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Prevalence and multidrug-resistant profile of methicillin-resistant

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pseudintermedius in dogs, cats, and pet owners in...

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Veterinary World, EISSN: 2231-0916 RESEARCH ARTICLE
Available at www.veterinaryworld.org/Vol.16/March-2023/14.pdf Open Access

Prevalence and multidrug-resistant profile of methicillin-resistant

Staphylococcus aureus and methicillin-resistant Staphylococcus
pseudintermedius in dogs, cats, and pet owners in Malaysia
Mohammad Farzad Afshar1,2 , Zunita Zakaria2,3 , Chen Hui Cheng4 , and Nur Indah Ahmad2

1. Department of Paraclinic, Faculty of Veterinary Sciences, Kabul University, 1001, Kabul, Afghanistan; 2. Department
of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400, Selangor,
Malaysia; 3. Institute of Bioscience, Universiti Putra Malaysia, 43400, Selangor, Malaysia; 4. Department of Companion
Animal Medicine and Surgery, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400, Selangor, Malaysia.
Corresponding author: Zunita Zakaria, e-mail: zunita@upm.edu.my
Co-authors: MFA: mfarzad.afshar@gmail.com, CHC: chen@upm.edu.my, NIA: nurindah@upm.edu.my
Received: 06-10-2022, Accepted: 07-02-2023, Published online: 22-03-2023

doi: www.doi.org/10.14202/vetworld.2023.536-545 How to cite this article: Afshar MF, Zakaria Z, Cheng HC, and
Ahmad NI (2023) Prevalence and multidrug-resistant profile of methicillin-resistant Staphylococcus aureus and methicillin-
resistant Staphylococcus pseudintermedius in dogs, cats, and pet owners in Malaysia, Veterinary World, 16(3): 536–545.

Abstract
Background and Aim: Staphylococcus aureus and Staphylococcus pseudintermedius are widespread skin and mucous
membrane colonizers and may cause opportunistic infections in humans and animals. This study aimed to identify and
characterize methicillin-resistant S. aureus (MRSA) and methicillin-resistant S. pseudintermedius (MRSP) isolates from
domestic and stray dogs and cats and pet owners in Malaysia using molecular epidemiology and antimicrobial profiling.
Materials and Methods: Three hundred and fifty oral and nasal swabs were taken from pet and stray dogs and cats and
pet owners; all samples were subjected to culture and biochemical tests and polymerase chain reaction; the selected isolates
were put through disk diffusion test and multilocus sequence typing.
Results: One S. aureus isolate and three S. pseudintermedius isolates were identified as MRSA and MRSP, respectively, of
which the MRSA isolate and one of the MRSP isolates showed multidrug resistance and the remaining two MRSP isolates
were resistant to one or two antimicrobials. Multilocus sequence typing showed that the MRSA isolate belongs to clonal
complex (CC) 789, while for the MRSP isolates, two were in CC45 and one was a singleton.
Conclusion: This study is the first study in Malaysia to perform molecular characterization of MRSP isolated from pet
dogs and cats and pet owners. The outcomes of this study reveal that even healthy pet dogs and cats and their owners can
be carriers of drug-resistant staphylococci, highlighting the role of pets and pet owners as carriers of MRSA and MRSP in
Malaysia.
Keywords: antimicrobial resistance, antimicrobial susceptibility testing, methicillin resistance, multilocus sequence typing,
public health, zoonotic infections.
Introduction come into contact with animals carrying S. pseudin-
Human and animal mucous membranes and termedius should not be overlooked, especially given
skin are frequently colonized by Staphylococcus the possibility of misidentifying S. pseudintermedius
aureus and Staphylococcus pseudintermedius, which as S. aureus or S. intermedius [1, 2].
may cause opportunistic infections in the carrier. As the prevalence of methicillin-resis-
Staphylococcus aureus is the predominant coagu- tant S. aureus (MRSA) and methicillin-resistant
lase-positive staphylococci found in humans, with S. pseudintermedius (MRSP) increases in the popu-
about a quarter of healthy people having long-term lace, it becomes unavoidable for household animals
colonization of S. aureus. On the other hand, S. pseud- to be exposed to the bacteria. Methicillin-resistant
intermedius is the most common coagulase-positive S. aureus is found in a small percentage of healthy
staphylococci detected in healthy cats and dogs. canines (0%–4%). Clonal relatedness and typing data
Nevertheless, S. aureus can be detected in dogs and showed that MRSA in domesticated animals has been
cats as well (approximately 20%), especially those evolving along with MRSA in humans [1]. Detection
living with their human counterparts [1]. In addition, of MRSA and MRSP in canines and felines suggested
the presence of S. pseudintermedius in people who that these pathogenic bacteria grow in these animals.
Since the incidence of MRSP in humans appears to
Copyright: Afshar, et al. Open Access. This article is distributed under be low, this indicates the possibility of its zoonotic
the terms of the Creative Commons Attribution 4.0 International
License (http://creativecommons.org/licenses/by/4.0/), which origin [1, 2]. Both MRSA and MRSP infections in ani-
permits unrestricted use, distribution, and reproduction in any mals can have a detrimental health effect on the ani-
medium, provided you give appropriate credit to the original
author(s) and the source, provide a link to the Creative Commons mals and humans. Even though most animals carrying
license, and indicate if changes were made. The Creative Commons MRSA and/or MRSP are asymptomatic, the possibil-
Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this
ity of opportunistic infections remains. The most com-
article, unless otherwise stated. mon infections include infections of the skin, surgical
Veterinary World, EISSN: 2231-0916 536
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site, nasal cavity, middle ear, urinary tract, and wound had no visible signs of pyoderma, sneezing, and nasal
from dog bites. Nonetheless, opportunistic infections discharge were included in this study, with the excep-
at other body sites may also occur [3, 4]. tion of stray cats and dogs as there was no history of
Both S. aureus and S. pseudintermedius may antimicrobial intake. In contrast to the previous studies
become resistant to a number of different antimicrobi- in Malaysia that focused on ill pets, this study included
als [5]. In the previous studies conducted in Malaysia, only apparently healthy animals to investigate the pres-
drug-resistant S. aureus and S. pseudintermedius ence of MRSA and MRSP in the animals, if any, and
were isolated from dogs and cats, which were found to explore the role of healthy animals as reservoirs of
to be resistant to tetracycline (TE), erythromycin (E), resistant staphylococci in Malaysia [6, 7].
penicillin (P), gentamicin (GEN), and doxycycline Isolation and identification of methicil-
(DOXY); in addition, multidrug-resistant MRSA iso- lin-resistant S. aureus and methicillin-resistant
lates that were intermediately resistant to vancomy- S. pseudintermedius
cin were isolated from humans [6, 7]. Considering The collected nasal and oral swabs were placed
S. aureus and S. pseudintermedius will continue to in Brain Heart Infusion broth (Oxoid, Basingstoke,
evolve to become stronger and more resistant to United Kingdom) supplemented with 6.5% sodium
various antimicrobials, monitoring the evolution of chloride for 24 h incubation at 35°C. After the incu-
S. aureus and S. pseudintermedius epidemiology has bation, a loopful of the suspension was transferred
hence become crucial. Regarding this, molecular typ- onto oxacillin (OXN) resistance screening agar base
ing techniques are essential tools for identifying and (ORSAB, Oxoid) and incubated at 35°C for 24 h;
tracking the clones and lineages of the predominant the blue and white-pale blue colonies formed were
MRSA and MRSP strains [5–7]. presumptively identified as MRSA and MRSP, respec-
In Malaysia, few studies were conducted to tively [12]. Coagulase test, catalase test, DNase test,
explore the roles of pet dogs and cats as reservoirs of and Gram staining were used to differentiate coagu-
MRSA and MRSP [8–11]. However, no Malaysian lase-positive staphylococci from others [6, 7].
studies focused on detecting MRSP from healthy dogs, Deoxyribonucleic acid (DNA) extraction and amplifi-
cats, or pet owners, as well as performing molecular cation of targeted genes
characterization of MRSP isolates. To understand the Fresh overnight cultures of isolates were used to
risks of S. aureus and S. pseudintermedius transmission obtain genomic DNA with the boiling method [13].
between humans and animals, it is necessary to esti- The presence of the nucA gene was used to confirm
mate their prevalence and molecular epidemiology [1]. the presumptive S. aureus and S. pseudintermedius iso-
Therefore, this study aimed to estimate the prev- lates. A thermal cycler (Eppendorf® pro S, Hamburg,
alence of S. aureus and S. pseudintermedius in pet and Germany) was used for nucA gene amplification,
stray dogs and cats and pet owners, as well as investi- with polymerase chain reaction (PCR) cycling con-
gate the antimicrobial profile and molecular relation- ditions as described earlier by Baron et al. [14] and
ship of the isolates. Sasaki et al. [15]. To confirm methicillin resistance in the
isolates, the presence of the mecA gene was examined
Materials and Methods through PCR amplification, with PCR thermal cycling
Ethical approval conditions as described in the study of Strommenger
This study was conducted in accordance with et al. [16]. The list of oligonucleotides used in this
the requirements of the Ethic Committee for Research study is shown in Table-1 [14–16]. Staphylococcus
Involving Human Subjects (approved on August 07, aureus ATCC 25923 and S. pseudintermedius CCUG
2020). The animal study protocol was approved by 49543 were used as positive controls in the PCR.
the Institutional Ethics Committee of the Institutional
Animal Care and Use Committee (AUP 101; approved Table-1: Oligonucleotide sequence for confirmation of
S. aureus, S. pseudintermedius, and methicillin resistance.
on July 03, 2020).
Primer Oligonucleotide Size (bp) References
Study period and location
sequence (5′‑3′)
This study was conducted as a cross-sectional
SAnucA F TGC TAT GAT TGT 420 [14]
study from August 2020 to March 2021. Stray dogs GGT AGC CAT C
and cats were selected using convenient sampling from SAnucA R TCT CTA GCA AGT
central region of Peninsular Malaysia. Meanwhile, CCC TTT TCC A
pet dogs and cats attended elective procedures at a Pse nucA F TRG GCA GTA GGA 926 [15]
TTC GTT AA
Veterinary Hospital. Pse nucA R CTT TTG TGC TYC
Data source and inclusion criteria MTT TTG G
mecA F AAA ATC GAT GGT 532 [16]
In this study, 150 oral swab samples were collected
AAA GGT TGG C
from pet and stray dogs, 100 oral swab samples from pet mecA R AGT TCT GCA GTA
and stray cats and 100 nasal swab samples were taken CCG GAT TTG C
from pet owners. Animals that had not received antimi- S. aureus=Staphylococcus aureus,
crobial agents for at least 14 days before sampling and S. pseudintermedius=Staphylococcus pseudintermedius

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The disk diffusion method, as stated in the clin- positive S. pseudintermedius isolates were detected
ical laboratory and standards, was used to test the in either stray dogs or cats. Three S. pseudinterme-
antimicrobial susceptibility of the isolates [17]. The dius isolates were confirmed as MRSP, of which one
isolates were tested against ten antimicrobial agents, (1.3%) was isolated from pet dogs (88_D_F), one
namely, OXA (1 µg), enrofloxacin (ENR, 5 µg), GEN (2.0%) was from pet cats (65_C_F), and one (1.0%)
(10 μg), rifampicin (RIF, 5 μg), E (15 μg), DOXY was from pet owners (18_W_M).
(30 μg), trimethoprim-sulfamethoxazole (SXT, Antimicrobial susceptibility testing
25 μg), chloramphenicol (C, 30 µg), cefoxitin (FOX, The results of the drug susceptibility test-
30 μg), and clindamycin (CLN, 2 mcg) (Oxoid™). ing showed that 8 of the 20 methicillin-susceptible
Staphylococcus aureus ATCC 25923 was used as the S. aureus and S. pseudintermedius isolates (40%) did
positive control in antimicrobial susceptibility testing. not exhibit multidrug resistance, of which 1 was iso-
Multilocus sequence typing (MLST) lated from dogs (1/20, 5%), 4 was from pet owners
Multilocus sequence typing of MRSA and MRSP (4/20, 20%), and 3 was from cats (3/20, 15%). In other
was performed using seven housekeeping genes, as words, the remaining 12 isolates (12/20, 60%) were
described by Enright et al. [18] and Solyman et al. multidrug-resistant, where 5 of the isolates were from
[19]. The genomic DNA of the isolates was extracted dogs (5/20, 25%), 4 were from cats (4/20, 20%), and 3
using the DNeasy Blood and Tissue DNA purification were from pet owners (3/20, 15%).
kit (Qiagen®, Germantown, Maryland, USA). The PCR Most isolates (62.5%) from pet owners were
products were subjected to Sanger sequencing, and the resistant to DOXY, whereas none of the isolates from
nucleotide sequences of the seven housekeeping genes pet owners had resistance to RIF. The S. aureus iso-
were analyzed using Molecular Evolutionary Genetics lates from stray cats showed 100% susceptibility to
Analysis version 7.0 software (Pennsylvania State CLN and RIF but were 33.3% resistant to other anti-
University, USA) and the MLST database (https:// microbials. Methicillin-susceptible S. aureus isolates
pubmlst.org/). In addition, the Multiple Sequence from owners showed (1/2, 50%) resistance against
Comparison by Log-Expectation (https://www.ebi. DOXY and ENR (Figure-1). Most S. pseudinterme-
ac.uk/Tools/msa/muscle/) was used to match the dius isolates (5/6, 83%) from pet dogs were resistant
sequences. The sequences were also compared with to DOXY and CLN, whereas the lowest resistance
known housekeeping genes in the database for the was against RIF (1/6, 17%). All the S. pseudinter-
assignment of allele numbers and sequence types (STs). medius isolates from pet cats were resistant to E 3/3,
The clonal complexes (CCs) of the isolates and (Figure-2). For both S. aureus and S. pseudinterme-
the minimum spanning tree were constructed using dius isolates, no co-occurrence was observed among
the goeBURST algorithm (Instituto de Engenharia de pet owners and pets.
Sistemas e Computadores, Lisbon, Portugal) in the For the four methicillin-resistant isolates, the
PHYLOViz (Instituto de Microbiologia and Instituto MRSA isolate from the pet cat was resistant to three
de Medicina Molecular, Lisbon, Portugal) [20]. The antimicrobials, namely ENR, GEN, and FOX. On the
MRSA isolates that shared six of the seven alleles other hand, two MRSP isolates were resistant only to
were assigned to the same CC. The MRSP ST that DOXY, while one MRSP isolate was resistant to mul-
linked with more than three single locus variants tiple antimicrobials.
(SLVs) was identified as the main group founder, and
Multilocus sequence typing
both SLVs and double locus variants were included in
a CC, as previously described by Damborg et al. [21]. In this study, the only MRSA isolate, 76CM,
Descriptive statistics were used for data analysis. was identified as ST789 and assigned to CC789
(Figure-3a). For the MRSP isolates, isolate 65CF was
Results identified as ST2296 and belonged to CC45, isolate
Identification of bacterial isolates 18WM was identified as ST2297, a related ST of
Of the 350 samples collected from dogs, cats, ST2296, and isolate 88DF was identified as ST2298,
and pet owners, only 17 (4.85%) were positive for a singleton isolated from the dog sample (Figure-3b).
S. pseudintermedius and 7 (2.00%) for S. aureus. It is worth noting that ST789 (MRSA) is the first
Among the seven samples that were positive for ST reported in Malaysia, and ST2296, ST2297, and
S. aureus, two were from pet cats (4% of pet cat sam- ST2298 (MRSP) are novel STs.
ples), two were from pet owners (2% of pet owner
Discussion
samples), and three were from stray cats (6% of stray
cat samples). No S. aureus was detected in pet and The findings of this study indicate that not only
stray dogs. Only one of the S. aureus isolates from can S. aureus colonize and transmit between stray
pet cats (2% of the pet cat samples) was identified as and pet cats and humans, but they can also be meth-
MRSA (76_C_M), and the rest were negative for meth- icillin-resistant strains. These findings are in line
icillin resistance. Among all the samples, six (6.0%) with the previous studies conducted in Malaysia and
pet owners, seven (9.3%) pet dogs, and four (8.0%) other geographic regions of the world. For instance,
pet cats were colonized with S. pseudintermedius. No the detection of MRSA in dogs, cats, and veterinary
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60%

50%

40%
Percentage
30%

20%

10%

0%
ENR E CLN C SXT DOXY GEN RIF

Owner 50% 0% 0% 0% 0% 50% 0% 0%

Pet cat 0% 0% 0% 0% 0% 0% 0% 0%

Stray cat 33.30% 33% 0% 33% 33% 33% 33% 0%

Antimicrobial agents

Figure-1: Antimicrobial resistance profile of methicillin-susceptible Staphylococcus aureus isolates. ENR: Enrofloxacin (5 µg);
E: Erythromycin (15 µg); CLN: Clindamycin (2 µg); C: Chloramphenicol (30 µg); SXT: Trimethoprim-sulphamethoxazole
(25 µg); DOXY: Doxycycline (30 µg) GEN: Gentamicin (10 µg); RIF: Rifampicin (5 µg).

120% in the rectum of dogs. Another factor that may affect

100%
the prevalence of MRSA or MRSP is the inclusion
criteria for sample collection. In the study by Aklilu
80%
et al. [6], samples were gathered from inpatient and
Percentage

60%
outpatient animals, whereas the samples collected
40% in this study were from apparently healthy dogs
20% and cats only. The previous studies showed that the
0%
prevalence of MRSA or MRSP tends to be higher
ENR E CLN C SXT DOXY GEN RIF in animals with skin problems. For example, Beck
Owner 40% 40% 60% 40% 20% 60% 20% 0%
Pet cat 67% 100% 33% 33% 33% 67% 67% 33% et al. [29] isolated 70 (40.5%) MRSP and 3 (1.7%)
Pet dog 67% 50% 83% 33% 67% 83% 33% 17% MRSA isolates from the skin cultures of 172 dogs
Figure-2: Antimicrobial resistance profile of methicillin-
with pyoderma. The study of Loncaric et al. [30]
susceptible Staphylococcus pseudintermedius isolates. reported that most of the MRSA isolates were iso-
ENR: Enrofloxacin (5 µg); E: Erythromycin (15 µg); lated from wounds, fistula, dermatitis, abscess, and
CLN: Clindamycin (2 µg); C: Chloramphenicol (30 sinus.
µg); SXT: Trimethoprim-sulphamethoxazole (25 µg);
DOXY: Doxycycline (30 µg) GEN: Gentamicin (10 µg); In this study, MRSP was detected in pet dogs,
RIF: Rifampicin (5 µg). pet cats, and their owners but at an overall low
prevalence of 0.9%. Similar findings were reported
personnel was reported in Poland, Bangladesh, Egypt, by previous studies in which 4.3% and 2.8% of
and Iran [22, 23, 24, 25]. However, the prevalence of pet owners and dogs with pyoderma were MRSP
MRSA (1/50, 2.00% of pet cat samples) in this study positive [31, 32]. In contrast, a higher prevalence
was lower than the prevalence reported by Aklilu et of S. pseudintermedius was reported by Mohamed
al. [6] (5/50, 10% of dog samples; 3/50, 6.00% of cat et al. [7] and Worthing et al. [33], which was 11.5%
samples), Ghani et al. [26] (7/55, 12.73% of stray cat (23/200) of dogs and cats in Malaysia and 8.0% (4/53)
samples), and Paul et al. [27] (10/129, 7.80% of dog of personnel-owned dogs in Australia, respectively.
samples). Moreover, Beck et al. [29] reported that MRSP preva-
The difference in the prevalence of MRSA lence in dogs was as high as 26.7% in dogs recovered
may be due to several reasons. The first reason from pyoderma in the dermatological ward in the der-
could be the difference in sampling sites. The sam- matological ward.
ples in this study were collected only from the oral The lower prevalence of MRSP in this study
cavity because, according to reports, S. aureus and could be due to the selection of sampling sites. As
S. pseudintermedius are most commonly found in mentioned before, this study only collected samples
this area and dual carriage of S. aureus and S. pseud- from nasal and oral cavities. However, more sampling
intermedius was detected in this area as well [28]. sites were included in the mentioned studies, includ-
On the other hand, the samples in the mentioned ing oral and nasal cavities, skin, and rectum. Another
studies were taken from the nasal cavity, oral cavity, possible cause for the lower prevalence of MRSP in
axilla, and perineum. Furthermore, Beck et al. [29] this study could be the health condition of the cats,
reported that S. aureus was found in the nasal cavity dogs, and pet owners. A previous study showed that
and rectum, and S. pseudintermedius was detected there is a high chance of detecting MRSP in sick
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humans and diseased animals compared to those that noting that the S. pseudintermedius isolates in another
are healthy [34]. For example, Mouney et al. [35] study conducted in Malaysia did not show resistance
reported a low prevalence of methicillin-resistant against OXA [7], which may imply that methicillin
staphylococci at 1.6% in healthy dogs. resistance is playing a role in the development of mul-
It seems that transmission of S. pseudinterme- tidrug resistance in S. pseudintermedius
dius from pets to humans is also possible. A study in In this study, an MRSP isolate from pet owners
Taiwan detected S. pseudintermedius in a child with
(18_W_M), which was positive for the mecA gene,
hemophilia who had a history of raising two dogs [36].
This finding demonstrated the possibility of pet-owner did not show resistance against OXA. A similar find-
transmission of S. pseudintermedius as this bacterium ing was reported in the study conducted by Fabri et
is a normal inhabitant of the ear and skin of dogs [37]. al. [41]; that is, OXA-susceptible MRSA was isolated
In this study, all S. pseudintermedius isolates were iso- from nasal cavities of healthy dogs and their caretak-
lated from healthy pets and owners that did not visit a ers. While the reasons behind the susceptibility to OXA
hospital or had any surgery in the past 6 months before in MRSA remain unclear, some possible explanations
sampling. These pet owners were having close contact
with their pet dogs, and hence, were exposed to the Table-2: Antimicrobial resistance profile of S. aureus and
possibility of transmission of MRSA or MRSP from S. pseudintermedius isolates.
their pets.
Sample Name of isolate Sample Antimicrobial
In this study, most S. pseudintermedius isolates ID resistance
from pet dogs and cats and pet owners were resistant profile
to TE, lincomycin, and macrolide classes of antimi- 77SP S. pseudintermedius Pet owner ENR, E, CLN,
crobials, which are common antibiotic classes used as C, SXT,
human medicines, while susceptible to RIF. Similarly, DOXY, GEN
the S. pseudintermedius isolates from dogs and cats in 90SP S. pseudintermedius Pet dog ENR, E, CLN,
SXT, DOXY, GEN
Australia did not exhibit RIF resistance, while 20.0% 63SP S. pseudintermedius Pet dog ENR, CLN, SXT,
and 0.4% of the isolates exhibited DOXY and CLN DOXY, GEN
resistance, respectively [38]. Furthermore, the per- 98SP S. pseudintermedius Pet dog ENR, E, CLN,
centage of S. pseudintermedius isolates that exhibited C, DOXY, RIF
68SP S. pseudintermedius Pet owner CLN, DOXY
resistance against C in this study (33%) is compara- 66SP S. pseudintermedius Pet cat ENR, E, CLN,
ble with the study conducted in Spain (25%), whereas DOXY, GEN
the resistance against SXT (12.5%) and E (31.1%) 44SP S. pseudintermedius Pet owner ENR, E, CLN,
reported in Spain was lower [1]. C, DOXY
Both S. aureus isolates from stray cats were sus- 74SP S. pseudintermedius Pet dog E, CLN, C,
SXT, DOXY
ceptible to CLN and RIF. This finding is similar to 23SP S. pseudintermedius Pet cat E, C, SXT,
the finding reported in a study conducted in Spain, in DOXY, RIF
which resistance against CLN was observed in some 1SA S. aureus Pet cat Susceptible
of the S. aureus isolates [1]. In the veterinary hos- to all
4SA S. aureus Stray cat C
pital, where this study was done the usage of RIF is 7SA S. aureus Stray cat Susceptible
infrequent, while DOXY, SXT, and ENR are used in to all
routine treatment of small animal cases (CH Cheng, 10 SA S. aureus Stray cat ENR, E, SXT,
personal communication). Therefore, the resistance to DOXY, GEN
125SA S. aureus Pet owner ENR, DOXY
RIF did not occur. 126SA S. aureus Pet owner Susceptible
In this study, the MRSA isolates detected from to all
pet cats was resistant to three antimicrobials, namely 101SP S. pseudintermedius Pet dog DOXY, OXA
ENR, GEN, and FOX (Table-2). This finding is similar 36SP S. pseudintermedius Pet owner CLN, OXA
to the findings of other studies conducted in Malaysia 56SP S. pseudintermedius Pet owner CLN, OXA
26 SP S. pseudintermedius Pet cat ENR, E, GEN
and neighboring countries (such as Singapore), which 150SP S. pseudintermedius Pet Dog ENR, CLN,
observed resistance against OXA, ENR, and board-spec- SXT, DOXY
trum antimicrobials among the MRSA isolates [39]. 18WM S. pseudintermedius Pet owner DOXY
The MRSP isolates detected from pet dogs and 76CM S. aureus Pet cat ENR, GEN,
FOX
cats were resistant to TE, fluoroquinolone, aminogly- 88DF S. pseudintermedius Pet dog DOXY, OXA
coside, and P classes of antimicrobials. This finding 65CF S. pseudintermedius Pet cat ENR, DOXY,
is in line with the study by Gagetti et al. [40], which GEN, OXA
reported that all the isolated S. pseudintermedius ENR=Enrofloxacin (5 µg), E=Erythromycin (15 µg ),
were resistant to OXA and TE. Similarly, a study in CLN=Clindamycin (2 µg); C=Chloramphenicol (30 µg),
Singapore also indicated that the S. pseudintermedius SXT=Trimethoprim-sulfamethoxazole (25 µg),
DOXY=Doxycycline (30 µg), GEN=Gentamicin (10 µg),
isolates detected from pet dogs and cats were methi- RIF=Rifampicin (5 µg), FOX=Cefoxitin (30 μg),
cillin-resistant, and 78% (40/51) of the isolates turned OXA=Oxacillin (1 µg), S. aureus=Staphylococcus aureus,
out to be multidrug-resistant [39]. However, it is worth S. pseudintermedius=Staphylococcus pseudintermedius

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include: (1) The presence of the transposable element sources in the United Kingdom), ST1411 (from the
IS1181 in the mecA gene, which leads to the suppres- Netherlands), ST6198 (from a human wound in
sion of PBP2a expression; (2) deletion of a single Myanmar), and ST7 (from blood in Thailand, from
nucleotide from the area that codes for the N-terminal nasal cavity in the United States, from Switzerland).
of PBP2a; (3) suppression of the mecA gene through To the best knowledge of the authors, this is
the plasmid-encoded non-functional N-terminally the first ST789 reported in Malaysia. Nevertheless,
truncated blaR1 sensor-transducer gene, even in the this ST was also detected in several other countries,
existence of beta-lactams; and (4) cell wall produc- such as Pakistan (from human pus), the Philippines
tion is affected by mutations in the femXAB genes, (from humans), Japan (from bovine mastitis, in milk),
which encode proteins tangled in pentaglycine bridge Ghana, and Kenya (SCCmec type IV and Panton-
production. Valentine leukocidin positive) [46, 47, 48]. This sug-
Incorrect or overutilization of antimicrobials in gests that ST789 usually originates from humans or
different geographical regions plays a significant part the environment, causing local or systematic MRSA
in the development of resistance in bacteria. The drug infections. However, in this study, isolate 76CM
resistance in the isolates in this study may be due to was isolated from an apparently healthy 1-year-old
the use of these drugs on the recruited pets or their cat. Since, according to MLST and SCCmec typing,
owners [22]. Therefore, to slow down the develop- ST789 is a community-associated strain (SCCmec
ment progress of multidrug resistance among bacteria type V), the cat may have acquired MRSA from its
and reduce the chance of spreading drug-resistant bac- owner or the environment.
teria in the community, both doctors and pet owners The MRSP isolates, 65CF and 18WM, were
must practice prudent use of antimicrobials and abide assigned new STs, ST2296 and ST2297, respectively,
by self-hygiene, including performing an antibiogram by the PubMSLT curated by Vincent Perreten. These
before prescribing antimicrobials. In addition, resis- STs are novel STs, and they are related to each other.
tance may also develop from mutations during bacte- ST2296 belongs to CC45, a worldwide spread CC
rial clonal expansion and the transfer of antimicrobial with members in Europe, the Middle East, Asia, and
resistance genes among bacteria from the same or Finland [49]. There were two STs related to ST2296,
different species [42]. The low resistance against RIF that is, ST69 and ST144 (methicillin-susceptible
among S. pseudintermedius isolates could be due to S. pseudintermedius isolated from dogs in the United
the ability of RIF to penetrate the cell wall, making it States). Similar to ST69 and ST144, ST2297 was
an effective antimicrobial even to MRSP [43]. also isolated from a pet owner, but it was resistant to
Antimicrobial resistance was announced as a methicillin. Based on the PubMLST database, there
global challenge by the World Health Organization in were other STs in CC45 detected in other countries:
2001, and it has been reported that antimicrobial resis- Methicillin-resistant ST1376 isolated from dog skin
tance costs more than one billion euros per year [44]. in the Netherlands; community-acquired, methicil-
Therefore, the one health approach was proposed lin-susceptible ST698 isolated from a dog with otitis
to cope with the destructive effects of antimicrobial in the Netherlands; methicillin-susceptible ST2286
resistance on humans, animals, and environments. isolated from dogs with pyoderma and otitis and
Conducting public campaigns regarding the effects of healthy human in Brazil; and methicillin-resistant
irrational use of antimicrobials; improving living stan- ST179 isolated from a cat with pyoderma in Israel.
dards, hygiene measures, and health-care systems; Further query in the PubMLST database [50] indi-
reducing irrational use of antimicrobials to decrease cated that ST311, a related ST of CC45, was isolated
the spread of antimicrobial agents to the environ- from a healthy human carrier in Thailand, which is
ment; conducting local, national, and international similar to ST2297 which was isolated from a healthy
antimicrobial resistance surveillance and research pet owner. ST2298 (88DF) isolated from a dog in
regarding the mechanisms behind the antimicrobial this study was a singleton, a triple locus variant from
resistance; finding and promoting novel and reliable ST1798, which was isolated from a dog with pyo-
diagnostic techniques and vaccines; training of micro- derma in China.
biologists, epidemiologists, and infectious diseases In Israel and Thailand, the bacteria from the
specialists; supporting research for finding new ways ST45 clonal lineage are the predominant strains [46].
of treatment; and finally, including the antimicrobial Furthermore, ST45 was detected in dogs and cats with
resistance issue in political agenda are some of the pyoderma in Australia [47]. Based on the resistance
strategies that can be used to battle against antimicro- genes, isolates typed as ST45 in Thailand are similar
bial resistance [45]. to isolates reported from Europe and North America
The MLST analysis conducted in this study [51]. Besides, non-typeable SCCmec STs belonging to
identified the MRSA isolate (76CM) from healthy pet CC45 were also isolated from symptomatic dogs and
cats as ST789. This ST is part of CC789, with several cats in Italy and clinical specimens from dogs in Italy
related STs as shown in Figure-3. The STs related to and Netherlands [52, 53]. These findings suggest the
ST789 include ST1159 (isolated from the nasal cavity possibility of the transmission of ST2296, ST2297, and
of a human in Switzerland), ST5905 (from unknown ST2298 from overseas to Malaysia through the entry of
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 Available at www.veterinaryworld.org/Vol.16/March-2023/14.pdf

b
Figure-3: Population snapshot of related sequence types of (a) methicillin-resistant Staphylococcus aureus and
(b) methicillin-resistant Staphylococcus pseudintermedius.

infected animals or humans from Southeast Asian and required to understand the prevalence of these bacteria
European countries. among them in the future. The results of antimicrobial
Although MRSA and MRSP can occur in both susceptibility testing in this study indicated that both
healthy and diseased animals and humans, the prev- methicillin-resistant and methicillin-susceptible iso-
alence is higher in diseased animals. In the present lates could be multidrug-resistant, which is a warning
study, even though MRSA and MRSP were detected in for the community and practitioners.
apparently healthy dogs, cats, and pet owners, the prev-
Conclusion
alence was low. The absence of MRSP isolates among
dogs and cats from the shelter and the low prevalence of Each MRSA and MRSP isolates from animals
MRSA among this group suggest that cats and dogs in and humans belong to a different ST, which were also
contact with humans are more likely to acquire MRSA found in other countries in Asia and Europe. Most of
and MRSP than those without contact with humans. the isolated S. aureus and S. pseudintermedius were
Therefore, screening and identification of MRSA multidrug-resistant, which is an alarm for the pub-
and MRSP in inpatient animals and their owners are lic regarding the significance of pets as reservoirs
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 Available at www.veterinaryworld.org/Vol.16/March-2023/14.pdf

of antimicrobial-resistant bacteria. As the first study Kamata, S. and Hiramatsu, K. (2007) Methicillin-resistant
investigating the molecular typing of MRSP in Staphylococcus pseudintermedius in a veterinary teaching
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studies on MRSP. As the number of antimicrobial-re- Molecular relatedness of methicillin-resistant S. aureus iso-
sistant bacteria is increasing worldwide, the need for lates from staff, environment and pets at university veteri-
devising and promoting new strategies, treatments, nary hospital in Malaysia. PLoS One, 7(8): e43329.
7. Mohamed, M.A., Abdul-Aziz, S., Dhaliwal, G.K. and
and drugs has become imperative. Hence, the One Bejo, S.K. (2017) Antibiotic resistance profiles of
Health approach, which is a way of utilizing different Staphylococcus pseudintermedius isolated from dogs and
strategies such as reducing unnecessary use of anti- cats. Malays. J. Microbiol., 13(3): 180–186.
microbials and improving hygiene measures, is rec- 8. Gómez-Sanz, E. (2013) Staphylococcus aureus and
ommended in the practice of medicine to slow down Staphylococcus pseudintermedius in Animals: Molecular
Epidemiology, Antimicrobial Resistance, Virulence and
the development and spread of antimicrobial-resistant Zoonotic Potential. Universidad de La Rioja Departamento,
bacteria. La Rioja, Spain.
9. Kumar, S., Anwer, R., Yadav, M., Sehrawat, N., Singh, M.
Authors’ Contributions and Kumar, V. (2021) Molecular typing and global epide-
ZZ, CHC, NIA, and MFA: Conceptualization. miology of Staphylococcus aureus. Curr. Pharmacol. Rep.,
7(5): 179–186.
ZZ, CHC, NIA, and MFA: Methodology. MFA and 10. Mohamed, M.A., Abd Aziz, S., Dhaliwal, G.K., Bejo, S.K.,
CHC: Data collection and analysis. ZZ, CHC, and Nordin, M.L., Shaari, R., Elmi, S.A., Kanamma, A.A.,
NIA: Supervised the study. MFA: Writing the original Goni, M.D. and Osman, A.Y. (2020) Detection of
draft. ZZ, CHC, NIA, and MFA: Review and editing Staphylococcus pseudintermedius in dogs and cats in
Selangor, Malaysia. Am. J. Anim. Vet. Sci., 15(1): 10–14.
of the manuscript. All authors have read, reviewed, 11. Kanagarajah, R.R., Lee, W.C.D., Lee, D.Z.F., Yusoff, K.,
and approved the final manuscript. Paramasivam, S.J., Low, W.Y., Jeevaratnam, K. and
Lim, S.H.E. (2017) Antibiotic profiling of methicillin-re-
Acknowledgments
sistant Staphylococcus aureus (MRSA) isolates in stray
This research was funded by Universiti Putra canines and felines. Cogent Biol., 3(1): 1412280.
12. Horstmann, C., Mueller, R.S., Straubinger, R.K. and
Malaysia, grant number GP-IPB/2019/9676501. The Werckenthin, C. (2012) Detection of methicillin-resistant
authors thank the staff of the Bacteriology Laboratory, Staphylococcus pseudintermedius with commercially avail-
Faculty of Veterinary Medicine, Universiti Putra able selective media. Lett. Appl. Microbiol., 54(1): 26–31.
Malaysia, Dr. Shahira from Majlis Perbandaran 13. Bitrus, A.A., Zunita, Z., Khairani-Bejo, S., Othman, S. and
Subang Jaya, Dr. Aiman from Dewan Bandaraya Nadzir, N.A.A. (2018) Staphylococcal cassette chromo-
some mec (SCCmec) and characterization of the attachment
Kuala Lumpur, and Dr. Wirdatul from the University site (attB) of methicillin-resistant Staphylococcus aureus
Veterinary Hospital, Universiti Putra Malaysia for (MRSA) and methicillin-susceptible Staphylococcus aureus
their kind assistance throughout this study. (MSSA) isolates. Microb. Pathog., 123: 323–329.
14. Baron, F., Cochet, O., Pellerin, J., Zakour, N.B.E.,
Competing Interests Lebon, A., Navarro, A., Proudy, I., Loir, Y.L.E. and
Gautier, M. (2004) Development of a PCR test to differ-
The authors declare that they have no competing entiate between Staphylococcus aureus and Staphylococcus
interests. intermedius. J. Food Prot., 67(10): 2302–2305.
15. Sasaki, T., Tsubakishita, S., Tanaka, Y., Sakusabe, A.,
Publisher’s Note Ohtsuka, M., Hirotaki, S., Kawakami, T., Fukata, T. and
Veterinary World remains neutral with regard to Hiramatsu, K. (2010) Multiplex-PCR method for species
identification of coagulase-positive staphylococci. J. Clin.
jurisdictional claims in published institutional affiliation. Microbiol., 48(3): 765–769.
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