Abstract
Background and Aim:
In the past, the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) infections in both humans and animals has increased across Thailand. Staphylococcus argenteus has been associated with infections among humans, exotic pets, and livestock. Both species have been identified in non-human primate species from geographically diverse locations but not from non-human primates in Thailand. This study aimed to determine the presence of MRSA/methicillin-susceptible S. aureus (MSSA) and S. argenteus isolates collected from buccal swab samples in Macaca fascicularis at Kosumpee Forest Park (KFP), Maha Sarakham, Northeast Thailand.
Materials and Methods:
Aseptic buccal swab samples were collected from 30 free-ranging macaques in November 2018. All isolates were tested using multiple biochemical tests and S. aureus latex slide agglutination test. Presumptive S. aureus isolates were tested for the presence of the mecA gene using polymerase chain reaction (PCR) assays. The isolates were phenotypically determined to be resistant to a β-lactam antibiotic using the disk diffusion method with a 30 mg cefoxitin disk. The isolates were analyzed by PCR for the non-ribosomal peptide synthetase (NRPS) gene to distinguish S. argenteus from S. aureus.
Results:
Fifteen macaques (50%) were colonized with S. aureus and 21 isolates were characterized. Three of the macaques carried both the MRSA and MSSA isolate. One animal carried both MRSA and S. argenteus isolate, and one animal carried only S. argenteus. The NRPS gene analysis confirmed that 2 isolates (9.52%) were S. argenteus and 19 isolates (90.48%) were S. aureus [five MSSA and 14 MRSA].
Conclusion:
This study is the first to identify MRSA/MSSA and S. argenteus in wild free-ranging M. fascicularis from Thailand at the KFP in Maha Sarakham. This study is also the first report on the occurrence of S. argenteus carriage in M. fascicularis from Thailand.
Keywords: Macaca fascicularis, methicillin-resistant Staphylococcus aureus, methicillin-susceptible Staphylococcus aureus, non-ribosomal peptide synthetase gene, Staphylococcus argenteus
Introduction
Thailand’s long-tailed macaques (Macaca fascicularis) are the most frequently encountered non-human primate species in the country [1]. These macaques are well adapted to living in close proximity to humans and are widely distributed in urban areas [2–5]. As such, interaction and conflict between humans and macaques are common in many areas, including the Kosumpee Forest Park (KFP) in Maha Sarakham, Northeast Thailand. Staphylococcus aureus is a widespread opportunistic bacterial pathogen that may cause community-acquired, hospital-related, and livestock-associated infections [6]. Methicillin-resistant S. aureus (MRSA) is an important antimicrobial resistant opportunistic pathogen, which can colonize humans, domestic pets, livestock, and wildlife [7]. The MRSA is different from methicillin-susceptible S. aureus (MSSA) due to the carriage of the mecA gene on a variety of distinct mobile genetic elements known as Staphylococcal Cassette Chromosome mec (SCCmec). The mecA gene codes for an alternative penicillin-binding protein [PBP2a] [8, 9].
Recent studies have demonstrated that wild rhesus macaques (Macaca mulatta) living around temple areas in the Kathmandu valley in Nepal with frequent human contact, and those in remote areas with limited human contact were colonized with MRSA and/or MSSA [2, 3, 10]. In the first pilot study, saliva samples were collected from 59 M. mulatta [10]. Four (6.8%) macaques were positive for MRSA with three isolates of ST22 SCCmec type IV. This sequence type (ST) is a pandemic strain found in Asia, Africa, Middle East, and Europe and identified in hospitalized patients in Nepal [10]. Subsequent studies of wild M. mulatta found that MRSA isolates were antibiotic resistant and were the same STs as other human MRSA isolates found both within Nepal and other parts of the world [2]. Some of the MSSA isolates from the macaques were also antibiotic resistant and had the same STs as found in humans or animals/livestock MSSA isolates. However, a number of MSSA isolates were not antibiotic resistant and not genetically related to human or other animal isolates, and appeared to be unique to non-human primates [3, 11]. These MSSA isolates were found in both macaques that interacted with people, as well as, those living in remote areas, and were from both M. mulatta and Macaca assamensis hosts [11]. The data from these studies suggest a transmission of MSSA/MRSA isolates between macaque species and an indication of anthropozoonotic transmission of “human” strains from contaminated environments and human and/or livestock contacts with wild macaques. Other studies have found MSSA isolates in African non-human primates and zoos [12, 13]. Recently, S. aureus clonal complex 75 (CC75) has been reclassified as a new species Staphylococcus argenteus [14]. The phenotypic characteristics of S. argenteus are very similar to S. aureus, except that the colonies often display a non-pigmented presence on blood agar due to the lack of genes producing staphyloxanthin [15, 16]. However, approximately 10% of S. aureus isolates produce white colonies, resulting in misidentification of S. argenteus isolates as the more common S. aureus [17, 18]. The routine use of the PCR assay targeting non-ribosomal peptide synthetase (NRPS) gene has been used as a rapid method for S. argenteus identification[19]. Staphylococcus argenteus has been identified in Thailand patients and animals [14, 16], and from non-human primate isolates around the world [20].
Recently, a number of clinical reports of S. argenteus, causing a disease similar to that of S. aureus, in both humans and animals has increased [21, 22]. This study aimed to investigate the prevalence of S. aureus and S. argenteus carriage in buccal swab samples from wild long-tailed macaques (M. fascicularis) at KFP, Thailand. The isolates were tested using PCR methods for detecting mecA to identify MRSA and NRPS genes for S. argenteus identification.
Materials and Methods
Ethical approval
This research was approved and conducted in accordance with the animal use protocol approved by the Institutional Animal Care and Use Committee at Mahasarakham University (MSU) (protocol numbers 0009/2016). All animal samples collection complied with the current laws of Thailand.
Study period and location
The cross-sectional study was conducted during November-2018 at KFP; N16° 15’ 12.6” E103° 04’ 02.0”, Kosum Phisai district, Maha Sarakham, Northeast Thailand (Figure-1). The KFP consists of a mixed deciduous forest of approximately 0.2 km2, located along the Chi River and bound by agricultural areas and the town of Kosum Phisai to the south. The KFP is home to a free-ranging population of long-tailed macaques (M. fascicularis) of approximately 850 macaques (at the time of the study), distributed among five social groups [23]. The macaques have extensive interaction with local residents and tourists (Figure-2). This can lead to various levels of conflict including aggressive interactions, crop raiding, damage to buildings, as well as, retaliatory responses by the people directed toward the macaques (e.g., throwing rocks/sticks, use of sling shots, etc.) [23, 24].
Figure-1.
Map of the Kosumpee Forest Park, Kosum Phisai District, Maha Sarakham, Northeast Thailand. The map illustrates the close proximity of the human community to the forest park study site [Source: Randall C. Kyes].
Figure-2.
Wild long-tailed macaques at Kosumpee Forest Park have extensive interaction with local residents and tourists [Source: Randall C. Kyes].
Sampling procedures
Buccal samples were collected from 30 randomly selected macaques living in KFP and the surrounding urban area during trapping for health screening checkups. The macaques were captured in a soft nylon mesh cage with a wooden frame (150 × 40 × 40 cm) baited with groundnuts and bananas. Tiletamine-zolazepam (Zoletil® 100 mg/mL, Virbac, Carros, France) was injected intramuscularly to sedate the macaques through 5 mL anesthetic blowpipes after visually assessing a body weight for each macaque in the mesh cage. After anesthesia, the macaques were removed from the cage and vital signs were monitored. Buccal swab samples were then collected aseptically using a sterile buccal swab collection kit with transport media (Deltalab, Barcelona, Spain). All trapping and sampling procedures were conducted by wildlife veterinary specialists from MSU following the protocol approved by the MSU Institutional Animal Care and Use Committee (ethics statement above) and the Thai Department of National Parks. All buccal swab samples were stored at 4°C and taken to the One Health Research Unit, Veterinary Public Health Laboratory, Faculty of Veterinary Sciences at MSU for bacterial testing within 6 h of collection.
Staphylococcus aureus screening
The 30 buccal swabs were cultured on Baird-Parker Agar supplemented with egg yolk tellurite emulsion (Oxoid, Hampshire, UK). Bacterial plates were placed in an incubator at 37°C for 24 h and suspected S. aureus colonies were further characterized. Tentative identification of suspected bacterial colonies was performed using Gram-staining, catalase test, tube coagulase test, mannitol salt agar test, deoxyribonuclease test, and Staphaurex™ Plus latex agglutination test (Thermo Fisher Scientific, Massachusetts, USA) [25].
Antimicrobial susceptibility testing for MRSA
Antimicrobial susceptibility for β-lactam resistance of the isolates was performed by disk susceptibility testing using Mueller-Hinton agar (Oxoid) and cefoxitin disk (30 mg Oxoid). The results were interpreted using the Clinical and Laboratory Standards Institute guidelines M100 to identify methicillin resistance [26]. Staphylococcus aureus ATTC®25923 was used as a control MSSA strain and S. aureus ATCC®43300 was used as MRSA control strain for antimicrobial drug susceptibility testing.
Polymerase chain assay
The isolates’ DNA was extracted using a DNA genomic extraction kit (Geneaid, Taipei, Taiwan), according to the manufacturer’s instructions. The DNA extraction products were measured by the OD 260/280 nm ratio using a NanoDrop 1000 Spectrophotometer (Thermo Scientific, New Jersey, USA) and kept at −20°C until tested. DNA samples were PCR tested for the presence of the mecA gene to confirm MRSA and NRPS genes to differentiate S. argenteus from S. aureus. The PCR reaction mixtures were prepared in a total volume of 25 μL with 10 μmol/L of both forward and reverse primers, KAPA2G™ Robust HotStart ReadyMix PCR Kit (Kapa Biosystems, Wilmington, MA, USA), DNA template, and sterile deionized water. Amplification of the mecA gene was performed using specific primers mecA F (5′-AAAATCGATGGTAAAGGTTGGC-3′) and mecA R (5′- AGTTCTGGAGTACCGGATTTGC-3′). These primers produced a PCR amplicon of 533 bp with the MRSA isolates while and the MSSA isolates were negative [27]. The NRPS gene detection was performed by PCR with specific primers (NPRS1 5′-TTGARWCGACATTACCAGT-3′ and NPRS2 5′-ATWRCRTACATYTCRTTATC-3′) which were derived from a previous study that published these nucleotide sequences [19]. For the analysis of the NRPS gene, the PCR products were 160 bp and 340 bp (S. aureus and S. argenteus, respectively) (Figure-3).
Figure-3.
Polymerase chain reaction (PCR) amplicons of non-ribosomal peptide synthetase gene (NRPS) of Staphylococcus aureus and Staphylococcus argenteus isolated from wild long-tailed macaques. Lane M, DNA marker; lanes 1–2, PCR amplicons of isolates number 17.1 (Monkey ID: M17) and 28.4 (Monkey ID: M28) which was suspected as S. argenteus, respectively; lanes 3–5, PCR amplicons of isolates number 1.1 (Monkey ID: M1) and 22.1 (Monkey ID: M22) which was suspected as S. aureus; lane 6, PCR amplicon of S. aureus ATTC 25923; and lane 7, negative control.
PCR amplification was performed using a thermocycler (Biometra GmbH, Jena, Germany) as follows: 4 min initial denaturation at 94°C, 35 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s (mecA gene primers) and 53°C for 30 s (NRPS gene primers), extension at 72°C for 40 s, and then final extension at 72°C for 10 min. The PCR products were analyzed by 1.5% agarose gels stained with 0.5 mg/mL ethidium bromide in 0.5× TBE buffer and visualized under ultraviolet light. Staphylococcus aureus ATCC®43300 served as the positive control strain for mecA gene. Staphylococcus aureus ATTC®25923 and ATCC®43300 were used as the positive control strains for the NRPS gene while distilled water was used as the negative control.
Results and Discussion
Prevalence of MSSA/MRSA and S. argenteus
Fifteen macaques (50%) were colonized with Staphylococcus spp. and 21 isolates were identified (Table-1). Of the 21 isolates, 5 (23.8%) were MSSA, 14 (66.7%) were MRSA, and 2 (9.5%) were S. argenteus. Four (27%) of the macaques carried two different isolates each: M1, M21, and M22 carried both a MRSA and MSSA isolates and M28 carried one MRSA and one S. argenteus isolate. One animal (M17) carried only a S. argenteus isolate (Table-1) and the remaining 10 (67%) macaques carried only S. aureus (Table-1). The NRPS gene analysis (Figure-3) confirmed that the two isolates were S. argenteus with an amplicon size of 340 bp versus 160 bp for S. aureus (Table-1). The two S. argenteus isolates (number 17.1 and 28.4) were from animals M28 and M17 (Table-1) and represented 9.52% of the staphylococci isolated from the macaques at KFP.
Table-1.
Staphylococcus spp. isolated from wild longtailed macaques.
| Monkey ID | Isolate no. | mecA gene | NRPS gene amplicon size (bp) | Bacterial identification |
|---|---|---|---|---|
| M 1 | 1.1 | + | 160 | MRSA |
| 1.2 | - | 160 | MSSA | |
| M 2 | 2.2 | + | 160 | MRSA |
| M 4 | 4.1 | + | 160 | MRSA |
| M 7 | 7.3 | + | 160 | MRSA |
| M 9 | 9.1 | + | 160 | MRSA |
| M 15 | 15.1 | + | 160 | MRSA |
| M 16 | 16.1 | + | 160 | MRSA |
| M 17 | 17.1 | - | 340 | S. argenteus |
| M 19 | 19.2 | - | 160 | MSSA |
| M 21 | 21.3 | - | 160 | MSSA |
| 21.1 | + | 160 | MRSA | |
| M 22 | 22.1 | - | 160 | MSSA |
| 22.4 | + | 160 | MRSA | |
| M 24 | 24.1 | + | 160 | MRSA |
| M 25 | 25.1 | + | 160 | MRSA |
| M 26 | 26.5 | - | 160 | MSSA |
| M 27 | 27.3 | + | 160 | MRSA |
| M 28 | 28.1 | + | 160 | MRSA |
| 28.4 | - | 340 | S. argenteus | |
| M 29 | 29.5 | + | 160 | MRSA |
MRSA=Methicillin-resistant Staphylococcus aureus, MSSA=Methicillin-susceptible Staphylococcus aureus, S. argenteus=Staphylococcus argenteus
Comparing the Thailand non-human primate carriage with previous studies
The prevalence of S. aureus carriage in this study (50%) was higher than the reported prevalence of 19.4% (six isolates) in other non-human primates including Colobus guereza, Papio anubis, Trachypithecus francoisi, and Rhinopithecus roxellana (31 samples) from Yangzhou Ecological Zoo in Jiangsu, China [12]. From their study, 1 isolate (16.67%) from T. francoisi (fecal sample) was identified as MRSA and 5 isolates (83.33%) were MSSA. The prevalence of S. aureus in Thailand is similar to that the reported in laboratory macaques (n=176, 58.7%) from Chicago, USA [28], which included 152 M. fascicularis and 148 M. mulatta. The carriage rate in this study was 10.8% for MRSA and the remaining 89.2% were identified as MSSA carriers. The results of this study are also similar to the research with M. mulatta and M. assamensis (n = 40) in Nepal [3, 29].
To the best of our knowledge, this is the first study to report the presence of S. argenteus in wild long-tailed macaques from Thailand. To date, S. argenteus has been found in both humans and animals from many regions of the world, including Thailand [21, 29]. Although S. argenteus has been identified in dairy cows [18, 30], rabbits [31], canine [22], and pigs [32], its prevalence in wildlife is understudied.
Conclusion
This study is the first to report the prevalence of S. aureus, MRSA, and S. argenteus from wild non-human primates in Thailand. Although the number of animals tested was limited, the prevalence rate of S. aureus and S. argenteus carriage was high (50%). The Nepalese macaque isolates could be distinguished based on antibiotic carriage which was associated with these isolates being part of known human and livestock clones, while novel clones did not carry antibiotic resistance genes [2, 3, 11]. Thus, further characterization of the isolates in the current study, including MIC for other antibiotics, as well as, multilocus sequence typing could help provide insight into whether the Thailand isolates are related to previously characterized clones from humans and/or livestock. Staphylococcus argenteus carriage has not previously been identified in the Nepalese macaques but two animals from Thailand carried S. argenteus in this study.
Authors’ Contributions
NP, TC, KS, and SP: Conceptualized and designed the study. NP, TC, KS, and SP: Collected the samples. RCK, PT, TT, PK, and AK: Filed sampling coordinator. TC, KS, and SP: Performed the laboratory experiments. NP, TT, PK, PT, and RCK: Supervised the study. NP, TC, KS, and SP: Conducted molecular work. NP, RCK, and MCR: Analyzed the data. NP, RCK, and MCR: Drafted and revised the manuscript. All authors have read and approved the final manuscript.
Acknowledgments
This research project was financially supported by Mahasarakham University 2021. The authors are thankful to the staff at Kosumpee Forest Park, Dr. Pitchakorn Petcharat from Petcharat Animal Clinic, Dr. Ratchanon Kusolsongkhrokul, Dr. Papichchaya Doemlim, and Dr. Panitporn Damrongsukij from One Health Research Unit of Mahasarakham University, the Wildlife and Exotic Friends Club at Mahasarakham University, and students from the Faculty of Environment and Resource Studies at Mahasarakham University for their valuable advice and assistance with the sampling in the field. We are grateful to the Faculty of Veterinary Sciences at Mahasarakham University for use of the diagnostic laboratory. Finally, we are grateful to the Thailand Department of National Parks – Wildlife and Plant Conservation (DNP) and the National Research Council of Thailand for their approval (NRCT project approval to RCK – Project ID: 2016/048; “Healthy Coexistence between Human and Non-human Primates: A One Health Approach”). RCK and PK’s effort was supported in part by the National Institutes of Health Office of Research Infrastructure Programs under award number P51OD010425 to the Washington National Primate Research Center, USA.
Competing Interests
The authors declare that they have no competing interests.
Publisher’s Note
Veterinary World remains neutral with regard to jurisdictional claims in published map and institutional affiliation.
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