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Byline: D. H. Kalhoro, S. Gao, M. S. Kalhoro, F. Parveen, M. Tariq, S. A. Pirzado and Y. J. Liu


Staphylococcus pseudintermedius is an emerging pathogen causing respiratory infection in dogs. In this experiment pathogenicity characteristic of S. pseudintermedius were determined. The research was mainly focused on three aspects including bacterial load, histopathological changes and virulence factors. BALB/c mice were intranasaly inoculated with S. pseudintermedius. The results showed that the bacteria can cause serious neurologic symptoms including walking in circles, bending of neck and produces obvious histopathological changes in lung and brain of the mice. In lungs and brain higher levels of bacterial load was observed during present study. Of all 11 oxacillin-resistant isolates of S. pseudintermedius, 2 carried SCCmec types II-III, 2 carried SCCmec I and 3 carried SCCmec types III according to PCR-based SCCmec typing. Exfoliative toxin (siet), lukS and luk F genes were also identified from the isolates.

Keywords: Staphylococcus pseudintermedius, Mouse model, Bacterial load, Histopathology, Virulence factors.


Respiratory problems are common in dogs. A varying flora of bacterial pathogens is normally present in the respiratory tract of the canines without causing any clinical signs. Methicillin-resistant Staphylococcus pseudintermedius (MRSP) is coagulase positive staphylococci identified by Devriese et al., (2005) has emerged globally in companion animals in the last decade (Damborget al., 2016) and is the most important opportunistic pathogen which belongs to the normal microbiota of companion animals andhumans (Bardiu et al., 2013;Van Duijkeren et al., 2011). Organism is isolated from groin and forehead, nares, mouth, anus of healthy dogs and cats (Abraham et al., 2007; Griffeth et al., 2008),mostly associated with skin, wound infection, otitis, pyoderma and urinary tract infections (Bannoehr and Guardabassi, 2012; Weese et al., 2009).

MRSP infections are generally linked with outbreaks (Weese and Van Duijkeren, 2010), colonization of healthy animals and contact of the persons working with the animals so they become carriers (Boost et al., 2011; Hanselman et al., 2008). It was reported from PFGE analysis, that pet owners suffering from deep pyoderma can carry the organism (Guardabassi et al., 2004), and recent reports confirmed transmission of MRSP from pets to their owners (Frank et al., 2009; Soedarmanto et al., 2011) and to veterinary staff working in the Veterinary clinics and staff owned healthy dogs carried MRSP of same resistance pattern and PFGE profile as the patients (Van Duijkeren et al., 2008). Methicillin resistance of S. pseudintermedius is mediated by mecA gene located on the chromosome of the bacterium on a mobile element called the 'staphylococcal chromosomal cassette' (SCCmec) (Weese and Van Duijkeren, 2010).

These elements can be transferred between different staphylococcal species (Wielders et al., 2002). S. pseudintermedius (previously S. intermedius) carry several virulence factors i.e coagulase, clumping factors, haemolysin and leukotoxin, pyogenic toxins comprising staphylococcal enterotoxins, toxic shock syndrome toxin 1, and S. intermediusexfoliative toxin (Futagawa-Saito et al., 2004). Another S. pseudintermediusexfoliative toxin (SIET) showed a rounding effect on cultured epithelial cells. SIET Animal models were used to observe the effect of exfoliative in day old chickens, hamsters and dogs, but not in rats and mice. Dogs injected with SIET showed symptoms of erythema, exfoliation and crusting, which were similar to human staphylococcal scalded skin syndrome and porcine exudative epidermitis, canine pyoderma(Terauchi et al., 2003).

Like Panton Valentine leucocidinleukotoxin of S. aureus, S. (pseud) intermedius also produces a bicomponentleukotoxin, Luk-I encoded by two cotranscribed genes, lukS and lukF(Futagawa-Saito et al., 2004; Prevost et al., 1995) a leukotoxin known as Luk-I having leucotoxicity towards polymorphonuclear cells (Futagawa-Saito et al., 2004) but only a little haemolytic activity on rabbit erythrocytes (Prevost et al., 1995). S. pseudintermedius produces an immunoglobulin-binding staphylococcal protein A (spa) that binds to the IgG from the fc portion, thereby affecting its ability of opsoninsation(Moodley et al., 2009) and form biofilms like S. aureus(Futagawa-Saito et al., 2006). Complete genome sequence of S. pseudintermedius was published recently for better understanding of the pathogenesis of S.pseudintermedius(Zakour et al., 2011).

The aim of this study was toinvestigate the occurrence and characteristics of S. pseudintermediusisolates and develop a mouse model to examine the factors associated with infection.


Ethics statement: Before conducting the study, approval for conducting the experiments was obtained from Ethical Committee for Animal Experiments of Nanjing Agricultural University, China.

Isolation and Identification:Forty nasal swabs were taken from dogs having respiratory symptoms, such as coughing, sneezing and copious nasal discharge. Samples were collected from Animal Clinics of Nanjing Agricultural University in Jiangsu Province of China to isolate S. pseudintermedius.PCR amplification of 16S rRNA gene was performed for the confirmation of the bacteria using a pair of oligonucleotide primer (5'AGAGTTTGATCMTGGCTCA/TACGGYTACCTT GTTACGACTT-3').

Detection of virulence factors: PCR assay was used and tested for the presence of mecA gene. Antibiotic oxacillin was used to detect resistant isolates of S. pseudintermedius for SCC mectypingas described by some reports (Baron et al., 2004, Zhang et al., 2005). Leukocid in genes viz lukS, lukF and siet were also identified (Becker et al., 1998; Futagawa-Saito et al., 2004; Lautz et al., 2006). The information of primers is shown in Table 1.

Table1. Primers used for PCR analysis.

Primer###Oligonucleotide sequence (5'3')###Amplicon size (bp)###References

SEC###GGCGGCAATATTGGCGCTCG###271###(Becker et al., 1998)


Sea###GCGAAACACACAATGCTTGC###127###(Becker et al., 1998)


Seb###GTGGCTGGCGGTGAGTCACG###477###(Becker et al., 1998)




LUK F###CCTGTCTATGCCGCTAATCAA###572###(Futagawa-Saito et al.,


LUK S###TGTAAGCAGCAGAAAATGGGG###503###(Futagawa-Saito et al.,


CIF2 F2###TTCGAGTTGCTGATGAAGAAGG###495###(Oliveira and de


RIF4 F3###GTGATTGTTCGAGATATGTGG###243###(Oliveira and de


DCS F2###CATCCTATGATAGCTTGGTC###342###(Oliveira and de


MECA P4###TCCAGATTACAACTTCACCAGG###162###(Oliveira and de


MECI P2###ATCAAGACTTGCATTCAGGC###209###(Oliveira and de


Type I-F###GCTTTAAAGAGTGTCGTTACAGG###613###(Zhang et al., 2005)


Type III-F###CCATATTGTGTACGATGCG###280###(Zhang et al., 2005)


Type V-F###GAACATTGTTACTTAAATGAGCG###325###(Zhang et al., 2005)


mec A gene, SCC mectyping: an initial denaturation step at 94degC for 4min, followed by 30 cycles with denaturation at 94degC for 30s, annealing at 53degC for 30s and extension at 72degC for 1 min. A final extension step was done at 72degC for 4 min.

sietgene: an initial denaturation step at 94degC for 2min, followed by 30 cycles with denaturation at 95degC for 1min, annealing at 55degC for 1min and extension at 72degC for 2min. A final extension step was done at 72degC for 4 min.

lukF and lukS genes: an initial denaturation step at 94degC for 5min, followed by 35 cycles with denaturation at 94degC for 1min, annealing at 57degC for 1min and extension at 72degC for 1min. A final extension step was done at 72degC for 5 min.

Aliquots from amplification reactions were analyzed by 1.5% agarose gel electrophoresis and viewed under UV light.

Experimental infection of mice: The S. pseudintermedius (Sp) NJ-1 strain isolated from a dog with respiratory syndrome was used. The bacterial strain was cultured on LB and incubated at 37degC. The bacterium was identified on the basis of its biochemical characteristics and through sequencing of the 16S rRNA gene. BALB/c female mice (6 weeks of age, 18-20 g) were purchased from the Animal Experiment Centre, Yangzhou University, China. Mice were divided into Sp and PBS groups with 25 mice in each group. Mice in Sp group were intranasally inoculated with Sp (1x109 CFU/ml, 50 u l/mouse) and PBS group was inoculated with PBS intranasally as control. Five mice from each group were sacrificed humanely according to a pre-designated schedule at indicated time points of 1, 2, 3, 4 and 5 days post-infection (d.p.i.).

Bacterial loads: The lung and brain from each mouse were weighed and homogenized individually in PBS to obtain a 10% weight-to-volume suspension. The number of CFUs of Sp was determined by plating serial 10-fold dilutions of homogenates on LB agar in duplicate. The plates were incubated overnight at 370C. Results were counted and expressed as CFU/g for brain and lung.

Histopathological examination: At 2 d.p.i. mice were euthanized; brain and lung tissues were harvested and fixed in 10% neutral buffered formalin. After fixation, the tissues were embedded in paraffin wax. Tissue sections with a thickness of 4um were stained with haematoxylin and eosin and examined under microscope.


During present study S. pseudintermediuswere isolated and confirmed by morphology, culture and biochemical characteristics. In addition PCR was performed for the confirmation of the bacteria.

Clinical symptoms: After 24 h of S. pseudintermediusinoculation, clinical signs were appeared in the mice. Clinical signs included coarse hair, not shiny, apathetic appearance of distinct neurological symptoms. Abnormal reactions were observed having sensitive to touching and paralyzed on one side has lost the ability to walk (Fig 1), when the tail was lift, quick circling movement was observed, this phenomena was more pronounced on 2d.p.i.

Bacterial loads: The bacterial load in the brain and lungs of mice infected with bacteria is presented in (Fig. 2). Twenty-five mice were intranasaly inoculated with 1x109 CFU/ml, 50 u l/mouse. Bacterial load was carried out from lung and brain. At 1 d.p.i bacterial load in lung and brain was more than 103 and 102 CFU/g respectively. At 2d.p.i bacterial load was more than 105 CFU/g in lung and more than 104 CFU/g in brain. Bacterial number continued to be slightly increased in brain and decreased in lung with the course of the infection. At day 2 bacterial load in lungs reached its maximum, whereas in brain bacterial load slightly decreased, while At 5 d.p.ibacterial load becomes 105 CFU/g in brain and lung.

Histopathological changes: In brain microglial cell numbers were increased and aggregated to form microglial nodules andneurophagia phenomena was observed (Fig 3A). Nerve fibres become dissolved as well as appearance of vascular cuff was noticeable (Fig 3B). In lung widening of alveolar septa and increased infiltration of the inflammatory cells including macrophages were observed. (Fig.3D, E). Brain and lungs from control group mice did not showed histopathological lesions (Fig. 3C, F).

Presence of mecA and SCCmec typing of S. pseudintermedius: All oxacillin resistant isolates of S.pseudintermediusfrom dogs had mecA gene while oxacillin susceptible isolates did not possess themecAgene. Among the mecA-positive isolates, 2(18.18 %) belonged to SCCmec type II-III, 2(18.18 %) belonged to SCCmec type I and 3(27.27 %) belonged to SCCmec type III. Results of mecA and SCCmec type are summarized in Table 2. The results for PCR amplification are shown in Fig.4-9.

Table 2.SCCmec typing of mecA resistant S.pseudintermediusstrains isolated from dogs.

Total###Number of###SCCmec###Number of

number###positive###type###positive strains



24###11 (45.83%)###II-III###2 (18.18%)

###III###3 (27.27%)

###I###2 (18.18%)


Dogs are the main reservoir of S. pseudintermedius having variable carriage rates subject to the different sites of the body (Bannoehr and Guardabassi, 2012). Studies have been done in past for the bacterial isolation from the upper and lower respiratory tract of both diseased and healthy dogs. In the present study twenty four Staphylococcus pseudintermedius spp were isolated from forty dogs having respiratory infection. Our results are in agreement with others authors who isolated S. pseudintermedius from indoor patient dogs (46.2%) and outdoor patient dogs (19.4%) in a Japanese veterinary teaching hospital (Sasaki et al., 2007). Onumaet al., (2012) reported high prevalence of S. pseudintermedius in dogs having pyoderma infection (76.1%during 1999-2000 and 76.4% in 2009). However, in Canada, low MRSP (2.1%) and MRSS (0.5%) isolates were detected (Hanselman et al., 2008).

S. pseudintermedius is not present in the nasopharyngeal flora of the humans but can be carriers when they come in contact with infected animals (Sasaki et al., 2007). A mouse model was designed to study pathogenicity of S.pseudintermedius. BALB/c mice were inoculated with S.pseudintermedius. The mice were killed at different intervals, and brains and lungs were taken and plated for bacterial count. In the present study, severe neurological signs including bending of the neck and walking in circles were observed. In previous studies, mice exhibited clinical signs of anorexia, ruffled hair, abdominal breathing, septicemic infection (Souza et al., 2012) and meningitis (Gerber et al., 2001). Higher level of bacterial loads in brains and lungs of the mice weredetected, leading to the severe histopathological lesions.

In brain,theincreased microglial cells resulted into the formation of microglial nodules, while in lungs alveolar septa was widened with increased infiltration of the inflammatory cells including macrophages. Our findings are in agreement with other authors who observed neuronal damage, focal necrosis with shrunken eosinophilic neurons (Gerber et al., 2001;Guoet al., 2014), specific necrotizing encephalitis and abscesses (Vecht et al., 1997). Necrosis, alveolar inflammation, interstitial edema and infiltration of the inflammatory cells have been observed after pneumococcal infection in the mice (Kalhoro et al., 2015;Wang et al., 2005).

Methicillin resistance of S. pseudintermedius is mediated bymecA gene. The mecA gene is located on a mobile element called the 'staphylococcal chromosomal cassette' (SCCmec) on the chromosome of the bacterium (Weese and Van Duijkeren, 2010). Present study showed that all oxacillin resistant strains possessed mecA and SCCmec type II-III in 2 isolates (18.18%), SCCmec type I in 2 isolates (18.18%) and SCCmec type III in 3 isolates (27.27%). A study by Bemis et al. (2006) reported 30 out of 31 staphylococci were resistant to oxacillin possessed mecA gene. Some studies have also shown that SCCmec II-III and SCCmec V are most prevalent in MRSP in China (Feng et al., 2012; Wang et al., 2012), Korea (Moon et al., 2012)and Japan (Onuma et al., 2012), whileSCCmec type V has been reported in USA (Moodley et al., 2009). Our results are in agreement with other authors who identified SCCmec type III (Moodley et al., 2009; Ruscher et al., 2009; Ruscher et al., 2010) as most prevalent.

Conclusion: It is concluded from present study thatmethicillin resistant S.pseudintermediusis potentially pathogenic in dogs. The study on pathogenicity and characterization of S.pseudintermedius in mouse model can be particularly important due to its ability of inducing brain damage by crossing the blood-brain barrier (BBB) and subsequent long term colonization.

Acknowledgements: This work was supported by the International SandT Cooperation Program of China (2014DFG32770) and Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).


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Date:Apr 30, 2017

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