Epidemiology and Antibiotic Succeptibility Profile of Methicillin Sensitive Staphylococcus aureus among Livestock and Pet Animals

Authors

  • Muhammad Aamir Naseer Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad-38000, Pakistan
  • Amjad Islam Aqib Department of Medicine, Cholistan University of Veterinary and Animal Sciences, Bahawalpur, 63100, Pakistan
  • Muhammad Shoaib Institute of Microbiology, University of Agriculture, Faisalabad, 38000, Pakistan
  • Iqra Muzammil Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad-38000, Pakistan
  • Zeeshan Ahmad Bhutta Royal (Dick) School of Veterinary Studies, The University of Edinburgh, United Kingdom
  • Iqra Gulzar Department of Zoology and Fisheries, University of Agriculture, Faisalabad-38000, Pakistan

DOI:

https://doi.org/10.30564/vsr.v2i1.1902

Abstract

Staphylococcus aureus is an important zoonotic pathogen that is responsible for a variety of infectious diseases in humans and animals. The present study was designed to check the prevalence and antimicrobial resistance of MSSA from three different animal origins (bovine, caprine and pet). A total of n= 450 samples (150 each source) were collected from bovine, caprine and pets. Collected samples were subjected to S. aurues identification by microbiological examination and confirmed S. aurues isolates were put to oxacillin disk diffusion test to declare them MSSA. The MSSA confirmed isolates were subjected to various antibiotics for susceptibility profiling using Kirby Baur Disk Diffusion test. The present study found higher prevalence of MSSA from caprine origin (goat 83.33%) as compared to pet (cat 69.33%; dog 65.33%) and bovine origin (buffalo 26.66%; cattle 31.66%). The in-vitro findings of current study revealed oxytetracycline and gentamicin presented 100% efficacy against MSSA of all origins while the vancomycin presented >35%, >40% and > 65% resistance against MSSA isolated from bovine, caprine and pet origin respectively. However, ciprofloxacin was equally effective (50%) against MSSA from buffalo and cattle while >80% efficacy was noted against MSSA from cat and dogs. Linezolid and amoxicillin+ clavulanic acid were 77.78% and 66.67% sensitive to MSSA isolates from caprine milk. The present study found higher prevalence of MSSA from bovine, caprine and pet isolates with diversified pattern of susceptibility of different antibiotics from all sources.

Keywords:

S. aureus; MSSA; Pet; Bovine; Caprine; Antibiotic susceptibility

References

[1] Curl AL, Bibbo J, Johnson RA. Dog Walking, the Human–Animal Bond and Older Adults’ Physical Health. Gerontologist. 2016, 57(5): 930–939. DOI:https://doi.org/10.1093/geront/gnw051

[2] Chumley PR. Historical perspectives of the human-animal bond within the Department of Defense. US Army Med Dep J. 2012: 18–21.

[3] Silcox D, Castillo YA, Reed BJVO-45. The Human Animal Bond: Applications for Rehabilitation Professionals. sgrjarc. (3): 27–2014. DOI:https://doi.org/10.1891/0047-2220.45.3.27

[4] Risley-Curtiss C. Social Work Practitioners and the Human—Companion Animal Bond: A National Study. Soc Work. 2010, 55(1): 38–46. DOI:https://doi.org/10.1093/sw/55.1.38

[5] Iqbal A, Khan BB, Tariq M, Mirza MA. Goat-A potential dairy animal: Present and future prospects. Pakistan J Agric Sci. 2008.

[6] Chu C, Wong MY, Tseng Y, Lin C, Tung C, Kao C, Huang Y. Vascular access infection by Staphylococcus aureus from removed dialysis accesses. Microbiologyopen. 2019: e800.

[7] Aqib AI, Nighat S, Rais A, Sana S, Jamal MA, Kulyar MF-A, Khan NU, Sarwar MS, Hussain MA, Rahman A. Drug susceptibility profile of Staphylococcus aureus isolated from mastitic milk of goats and risk factors associated with goat mastitis in Pakistan. Pak J Zool. 2019, 51(1).

[8] Aqib AI, Ijaz M, Farooqi SH, Ahmed R, Shoaib M, Ali MM, Mehmood K, Zhang H. Emerging discrepancies in conventional and molecular epidemiology of methicillin resistant Staphylococcus aureus isolated from bovine milk. Microb Pathog. 2018, 116: 38–43.

[9] Hu D, Li H, Wang B, Ye Z, Lei W, Jia F, Jin Q, Ren K-F, Ji J. Surface-Adaptive Gold Nanoparticles with Effective Adherence and Enhanced Photothermal Ablation of Methicillin-Resistant Staphylococcus aureus Biofilm. ACS Nano. 2017, 11(9): 9330–9339. DOI:https://doi.org/10.1021/acsnano.7b04731

[10] Ma Y, Zhao Y, Tang J, Tang C, Chen J, Liu J. Antimicrobial susceptibility and presence of resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CyTA-Journal Food. 2018, 16(1): 76–84.

[11] Cuny C, Friedrich A, Kozytska S, Layer F, Nübel U, Ohlsen K, Strommenger B, Walther B, Wieler L, Witte W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int J Med Microbiol. 2010, 300(2–3): 109–117.

[12] Pinchbeck LR, Cole LK, Hillier A, Kowalski JJ, Rajala-Schultz PJ, Bannerman TL, York S. Genotypic relatedness of staphylococcal strains isolated from pustules and carriage sites in dogs with superficial bacterial folliculitis. Am J Vet Res. 2006, 67(8): 1337–1346.

[13] Kluytmans J, Wertheim HFL. Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections. Infection. 2005, 33(1): 3–8.

[14] Van Duijkeren E, Box ATA, Heck M, Wannet WJB, Fluit AC. Methicillin-resistant staphylococci isolated from animals. Vet Microbiol. 2004, 103(1–2): 91–97.

[15] Wang W, Lin X, Jiang T, Peng Z, Xu J, Yi L, Li F, Fanning S, Baloch Z. Prevalence and Characterization of Staphylococcus aureus Cultured From Raw Milk Taken From Dairy Cows With Mastitis in Beijing, China. Front Microbiol. 2018, 9: 1123. DOI:https://doi.org/10.3389/fmicb.2018.01123

[16] Braoudaki M, Hilton AC. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J Clin Microbiol. 2004, 42(1): 73–78. DOI:https://doi.org/10.1128/JCM.42.1.73-78.2004

[17] Ko HHT, Lareu RR, Dix BR, Hughes JD. Statins: antimicrobial resistance breakers or makers? PeerJ. 2017, 5: e3952–e3952. DOI:https://doi.org/10.7717/peerj.3952

[18] Pantosti A, Sanchini A, Monaco M. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiol. 2007, 2(3): 323–334. DOI:https://doi.org/10.2217/17460913.2.3.323

[19] Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol. 2017, 62: 141–146. DOI: https://doi.org/10.1016/j.fm.2016.10.020

[20] Vincze S, Brandenburg AG, Espelage W, Stamm I, Wieler LH, Kopp PA, Lübke-Becker A, Walther B. Risk factors for MRSA infection in companion animals: Results from a case–control study within Germany. Int J Med Microbiol. 2014, 304(7): 787–793. DOI:https://doi.org/10.1016/j.ijmm.2014.07.007

[21] Vidhani S, Mehndiratta P, Mathur M. Study of methicillin resistant S. aureus (MRSA) isolates from high risk patients. Indian J Med Microbiol. 2001, 19(2): 13–16. Available at: http://www.ijmm.org/article.asp?issn=0255-0857;year=2001;volume=19;issue=2;spage=13;epage=16;aulast=Vidhani

[22] Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, Mielke M, Peters G, Skov RL, Struelens MJ. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Eurosurveillance. 2010.

[23] Holden MTG, et al. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A. 2004, 101(26): 9786–9791. DOI:https://doi.org/10.1073/pnas.0402521101

[24] He W, Liu Y, Qi J, Chen H, Zhao C, Zhang F, Li H, Wang H. Food-Animal Related Staphylococcus aureus Multidrug-Resistant ST9 Strains with Toxin Genes. Foodborne Pathog Dis. 2013, 10(9): 782–788. DOI:https://doi.org/10.1089/fpd.2012.1452

[25] Haran KP, Godden SM, Boxrud D, Jawahir S, Bender JB, Sreevatsan S. Prevalence and Characterization of Staphylococcus aureus, Including Methicillin-Resistant S. aureus. J Clin Microbiol. 2012, 50(3): 688 LP – 695. DOI:https://doi.org/10.1128/JCM.05214-11

[26] Loeffler A, Pfeiffer DU, Lloyd DH, Smith H, Soares-Magalhaes R, Lindsay JA. Meticillin-resistant Staphylococcus aureus carriage in UK veterinary staff and owners of infected pets: new risk groups. J Hosp Infect. 2010, 74(3): 282–288.

[27] Thrusfield M. Veterinary epidemiology. John Wiley & Sons, 2018.

[28] Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST. Bergey’s manual of determinative bacteriology. 9th. Balt William Wilkins. 1994.

[29] Clinical, Institute LS. Performance Standards for Antimicrobial Susceptibility Testing of Anaerobic Bacteria: Informational Supplement. Clinical and Laboratory Standards Institute (CLSI), 2009.

[30] Bauer AW. Antibiotic susceptibility testing by a standardized single disc method. Am J clin pathol. 1966, 45: 149–158.

[31] Li L, Zhou L, Wang L, Xue H, Zhao X. Characterization of methicillin-resistant and-susceptible staphylococcal isolates from bovine milk in northwestern China. PLoS One. 2015, 10(3).

[32] Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, Smith H, Stevens KB, Lloyd DH. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J Antimicrob Chemother. 2005, 56(4): 692–697.

[33] Kottler SJ. Prevalence of Staphylococcus aureus and MRSA carriage in three populations. 2008.

[34] Bierowiec K, Płoneczka-Janeczko K, Rypuła K. Prevalence and risk factors of colonization with Staphylococcus aureus in healthy pet cats kept in the city households. Biomed Res Int. 2016, 2016.

[35] Shoaib M, Rahman SU, Aqib AI, Ashfaq K, Naveed A, Kulyar MF-A, Bhutta ZA, Younas MS, Sarwar I, Naseer MA, others. Diversified Epidemiological Pattern and Antibiogram of mecA Gene in Staphylococcus aureus Isolates of Pets, Pet Owners and Environment.

[36] El-Deeb W, Fayez M, Elmoslemany A, Kandeel M, Zidan K. Methicillin resistant Staphylococcus aureus among goat farms in Eastern province, Saudi Arabia: Prevalence and risk factors. Prev Vet Med. 2018, 156: 84–90.

[37] Bochev I, Russenova N. Resistance of Staphylococcus spp. strains isolated from goats with subclinical mastitis. Bulg J Vet Med. 2005, 8(2): 109–118.

[38] Haran KP, Godden SM, Boxrud D, Jawahir S, Bender JB, Sreevatsan S. Prevalence and characterization of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. J Clin Microbiol. 2012, 50(3): 688–695. DOI:https://doi.org/10.1128/JCM.05214-11

[39] Cortimiglia C, et al., Bianchini V, Franco A, Caprioli A, Battisti A, Colombo L, Stradiotto K, Vezzoli F, Luini M. Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus in bulk tank milk from dairy goat farms in Northern Italy. J Dairy Sci. 2015, 98(4): 2307–2311.

[40] Giacinti G, Sagrafoli D, Tammaro A, Bovi E, Marri N, Giangolini G, Carfora V, Cordaro G, Ianzano A, Lorenzetti S, others. Methicillin-sensible Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus isolated in raw milk from dairy sheep farms located in Central Italy.

[41] Rubin JE, Ball KR, Chirino-Trejo M. Antimicrobial susceptibility of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from various animals. Can Vet J = La Rev Vet Can. 2011, 52(2): 153–157. Available at: https://www.ncbi.nlm.nih.gov/pubmed/21532820

[42] Oppliger A, Moreillon P, Charrière N, Giddey M, Morisset D, Sakwinska O. Antimicrobial Resistance of <span class="named-content genus-species" id="named-content-1">Staphylococcus aureus</span> Strains Acquired by Pig Farmers from Pigs. Appl Environ Microbiol. 2012, 78(22): 8010. DOI:https://doi.org/10.1128/AEM.01902-12

[43] Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R, System NNIS. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis. 2006, 42(3): 389–391.

[44] Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002, 70(2): 631–641. DOI:https://doi.org/10.1128/IAI.70.2.631-641.2002

[45] Carfora V, Caprioli A, Marri N, Sagrafoli D, Boselli C, Giacinti G, Giangolini G, Sorbara L, Dottarelli S, Battisti A, Amatiste S. Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy. Int Dairy J. 2015, 42: 12–15. DOI: https://doi.org/10.1016/j.idairyj.2014.10.009

[46] Marques JB, Dalmolin TV, Bonez PC, Agertt VA, Campos MMA de, Santos RCV. Detection of Staphylococcus aureus with an intermediate profile to vancomycin (VISA) isolate from Santa Maria, RS. Brazilian J Microbiol. 2013, 44(1): 277–279.

[47] Edslev SM, Clausen M-L, Agner T, Stegger M, Andersen PS. Genomic analysis reveals different mechanisms of fusidic acid resistance in Staphylococcus aureus from Danish atopic dermatitis patients. J Antimicrob Chemother. 2018, 73(4): 856–861. DOI:https://doi.org/10.1093/jac/dkx481

[48] Chen H-J, Hung W-C, Tseng S-P, Tsai J-C, Hsueh P-R, Teng L-J. Fusidic Acid Resistance Determinants in <em>Staphylococcus aureus</em> Clinical Isolates. Antimicrob Agents Chemother. 2010, 54(12): 4985. DOI:https://doi.org/10.1128/AAC.00523-10

[49] Aqib AI, Ijaz M, Anjum AA, Malik MAR, Mehmood K, Farooqi SH, Hussain K. Antibiotic susceptibilities and prevalence of Methicillin resistant Staphylococcus aureus (MRSA) isolated from bovine milk in Pakistan. Acta Trop. 2017, 176: 168–172.

[50] Ali, Muhammad G, Ahmad T, Khan R, Anwar H, Farooqi FA, Manzoor MN, Usama AR. Prevalence of caprine sub-clinical Mastitis, its etiological agents and its sensitivity to antibiotics in indigenous breeds of Kohat, Pakistan. Pakistan J Life Soc Sci. 2010, 8: 63–67.

[51] Saleem MI, Saqib M, Khan MS, Muhammad G, ur Rehman S. Epidemiological Study of Mastitis in Three Different Strains of Beetal Goat in Selected Districts of Punjab, Pakistan. 2018.

[52] Befekadu T, Genene T, Bizuayehu B, Abebe M. Prevalence and antimicrobial susceptibility pattern of Staphylococcus aureus from raw camel and goat milk from somali region of Ethiopia. African J Microbiol Res. 2016, 10(28): 1066–1071. DOI:https://doi.org/10.5897/ajmr2015.7517.

[53] Aqib A, Ijaz M, Zameer Durrani A, Ahmad Anjum A, Hussain R, Sana S, Shahid F, Hussain K, Saleem Ahmad S. Prevalence and Antibiogram of Staphylococcus aureus, a Camel Mastitogen from Pakistan. Pakistan J. Zool., Vol. 49, Iss. 3, pp 861-867 Read more at http://researcherslinks.com/current-issues/Prevalence-Antibiogram-Staphylococcus-aureus-Camel-Mastitogen-Pakistan/20/1/428/html#IGAoewLi3cCiDZM1.99, 2017. DOI:https://doi.org/10.17582/journal.pjz/2017.49.3.861.867

[54] Ali M, Avais M, Ijaz M, Chaudhary M, Hussain R, Aqib AI, Khan NU, Sohail ML, Khan M, Khan MA, others. Epidemiology of subclinical mastitis in dromedary camels (Camelus dromedarius) of two distinct agro-ecological zones of Pakistan. Pakistan J Zool. 2019, 51(2): 527–532.

[55] Abo-Shama U. Prevalence and antimicrobial susceptibility of staphylococcus aureus isolated from cattle, buffalo, sheep and goats. Assiut Vet Med J. 2014, 60(141): 63–72.

[56] Ceniti C, Britti D, Santoro AML, Musarella R, Ciambrone L, Casalinuovo F, Costanzo N. Phenotypic antimicrobial resistance profile of isolates causing clinical mastitis in dairy animals. Ital J Food Saf. 2017, 6(2): 84–87. DOI:https://doi.org/ 10.4081/ijfs.2017.6612

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Copyright © 2020 Iqra Muzammil, Muhammad Shoaib, Amjad Islam Aqib, Muhammad Aamir Naseer, Zeeshan Ahmad Bhutta

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