Species diversity and antibiotic resistance properties of Staphylococcus of farm animal origin in Nkonkobe Municipality, South Africa

Folia Microbiologica

Volumn 59, Issue 2, 2014, Pages 133-140

  Adegoke, Anthony A ^a   Okoh, Anthony I ^a  

^a UNIVERSITY OF FORT HARE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; COAGULASE;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CATTLE; CHICKEN; CLASSIFICATION; DOMESTIC ANIMAL; DRUG EFFECT; FECES; GENETICS; GENOTYPE; GOAT; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHENOTYPE; SOUTH AFRICA; STAPHYLOCOCCUS; SWINE;

ANIMALS; ANIMALS, DOMESTIC; ANTI-BACTERIAL AGENTS; CATTLE; CHICKENS; COAGULASE; DRUG RESISTANCE, BACTERIAL; FECES; GENES, BACTERIAL; GENOTYPE; GOATS; MICROBIAL SENSITIVITY TESTS; PHENOTYPE; SOUTH AFRICA; STAPHYLOCOCCUS; SWINE;

EID: 84894610863     PISSN: 00155632     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12223-013-0275-1     Document Type: Article

References (70)

1. Alexander TA, Yanke JL, Reuter T, Topp E, Read RR, Selinger BL, McAllister TA (2011) Longitudinal characterization of antimicrobial resistance genes in feces shed from cattle fed different subtherapeutic antibiotics. BMC Microbiol 11: 19. doi: 10. 1186/1471-2180-11-19.
2. Bagcigil AF, Moodley A, Jensen VE, Guardabassi L (2007) Occurrence, species distribution, antimicrobial resistance, and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Vet Microbiol 121: 307-315.
3. Bannerman TL (2003) Staphylococcus, Micrococcus, and other catalase-positive cocci that grow aerobically. In: Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH (eds) Manual of Clinical Microbiology. American Society Microbiology, Washington, pp 384-404.
4. Barbosa TM, Levy SB (2000) The impact of antibiotic use on resistance development and persistence. Drug Res Updates 3: 303-311.
5. Bhalakia N, Morris D (2005) Isolation and Plasmid Analysis of Vancomycin- Resistant Staphylococcus aureus. J Young Invest. 13 (4), retrieved 11 December 2010 from http://www. jyi. org/research/re. php?id=573.
6. Boucher H, Miller LG, Razonable RR (2010) Serious infections caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 51(Suppl 2): S183-S197.
7. Chang S, Sievert DM, Hageman JC (2003) Infection with vancomycin resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 348: 1342-1347.
8. Cheesebrough M (2006) District Laboratory Practice in Tropical Countries. Part 2, 2nd edition, Cambridge University Press pp. 132-143.
9. Clinical and Laboratory Standards Institute, CLSI (2008) Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals-Third Edition: Approved Standard M31-A3. CLSI, Wayne, PA, USA.
10. Cohen ML (1992) Epidemiology of drug resistance: implications for a post antimicrobial era. Science 257: 1050-1055.
11. Corbière MS, Talon R, Leroy S (2004) Development of a multiplex PCR for the identification of Staphylococcus genus and four staphylococcal species isolated from food. J Appl Microbiol 97: 1087-1094.
12. Cuny C, Friedrich A, Kozytska S, Layer F, Nubel U et al (2010) Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int J Med Microbiol 300(2-3): 109-117.
13. Dahiru T (2008) P value, a true test of statistical significance? A cautionary note. Ann. Ibad. Postgrad. Medicine 6(1): 21-26.
14. De Neeling AJ, van den Broek MJM, Spalburg EC, van Santen-Verheuvel MG, Dam-Deisz WDC et al (2007) High prevalence of methicillin-resistant Staphylococcus aureus in pigs. Vet Microbiol 122: 366-372.
15. Denis O, Suetens C, Hallin M, Catry B, Ramboer I et al (2009) Methicillin-resistant Staphylococcus aureus ST398 in swine farm personnel, Belgium. Emerg Infect Dis 15(7): 1098-1101.
16. Deurenberg RH, Stobberingh EE (2008) "The evolution of Staphylococcus aureus" available at .
17. D'mello D, Daley AJ, Rahman MS, Garland S, Pearce C et al (2008) Vancomycin heteroresistance in bloodstream isolates of Staphylococcus capitis. J Clin Microbiol 46(9): 3124-3126.
18. Duquette RA, Nuttall TJ (2004) Methicillin-resistant Staphylococcus aureus in dogs and cats: an emerging problem? J Small Anim Pract 45(12): 591-597.
19. Dutka-Malen S, Evers S, Courvalin P (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 33: 24-27.
20. Essack SY (2001) The development of β-lactam antibiotics in response to the evolution of β-lactamases. Pharm Res 18(10): 1391-1399.
21. Fairbrother RW (2005) Coagulase production as a criterion for the classification of the staphylococci. J Pathol Bacteriol 50(1): 83-88.
22. Fitzgerald JR, Sturdevant DE, Mackie SM, Gill SR, Musser JM (2001) Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc Natl Acad Sci U S A 98(15): 8821-8826.
23. Geha DJ, Uhl JR, Gustaferro CA, Persing DH (1994) Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 32: 1768-1772.
24. Gortel K, Campbell KL, Kakoma I, Whittem T, Schaeffer DJ et al (1999) Methicillin resistance among staphylococci isolated from dogs. Am J Vet Res 60: 1526-1530.
25. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E (2006) Emergence and resurgence of methicillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368(9538): 874-885.
26. Hammerum AM, Lester CH, Heuer OE (2010) Antimicrobial-resistant enterococci in animals and meat: a human health hazard? Foodborne Pathog Dis 7(10): 1137-46.
27. Harada K, Asai T (2010) Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan. J Biomed Biotechnol. doi: 10. 1155/2010/180682.
28. Iwase T, Seki K, Shinji H, Mizunoe Y, Masuda S (2007) Development of a real- time PCR assay for the detection and identification of Staphylococcus capitis, Staphylococcus haemolyticus, and Staphylococcus warneri". J Med Microbiol 56(Pt 10): 1346-1349.
29. Jensen LB, Frimodt-Moller N, Aarestrup FM (1999) Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol Lett 170: 151-158.
30. Kania SA, Williamson NL, Frank LA, Wilkes RP, Jones RD et al (2004) Methicillin resistance of staphylococci isolated from the skin of dogs with pyoderma. Am J Vet Res 65: 1265-1268.
31. Kaur R, Pathania R (2010) Drug Resistance in Food Animals - A Public Health Concern. Onl. Vet J. 5(1), Article 48. Available at: .
32. Kitara LD, Anywar AD, Acullu D, Odongo-Aginya E, Aloyo J et al (2011) Antibiotic susceptibility of Staphylococcus aureus in suppurative lesions in Lacor Hospital. Uganda Afr Health Sci 11(S1): S34-S39.
33. Kloos WE, Bannerman TL (1994) Update on clinical significance of coagulase-negative staphylococci. Clin Microbiol Rev 7(1): 117-140.
34. Komolafe AO, Adegoke AA (2008) Incidence of bacterial septicemia in Ile-Ife Metropolis, Malaysian J. Microbiology 4(2): 51-61.
35. Kriegeskorte A, Ballhausen B, Idelevich AE, Kock R, Friedrich AW, Karch H, Peters G, Becker K (2012) Human MRSA isolates with novel genetic homolog, Germany. Emerg Infec Dis 18(6): 1016-1018.
36. Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46(1): 165-170.
37. Laxminarayan R, Klugman KP (2011) Communicating trends in resistance using a drug resistance index. BMJ Open;1: e000135 doi: 10. 1136/bmjopen-2011-000135.
38. LeLoir Y, Baron F, Gautier M (2003) Staphylococcus aureus and food poisoning. Gen Mol Res 2(1): 63-76.
39. Levy SB (1986) Ecology of antibiotic resistance determinants. In: Press CSHL (ed) Antibiotic resistance genes: ecology, transfer and expression. Cold Spring Harbor Press, New York, pp 17-30.
40. Lüthje P, Schwarz S (2006) Antimicrobial resistance of coagulase-negative Staphylococci from bovine subclinical mastitis with particular reference to macrolide-lincosamide resistance phenotypes and genotypes. J Antimicrob Chemother 57: 966-969.
41. Martineau F, Picard FJ, Ke D, Paradis S, Roy PH et al (2001) Development of a PCR assay for identification of staphylococci at genus and species levels. J Clinical Microbiol 39: 2541-2547.
42. Montanari MP, Tonin E, Biavasco F, Varaldo PE (1990) Further characterization of borderline methicillin-resistant Staphylococcus aureus and analysis of penicillin-binding proteins. Antimicrob Agents Chemother 34: 911-913.
43. Morot-Bizot SC, Talon R, Leroy S (2004) Development of a multiplex PCR for the identification of Staphylococcus genus and four staphylococcal species isolated from food. J Appl Microbiol 97: 1087-1094.
44. nd International Conference of the Office International des Epizoosties, 2001; Paris; 2001.
45. NCCLS (1999) Performance Standards for Antimicrobial Disk and Dilution Susceptibility, Tests for Bacteria Isolated from Animals; Approved Standard. NCCLS Document M31-A.
46. Ogbodo SO, Okeke AC, Ugwuoru CDC, Chukwurah EF (2011) Possible Alternatives to Reduce Antibiotic Resistance. Life Sc. Med Res available at: [Accessed 12 December 2011].
47. Otter JA, French GL (2010) Molecular epidemiology of community-associated methicillin-resistant Staphylococcus aureus in Europe. Lancet Infect Dis 10(4): 227-239.
48. Perrier-Gros-Claude J, Courrier P, Bréard J, Vignot J, Masseront T et al (1998) Entérocoques résistants aux glycopeptides dans les viandes. Bull Epidemiol Hebdomadaire 50-51.
49. Pinho MG, de Lencastre H, Tomasz A (2001) An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc Natl Acad Sci U S A 98(19): 10886-10891.
50. Ramos-Trujillo E, Perez-Roth E, Mendez-Alvarez S, Claverie-Martin F (2003) Multiplex PCR for simultaneous detection of enterococcal genes vanA and vanB and staphylococcal genes mecA, ileS-2, and femB. Int Microbiol 6: 113-115.
51. Saha B, Singh AK, Abhrajyoti G, Bal M (2007) Identification and characterization of a vancomycin resistant Staphylococcus aureus isolated from Kolkata (South Asia). J Med Microbiol 57: 72-79.
52. Saleha A, 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(7): 1094-1098.
53. Sauer P, Sila J, Stosova T, Vecerova R, Hejnar P et al (2008) Prevalence of genes encoding extracellular factors among methicillin-resistant Staphylococcus aureus isolates from the University Hospital, Olomouc Czech Republic. J Med Microbiol 57: 403-410.
54. Schlegelova J, Vlkova H, Babak V, Holasova M, Jaglic Z et al (2008) Resistance to erythromycin of Staphylococcus spp. isolates from the food chain. Vet Med 53(6): 307-314.
55. Sergio DM, Koh TH, Hsu LY, Ogden BE, Goh AL et al (2007) Investigation of methicillin-resistant Staphylococcus aureus in pigs used for research. J Med Microbiol 56(Pt 8): 1107-1109.
56. Shittu A, Lin J, Morrison D, Kolawole D (2004) Isolation and molecular characterization of multiresistant Staphylococcus sciuri and Staphylococcus haemolyticus associated with skin and soft-tissue infections. J Med Microbiol 53(1): 51-55.
57. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP et al (2009) Methicillin- resistant Staphylococcus aureus (MRSA) strain ST398 is present in Midwestern US swine and swine workers. PLoS One 4(1): e4258.
58. Summers AO (2002) Generally overlooked fundamentals of bacterial genetics and ecology. Clin Infect Dis 34(Suppl 3): S85-S92.
59. Suresh T, Srinivasan D, Hatha AAM, Lakshmanaperumalsamy P (2000) The incidence, antibiotics resistance, and survival of Salmonella and Escherichia coli isolated from broiler chicken retail outlets. Microb Environ 15: 173-181.
60. Tenover FC, Goering RV (2009) Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother 64(3): 441-446.
61. Thorberg B (2008) Coagulase-Negative Staphylococci in Bovine Sub-Clinical Mastitis. Licentiate Thesis Department of Biomedical Sciences and Veterinary Public Health Swedish University of Agricultural Sciences Report no. 2.
62. Trulzsch K, Rinder H, Treek J, Bader L, Wilhelm U et al (2002) "Staphylococcus pettenkoferi", a novel Staphylococcal species isolated from clinical specimens. Diag Microbiol Infect Dis 43: 175-182.
63. van den Broek IV, van Cleef BA, Haenen A, Broens EM, van der Wolf PJ et al (2009) Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect 137(5): 700-708.
64. van Der Zwet WC, Debets-Ossenkopp YJ, Reinders E, Kapl M, Savelkoul PHM et al (2002) Nosocomial spread of a Staphylococcus capitis strain with hetero-resistance to vancomycin in a neonatal intensive care unit. J Clin Microbiol 40(7): 2520-2525.
65. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N et al (2007) Emergence of methicillin-resistant Staphylococcus aureus of animal origin. Emerg Infect Dis 13(12): 1834-1839.
66. Walther B, Wieler LH, Friedrich AW, Hanssen AM, Kohn B, Brunnberg L, Lubke-Becker A (2008) Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routing microbiological examinations. Vet Microbiol 127(1-2): 171-178.
67. Weese JS, Archambault M, Willey BM, Hearn P, Kreiswirth BN et al (2005) Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002. Emerg Infect Dis 11(3): 430-435.
68. Werckenthin C, Schwarz S (2000) Molecular analysis of the translational attenuator of a constitutively expressed ermA gene from Staphylococcus intermedius. J Antimicrob Chemother 46: 785-788.
69. WHO (2011) Removing obstacles to healthy development. http://www. who. int/infectious-disease-report/pages/textonly. html#Anchor1. [Accessed 10 December 2011].
70. Wondrack L, Massa M, Yang V, Sutcliffe J (1996) Clinical strain of Staphylococcus aureus inactivates and causes efflux of macrolides. Antimicrob Agents Chemother 40: 992-998.