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Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study



Ruchi Tiwari, Sharad Kumar Yadav and Shanker Singh
 
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ABSTRACT

Background: Staphylococcus aureus is the most common bacterial pathogen responsible for acute as well as many chronic infections in humans and animals as well. The emergence of antibiotic resistance among these pathogens is an issue of global worry. Among them, methicillin-resistant Staphylococcus aureus (MRSA) is staphylococci showing multiple drug resistance to a large number of antimicrobials including penicillin, methicillin, β-lactam antibiotics, aminoglycoside antibiotics, macrolide antibiotics, etc. Objective: The aim of present study was to determine the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) isolated from clinical cases of wounds in animals of different species of various age groups in Mathura and nearby areas of Uttar Pradesh, India. Materials and Methods: A total of 194 wound samples from cattle, buffalo, dogs, goats, sheep and horses were collected aseptically between 2012-2014. Samples were subjected to microbiological investigation for laboratory isolation, identification and confirmation of causative agents as per the standard protocols. All S. aureus isolate were identified and confirmed on the basis of morphology, cultural characteristics and biochemical tests. Result: Out of 194 samples, 9 were negative while 185 wound samples revealed 69 isolates of Staphylococcus aureus with the prevalence rate of 37.3%. The results also revealed that the incidences of Staphylococcus aureus in wound cases were higher in equines (57.14%), cattle (48.28%) and dogs (48.08%) in comparison to buffaloes (24.32%). All the isolates were subjected to drug sensitivity by disc diffusion method to assess the antibiotic resistance against 23 antimicrobials. Results of the current study revealed maximum sensitivity to gatifloxacin (94.20%) and 100% resistance against kanamycin, colistin, clindamycin, penicillin-G, cotrimoxazole and cefotaxime. Conclusion: Out of 69, 66 isolates were found to be methicillin-resistant, while 63 were vancomycin resistant and is a noble finding in case of animals in UP. The higher prevalence of methicillin resistant bacterial strains of Staphylococcus aureus bacteria from wound infections was an important finding of the study and clearly indicated increase in drug resistance with alert to look for alternate therapeutic treatment.

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Ruchi Tiwari, Sharad Kumar Yadav and Shanker Singh, 2016. Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study. International Journal of Pharmacology, 12: 821-829.

DOI: 10.3923/ijp.2016.821.829

URL: https://scialert.net/abstract/?doi=ijp.2016.821.829

INTRODUCTION

Indiscriminate uses of antibiotics and drugs prescription without proper susceptibility tests for quick medication are some key factors for emergence of resistant organisms against antimicrobial drugs especially in developing nations1,2. The emergence of antibiotic resistance among pathogens is a rising issue of global worry3,4. Among various pathogens, methicillin-resistant Staphylococcus aureus (MRSA) is staphylococci showing multiple drug resistance to a large number of antimicrobials including penicillin, methicillin, β-lactam antibiotics, aminoglycoside antibiotics, macrolide antibiotics, etc. Over past several years different studies conducted all around the world have alarmed the presence of MRSA strains of bacteria from hospital, clinics, community, farm and environmental settings5-8.

The presence of MRSA is reported from human as well as from different species of animals including cattle, horses, sheep, cats, dogs and chickens in different regions of world9. The MRSA can be transferred among closely kept animals and from animals to human which reflects that farm workers, veterinarians, persons working at abattoirs are more prone and at highest risk. Due to transfer of MRSA bacteria among domestic pets, farm animals, livestock, human and feral/wild animals probability of emergence of new strains of MRSA also expanded due to genetic recombination10,11.

The present study was planned to determine the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) isolated from clinical cases of wounds in animals of different species of various age groups in Mathura and nearby areas of Uttar Pradesh, India. For this, a total of 194 wound samples from cattle, buffalo, dogs, goats, sheep and horses were collected aseptically by Levine’s technique in period of 2 years between 2012-2014. Collected clinical samples were subjected to microbiological investigation for laboratory isolation, identification and confirmation of causative agents as per the standard protocols. All the isolates were subjected to drug sensitivity by disc diffusion method to assess the pattern of antibiotic resistance against 23 antimicrobials.

In the absence of appropriate surveillance of antimicrobial resistance, growing increase in MRSA bacteria appended worries in the incidence of infections among variety of wounds and demands constant bacteriological monitoring of the pathogen even from minor injuries to know their current antibiotic susceptibility pattern12-15. Therefore, this study was intended to determine the prevalence of MRSA from infected wounds to support the empirical therapy with precise medication as per the specific cause.

MATERIALS AND METHODS

Study design and wound sample collection: A total of 194 samples of wound were collected from various animal species including cattle, buffalo, goats, sheep, horses and dogs to screen for bacterial causes from clinical cases and field in and around the Mathura city (Table 1). Swab samples from wounds of various types viz., horn abscess, gangrenous wound, chronic abscess, deep suppurative wounds, open, gun-shot, lacerated, abrasive, incised, ulcerated and post-operative wounds (Fig. 1, 2) were collected by Lavine’s aseptic technique after cleaning the periphery of wound with 70% ethanol swabs. Samples from deep wounds were collected using sterile cotton-tipped swabs (PW003, HiMedia) by taking all aseptic precautions to check the contamination while sample collection. The swab samples were directly submitted to the Department of Veterinary Microbiology, College of Veterinary Sciences, DUVASU University, Mathura (U.P.), India for further laboratory processing by standard procedures.

Wound sample processing for isolation and identification of bacterial agents: During the study period, a total of 194 infected wound samples were selected and swab samples were processed for isolation and identification of different aerobic and anaerobic bacterial agents based on the initial screening and characteristics according to the standard operating procedures of the laboratory.

Table 1:Species-wise distribution of wound samples and isolates percentage of Staphylococcus aureus
Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 1:Open deep wound in buffalo

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 2:Lacerated wound in horse

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 3:Staphylococcus aureus over NA

Upon receipt as per the history of sample each swab was inoculated into Nutrient Broth (NB) or Robertson Cooked Meat (RCM) media and accordingly incubated at 37oC upto 24-48 h under aerobic or anaerobic conditions, respectively before attempting pure colony isolation over solid nutrient medium. Upon isolation, identification was followed as per cultural, morphological and biochemical tests (Fig. 3-5).

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 4:Haemolysis on blood agar

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 5:Staphylococcus spp., over MSA

The generic identification of bacterial isolates was carried out as per the techniques of Cowan and Steel16 and further speciation was performed as described by Quinn et al.17.

Susceptibility of bacterial isolates to antimicrobial agents: Bacterial isolates were subjected to antibiotic sensitivity testing against 23 different antimicrobial discs by disc diffusion method according to CLSI18 to assess the pattern of antibiotic activity (Fig. 6). All the bacteria were subjected to antibiotic sensitivity testing (ABST) against different classes of antimicrobials: Penicillin class (ampicillin (AMP), amoxycillin, ampicillin/sulbactum (A/S), penicillin-G (P-G), methicillin (MET)), fluorquinolones class (ciprofloxacin (CIP), norfloxacin (Nx)), cephalosporin class (cefotaxim (CTX), ceftriaxone (CTR)), aminoglycosides class (streptomycin (S), gentamycin (Gen)), tetracycline class (T), folate pathway Inhibitors (cotrimoxazole (Co-T)), phenicols class (chloramphenicol (C)), glycopeptides class (vancomycin (Va)), macrolides class (erythromycin (E)) and lincosamides class (clindamycin (CD), amikacin (AK), kanamycin (K), enrofloxacin (En), gatifloxacine (GAT) sparfloxacine (SPK) and colistin (CL)) by disc diffusion technique of Kirby-Bauer and results were interpreted as per the standard charts provided from the drug supplier (HiMedia, India)19.

Table 2:Result of antibiotic sensitivity testing of various isolates and percentage sensitivity of isolates recovered from wounds of animals
Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
AMP: Ampicillin, AMC: Amoxycillin, A/S: Ampicillin/sulbactum, AK: Amikacin, E: Erythromycin, CTX: Cefotaxime, GEN: Gentamicin, CIP: Ciprofloxacin, K: Kanamycin, MET: Methicillin, T: Tetracycline, Nx: Norfloxacin, P-G: Penicillin-G, C: Chloramphenicol, S: Streptomycin, En: Enrofloxaacin, Va: Vancomycin, CTR: Ceftriaxone, Co-T: Cotrimoxazole, GAT: Gatifloxacin, SPX: Sparfloxacin, CD: Clindamycin, CL: Colistin, R: Resistance, S: Sensitive

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 6:Disc diffusion method (ABST)

RESULTS

In present study out of 194, a total of 185 samples revealed presence of different species of bacteria with 69 isolates of Staphylococcus aureus. Out of 194, 9 (4.64%) samples of wounds were negative and 185 ((95.36%) were positive. Microbiological investigation based upon cultural, morphological and biochemical studies revealed isolation of strains of S. aureus, Pseudomonas aeruginosa, E. coli, Klebsiella spp., Protius, Bacillus, Clostridium, Streptococcus, Micrococcus with maximum prevalence of S. aureus strains comprising 37.3% of total. The majority of wounds contained a mixture of aerobes and anaerobic bacteria reflecting the diverse micro-biota present in the atmosphere in vicinity of the affected animals. Among animals, recovery of S. aureus was maximum from wound samples of canines (36.23%) followed by buffalo (26.09%) and cattle (20.29%). Though within a particular animal species wound samples from equines revealed maximum occurrence of S. aureus (57.14%), followed by cattle (48.28%), canines (48.08%), buffaloes (24.32%), goats (37.5%) and sheep (16.67%). The results of frequency distribution of S. aureus from different species were presented in (Table 1).

The result of in vitro antibiotic sensitivity testing of all isolates against 23 different antibiotics such as ampicillin, amoxycillin, ampicillin/sulbactum, amikacin, erythromycin, gentamicin, kanamycin, methicillin, norfloxacin, penicillin-G, ciprofloxacin, chloramphenicol, streptomycin, tetracycline, enrofloxacin, vancomycin, ceftriaxone, cefotaxime, cotrimoxazole, gatifloxacine, sparfloxacine, clindamycin and colistin was recorded and compared with the standard charts (Fig. 7). Antibiotic sensitivity pattern of the S. aureus, isolated from different cases of skin/wound infections, revealed resistant strains even against multiple drugs. Most of strains were sensitive to gatifloxacin (94.20%). Other drugs were comparatively less effective as depicted from percentage of drug sensitivity in Table 2. About 94.20% strains were sensitive to gatifloxacin followed by chloramphenicol (37.31%), amikacin (32.84%), streptomycin (22.39%), gentamicin (19.4%), tetracycline (17.91%), sparfloxacin (16.42%), norfloxacin (14.9%), erythromycin (11.94%), ceftriaxone (10.45%), ampicillin/sulbactum (8.96%), vancomycin (8.96%), enrofloxacin (5.97%), methicillin (4.47%), amoxycillin (2.98%), ampicillin (1.49%) and ciprofloxacin (1.49%) as evident from Table 2. The isolated bacteria were cent-percent resistant to penicillin-G, cefotaxime, kanamycin, colistin sulphate, clindamycin and cotrimoxazole (Fig. 8). The drug resistance profile of tested S. aureus isolates showed that 100% of S. aureus strains were resistant to penicillin, 98.51% to ampicillin, 97.02% to amoxicillin, 95.53% to methicillin and 91.04% to vancomycin. No drug showed 100% efficacy against S. aureus isolates. These methicillin resistant isolates showed resistance to other drugs also which reflects their multi-drug resistance pattern. This study indicated that many isolates were resistant to three or more classes of antimicrobials.

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 7:Antibiogram of Staphylococcus aureus

Image for - Methicillin Resistant Staphylococcus aureus Isolated from Wounds of Livestock and Companion Animals of Uttar Pradesh India: A Preliminary Study
Fig. 8:Percentage sensitivity of Staphylococcus aureus against various antimicrobial drugs

DISCUSSION

In the study performed over animals to screen the bacterial pathogens of wounds, among significant isolates Staphylococcus aureus was the most common isolate (37.3%). This finding is in accordance with the findings of Qureshi et al.20 who reported Staphylococcus aureus as maximum isolated bacteria from wounds in camel with the recovery of 40% hemolytic S. aureus. These results are also in agreement with other studies depicting 41% Staphylococcus aureus isolated from wound infections21, 60.60% recovery22 of S. aureus from wound cases and 66.7% from another study23, however percentage of recovery is higher which could be due to change in the study population as higher percentage is reported from hospital cases. Staphylococcus aureus is amongst important and major resistant bacterial pathogens to the general population. Bacterial skin infections common in animal veterinary practice are most frequently occurred by Staphylococcus aureus as evident from the results. These results are supported by earlier findings of researchers21, who reported Staphylococcus as most common pathogen (23%) isolated from wounds in dogs. The anti-microbial resistance profile of these isolates indicated that methicillin-resistant Staphylococcus aureus (MRSA) is now a days frequently involved in animal wound infections and such bacteria are resistant to more than one class of drug which explain the reason behind the chronicity of infection and difficulty in treatment of infections due to multi-drug resistant bacterial strains. These results are in conformity with the reports of Van Duijkeren et al.24 who documented that out of 300 staphylococci isolated from animals 100 strains of S. aureus were multi-drug resistant. Work done in developed countries highlighted the emergence and spread of resistance in Staphylococcus aureus against penicillin, methicillin, tetracycline and erythromycin groups of drugs with pace7,25. This statement is in agreement to the findings of present study where isolated S. aureus showed 100% resistant to penicillin, 95.53% to methicillin, 82.09% to tetracycline and 88.06% to erythromycin. But results are in contrast with the study23 showing only 45.76% isolates to be MRSA out of 236 isolates of S. aureus. The emergence of glycopeptide intermediate Staphylococcus aureus (GISA) or vancomycin-intermediate Staphylococcus aureus (VISA) and resistance against aminoglycoside antibiotics have made the situation more critical26. The S. intermedius, which is a normal resident in the nasal cavity, oropharynx and the perianal region of animals, can be a transient resident in other sites especially in case of traumatic injury and the organism can be transferred to these sites from the oral and anal mucosa during grooming practices. Antibiogram study revealed that among the isolated Staphylococcus aureus maximum 94.2% isolates were highly sensitive to gatifloxacin while cent-percent resistance was observed against cefotaxime. Results are confirmed by other studies22 also reporting 81% resistance of S. aureus isolates obtained from wound cases to cefotaxime as resistance is towards higher side. Difference in the percentage could be due to geographical variation and frequency of drug usage. Among resistant strains 100% of S. aureus strains were resistant to penicillin, 98.51% to ampicillin, 97.02% to amoxicillin, 95.53% to methicillin and 91.04% to vancomycin. Results were supported by findings of other studies which evidenced that S. aureus isolates recovered from wounds showed resistance of 100 and 96% to ampicillin, respectively22,27. Similar findings were earlier documented by Bozdogan et al.28, Trakulsomboon et al.29 and Falagas and Karveli30 in their research who had reported the isolation of multi drug resistant bacterial strains from wounds. The result of study conducted by Godebo et al.31 showed that 94.5% of S. aureus was resistant to penicillin, 91.8% to ampicillin and 76.7% to oxacillin. The pattern of their result supports the finding of present study and slightly lower percentage could be due to difference in the population under study. The extensive antimicrobial susceptibility to gatifloxacin in the current study may be due to their infrequent use in veterinary practice. In current study 91.04% isolates were resistant to vancomycin and this is in contrast with the study performed earlier at Iran32 and Nepal33 which reported resistance percentage of 40 and 21% against vancomycin. It shows that with the continuous use of vancomycin with the time span more resistant strains are evolving globally.

This study also revealed that among animals, recovery of S. aureus was maximum from wound samples of canines (36.23%) followed by buffalo (26.09%) and cattle (20.29%). Though within a particular animal species wound samples from equines revealed maximum occurrence of S. aureus (57.14%), followed by cattle (48.28%), canines (48.08%), buffaloes (24.32%), goats (37.5%) and sheep (16.67%). These results are supported by another study34 where recovery of MRSA from canines was 56%.

Several researchers have stated numerous reports/cases of oxacillin/methicillin resistant S. aureus from cows in different countries including India, Brazil, Italy, Pakistan, Nigeria, Turkey and the USA35. These findings are in almost confirmity with result of another study in Ethiopia36 where S. aureus showed 100% resistant to oxacillin/methicillin (MRSA). However, in present study resistance percentage against methicillin is higher as compared to other reports obtained from Iraq (88%)22, Ethopia (83%)37, Nepal (60.6%)33 and 57.7% from Tamilnadu, India23. Documents detailed the recovery of MRSA from equines also from USA, UK, Canada, Austria, Japan and Ireland38. O'Mahony et al.34 also supported the finding of present study in which MRSA was isolated from 25 animals with recovery of 56% from canines and 32% from equines and MRSA isolates were resistant to macrolides, lincosamines, tetracyclines and/or fluoroquinolones groups of antimicrobials and are in conformity with our findings.

Comparatively higher recovery of MRSA from dogs could be due to close contact of human with pet animals. Earlier documents also suggested that colonisation of hospital strain of MRSA is increasingly recorded from pets, including cats and dogs, which is an indicative of close contact of human and dogs39. In this way pets are acting as reservoir of resistant MRSA strains for re-infecting in-contact human population. This is supported by literature40 which mentioned the homology of MRSA isolated from animals with human MRSA through PFGE. The MRSA of animal origin is capable of producing the human infections. Through Random Amplification Polymorphic DNA (RAPD) technique it was confirmed that41 RAPD pattern of bovine MRSA was alike the human MRSA pattern and human/consumers may get the infection of livestock associated MRSA bacteria by contact with infected cattle and consumption of contaminated animal food products35,42. Molecular approaches showed that all the methicillin resistant S. aureus may not always be "True MRSA" because sometimes horizontal gene transfer helps in genetic exchange of resistant gene among bacteria if they are shared in between different sources. It is documented that farm-animal MRSA and community-acquired MRSA are genetically more identical as compared to hospital-acquired MRSA38,43.

Not only with direct contact but literature evidenced that MRSA is seeded in manure of MRSA-positive farms and can be a source of environmental spread of this resistant pathogen and helps in ecological emergence of new multi drug resistant strains 44,45. As vancomycin-resistant MRSA has been emerged due to transfer of vancomycin resistant gene to MRSA. Earlier in European countries some feed additives for farm animals were extensively used which had similarity with vancomycin and drug vancomycin was used for treatment of MRSA. Hence, because of survival pressure MRSA bacteria received vancomycin resistant gene and vancomycin-resistant MRSA emerged32,46. Use of certain antibiotics to which MRSA is already resistant, helps in emergence of new multi-drug resistant strains and their eradication would be very difficult.

CONCLUSION

In veterinary practice, wound infections are the most frequent complications which are many times treated without proper anti-microbial tests. The results of the current study projected the growing prevalence of MRSA, VRSA and multi-drug resistant pathogenic strains to support the monitoring and veterinary assistance for specific therapy implementation. This study also recommended that regular testing and survey for detection of resistant S. aureus should be critically followed to have a data base regarding drug resistance profile of emerging new strains of bacterial pathogens. It is imperative that government and animal owners both should follow a series of effective measures for preventing spread of MRSA to livestock with specific use of antibiotics after thorough testing.

SIGNIFICANT STATEMENTS

In the present study out of 194, a total of 185 samples revealed presence of different species of bacteria with 69 isolates of Staphylococcus aureus. Out of 69, 66 isolates were found to be methicillin-resistant which is a noble finding in case of animals in UP. The higher prevalence of methicillin resistant bacterial strains of Staphylococcus aureus bacteria from wound infections was an important finding of the study and as MRSA can be transferred among closely kept animals and from animals to human it reflects that farm workers, veterinarians, persons working at abattoirs are more prone and at highest risk. Study projects the need of new pharmaceuticals to be developed and validated to combat the MRSA infections in animals and humans.

ACKNOWLEDGMENT

The authors cordially thank and acknowledge Dean, College of Veterinary Sciences and Animal Husbandary, DUVASU, Mathura (Uttar Predash) for administrative financial support and institutional research funding.

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