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Detection, molecular characterization, and antibiogram of multi-drug resistant and methicillin-resistant Staphylococcus aureus (MRSA) isolated from pets and pet owners in Malaysia | ||
| Iranian Journal of Veterinary Research | ||
| دوره 22، شماره 4 - شماره پیاپی 77، 2021، صفحه 277-287 اصل مقاله (692.43 K) | ||
| نوع مقاله: Full paper (Original article) | ||
| شناسه دیجیتال (DOI): 10.22099/ijvr.2021.39586.5752 | ||
| نویسندگان | ||
| M. H. Chai1؛ M. Z. Sukiman1؛ Y. W. Liew2؛ M. S. Shapawi2؛ F. S. Roslan2؛ S. N. Hashim2؛ N. M. Mohamad3؛ S. M. Z. Ariffin4؛ M. F. Ghazali* 5 | ||
| 1Ph.D. Student in Veterinary Public Health, School of Animal Science, Aquatic Science and Environment, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia | ||
| 2BSc Student in Animal Production and Health, School of Animal Science, Aquatic Science and Environment, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia | ||
| 3Centralised Laboratory Management Centre, Universiti Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia | ||
| 4Department of Veterinary Preclinical Sciences, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia | ||
| 5School of Animal Science, Aquatic Science and Environment, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia | ||
| چکیده | ||
| Background: The emergence of multidrug-resistant strains such as methicillin-resistant Staphylococcus aureus (MRSA) and multidrug-resistant Staphylococcus aureus (MDRSA) in animals and humans with continuous contact are a great zoonotic concern. Aims: This cross-sectional study was performed to investigate the carriage rate, genotypic characteristics, and to determine the antibiogram of S. aureus isolated from pets and pet owners in Malaysia. Methods: Nasal and oral swab samples from 40 cats, 30 dogs, and 70 pet owners were collected through convenient sampling. Presumptive colonies on mannitol salt agar were subjected to biochemical identification. S. aureus and MRSA were confirmed by PCR detection of nuc and mecA genes, respectively. Molecular profiles for antimicrobial resistance and virulence genes in S. aureus were also determined. The antibiogram was carried out via Kirby-Bauer test using 18 antibiotics. Results: 17.5% of cats, 20% of dogs, and 27% of pet owners were S. aureus positive. MRSA was also detected in dogs, and pet owners. S. aureus isolates displayed high resistance against penicillin (72.7%), and amoxicillin/clavulanate (66.7%). 39.4% of S. aureus isolates showed multidrug-resistance traits, phenotypically. Molecular characterization of S. aureus revealed the presence of mecA, tetk, tetL, ermA, ermB, ermC, msrA, scn, chp, sak, sep, and sea genes. Conclusion: This study showed the emergence of MRSA and MDRSA in pets and pet owners in Malaysia. The antibiogram findings showed resistance of S. aureus to multiple antibiotics. Furthermore, molecular analysis of immune evasion cluster (IEC) strongly suggests the spread of animal-adapted S. aureus lineages among pets and pet owners. | ||
| کلیدواژهها | ||
| Antibiogram؛ Methicillin-resistant Staphylococcus aureus؛ Multidrug-resistant Staphylococcus aureus؛ Pet animals؛ Pet owners | ||
| مراجع | ||
|
Abolghait, SK; Fathi, AG; Youssef, FM and Algammal, AM (2020). Methicillin-resistant Staphylococcus aureus (MRSA) isolated from chicken meat and giblets often produces staphylococcal enterotoxin B (SEB) in non-refrigerated raw chicken livers. Int. J. Food Microbiol., 328: 1-9. doi: 10.1016/j.ijfoodmicro.2020.108669.
Ahmad, N; Ruzan, IN; Ghani, MKA; Hussin, A; Nawi, S; Aziz, MN; Maning, N and Eow, VLK (2009). Characteristics of community- and hospital-acquired meticillin-resistant Staphylococcus aureus strains carrying SCCmec type IV isolated in Malaysia. J. Med. Microbiol., 58: 1213-1218. https://doi.org/10.1099/jmm.0.011353-0.
Ahmadrajabi, R; Khavidaki, SL; Kalantar-Neyestanaki, D and Fasihi, Y (2017). Molecular analysis of immune evasion cluster (IEC) genes and intercellular adhesion gene cluster (ICA) among methicillin-resistant and methicillin-sensitive isolates of Staphylococcus aureus. J. Prev. Med. Hyg., 58: E308-E314. https://doi.org/10.15167/2421-4248/jpmh2017.58.4.711.
Aklilu, E; Zakaria, Z; Hassan, L and Chen, HC (2012). Molecular relatedness of methicillin-resistant S. aureus isolates from staff, environment and pets at university veterinary hospital in Malaysia. PLoS One. 7: e43329. https://doi.org/10.1371/journal.pone.0043329.
Aklilu, E; Zakaria, Z; Hassan, L and Chen, HC (2013). Molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) among veterinary students and personnel at a veterinary hospital in Malaysia. Vet. Microbiol., 164: 352-358. https://doi.org/10.1016/j.vetmic. 2013.02.030.
Algammal, AM; El-Sayed, ME; Youssef, FM; Saad, SA; Elhaig, MM; Batiha, GE; Hozzein, WN and Ghobashy, MO (2020). Prevalence, the antibiogram and the frequency of virulence genes of the most predominant bacterial pathogens incriminated in calf pneumonia. AMB Express., 10: 1-8. doi: 10.1186/s13568-020-01037-z.
Ariffin, MF; Hasmadi, N; Chai, MH; Ghazali, MF and Ariffin, SMZ (2020). Prevalence and antimicrobial sensitivity pattern of Staphylococcus aureus isolated from clinical and subclinical mastitis in small ruminant in Besut and Setiu, Terengganu, Malaysia. Malays. J. Microbiol., 16: 104-110. https://doi.org/http://dx.doi.org/10.21161/ mjm.180328.
Ariffin, SM; Hasmadi, N; Syawari, NM; Sukiman, MZ; Ariffin, MFT; Chai, MH and Ghazali, MF (2019). Prevalence and antibiotic susceptibility pattern of Staphylococcus aureus, Streptococcus agalactiae and Escherichia coli in dairy goats with clinical and subclinical mastitis. J. Anim. Health Prod., 7: 32-37. https://doi.org/ 10.17582/journal.jahp/2019/7.1.32.37.
Ariyarad, S; Rezatofighi, SE and Motamedi, H (2019). Evaluation of antimicrobial resistance and immune evasion cluster genes in clinical methicillin-resistant Staphylococcus aureus (MRSA) isolates from Khuzestan Province, Iran. Epidemiol. Infect., 5: 7-14.
Becker, K; Van Alen, S; Idelevich, EA; Schleimer, N; Seggewiß, J; Mellmann, A; Kaspar, U and Peters, G (2018). Plasmid-encoded transferable mecB-mediated methicillin resistance in Staphylococcus aureus. Emerg. Infect. Dis., 24: 242-248.
Bien, J; Sokolova, O and Bozko, P (2011). Characterization of virulence factors of Staphylococcus aureus: Novel function of known virulence factors that are implicated in activation of airway epithelial proinflammatory response. J. Pathog., 2011: 1-13. https://doi.org/10.4061/2011/601905.
Bierowiec, K; Korzeniowska-Kowal, A; Wzorek, A; Rypuła, K and Gamian, A (2019). Prevalence of Staphylococcus species colonization in healthy and sick cats. BioMed. Res. Int., 2019: 1-10. doi: 10.1155/2019/4360525.
Boost, MV; O’Donoghue, M and James, A (2008). Investigation of the role of dogs as reservoirs of Staphylococcus aureus and the transmission of strains between pet owners and their dogs. Hong Kong Med. J., 14: 15-18.
Chai, MH; Arrifin, MFT; Ariffin, SMZ; Suhaili, Z; Sukiman, MZ and Ghazali, MF (2020). Prevalence of methicillin-resistant Staphylococcus aureus in raw goat milks from selected farms in Terengganu, Malaysia. Trop. Anim. Sci. J., 43: 64-69. https://doi.org/https://doi.org/ 10.5398/tasj.2020.43.1.64.
Che Hamzah, AM; Yeo, CC; Puah, SM; Chua, KH and Chew, CH (2019). Staphylococcus aureus infections in Malaysia: A review of antimicrobial resistance and characteristics of the clinical isolates, 1990-2017. Antibiotics. 8: 1-29. https://doi.org/10.3390/ antibiotics8030128.
Collignon, PJ; Conly, JM; Andremont, A; McEwen, SA; Aidara-Kane, A; World Health Organization Advisory Group, Bogotá Meeting on Integrated Surveillance of Antimicrobial Resistance (WHO-AGISAR); Agerso, Y; Andremont, A; Collignon, P; Conly, J; Dang Ninh, T; Donado-Godoy, P; Fedorka-Cray, P; Fernandez, H; Galas, M; Irwin, R; Karp, B; Matar, G; McDermott, P; McEwen, S; Mitema, E; Reid-Smith, R; Scott, HM; Singh, R; DeWaal, CS; Stelling, J; Toleman, M; Watanabe, H and Woo, GJ (2016). World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin. Infect. Dis., 63: 1087-1093. doi: 10.1093/cid/ciw475.
Corona, F and Martinez, JL (2013). Phenotypic resistance to antibiotics. Antibiotics. 2: 237-255. https://doi.org/10.3390/ antibiotics2020237.
Cuny, C; Abdelbary, M; Layer, F; Werner, G and Witte, W (2015). Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet. Microbiol., 177: 219-223. https://doi.org/10.1016/j.vetmic.2015.02.031.
De Haas, CJC; Veldkamp, KE; Peschel, A; Weerkamp, F; Van Wamel, WJB; Heezius, ECJM; Poppelier, MJJG; Van Kessel, KPM and Van Strijp, JAG (2004). Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory Agent. J. Exp. Med., 199: 687-695. https://doi.org/10.1084/jem.20031636.
Enany, ME; Algammal, AM; Shagar, GI; Hanora, AM; Elfeil, WK and Elshaffy, NM (2018). Molecular typing and evaluation of Sidr honey inhibitory effect on virulence genes of MRSA strains isolated from catfish in Egypt. Pak. J. Pharma. Sci., 31: 1865-1870.
Foster, TJ (2017). Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol. Rev., 41: 430-449. https://doi.org/10.1093/ femsre/fux007.
Ghanbari, F; Ghajavand, H; Havaei, R; Jami, MS; Khademi, F; Heydari, L; Shahin, M and Havaei, S (2016). Distribution of erm genes among Staphylococcus aureus isolates with inducible resistance to clindamycin in Isfahan, Iran. Adv. Biomed. Res., 5: 1-5. https://doi.org/10.4103/2277-9175.179184.
Gómez-Sanz, E; Torres, C; Lozano, C and Zarazaga, M (2013). High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members. Underestimating normal household contact? Comp. Immunol. Microbiol. Infect. Dis., 36: 83-94. https://doi.org/ 10.1016/j.cimid.2012.10.001.
Hau, SJ; Sun, J; Davies, PR; Frana, TS and Nicholson, TL (2015). Comparative prevalence of immune evasion complex genes associated with β-hemolysin converting bacteriophages in mrsa st5 isolates from swine, swine facilities, humans with swine contact, and humans with no swine contact. PLoS One. 10: 1-13. https://doi.org/ 10.1371/journal.pone.0142832.
Holmes, A; Ganner, M; McGuane, S; Pitt, TL; Cookson, BD and Kearns, AM (2005). Staphylococcus aureus isolates carrying panton-valentine leukocidin genes in England and Wales: Frequency, characterization, and association with clinical disease. J. Clin. Microbiol., 43: 2384-2390. https://doi.org/10.1128/JCM.43.5.2384-2390. 2005.
Huang, T and Chou, C (2019). Methicillin-sensitive and methicillin-resistant Staphylococcus aureus strains and their toxin genes in the nostrils of dogs and workers at an animal shelter. J. Appl. Microbiol., 126: 1899-1909.
Kanagarajah, RR; Lee, DCW; Lee, DZF; Yusoff, K; Paramasivam, SJ; Low, WY; Jeevaratnam, K and Lim, SHE (2017). Antibiotic profiling of Methicillin-Resistant Staphylococcus aureus (MRSA) isolates in stray canines and felines. Cogent Biol., 3: 1-10. https://doi.org/10.1080/ 23312025.2017.1412280.
Kandel, SN; Adhikari, N; Dhungel, B; Shrestha, UT; Angbuhang, KB; Karki, G; Adhikari, B; Banjara, MR; Rijal, KR and Ghimire, P (2020). Characteristics of Staphylococcus aureus isolated from clinical specimens in a tertiary care hospital, Kathmandu, Nepal. Microbiol. Insights. 13: 1-6. doi: 10.1177/1178636120972695.
Köck, R; Harlizius, J; Bressan, N; Laerberg, R; Wieler, LH; Witte, W; Deurenberg, RH; Voss, A; Becker, K and Friedrich, AW (2009). Prevalence and molecular characteristics of Methicillin-Resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur. J. Clin. Microbiol. Infect. Dis., 28: 1375-1382. https://doi.org/10. 1007/s10096-009-0795-4.
Lim, KT; Yeo, CC; Suhaili, Z and Thong, KL (2012). Comparison of methicillin-resistant and methicillin-sensitive Staphylococcus aureus strains isolated from a tertiary hospital in Terengganu, Malaysia. Jpn. J. Infect. Dis., 65: 502-509. https://doi.org/10.7883/yoken.65.502.
Lina, G; Piémont, Y; Godail-Gamot, F; Bes, M; Peter, MO; Gauduchon, V; Vandenesch, F and Etienne, J (1999). Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis., 29: 1128-1132. https://doi. org/10.1086/313461.
Ma, Y; Zhao, Y; Tang, J; Tang, C; Chen, J and Liu, J (2018). Antimicrobial susceptibility and presence of resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CYTA J. Food. 16: 76-84. https://doi.org/10.1080/19476337.2017.1340341.
Magiorakos, AP; Srinivasan, A; Carey, RB; Carmeli, Y; Falagas, ME; Giske, CG; Harbarth, S; Hindler, JF; Kahlmeter, G; Olsson-Liljequist, B; Paterson, DL; Rice, LB; Stelling, J; Struelens, MJ; Vatopoulos, A; Weber, JT and Monnet, DL (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect., 18: 268-281. https://doi.org/10.1111/j.1469-0691.2011. 03570.x.
Miranda, C; Silva, V; Igrejas, G and Poeta, P (2021). Impact of European pet antibiotic use on enterococci and staphylococci antimicrobial resistance and human health. Future Microbiol., 16: 185-203.
Neela, V; Zafrul, AM; Mariana, NS; Van Belkum, A; Liew, YK and Rad, EG (2009). Prevalence of ST9 methicillin-resistant Staphylococcus aureus among pigs and pig handlers in Malaysia. J. Clin. Microbiol., 47: 4138-4140. https://doi.org/10.1128/JCM.01363-09.
Ng, L; Martin, I; Alfa, M and Mulvey, M (2001). Multiplex PCR for the detection of tetracycline resistant genes. Mol. Cell Probes., 15: 209-215. https://doi.org/10.1006/mcpr. 2001.0363.
Nicolaou, KC and Rigol, S (2018). A brief history of antibiotics and select advances in their synthesis. J. Antibiot., 71: 153-184. https://doi.org/10.1038/ja.2017.62.
Peacock, SJ and Paterson, GK (2015). Mechanisms of methicillin resistance in Staphylococcus aureus. Annu. Rev. Biochem., 84: 577-601. https://doi.org/10.1146/ annurev-biochem-060614-034516.
Qekwana, DN; Oguttu, JW and Sithole, F (2017). Burden and predictors of Staphylococcus aureus and S. pseudintermedius infections among dogs presented at an academic veterinary hospital in South Africa (2007-2012). PeerJ. 5: e3198.
Rankin, S; Roberts, S; O’Shea, K; Maloney, D; Lorenzo, M and Benson, CE (2005). Panton valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion animals. Vet. Microbiol., 108: 145-148.
Riaz, S; Faisal, M and Hasnain, S (2011). Antibiotic susceptibility pattern and multiple antibiotic resistances (MAR) calculation of extended spectrum β-lactamase (ESBL) producing escherichia coli and klebsiella species in Pakistan. Afr. J. Biotechnol., 10: 6325-6331. https://doi. org/10.5897/AJB11.086.
Rooijakkers, SHM; Ruyken, M; Roos, A; Daha, MR; Presanis, JS; Sim, RB; van Wamel, WJB; van Kessel, KPM and van Strijp, JAG (2005). Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol., 6: 920-927. https://doi.org/10. 1038/ni1235.
Saiful, AJ; Mastura, M; Zarizal, S; Mazurah, MI; Shuhaimi, M and Ali, AM (2006). Detection of methicillin-resistant Staphylococcus aureus using mecA/nuc genes and antibiotic susceptibility profile of Malaysian clinical isolates. World J. Microbiol. Biotechnol., 22: 1289-1294. https://doi.org/10.1007/ s11274-006-9174-9.
Saleha, AA; Shamzarina, M; Othman, F and Zunita, Z (2006). Methicillin-resistant Staphylococcus aureus (MRSA) isolated from pet animals and pet and non-pet owners. J. Vet. Malays., 18: 13-16.
Saleha, AA and Zunita, Z (2010). Methicillin resistant Staphylococcus aureus (MRSA): An emerging veterinary and zoonotic pathogen of public health concern and some studies in Malaysia. J. Anim. Vet. Adv., 9: 1094-1098.
Sit, PS; Teh, CSJ; Idris, N; Sam, IC; Syed Omar, SF; Sulaiman, H; Thong, KW; Adeeba Kamarulzaman, A and Ponnampalavanar, S (2017). Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) infection and the molecular characteristics of MRSA bacteraemia over a two-year period in a tertiary teaching hospital in Malaysia. BMC Infect. Dis., 17: 1-14. https://doi.org/10.1186/s12879-017-2384-y.
Stegger, M; Liu, CM; Larsen, J; Soldanova, K; Aziz, M; Contente-Cuomo, T; Petersen, A; Vandendriessche, S; Jiménez, JN; Mammina, C; Van Belkum, A; Salmenlinna, S; Laurent, F; Skov, RL; Larsen, AR; Andersen, PS and Price, LB (2013). Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 Clades, PLoS One. 8: e79645. https://doi.org/10.1371/journal.pone.0079645.
Suhaili, Z; Yeo, CC; Ghazali, MF; Chew, CH; Zainul, AZ; Mazen, MJAO; Nordin, SA and Mohd Desa, MN (2018). Nasal colonisation, antimicrobial susceptibility and genotypic pattern of staphylococcus aureus among agricultural biotechnology students in besut, terengganu, east coast of malaysia. Trop. Med. Int. Health. 23: 905-913. https://doi.org/10.1111/tmi.13090.
Trzcinski, K; Cooper, BS; Hryniewicz, W and Dowson, CG (2000). Expression of resistance to tetracyclines in strains of methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother., 45: 763-770.
Van Balen, JC; Landers, T; Nutt, E; Dent, A and Hoet, AE (2017). Molecular epidemiological analysis to assess the influence of pet-ownership in the biodiversity of Staphylococcus aureus and MRSA in dog- and non-dog-owning healthy households. Epidemiol. Infect., 145: 1135-1147. https://doi.org/10.1017/S0950268816003228.
Van Wamel, WJ; Rooijakkers, SH; Ruyken, M; Van Kessel, KP and Van Strijp, JA (2006). The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on β-hemolysin-converting bacteriophages. J. Bacteriol., 188: 1310-1315.
Verkaik, NJ; Benard, M; Boelens, HA; De Vogel, CP; Nouwen, JL; Verbrugh, HA; Melles, DC; Van Belkum, A and Van Wamel, WJB (2011). Immune evasion cluster-positive bacteriophages are highly prevalent among human Staphylococcus aureus strains, but they are not essential in the first stages of nasal colonization. Clin. Microbiol. Infect., 17: 343-348. https://doi.org/10.1111/j.1469-0691.2010.03227.x. Vyletělova, M; Hanuš, O; Karpíšková, R and Štástková, Z (2011). Occurrence and antimicrobial sensitivity in staphylococci isolated from goat, sheep and cow’s milk. Acta Univ. Agric. Silvic. Mendel. Brun., 59: 209-213.
Walther, B; Hermes, J; Cuny, C; Wieler, LH; Vincze, S; Elnaga, YA; Stamm, I; Kopp, PA; Kohn, B; Witte, W; Jansen, A; Conraths, FJ; Semmler, T; Eckmanns, T and Lübke-Becker, A (2012). Sharing more than friendship - Nasal colonization with coagulase-positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PLoS One. 7: e35197. https://doi.org/10. 1371/journal.pone.0035197.
You, Y; Song, L; Nonyane, BAS; Price, LB and Silbergeld, EK (2018). Genomic differences between nasal Staphylococcus aureus from HOG slaughterhouse workers and their communities. PLoS One. 13: e0193820. https://doi.org/10.1371/journal.pone.0193820.
Zehra, A; Singh, R; Kaur, S and Gill, JPS (2017). Molecular characterization of antibiotic-resistant Staphylococcus aureus from livestock (bovine and swine). Vet. World., 10: 598-604. https://doi.org/10.14202/vetworld.2017.598-604. | ||
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