Document Type : Research Paper

Authors

1 Department of Biology, School of Sciences, University of Duhok, Duhok, Iraq

2 Department of Biology, Faculty of Sciences, University of Zakho, Zakho, Duhock, Iraq

3 Department of Pharmaceutic, College of Pharmacy, University of Duhock, Duhok, Iraq

Abstract

Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) has become a global public health concern. The purpose of this study was to investigate the prevalence rates of MRSA infection amongst broiler chickens and broilers farm workers. The total samples used in this study were 306. Cloacal swab samples from 231 broilers and nasal swab samples from 75 broilers farm workers were collected from five farms in Duhok city, Iraq. Isolation and identification of MRSA isolates were carried out and the antibiotic susceptibility were screened. Molecular characterization of all isolates was performed by using polymerase chain reaction (PCR) technique to detect the mecA gene.S. aureus was detected among 84% (63/75) of the farms workers samples and among 84.8% (196/231) of the broiler's samples. The S. aureus isolated from farm workers and broilers appeared resistant to oxacillin 28.6% (18/63), and 32.1% (63/196), respectively. MRSA colonization in farm workers and broilers was 24% (18/75) and 27.3% (63/231) respectively. The S. aureus isolates showed the most resistant to chloramphenicol and the least resistant to vancomycin. The results of the PCR assays revealed that 85.7% (12/14) of S. aureus isolates from farm workers and 44.4% (16/36) of S. aureus isolates from broilers were positive for the mecA gene. The direct handling of broilers by farm workers plays the important role for transport the MRSA isolates from broilers to broilers farm workers.

Keywords

Main Subjects

1.     Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751-762. DOI: 10.1016/S1473-3099(05)70295-4.
2.     Kirby WM. Extraction of a highly potent penicillin inactivator from penicillin resistant Staphylococci. Science. 1944;99(2579):452-453.  DOI: 10.1126/science.99.2579.452.
3.      Jevons MP. Celbenin-resistant staphylococci. Bangladesh Med J. 1961;1:124-125.
4.     Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Devriese LA, Pasmans F, Haesebrouck F.  Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother. 2008;52(10):3817-3819. DOI: 10.1128/AAC.00613-08.
5.     Murra M, Mortensen KL, Wang M. Livestock-associated methicillin-resistant Staphylococcus aureus (clonal complex 398) causing bacteremia and epidural abscess. Int J Infect Dis. 2019;81:107-109. DOI: 10.1016/j.ijid.2019.01.012.
6.     Kevorkijan BK, Petrovic Z, Kocuvan A, Rupnik M. MRSA diversity and the emergence of LA-MRSA in a large teaching hospital in Slovenia. Acta Microbiol Immunol Hung. 2019:1-12. DOI: 10.1556/030.65.2018.052.
7.      Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, Simpson AJ, Rambaut A, Nubel U, Fitzgerald JR. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A. 2009;106(46):19545-19550. DOI: 10.1073/pnas.0909285106.
8.      Dweba CC, Zishiri OT, El Zowalaty ME. Methicillin-resistant Staphylococcus aureus: livestock-associated, antimicrobial, and heavy metal resistance. Infect Drug Resist. 2018;11:2497-2509. DOI: 10.2147/IDR.S175967.
9.      Schulz J, Boklund A, Toft N, Tariq H. Effects of control measures on the spread of LA-MRSA among Danish pig herds between 2006 and 2015 - a simulation study. Scic Rep. 2019;9(1):691. DOI: 10.1038/s41598-018-37075-8.
10.   Latour K, Huang TD, Jans B, Berhin C, Bogaerts P, Noel A, Nonhoff C, Dodemont M, Denis O, Ieven M, Loens K, Schoevaerdts D, Catry B, Glupczynski Y. Prevalence of multidrug-resistant organisms in nursing homes in Belgium in 2015. PLoS One. 2019;14(3):e0214327. DOI: 10.1371/journal.pone.0214327.
11.   Conlon GM, Aldeyab M, Scott M Kearney MP, Farren D, Gilmore F, McElnay J. Effects of antibiotic cycling policy on incidence of healthcare-associated MRSA and Clostridioides difficile infection in secondary healthcare settings. Emerg Infect Dis. 2019;25(1):52-62. DOI: 10.3201/eid2501.180111.
12.   CLSI. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing; Twenty-Fifth informational supplement. CLSI-NCCLS document M100-S25. Clinical and laboratory standards institute, Wayne, PA. 2015.
13.   Tokue Y, Shoji S, Satoh K, Satoh K, Watanabe A, Motomiya M. Comparison of a polymerase chain reaction assay and a conventional microbiologic method for detection of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1992;36(1):6-9. DOI: 10.1128/aac.36.1.6.
14.   Hussein NR, Basharat Z, Muhammed AH, Al-Dabbagh SA. Comparative evaluation of MRSA nasal colonization epidemiology in the urban and rural secondary school community of Kurdistan, Iraq. PLoS One. 2015;10(5):e0124920.DOI: 10.1371/journal.pone.0124920.
15.   Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol. 1991;29:2240-2244.
16.   Krupa P, Bystron J, Bania J,  Podkowik M, Empel J, Mroczkowska A. Genotypes and oxacillin resistance of Staphylococcus aureus from chicken and chicken meat in Poland. Poult Sci. 2014;93(12):3179-3186. DOI: 10.3382/ps.2014-04321.
17.   Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, Roberts LK, Kroeger JS, Smith TC. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health. 2011;4(4):169-174. DOI: 10.1016/j.jiph.2011.06.001.
18.   Shareef AM, Mansour RS, Ibrahim KK. Staphylococcus aureus in commercial breeder layer flocks. Iraqi J Vet Sci. 2009;23(I):63-68.  
19.   Bakeet AAM, Darwish SF. Phenotypic and genotypic detection of methicillin- resistant Staphylococcus aureus (MRSA) in broiler chickens. Assiut Vet Med J. 2014;60(143):142-151.
20.   Thompson JK, Gibbs PA, Patterson JT. Staphylococcus aureus in commercial laying flocks: incidence and characteristics of strains isolated from chicks, pullets and hens in an integrated commercial enterprise. Br Poult Sci. 1980;21(4):315-330. DOI: 10.1080/00071668008416675.
21.   Hussein NR, Alyas A, Majeed M, Assafi MS. Prevalence rate and prevalent genotypes of CA-MRSA in Kurdistan region: First report from Iraq. Int J Pure Appl Sci Technol. 2015;27(1):44-49. DOI: 10.17795/iji-35375.
22.   Habeeb A, Hussein NR, Assafi MS, Al-Dabbagh SA. Methicillin resistant Staphylococcus aureus nasal colonization among secondary school students at Duhok city - Iraq. J Microbiol Infect Dis. 2014;4(2):59-63. DOI: 10.5799/ahinjs.02.2014.02.0128. DOI: 10.5799/ahinjs.02.2014.02.0128.
23.   Hussein NR, Muhammed AH, Al-Dabbagh S, Abdulkareem WL, Assafi MS. The Prevalence of USA300 CA-MRSA in Kurdistan region, northern Iraq. Int J Pure Appl Sci Technol. 2014;21(2):8-10.
24.   Hussein NR, Assafi MS, Ijaz T. Methicillin-resistant Staphylococcus aureus nasal colonization amongst healthcare workers in Kurdistan Region, Iraq. J Glob Antimicrob Resist. 2017;9:78-81. DOI: 10.1016/j.jgar.2017.01.010.
25.   Soliman SE, Reddy PG, Mohamed Sobeih AA, Busby H, Rowe ES. Epidemiological surveillance on environmental contaminants in poultry farms. Inter J Poul Sci. 2009;8(2):151-155. DOI: 10.3923/ijps.2009.151.155.
26.   Adegunloye DV. Microorganisms associated with poultry faeces. J Food Agricul Environ. 2006;4:41-42.
27.   Neela V, Ghaznavi E, Ghasemzadeh-Moghaddam, Shamsudin MN, van Belkum A, Karunanidhi A. Frequency of methicillin resistant Staphylococcus aureus in the noses of Malaysian chicken farmers and their chicken. Iranian J Vet Res. 2013;14(3):226-231. DOI: 10.22099/ijvr.2013.1685.
28.   Assafi MS, Polse RF, Hussein NR, Haji AH, Issa AR. The Prevalence of S. aureus Nasal colonization and its Antibiotic Sensitivity Pattern amongst Primary School Pupils. SJUOZ. 2017;5(1):7-10. DOI: 10.25271/2017.5.1.291.
29.   Richter A, Sting R, Popp C, Rau J, Tenhagen BA, Guerra B, Hafez HM, Fetsch A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol Infect. 2012;140(12):2223-2232.DOI: 10.1017/S095026881200009X.
30.   Suk S, Nam L, Park H, Lee H, Choi H, Jung M, Santos SI, Mato R, de Lencastre H, Tomasz AS, Lee J, Kim Y, Sang S, Wee S. Prevalencea and characterization of methicillin-resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotechnol. 2010;20(4):775-778. DOI: 10.4014/jmb.0912.12022.
31.   Bhargava K, Wang X, Donabedian S, Zervos M, de Rocha L, Zhang Y. Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg Infect Dis. 2011;17(6):1135-1137. DOI: 10.3201/eid/1706.101905.
32.   Oke AJ, Oke A. Incidence of Methicillin-Resistant Staphylococcus aureus (MRSA) In a Small Poultry in South-West, Nigeria. IOSR J Agricul Vete Sci. 2013;5:53-55. DOI: 10.9790/2380.0535355.
33.   Geenen PL, Graat EA, Haenen A, Hengeveld PD, Van Hoek AH, Huijsdens XW, Kappert CC, Lammers GA, Van Duijkeren E, Van De Giessen AW. Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiol Infect. 2013;141(5):1099-1108. DOI: 10.1017/S0950268812001616.
34.   Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis. 2005;11(12):1965-1966. DOI: 10.3201/eid1112.050428.
35.   Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol. 2009;75(1):265-267. DOI: 10.1128/AEM.01110-08.
36.   Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, Foster JT, Bowers J, Driebe EM,  Engelthaler DM, Keim PS, Price LB. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infec Dis. 2011;52(10):1227-1230DOI: 10.1093/cid/cir181.
37.   Rinsky JL, Nadimpalli M, Wing S, Hall D, Baron D, Price LB, Larsen J, Stegger M, Stewart J, Heaney CD. Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in north Carolina. PLoS ONE. 2013;8(7):e67641. DOI: 10.1371/journal.pone.0067641.
38.   Mulders MN, Haenen AP, Geenen PL, Vesseur PC, Poldervaart ES, Bosch T, Huijsdens XW, Hengeveld PD, Dam-Deisz WD, Graat EA, Mevius D, Voss A, Van De Giessen AW. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in the Netherlands. Epidemiol Infect. 2010;138(5):743-755. DOI: 10.1017/S0950268810000075.
39.   Quddoumi SS, Bdour SM, Mahasneh AM. Isolation and characterization of methicillin-resistant Staphylococcus aureus from livestock and poultry meat. Annals Microbiol. 2006;56(2):155-161. DOI: 10.1007/BF03174998.
40.   Otalu OJ, Kabir J, Okolocha EC, Umoh VJ. Multi-drug resistant coagulase positive Staphylococcus aureus from live and slaughtered chickens in Zaria, Nigeria. Internat J Poul Sci. 2011;10(11):871-875DOI: 10.3923/ijps.2011.871.875.
41.   Lee JH. Occurrence of methicillin-resistant Staphylococcus aureus strains from cattle and chicken, and analyses of their mecA, mecR1 and mecI genes. Vet Microbiol. 2006;114:155-159. DOI: 10.1016/j.vetmic.2005.10.024.
42.   Uttley AH, George RC, Naidoo J, Woodford N, Johnson AP, Collins CH, Morrison D, Gilfillan AJ, Fitch LE, Heptonstall J. High-level vancomycin-resistant enterococci causing hospital infections. Epidemiol Infect. 1989;103(1):173-181. DOI: 10.1017/s0950268800030478.
43.   Papadopoulou C, Dimitriou D, Levidiotou S, Gessouli H, Panagiou A, Golegou S, Antoniades G. Bacterial strains isolated from eggs and their resistance to currently used antibiotics: is there a health hazard for consumers? Comp Immunol Microbiol Infect Dis. 1997;20(1):35-40. DOI: 10.1016/S0147-9571(96)00024-0.
44.   Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. Absence of the mecA gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi city, Sudan. Biomed Res Int. 2015;2015:895860. DOI: 10.1155/2015/895860.
45.   Olayinka BO, Olayinka AT, Obajuluwa AF, Onaolapo JA, Olurinola PF. Absence of mecA gene in methicillin-resistant Staphylococcus aureus isolates. Afr J Infect Dis. 2009;3(2):49-56. DOI: 10.4314/ajid.v3i2.55081.
46.   Ba X, Harrison EM, Edwards GF, Holden MTG, Larsen AR, Petersen A, Skov RL, Peacock SJ, Parkhill J, Paterson GK, Holmes MA. Novel mutations in penicillin-binding protein genes in clinical Staphylococcus aureus isolates that are methicillin resistant on susceptibility testing, but lack the mecA gene. J Antimicrob Chemother. 2014;69(3):594-597. DOI: 10.1093/jac/dkt418.
 
1.     Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751-762. DOI: 10.1016/S1473-3099(05)70295-4.
2.     Kirby WM. Extraction of a highly potent penicillin inactivator from penicillin resistant Staphylococci. Science. 1944;99(2579):452-453.  DOI: 10.1126/science.99.2579.452.
3.      Jevons MP. Celbenin-resistant staphylococci. Bangladesh Med J. 1961;1:124-125.
4.     Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Devriese LA, Pasmans F, Haesebrouck F.  Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother. 2008;52(10):3817-3819. DOI: 10.1128/AAC.00613-08.
5.     Murra M, Mortensen KL, Wang M. Livestock-associated methicillin-resistant Staphylococcus aureus (clonal complex 398) causing bacteremia and epidural abscess. Int J Infect Dis. 2019;81:107-109. DOI: 10.1016/j.ijid.2019.01.012.
6.     Kevorkijan BK, Petrovic Z, Kocuvan A, Rupnik M. MRSA diversity and the emergence of LA-MRSA in a large teaching hospital in Slovenia. Acta Microbiol Immunol Hung. 2019:1-12. DOI: 10.1556/030.65.2018.052.
7.      Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, Simpson AJ, Rambaut A, Nubel U, Fitzgerald JR. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A. 2009;106(46):19545-19550. DOI: 10.1073/pnas.0909285106.
8.      Dweba CC, Zishiri OT, El Zowalaty ME. Methicillin-resistant Staphylococcus aureus: livestock-associated, antimicrobial, and heavy metal resistance. Infect Drug Resist. 2018;11:2497-2509. DOI: 10.2147/IDR.S175967.
9.      Schulz J, Boklund A, Toft N, Tariq H. Effects of control measures on the spread of LA-MRSA among Danish pig herds between 2006 and 2015 - a simulation study. Scic Rep. 2019;9(1):691. DOI: 10.1038/s41598-018-37075-8.
10.   Latour K, Huang TD, Jans B, Berhin C, Bogaerts P, Noel A, Nonhoff C, Dodemont M, Denis O, Ieven M, Loens K, Schoevaerdts D, Catry B, Glupczynski Y. Prevalence of multidrug-resistant organisms in nursing homes in Belgium in 2015. PLoS One. 2019;14(3):e0214327. DOI: 10.1371/journal.pone.0214327.
11.   Conlon GM, Aldeyab M, Scott M Kearney MP, Farren D, Gilmore F, McElnay J. Effects of antibiotic cycling policy on incidence of healthcare-associated MRSA and Clostridioides difficile infection in secondary healthcare settings. Emerg Infect Dis. 2019;25(1):52-62. DOI: 10.3201/eid2501.180111.
12.   CLSI. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing; Twenty-Fifth informational supplement. CLSI-NCCLS document M100-S25. Clinical and laboratory standards institute, Wayne, PA. 2015.
13.   Tokue Y, Shoji S, Satoh K, Satoh K, Watanabe A, Motomiya M. Comparison of a polymerase chain reaction assay and a conventional microbiologic method for detection of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1992;36(1):6-9. DOI: 10.1128/aac.36.1.6.
14.   Hussein NR, Basharat Z, Muhammed AH, Al-Dabbagh SA. Comparative evaluation of MRSA nasal colonization epidemiology in the urban and rural secondary school community of Kurdistan, Iraq. PLoS One. 2015;10(5):e0124920.DOI: 10.1371/journal.pone.0124920.
15.   Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol. 1991;29:2240-2244.
16.   Krupa P, Bystron J, Bania J,  Podkowik M, Empel J, Mroczkowska A. Genotypes and oxacillin resistance of Staphylococcus aureus from chicken and chicken meat in Poland. Poult Sci. 2014;93(12):3179-3186. DOI: 10.3382/ps.2014-04321.
17.   Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, Roberts LK, Kroeger JS, Smith TC. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health. 2011;4(4):169-174. DOI: 10.1016/j.jiph.2011.06.001.
18.   Shareef AM, Mansour RS, Ibrahim KK. Staphylococcus aureus in commercial breeder layer flocks. Iraqi J Vet Sci. 2009;23(I):63-68.  
19.   Bakeet AAM, Darwish SF. Phenotypic and genotypic detection of methicillin- resistant Staphylococcus aureus (MRSA) in broiler chickens. Assiut Vet Med J. 2014;60(143):142-151.
20.   Thompson JK, Gibbs PA, Patterson JT. Staphylococcus aureus in commercial laying flocks: incidence and characteristics of strains isolated from chicks, pullets and hens in an integrated commercial enterprise. Br Poult Sci. 1980;21(4):315-330. DOI: 10.1080/00071668008416675.
21.   Hussein NR, Alyas A, Majeed M, Assafi MS. Prevalence rate and prevalent genotypes of CA-MRSA in Kurdistan region: First report from Iraq. Int J Pure Appl Sci Technol. 2015;27(1):44-49. DOI: 10.17795/iji-35375.
22.   Habeeb A, Hussein NR, Assafi MS, Al-Dabbagh SA. Methicillin resistant Staphylococcus aureus nasal colonization among secondary school students at Duhok city - Iraq. J Microbiol Infect Dis. 2014;4(2):59-63. DOI: 10.5799/ahinjs.02.2014.02.0128. DOI: 10.5799/ahinjs.02.2014.02.0128.
23.   Hussein NR, Muhammed AH, Al-Dabbagh S, Abdulkareem WL, Assafi MS. The Prevalence of USA300 CA-MRSA in Kurdistan region, northern Iraq. Int J Pure Appl Sci Technol. 2014;21(2):8-10.
24.   Hussein NR, Assafi MS, Ijaz T. Methicillin-resistant Staphylococcus aureus nasal colonization amongst healthcare workers in Kurdistan Region, Iraq. J Glob Antimicrob Resist. 2017;9:78-81. DOI: 10.1016/j.jgar.2017.01.010.
25.   Soliman SE, Reddy PG, Mohamed Sobeih AA, Busby H, Rowe ES. Epidemiological surveillance on environmental contaminants in poultry farms. Inter J Poul Sci. 2009;8(2):151-155. DOI: 10.3923/ijps.2009.151.155.
26.   Adegunloye DV. Microorganisms associated with poultry faeces. J Food Agricul Environ. 2006;4:41-42.
27.   Neela V, Ghaznavi E, Ghasemzadeh-Moghaddam, Shamsudin MN, van Belkum A, Karunanidhi A. Frequency of methicillin resistant Staphylococcus aureus in the noses of Malaysian chicken farmers and their chicken. Iranian J Vet Res. 2013;14(3):226-231. DOI: 10.22099/ijvr.2013.1685.
28.   Assafi MS, Polse RF, Hussein NR, Haji AH, Issa AR. The Prevalence of S. aureus Nasal colonization and its Antibiotic Sensitivity Pattern amongst Primary School Pupils. SJUOZ. 2017;5(1):7-10. DOI: 10.25271/2017.5.1.291.
29.   Richter A, Sting R, Popp C, Rau J, Tenhagen BA, Guerra B, Hafez HM, Fetsch A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol Infect. 2012;140(12):2223-2232.DOI: 10.1017/S095026881200009X.
30.   Suk S, Nam L, Park H, Lee H, Choi H, Jung M, Santos SI, Mato R, de Lencastre H, Tomasz AS, Lee J, Kim Y, Sang S, Wee S. Prevalencea and characterization of methicillin-resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotechnol. 2010;20(4):775-778. DOI: 10.4014/jmb.0912.12022.
31.   Bhargava K, Wang X, Donabedian S, Zervos M, de Rocha L, Zhang Y. Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg Infect Dis. 2011;17(6):1135-1137. DOI: 10.3201/eid/1706.101905.
32.   Oke AJ, Oke A. Incidence of Methicillin-Resistant Staphylococcus aureus (MRSA) In a Small Poultry in South-West, Nigeria. IOSR J Agricul Vete Sci. 2013;5:53-55. DOI: 10.9790/2380.0535355.
33.   Geenen PL, Graat EA, Haenen A, Hengeveld PD, Van Hoek AH, Huijsdens XW, Kappert CC, Lammers GA, Van Duijkeren E, Van De Giessen AW. Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiol Infect. 2013;141(5):1099-1108. DOI: 10.1017/S0950268812001616.
34.   Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis. 2005;11(12):1965-1966. DOI: 10.3201/eid1112.050428.
35.   Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol. 2009;75(1):265-267. DOI: 10.1128/AEM.01110-08.
36.   Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, Foster JT, Bowers J, Driebe EM,  Engelthaler DM, Keim PS, Price LB. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infec Dis. 2011;52(10):1227-1230DOI: 10.1093/cid/cir181.
37.   Rinsky JL, Nadimpalli M, Wing S, Hall D, Baron D, Price LB, Larsen J, Stegger M, Stewart J, Heaney CD. Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in north Carolina. PLoS ONE. 2013;8(7):e67641. DOI: 10.1371/journal.pone.0067641.
38.   Mulders MN, Haenen AP, Geenen PL, Vesseur PC, Poldervaart ES, Bosch T, Huijsdens XW, Hengeveld PD, Dam-Deisz WD, Graat EA, Mevius D, Voss A, Van De Giessen AW. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in the Netherlands. Epidemiol Infect. 2010;138(5):743-755. DOI: 10.1017/S0950268810000075.
39.   Quddoumi SS, Bdour SM, Mahasneh AM. Isolation and characterization of methicillin-resistant Staphylococcus aureus from livestock and poultry meat. Annals Microbiol. 2006;56(2):155-161. DOI: 10.1007/BF03174998.
40.   Otalu OJ, Kabir J, Okolocha EC, Umoh VJ. Multi-drug resistant coagulase positive Staphylococcus aureus from live and slaughtered chickens in Zaria, Nigeria. Internat J Poul Sci. 2011;10(11):871-875DOI: 10.3923/ijps.2011.871.875.
41.   Lee JH. Occurrence of methicillin-resistant Staphylococcus aureus strains from cattle and chicken, and analyses of their mecA, mecR1 and mecI genes. Vet Microbiol. 2006;114:155-159. DOI: 10.1016/j.vetmic.2005.10.024.
42.   Uttley AH, George RC, Naidoo J, Woodford N, Johnson AP, Collins CH, Morrison D, Gilfillan AJ, Fitch LE, Heptonstall J. High-level vancomycin-resistant enterococci causing hospital infections. Epidemiol Infect. 1989;103(1):173-181. DOI: 10.1017/s0950268800030478.
43.   Papadopoulou C, Dimitriou D, Levidiotou S, Gessouli H, Panagiou A, Golegou S, Antoniades G. Bacterial strains isolated from eggs and their resistance to currently used antibiotics: is there a health hazard for consumers? Comp Immunol Microbiol Infect Dis. 1997;20(1):35-40. DOI: 10.1016/S0147-9571(96)00024-0.
44.   Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. Absence of the mecA gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi city, Sudan. Biomed Res Int. 2015;2015:895860. DOI: 10.1155/2015/895860.
45.   Olayinka BO, Olayinka AT, Obajuluwa AF, Onaolapo JA, Olurinola PF. Absence of mecA gene in methicillin-resistant Staphylococcus aureus isolates. Afr J Infect Dis. 2009;3(2):49-56. DOI: 10.4314/ajid.v3i2.55081.
46.   Ba X, Harrison EM, Edwards GF, Holden MTG, Larsen AR, Petersen A, Skov RL, Peacock SJ, Parkhill J, Paterson GK, Holmes MA. Novel mutations in penicillin-binding protein genes in clinical Staphylococcus aureus isolates that are methicillin resistant on susceptibility testing, but lack the mecA gene. J Antimicrob Chemother. 2014;69(3):594-597. DOI: 10.1093/jac/dkt418.