Indian Journal of Animal Research

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Research Article

​Multidrug-resistance Pattern of Antibiogram of Escherichia coli and Staphylococcus aureus Isolated from Mastitis Affected Buffaloes in Eastern Uttar Pradesh

 

S.V. Singh1, J.P. Singh1, Vibha Yadav2, Sandeep Kumar Yadav1, Ramakant1,*, P.K. Maurya3, R.K. Joshi2
1Department of Veterinary Medicine, College of Veterinary Science and Animal Husbandry, Acharya Narendra Deva University of Agriculture and Technology Kumarganj, Ayodhya-224 229, Uttar Pradesh, India.
2Department of Veterinary Microbiology, College of Veterinary Science and Animal Husbandry, Acharya Narendra Deva University of Agriculture and Technology Kumarganj, Ayodhya -224 229, Uttar Pradesh, India.
3Department of Veterinary Physiology and Biochemistry, College of Veterinary Science and Animal Husbandry, Acharya Narendra Deva University of Agriculture and Technology, Kumarganj, Ayodhya -224 229, Uttar Pradesh, India.

  • Submitted24-02-2021|

  • Accepted18-05-2021|

  • First Online 19-07-2021|

  • doi 10.18805/B-4435

ABSTRACT

Background: Mastitis is a problem of dairy animals including buffaloes. Treatment failure has become a common problem and the most cited reason is antibiotic resistance. The paper presents the scenario of antibiotic resistance with special reference to multi drug resistance pattern. 

Methods: Microbiological assay of mastitis affected 48 milk samples was carried out using standard protocols to establish the prevalence of mastitis caused by E. coli and S. aureus. Antibiotic sensitivity test was carried out against these organisms and the whole milk culture for commonly used antibiotics. The drug resistance pattern was established.

Result: The overall prevalence of mastitis was 20%. The prevalence of E. coli and S. aureus was 29.17% and 54.17% respectively. The antibiotic sensitivity revealed that E.coli isolates were 100% susceptible to tetracycline, gentamicin, enrofloxacin and streptopenicillin followed by Ceftriaxone and sulbactum combination and streptomycin (92.86%) and ceftriaxone and methicillin (85.71%). The isolates of S. aureus were 100% sensitive to only two antibiotics gentamicin and streptopenicillin. The antibiogram of whole milk culture revealed maximum susceptibility to enrofloxacin, gentamicin and streptopeniciliin (95.83% each). Multiple drug resistance has been observed in this study.

INTRODUCTION

Mastitis is an inflammatory disease of udder, which is an outcome of interaction of various associated factors viz. the host, pathogen(s), environment and poor managemental conditions. Large numbers of micro-organisms are known to cause inflammation of udder parenchyma and because of this diverse array of etiological factors like bacteria, virus, fungus, physical, chemical, toxins and other environmental factors etc., the treatment of the disease is always a challenge to the veterinarian. This has prompted scientists from all over the world to identify different aspects related to the health of the mammary gland and milk products of buffaloes as in Brazil (Medeiros et al., 2011), India (Yadav et al., 2020), Pakistan (Hussain et al., 2013), Nepal (Dhakal et al., 2007), Italy (Fagiolo and Lai 2007) and Germany (Braun and Preuss, 2007). This is because of the menace of the antibiotic resistance as reported by several workers (Chavan et al., 2007; Roychoudhury and Dutta, 2009; Sharma et al., 2010; Tanzin et al., 2016, Yadav et al., 2020). Selection of appropriate antibiotic against the common mastitis causing pathogens namely S. aureus and E. coli is crucial for proper treatment of mastitis in cattle and buffaloes. Time to time evaluation of area specific antibiogram can be a step promoting judicious use of antibiotics and can improve treatment percentage as well as must for welfare of animal. Therefore, the objective of this study was to isolate and study the prevalence of common mastitogens from buffalo in Eastern Plain Zone of Eastern Uttar Pradesh and to evaluate the antibiotic sensitivity pattern against different isolates from milk.

MATERIALS AND METHODS

A total of 240 milk samples were collected from the buffaloes of the Sultanpur and Faizabad district. Two blocks from each district were selected and from each block three villages were chosen. From each village 20 samples were collected. In this way a total of 240 milk samples were collected from the buffaloes.
 
Clinical inspection of the udder
 
Udders of the buffaloes were examined by visual inspection and palpation for the presence of any lesion, pain, heat and swelling. In addition, milk from each quarter was withdrawn and checked for any change in colour and consistency.
 
Collection of milk sample 
 
Milk samples were collected following all aseptic norms. The affected quarter was washed with tap water, dried properly and teat and udder was sterilized with cotton soaked with 70% ethyl alcohol. Approximately 10 ml of milk was then collected aseptically from a mastitic quarter into sterile bottle after discarding the first 3 to 4 milking streams. Sample from each quarter were transported on ice to the bacteriology laboratory of department of veterinary microbiology and were immediately cultured or stored at 4°C for a maximum of 24 hrs until cultured on standard bacteriological media.
 
Microbiological assay of milk sample
 
Sample processing was carried out in the laboratory of bacteriology in the department of veterinary microbiology. The method used for isolation of bacteria was described by Cruickshank et al., (1975) and isolates were identified on the basis of method described by Edwards and Ewing (1972).The collected sample were inoculated into sterile nutrient broth and incubated at 37°C for 24 hrs to see the growth of bacteria. The grown bacteria was streaked onto sterile Mac Conkey lactose agar plate and incubated at 37°C for 24 hrs. Single colony of bacteria was picked and a gram staining was performed. In the same way, one loopful of broth culture was streak upon mannitol salt agar (MSA) plates and plates were incubated at 37°C for 24 hrs. The single colony from MSA plates transferred to nutrient agar slant and incubated aerobically at 37°C for 24 hrs. Bacterial identification was carried out by studying morphology, culture characteristics and Gram’s staining (Quinn et al., 2004). Lastly antibiotic sensitivity test (ABST) of all isolates was performed.
 
Isolation of staphylococcus aureus
 
Primary culture was done in nutrient broth for enrichment of bacteria. Pure culture of S. aureus was obtained based on Gram staining, morphological study, biochemical characteristics, catalase test, coagulase test, as per the procedures mentioned by Cheesbrough (1985) and Jahan et al., (2015).
 
Isolation of E. coli
 
MC agar media were streaked aseptically with 200 μL of milk sample and incubated at 37°C for overnight. Appearance of bright red or pink color colony was used to culture in EMB agar. Appearance of the colony of pink/red and greenish black with metallic sheen was considered positive for E. coli in EMB agar. The positive colonies were sub cultured into EMB agar to obtain pure colony. The pure colonies were subjected for sugar fermentation, biochemical tests, as per the procedure described by Cheesbrough (1985) and Nazir et al., (2005).
 
Antimicrobial susceptibility procedure
 
The disc diffusion sensitivity test also known as Kirby Bauer disk method is a simple and practical test which uses antibiotic-impregnated discs to test whether particular bacteria is susceptible to specific antibiotic. The bacterial inoculums were uniformly spread using sterile cotton swab on a sterile Petri dish. The antibiotic discs were placed on top of the previously inoculated nutrient agar medium surface with the help of sterile forceps. Each disc was pressed down to ensure complete contact with the agar surface. The plates were incubated for 18-24 hrs at 37°C temperature in bacteriological incubator before interpretation of the result. A zone of inhibition was measured in millimeters by either measuring: (a) Radius: Measure half the distance of the zone and then multiply by two. This method was used when part of the zone is not clear or has grown into another zone. (b) Diameter: Measure the entire length of the zone and subtract the disc diameter (Standard disc size 5 mm). The result of the test can be interpreted by using the criteria published by Clinical and Laboratory Standard Institute. If the organisms were inhibited by the concentration of the antibiotic, there will be no growth in the immediate area around the disks represented as zone of growth inhibition. The diameter of the zone of inhibition is considered directly proportional to the sensitivity of the isolate and to the diffusion rate of antibiotics through the agar medium. The antibiotics used in this study are given in (Table 1).

Table 1: Codes and concentration of selected antibiotic discs.


 
Ethical approval
 
The research work was duly permitted by the Institutional Animal Ethics Committee (IAEC) viz. Approval No: IAEC/CVSc/2/P-28/2020/22, dated- 23.01.2020. All samples were collected as per standard procedure without harming or giving stress to the animals.

RESULTS AND DISCUSSION


The present investigation was planned to study the prevalence of mastitis pathogens namely E. coli and S. aureus and the antibiogram pattern against E. coli, S. aureus and whole milk culture with special reference to drug resistance pattern scenario in buffaloes of middle gangetic plains of eastern Uttar Pradesh. Out of the total 240 buffalo milk samples screened 48 samples were tested positive for mastitis. These 48 samples from mastitis affected buffaloes were collected and screened microbiologically for the presence of and S. aureus (Fig 1,3 and 5) and E. coli (Fig 2, 4 and 6). The overall prevalence of mastitis was 20%. The prevalence of E. coli and S. aureus was 29.17% (14/48) and 54.17% (26/48) respectively.

Fig 1: S. aureus colony on mannitol salt agar.



Fig 2: E. coli colony on EMB agar.



Fig 3: Gram stain of S. aureus in characteristic arrangement of “bunch of grapes”.



Fig 4: Gram stain of E.coli characterised by rod.



Fig 5: Catalase positive test of S. aureus.



Fig 6: Catalase positive E coli.


       
The frequency of E. coli observed in present study is in close agreement with the data obtained by El-Razik et al., (2010) , Khan and Muhammad (2005), Farooq et al., (2008), Hameed et al., (2008), Ali et al., (2011), Bhanot et al., (2012), El-Sayed Lamey et al., (2013) who observed 23.75%, 18%, 16%, 15.38%, 16.18%, 16.3%, 18.47% frequency of E. coli, respectively in buffalo milk samples but less than 52.333% prevalence reported by Singh et al.,(2018) .
       
The prevalence of S. aureus observed in the present study is in close association with the reports of Patnaik et al., (2014) who reported 53.33% prevalence due to S. aureus.  Saidi et al., (2013) and Srinivasan et al., (2013) subjected the milk samples positive for California Mastitis Test to bacteriological culture and revealed that S. aureus was the most prevalent organism 40.0% and  46.30% respectively. Antibiotic sensitivity of different antibiotics namely Amoxicillin, Ceftriaxone, Ceftriaxone  + Sulbactum, Enrofloxacin, Gentamicin,  Strepto-penicillin, Methicillin, Tetracycline, Streptomycin, Vancomycin, Penicillin, Oxacillin were studied against S. aureus, E. coli and milk culture (Table 2.). These 15 antibiotics belonged to the seven groups viz. fluoroquinolones, aminoglycosides, tetracycline, cephalosporins, penicillin and beta lactum. The resistance pattern especially the multi drug resistance pattern was established (Table 3).

Table 2: Antibiotic sensitivity pattern of common antibiotics against S. aureus, E. coli and Whole milk culture of buffalo milk.



Table 3: Multi drug resistant pattern against S. aureus, E.coli and Whole milk culture of buffalo milk.


       
The antibiotic sensitivity revealed that E.coli isolates were 100% susceptible to Tetracycline, Gentamicin, Enrofloxacin and Streptopenicillin followed by Ceftriaxone and sulbactum combination and streptomycin (92.86%)  and Ceftriaxone and Methicillin (85.71%) (Fig 7). The isolates were least susceptible to Amoxicillin and vancomycin (71.43%) and oxacillin (78.57%). The isolates of S. aureus were 100% sensitive to only two antibiotics Gentamicin and Streptopenicillin (Fig 8). The antibiotics in order of sensitivity are Enrofloxacin (96.15%)> vancomycin (92.31%) > penicillin (88.46%)> streptomycin (84.62%) >tetracycline (80.77%) > Ceftriaxone and sulbactum combination and amoxicillin (76.92% each) > oxacillin  (73.07%) > Ceftriaxone and Methicillin (69.23% each). Methicillin resistance was reported in 30.77% S. aureus isolates.  The antibiogram of whole milk culture (Fig 9) revealed maximum susceptibility to Enrofloxacin, gentamicin and streptopeniciliin (95.83% each) followed in decreasing order by tetracycline, combination of Ceftriaxone and sulbactum (93.75%), penicillin (91.66%), amoxicillin (87.5%) and streptomycin (83.33%), vancomycin and Methicillin (81.25% each), oxacillin (77.08% ) and Ceftriaxone (68.75%).

Fig 7: Antibiogram against E. coli isolated from buffalo milk.



Fig 8: Antibiogram against S. aureus isolated from buffalo milk.



Fig 9: Antibiogram against whole milk culture.


       
Other workers too have reported resistance to wide range of common antibiotics in E. coli from animals in India and abroad as in this study (Preethirani et al., 2015, Ranjan et al., 2011, Kisku and Samad, 2013, Verma et al., 2018,  Kalmus et al., 2011 and Jeykumar et al., 2013). Ranjan et al., (2010) has also reported higher resistance of mastitis pathogens to amoxicillin. In S. aureus resistance to Ceftriaxone is in concordance with most of the recent reports of drug resistance pattern in investigations conducted on mastitis pathogens (Upadhyay and Kataria, 2009 and Nathawat et al., 2013). This high emergence of resistance to cephalosporin’s is due to its broad spectrum of action and frequent use by most of the clinicians and all the quacks practicing in the field as the first line of treatment in recent years. Thus, the probable long-term indiscriminate use of these antibiotics in the region has led to the appearance of resistance in mastitogenic bacteria against third generation cephalosporin (Ankita, 2015). Yadav et al., (2020) have reported the Methicillin resistance in 19.28% from this region. Studies from North west India and Chennai reported relatively lesser methicillin resistant Staphylococcus aureus positive percentages as 13% and 10.44% respectively (Kumar, et al., 2010 and Chandrasekaran, 2014). Dar et al., (2014) from Jammu and Kashmir reported that enrofloxacin, gentamicin, tetracycline and amoxicillin clavulanic acid were effective in descending order of susceptibility against the whole milk cultures positive for SCM.
       
Multiple drug resistance has been observed in this study (Table 3, Fig 7,8,9).  Among the 14 E. coli isolates, 05 isolates (35.71%) showed resistance against 2 antibiotics and 02 isolates (14.29%) were found resistant to three antibiotics (Amoxicillin + Methicillin and Oxacillin). Resistance against Amoxicillin and ceftriaxone was observed in 03 isolates (21.43%) and resistance against Methicillin and vancomycin was observed in 02 isolates (14.29%). Out of 26 isolates of S. aureus, 8 isolates (30.77 %) were found to be resistant against 02 or more than 02 antibiotics. Maximum S. aureus isolates (15.38%) were resistant to 02 antibiotics namely amoxillin +methicillin. In whole milk culture 35.42 % cultures exhibited resistance to 02 or more antibiotics.  Maximum isolates (06; 12.5%) were resistant to Streptomycin + Methicillin. Resistance against 05 antibiotics (Ceftriaxone + Ceftriaxone and sulbactum+Tetracycline+ Methicillin+ Oxacillin) were observed in 03 (6.25%) isolates.
       
There are large numbers of reports from different parts of the world that describe increased trend of developing multiple resistance strains (Shana et al., 2009; Rinsky et al., 2013, Chavan et al., 2007, Sharma et al., 2007 Roychodhary and Dutta 2009). In this region too Ankita (2015) and Yadav et al., (2020) observed multidrug resistance in S. aureus isolates. The multiple drug resistance in Staphylococcal was also reported by other workers (Ombui et al., 2000; Gentilini et al., 2002; Rajala- Schultz et al., 2004; Adwan et al., 2006; Wang et al., 2013; Kumar et al., 2010). A high level of antimicrobial resistance to many antibiotics and an elevated number of multiresistant strains among mastitis-associated E. coli strains have been reported in an earlier studies too (Allen et al., 2011, Rangel and Marin 2009). Development of resistance has been attributed to the extensive therapeutic use of antimicrobials (Abo-Shama, 2014). Multidrug resistance in E. coli from milk sample was also reported by Zdolec et al., (2016).  Mahantesh  and Basappa (2011) and  Jeykumar et al., 2013 were of the view that resistance to multiple antibiotics can be attributed to the injudicious use of antibiotics or selection pressure of antimicrobials on pathogens or colonization of the mammary gland by resistant strains along with the negligence towards bacteriological examination of the mastitis suspected milk.
       
Susceptibility to gentamicin of the cultures under study was in close agreement with many workers (Sarangi et al., 2009; Ranjan et al., 2010; Moges et al., 2011) . Farooq et al., (2008) during their study period have found that norfloxacin, gentamicin and chloramphenicol were the most effective drugs whereas Sumathi et al., (2008) reported gentamicin to be most effective among the antimicrobials used in study. The susceptibility to qunilones can be attributed to their lesser use in treatment of mastitis due to its higher dose and twice a day application resulting in higher efficacy of these drugs and corroborates with the quick response to the treatment with Gentamicin.

CONCLUSION

Drug resistance has been established in buffaloes in this region. The overall prevalence of mastitis was 20%. The prevalence of E. coli and S. aureus was 29.17% and 54.17% respectively. The antibiotic sensitivity revealed that E. coli isolates were 100% susceptible to Tetracycline, Gentamicin, Enrofloxacin and Streptopenicillin. The isolates of S. aureus were 100% sensitive to only two antibiotics Gentamicin and Streptopenicillin. The antibiogram of whole milk culture revealed maximum susceptibility to Enrofloxacin, Gentamicin and Streptopeniciliin (95.83% each). Multiple drug resistance has been observed in this study.  The antibiotics should be used judiciously to curb this menace of antibiotic resistance.

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