carried the blaZ gene responsible for resistance to penicillin. MRSA is widely distributed in patient isolates and is rare in food isolates. The food MRSA isolates accounted for 6.7%, which was consistent with isolates from food samples from 2011-2019 in our previous studies [3]. This result was similar to other results from research in China. A total of 6.83% of S. aureus isolates from retail foods were MRSA, 7.14% of those from retail meat and meat products in China were MRSA [19,20], and 10.17% of isolates from food animals were MRSA in Sichuan [26].
MRSA is rarely detected in food isolates but is widely distributed in patient isolates. In this study, the proportion of MRSA in patient isolates was 44.2%. It was also 44.2% in Shanghai, but it was 33.5% in Hainan [13,16]. 23.8% of S. aureus from blood was MRSA in Shandong [27]. Moreover, MRSA isolates have a more severe resistance than MSSA isolates in terms of a higher resistance rate and a greater number of antibiotic-resistant species [26,28,29].
MLST was performed to analyze the molecular characteristics of the S. aureus isolates. The patient isolates were assigned to six CCs and 12 singletons, as shown in Figure 2. The predominant CCs were CC59, CC5, CC22, and CC398. These predominant S. aureus CCs were also the dominant blood CCs in Shandong [27]. The dominant CCs have some differences in different regions in China. The dominate CCs in hospitals were CC398, CC59, CC188, and CC45 in Hainan [16], which CC5 and CC398 were the dominant S. aureus CCs from bloodstream infections between 2013 and 2018 in Shanghai [13].
The prevalent CCs of patient isolates are different in different countries. CC5, CC8, CC188, CC59, CC7, and CC398 were the most prevalent CCs of S. aureus from 22 teaching hospitals in China [21]. In Denmark, the most frequent CCs of S. aureus isolates from atopic dermatitis were CC1, CC8 and CC15 [30]. In Poland, CC45, CC30, CC5, and CC15 were the predominant CCs isolated from the oral cavities of dental patients [31]. The majority of the CCs in Kenya were CC152 and CC8 [32]. The prevalence status of S. aureus in infectious diseases has important implications for understanding the transmission of the pathogen.
The foodborne S. aureus isolates were assigned to three CCs and four singletons STs. The dominant CCs or singletons were CC1, CC5, CC7 and CC59. The most prevalent CCs have not changed in this region. They were also the prevalent CCs in foodborne S. aureus isolates during 2011–2019 in our previous study [3]. CC1, CC5, CC7, and CC59 were the common CCs of foodborne S. aureus isolates in China [19]. CC59 and CC5 were the predominant clones and are often detected in foods, disease infections, and healthy people in China [19,21,27]. The prevalent CCs in foodborne S. aureus isolates vary greatly throughout the world. In Northern Algeria, CC1 and CC97 were prevalent CCs of S. aureus from food samples [33]. CC5, CC30, CC15, and CC1 were common in foodborne S. aureus in Iowa, USA [29]. In Switzerland, CC705, CC97, CC20, CC479, CC1, CC8, and CC15 were common CCs of S. aureus from milk samples [10]. The MLST data can describe the spread of S. aureus in foods.
In this study, 22 STs were detected in patient isolates. Among them, ST59, ST5, ST22, and ST398 were the predominant STs (Table 2). ST59, ST5, ST398 were also the common foodborne isolates of S. aureus in this study. These are common foodborne STs in China. ST59 is common in retail food samples [20]. ST398 is the main livestock-associated S. aureus and the one in retail meat and meat products in China [9,19]. Including both MRSA and MSSA isolates, ST398 is also reported as the predominant clinical isolate in China [16,21,28].
ST5 is commonly isolated from retail meat and meat products, and causes infectious diseases in China [19,21,28]. As a common S. aureus isolate in infectious diseases, ST22 was the predominant blood MSSA in Shandong [27], and the main isolate from community-associated skin infections in Beijing, China [34]. ST22 has been one of the most important MRSA clones in infectious diseases in hospitals globally [35,36]. However, it is rarely detected in foods from China [3,19,20].
ST1 was the most predominant ST among the foodborne S. aureus isolates in this study. It is also a common food contamination isolate in China [3,19]. ST1 has been isolated from infectious diseases in other regions [16,21,29]. However, it has not been isolated from patients in this study, and no food poisoning outbreaks have been caused by ST1 for the past 10 years in this region [3].
A total of 39 MRSA strains were isolated in this study, including thirty-eight strains from patient isolates and one MRSA-ST59 from foodborne isolates. The predominant STs of MRSA isolates from patient were ST5, ST59, ST239 and ST398. The predominant STs of MRSA isolates are consistent with the epidemiological distributions in China. ST5, ST59, and ST239 were the predominant clinical MRSA isolates in Chinese hospitals [17,18,32] and have been the major epidemic MRSA STs in bloodstream infections by S. aureus in China [13,21,27]. MRSA-ST5 was the most predominant MRSA in clinical S. aureus isolates in Shijiazhuang, Wuhan, and Shanghai [13,18]. However, MRSA-ST5 has a low distribution in foods [3,20].
As a common MRSA isolate, ST239 is widely distributed in hospitals and is rarely detected in foodborne S. aureus [17,18,20,37]. ST239 has been the most predominant MRSA ST in Chinese hospitals [17]. However, the dominant MRSA has gradually changed from ST239 to ST59 [29,38]. MRSA-ST59 is widely found in patient and food samples [3,18,20,21,37,38] and is becoming the predominant MRSA isolate of foodborne S. aureus and patient isolates in China.

5. Conclusions

This study has shown the resistance and prevalence characteristics of S. aureus isolated from patients and food in Shijiazhuang, China. Many MRSA isolates are distributed in patient isolates, while they are rarely detected in food samples. MRSA isolates had higher resistance to a variety of antibiotics in comparison to MSSA strains. MRSA-ST5, MRSA-ST59, and MRSA-ST239 were the predominant MRSA isolates in hospitals. The S. aureus isolates from patient and food samples have different characteristics. CC5, CC59, CC22, and CC398 were the most dominant CCs in patient specimens, while CC1, CC5, CC7 and CC59 were the epidemic CCs in food samples. The molecular characteristics can be used to describe S. aureus populations in infectious diseases and food contamination and provide evidence for the epidemic characteristics in transmissions. These data could help us understand the prevalence and resistance to antibiotics of this bacterium.

Author Contributions

Conceptualization, G.L., F.L. and L.Q.; methodology, H.Z. (Han Zhang), L.Q. and C.J.; software, H.Z. (Han Zhang), H.J. and G.L.; validation, R.J., L.L., H.Z. (Hong Zhang), and W.G.; writing—original draft preparation, H.Z. (Han Zhang); writing—review and editing, G.L.; supervision, L.Q.; data curation, H.J., H.D. and X.W.; project administration, W.G.; funding acquisition, W.G. and F.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Science and Technology Program of Hebei Province (No. 17275506D).

Institutional Review Board Statement

This study was approved by the Ethics Committee of Hebei University of Chinese Medicine. This was a retrospective study without any collections of clinical and personal information from patients, so informed consent was not required.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We sincerely thank all the participants who took part in this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Horino, T.; Hori, S. Metastatic infection during Staphylococcus aureus bacteremia. J. Infect. Chemother. 2020, 26, 162–169. [Google Scholar] [CrossRef]
  2. Oliveira, D.; Borges, A.; Simoes, M. Staphylococcus aureus Toxins and Their Molecular Activity in Infectious Diseases. Toxins 2018, 10, 252. [Google Scholar] [CrossRef] [Green Version]
  3. Lv, G.; Jiang, R.; Zhang, H.; Wang, L.; Li, L.; Gao, W.; Zhang, H.; Pei, Y.; Wei, X.; Dong, H.; et al. Molecular Characteristics of Staphylococcus aureus From Food Samples and Food Poisoning Outbreaks in Shijiazhuang, China. Front. Microbiol. 2021, 12, 1436. [Google Scholar] [CrossRef]
  4. Taccetti, G.; Cocchi, P.; Festini, F.; Braggion, C.; Campana, S. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 2010, 376, 1557–1568. [Google Scholar] [CrossRef]
  5. Del, G.P.; Gillon, J.; Roudiere, L.; Reverte, M. Impact of containment and social distancing on the number of community-acquired Staphylococcus aureus skin infections. J. Eur. Acad. Derm. Venereol. 2022, 36, e599–e601. [Google Scholar]
  6. Aratani, T.; Tsukamoto, H.; Higashi, T.; Kodawara, T.; Yano, R.; Hida, Y.; Iwasaki, H.; Goto, N. Association of methicillin resistance with mortality of hospital-acquired Staphylococcus aureus bacteremia. J. Int. Med. Res. 2021, 49, 03000605211058872. [Google Scholar] [CrossRef]
  7. Sato’o, Y.; Hisatsune, J.; Hirakawa, H.; Ono, H.K.; Omoe, K.; Sugai, M. Complete Sequence of a Staphylococcus aureus Clonal Complex 81 Strain, the Dominant Lineage in Food Poisoning Outbreaks in Japan. Genome Announc. 2017, 5, e00853-17. [Google Scholar] [CrossRef] [Green Version]
  8. Fitzgerald, J.R. Livestock-associated Staphylococcus aureus: Origin, evolution and public health threat. Trends Microbiol. 2012, 20, 192–198. [Google Scholar] [CrossRef]
  9. Wang, D.; Wang, Z.; Yan, Z.; Wu, J.; Ali, T.; Li, J.; Lv, Y.; Han, B. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect. Genet. Evol. 2015, 31, 9–16. [Google Scholar] [CrossRef]
  10. Kappeli, N.; Morach, M.; Corti, S.; Eicher, C.; Stephan, R.; Johler, S. Staphylococcus aureus related to bovine mastitis in Switzerland: Clonal diversity, virulence gene profiles, and antimicrobial resistance of isolates collected throughout 2017. J. Dairy Sci. 2019, 102, 3274–3281. [Google Scholar] [CrossRef] [Green Version]
  11. Matuszewska, M.; Murray, G.G.R.; Harrison, E.M.; Holmes, M.A.; Weinert, L.A. The Evolutionary Genomics of Host Specificity in Staphylococcus aureus. Trends Microbiol. 2020, 28, 465–477. [Google Scholar] [CrossRef]
  12. Lee, A.S.; de Lencastre, H.; Garau, J.; Kluytmans, J.; Malhotra-Kumar, S.; Peschel, A.; Harbarth, S. Methicillin-resistant Staphylococcus aureus. Nat. Rev. Dis. Primers 2018, 4, 18033. [Google Scholar] [CrossRef] [Green Version]
  13. Gu, F.; He, W.; Xiao, S.; Wang, S.; Li, X.; Zeng, Q.; Ni, Y.; Han, L. Antimicrobial Resistance and Molecular Epidemiology of Staphylococcus aureus Causing Bloodstream Infections at Ruijin Hospital in Shanghai from 2013 to 2018. Sci. Rep. 2020, 10, 6019. [Google Scholar] [CrossRef] [Green Version]
  14. Mlynarczyk-Bonikowska, B.; Kowalewski, C.; Krolak-Ulinska, A.; Marusza, W. Molecular Mechanisms of Drug Resistance in Staphylococcus aureus. Int. J. Mol. Sci. 2022, 23, 8088. [Google Scholar] [CrossRef]
  15. Ngoi, S.T.; Muhamad, A.N.; Teh, C.S.J.; Chong, C.W.; Abdul Jabar, K.; Chai, L.C.; Leong, K.C.; Tee, L.H.; AbuBakar, S. β-Lactam Resistance in Upper Respiratory Tract Pathogens Isolated from a Tertiary Hospital in Malaysia. Pathogens 2021, 10, 1602. [Google Scholar] [CrossRef]
  16. Li, X.; Huang, T.; Xu, K.; Li, C.; Li, Y. Molecular characteristics and virulence gene profiles of Staphylococcus aureus isolates in Hainan, China. BMC Infect. Dis. 2019, 19, 873. [Google Scholar] [CrossRef] [Green Version]
  17. Liu, Y.; Wang, H.; Du, N.; Shen, E.; Chen, H.; Niu, J.; Ye, H.; Chen, M. Molecular evidence for spread of two major methicillin-resistant Staphylococcus aureus clones with a unique geographic distribution in Chinese hospitals. Antimicrob. Agents Chemother. 2009, 53, 512–518. [Google Scholar] [CrossRef] [Green Version]
  18. Li, X.; Zhang, J.; Zhang, Y.; Zhou, J.; Li, X.; Feng, R.; Li, Y. Methicillin-resistant Staphylococcus aureus of the clonal lineage ST5-SCCmecII-t2460 was associated with high mortality in a Wuhan hospital. Braz. J. Microbiol. 2021, 52, 1929–1936. [Google Scholar] [CrossRef]
  19. Wu, S.; Huang, J.; Wu, Q.; Zhang, J.; Zhang, F.; Yang, X.; Wu, H.; Zeng, H.; Chen, M.; Ding, Y.; et al. Staphylococcus aureus Isolated from Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity. Front. Microbiol. 2018, 9, 2767. [Google Scholar] [CrossRef]
  20. Wu, S.; Huang, J.; Zhang, F.; Wu, Q.; Zhang, J.; Pang, R.; Zeng, H.; Yang, X.; Chen, M.; Wang, J.; et al. Prevalence and Characterization of Food-Related Methicillin-Resistant Staphylococcus aureus (MRSA) in China. Front. Microbiol. 2019, 10, 304. [Google Scholar] [CrossRef] [Green Version]
  21. Tan, S.; Wan, C.; Wang, H.; Zhou, W.; Shu, M. Relationship between nasal Carrier isolates and clinical isolates in children with Staphylococcus aureus infections. Microb. Pathog. 2019, 127, 233–238. [Google Scholar] [CrossRef] [PubMed]
  22. Sun, J.; Yang, M.; Sreevatsan, S.; Davies, P.R. Prevalence and Characterization of Staphylococcus aureus in Growing Pigs in the USA. PLoS ONE 2015, 10, e0143670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Hughes, C.; Ferguson, J. Phenotypic chlorhexidine and triclosan susceptibility in clinical Staphylococcus aureus isolates in Australia. Pathology 2017, 49, 633–637. [Google Scholar] [CrossRef] [PubMed]
  24. M100-S30; Performance Standards for Antimicrobial Susceptibility Testing. 30th ed, Clinical and Laboratory Standards Institute: Malvern, PA, USA, 2022; pp. 58–66.
  25. Liu, Y.; Ji, Y. Multilocus sequence typing of Staphylococcus aureus. Methods Mol. Biol. 2017, 14, 5–9. [Google Scholar]
  26. Gan, T.; Shu, G.; Fu, H.; Yan, Q.; Zhang, W.; Tang, H.; Yin, L.; Zhao, L.; Lin, J. Antimicrobial resistance and genotyping of Staphylococcus aureus obtained from food animals in Sichuan Province, China. BMC Vet. Res. 2021, 17, 177. [Google Scholar] [CrossRef]
  27. Wang, X.; Lin, D.; Huang, Z.; Zhang, J.; Xie, W.; Liu, P.; Jing, H.; Wang, J. Clonality, virulence genes, and antibiotic resistance of Staphylococcus aureus isolated from blood in Shandong, China. BMC Microbiol. 2021, 21, 281. [Google Scholar] [CrossRef]
  28. Zhang, F.; Bai, B.; Xu, G.J.; Lin, Z.W.; Li, G.Q.; Chen, Z.; Cheng, H.; Sun, X.; Wang, H.Y.; Chen, Y.W.; et al. Eravacycline activity against clinical S. aureus isolates from China: In vitro activity, MLST profiles and heteroresistance. BMC Microbiol. 2018, 18, 211. [Google Scholar] [CrossRef]
  29. Thapaliya, D.; Forshey, B.M.; Kadariya, J.; Quick, M.K.; Farina, S.; O’Brien, A.; Nair, R.; Nworie, A.; Hanson, B.; Kates, A.; et al. Prevalence and molecular characterization of Staphylococcus aureus in commercially available meat over a one-year period in Iowa, USA. Food Microbiol. 2017, 65, 122–129. [Google Scholar] [CrossRef] [Green Version]
  30. Clausen, M.L.; Edslev, S.M.; Norreslet, L.B.; Sorensen, J.A.; Andersen, P.S.; Agner, T. Temporal variation of Staphylococcus aureus clonal complexes in atopic dermatitis: A follow-up study. Br. J. Dermatol. 2019, 180, 181–186. [Google Scholar] [CrossRef] [Green Version]
  31. Kwapisz, E.; Garbacz, K.; Kosecka-Strojek, M.; Schubert, J.; Bania, J.; Miedzobrodzki, J. Presence of egc-positive major clones ST 45, 30 and 22 among methicillin-resistant and methicillin-susceptible oral Staphylococcus aureus strains. Sci. Rep. 2020, 10, 18889. [Google Scholar] [CrossRef]
  32. Kyany’a, C.; Nyasinga, J.; Matano, D.; Oundo, V.; Wacira, S.; Sang, W.; Musila, L. Phenotypic and genotypic characterization of clinical Staphylococcus aureus isolates from Kenya. BMC Microbiol. 2019, 19, 245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Achek, R.; El-Adawy, H.; Hotzel, H.; Hendam, A.; Tomaso, H.; Ehricht, R.; Neubauer, H.; Nabi, I.; Hamdi, T.M.; Monecke, S. Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria. Pathogens 2021, 10, 1276. [Google Scholar] [CrossRef] [PubMed]
  34. Xiao, N.; Yang, J.; Duan, N.; Lu, B.; Wang, L. Community-associated Staphylococcus aureus PVL (+) ST22 predominates in skin and soft tissue infections in Beijing, China. Infect. Drug Resist. 2019, 12, 2495–2503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Gostev, V.; Ivanova, K.; Kruglov, A.; Kalinogorskaya, O.; Ryabchenko, I.; Zyryanov, S.; Kalisnikova, E.; Likholetova, D.; Lobzin, Y.; Sidorenko, S. Comparative genome analysis of global and Russian strains of community-acquired methicillin-resistant Staphylococcus aureus ST22, a ‘Gaza clone’. Int. J. Antimicrob. Agents 2021, 57, 106264. [Google Scholar] [CrossRef]
  36. Zhou, W.; Jin, Y.; Liu, X.; Chen, Y.; Shen, P.; Xiao, Y. Comparison of genetic features and evolution of global and chinese strains of community-associated methicillin-resistant Staphylococcus aureus ST22. Microbiol. Spectr. 2022, 10, e0203721. [Google Scholar] [CrossRef]
  37. Liu, D.; Hu, D.; Bao, J.; Gu, W.; Yao, W. Multilocus Sequence Typing of 111 Methicillin-Staphylococcus aureus Strains. Chin. J. Clin. Ration. Drug Use 2017, 14, 5–9. [Google Scholar]
  38. Chen, H.; Yin, Y.; van Dorp, L.; Shaw, L.P.; Gao, H.; Acman, M.; Yuan, J.; Chen, F.; Sun, S.; Wang, X.; et al. Drivers of methicillin-resistant Staphylococcus aureus (MRSA) lineage replacement in China. Genome Med. 2021, 13, 171. [Google Scholar] [CrossRef]
Pathogens 11 01333 g001 550
Figure 1. Antimicrobial resistance profiles of S. aureus isolated from patient and food samples to the same antibiotic. PEN penicillin, FOX cefoxitin, OXA oxacillin, TET tetracycline, DOX doxycycline, CAP chloramphenicol, RFP rifampicin, ERY erythromycin, CLR clarithromycin, SMZ sulfamethoxazole, GM gentamicin, CLI clindamycin, CIP ciprofloxacin, LEV levofloxacin.
Figure 1. Antimicrobial resistance profiles of S. aureus isolated from patient and food samples to the same antibiotic. PEN penicillin, FOX cefoxitin, OXA oxacillin, TET tetracycline, DOX doxycycline, CAP chloramphenicol, RFP rifampicin, ERY erythromycin, CLR clarithromycin, SMZ sulfamethoxazole, GM gentamicin, CLI clindamycin, CIP ciprofloxacin, LEV levofloxacin.
Pathogens 11 01333 g001
Pathogens 11 01333 g002 550
Figure 2. Phylogenetic tree of 86 patient S. aureus isolates based on MLST allelic profiles. Each circle represents CC type or singleton, and the size and color depth of each circle correspond to the number of samples (1, 2–5, 6–10, 11–20, and ≥21).
Figure 2. Phylogenetic tree of 86 patient S. aureus isolates based on MLST allelic profiles. Each circle represents CC type or singleton, and the size and color depth of each circle correspond to the number of samples (1, 2–5, 6–10, 11–20, and ≥21).
Pathogens 11 01333 g002
Table
Table 1. The antibiotics resistance ratio (%) of MRSA and MSSA.
Table 1. The antibiotics resistance ratio (%) of MRSA and MSSA.
Antimicrobial AgentsPatient Samples (n = 86) Resistance Rate (%)
Overall (n = 86)MRSA (n = 38)MSSA (n = 48)
PEN84 (97.7%)38 (100)46 (95.8)
FOX38 (44.2%)38 (100) **0 (0)
OXA37 (43.0%)37 (97.4) **0 (0)
TET34 (39.5%)26 (68.4) **8 (16.7)
DOX14 (16.3%)14 (36.8) **0 (0)
CAP3 (3.5%)1 (2.6)2 (4.2)
RFP5 (5.8%)4 (10.5)1 (2.1)
ERY65 (75.6%)28 (73.7)37 (77.1)
CLR65 (75.6%)28 (73.7)37 (77.1)
SMZ64 (74.4%)26 (68.4)38 (79.2)
GM17 (19.8%)9 (23.7)8 (16.7)
CLI53 (61.6%)28 (73.7) *25 (52.1)
CIP25 (29.1%)21 (55.3) **4 (8.3)
LEV22 (25.6%)20 (52.6) **2 (4.2)
PEN penicillin, FOX cefoxitin, OXA oxacillin, TET tetracycline, DOX doxycycline, CAP chloramphenicol, RFP rifampicin, ERY erythromycin, CLR clarithromycin, SMZ sulfamethoxazole, GM gentamicin, CLI clindamycin, CIP ciprofloxacin, LEV levofloxacin. * p < 0.05, ** p < 0.01.
Table
Table 2. Molecular characteristics of STs in patient and food S. aureus.
Table 2. Molecular characteristics of STs in patient and food S. aureus.
CCsSTs NumberPatient SamplesFood Samples
SputumPus and SecretionBloodWound and SwabsOthersMeats
CC1ST1000004
ST9000002
ST2315000100
ST6769100000
CC5ST51402320
ST6000012
ST306000010
CC8ST72100000
ST239210020
CC15ST15100021
CC22ST22200350
CC121ST121000010
ST7ST7200002
ST20ST20110000
ST25ST25010000
ST59ST59681252
ST88ST88000010
ST398ST398121030
ST522ST522000001
ST1281ST1281000010
ST2472ST2472000001
ST3068ST3068100000
ST3355ST3355100000
NEWNEW100000
ST3069ST3069000100
ST4845ST4845000100
Total 34134112415
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Zhang, H.; Qin, L.; Jin, C.; Ju, H.; Jiang, R.; Li, L.; Zhang, H.; Gao, W.; Wei, X.; Dong, H.; et al. Molecular Characteristics and Antibiotic Resistance of Staphylococcus aureus Isolated from Patient and Food Samples in Shijiazhuang, China. Pathogens 2022, 11, 1333. https://doi.org/10.3390/pathogens11111333

AMA Style

Zhang H, Qin L, Jin C, Ju H, Jiang R, Li L, Zhang H, Gao W, Wei X, Dong H, et al. Molecular Characteristics and Antibiotic Resistance of Staphylococcus aureus Isolated from Patient and Food Samples in Shijiazhuang, China. Pathogens. 2022; 11(11):1333. https://doi.org/10.3390/pathogens11111333

Chicago/Turabian Style

Zhang, Han, Liyun Qin, Caiping Jin, Huidong Ju, Ruiping Jiang, Lijie Li, Hong Zhang, Weili Gao, Xiuping Wei, Hongyan Dong, and et al. 2022. "Molecular Characteristics and Antibiotic Resistance of Staphylococcus aureus Isolated from Patient and Food Samples in Shijiazhuang, China" Pathogens 11, no. 11: 1333. https://doi.org/10.3390/pathogens11111333

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop