Characteristics of staphylococcus aureus small colony variant and its parent strain isolated from chronic mastitis at a dairy farm in Beijing, China

Microbial Drug Resistance

Volumn 19, Issue 2, 2013, Pages 138-145

  Alkasir, Rashad ^a   Liu, Xiuquan ^a,b   Zahra, Mohammad ^a   Ferreri, Miro ^a   Su, Jingliang ^a   Han, Bo ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Animal Science and Veterinary Station   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL; SULFADIMETHOXINE; THYMIDINE;

ANTIBIOTIC SENSITIVITY; ARTICLE; AUXOTROPHY; BACTERIAL GROWTH; BACTERIAL STRAIN; BOVINE MASTITIS; CHINA; DAIRY CATTLE; GROWTH CURVE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; CHINA; CHLORAMPHENICOL; CHRONIC DISEASE; COLONY COUNT, MICROBIAL; EPITHELIAL CELLS; FEMALE; HUMANS; MASTITIS, BOVINE; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SULFADIMETHOXINE; THYMIDINE;

BOVINAE; STAPHYLOCOCCUS AUREUS; STRAWBERRY CRINKLE VIRUS;

EID: 84875616807     PISSN: 10766294     EISSN: 19318448     Source Type: Journal    
DOI: 10.1089/mdr.2012.0086     Document Type: Article

References (45)

1. Atalla, H., C. Gyles, C.L. Jacob, H. Moisan, F. Malouin, and B. Mallard. 2008. Characterization of a Staphylococcus aureus small colony variant (SCV) associated with persistent bovine mastitis. Foodborne Pathog. Dis. 5:785-799.
2. Balwit, J.M., P. van Langevelde, J.M. Vann, and R.A. Proctor. 1994. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170:1033-1037.
3. Barkema, H.W., Y.H. Schukken, and R.N. Zadoks. 2006. Invited Review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J. Dairy Sci. 89:1877-1895.
4. Besier, S., C. Smaczny, C. von Mallinckrodt, A. Krahl, H. Ackermann, V. Brade, and T.A. Wichelhaus. 2007. Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J. Clin. Microbiol. 45:168-172.
5. Besier, S., J. Zander, B.C. Kahl, P. Kraiczy, V. Brade, and T.A. Wichelhaus. 2008. The thymidine-dependent smallcolony- variant phenotype is associated with hypermutability and antibiotic resistance in clinical Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 52:2183-2189.
6. Brakstad, O.G., K. Aasbakk, and J.A. Maeland. 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol. 30: 1654-1660.
7. Chambers, H.F., and M.H. Miller. 1987. Emergence of resistance to cephalothin and gentamicin during combination therapy for methicillin-resistant Staphylococcus aureus endocarditis in rabbits. J. Infect. Dis. 155:581-585.
8. Chatterjee, I., P. Becker, M. Grundmeier, M. Bischoff, G.A. Somerville, G. Peters, B. Sinha, N. Harraghy, R.A. Proctor, and M. Herrmann. 2005. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol. 187:4488-4496.
9. Chatterjee, I., M. Herrmann, R.A. Proctor, G. Peters, and B.C. Kahl. 2007. Enhanced post-stationary-phase survival of a clinical thymidine-dependent small-colony variant of Staphylococcus aureus results from lack of a functional tricarboxylic acid cycle. J. Bacteriol. 189:2936-2940.
10. Chatterjee, I., A. Kriegeskorte, A. Fischer, S. Deiwick, N. Theimann, R.A. Proctor, G. Peters, M. Herrmann, and B.C. Kahl. 2008. In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J. Bacteriol. 190:834-842.
11. Clement, S., P. Vaudaux, P. Francois, J. Schrenzel, E. Huggler, S. Kampf, C. Chaponnier, D. Lew, and J.-S. Lacroix. Evidence of an intracellular reservoir in the nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis. J. Infect. Dis. 192:1023-1028.
12. Clinical and Laboratory Standards Institute. 2006. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. No. 2 Wayne, PA: Clinical and Laboratory Standards Institute 26: Approved standard, 7th ed., M7-A7.
13. Devriese, L. 1973. Hemin-dependent mutants isolated from methicillin-resistant Staphylococcus aureus strains. Antonie van Leeuwenhoek 39:33-40.
14. Foster, T.J. 2004. The Staphylococcus aureus "superbug". J. Clin. Invest. 114:1693-1696.
15. Gao, J., M. Ferreri, F. Yu, X. Liu, L. Chen, J. Su, and B. Han. Molecular types and antibiotic resistance of Staphylococcus aureus isolates from bovine mastitis in a single herd in China. Vet. J. 192:550-552.
16. Hardy, K.J., B.A. Oppenheim, S. Gossain, F. Gao, and P.M. Hawkey. 2006. Use of variations in staphylococcal interspersed repeat units for molecular typing of methicillin-resistant Staphylococcus aureus strains. J. Clin. Microbiol. 44:271-273.
17. Hess, D.J., M.J. Henry-Stanley, E.A. Erickson, and C.L. Wells. 2003. Intracellular survival of Staphylococcus aureus within cultured enterocytes. J. Surg. Res. 114:42-49.
18. Kahl, B., M. Herrmann, A.S. Everding, H.G. Koch, K. Becker, E. Harms, R.A. Proctor, and G. Peters. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis. 177:1023-1029.
19. Kahl, B.C., G. Belling, R. Reichelt, M. Herrmann, R.A. Proctor, and G. Peters. 2003. Thymidine-dependent smallcolony variants of Staphylococcus aureus exhibit gross morphological and ultrastructural changes consistent with impaired cell separation. J. Clin. Microbiol. 41:410-413.
20. Kohler, C., C. von Eiff, G. Peters, R.A. Proctor, M. Hecker, and S. Engelmann. 2003. Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J. Bacteriol. 185:6928-6937.
21. Kuhn, G., P. Francioli, and D.S. Blanc. 2006. Evidence for clonal evolution among highly polymorphic genes in methicillin-resistant Staphylococcus aureus. J. Bacteriol. 188: 169-178.
22. Melter, O., and B. Radojevc. 2010. Small colony variants of Staphylococcus aureus-review. Folia Microbiol. 55:548-558.
23. Mitchell, G., G. Grondin, G. Bilodeau, A.M. Cantin, and F. Malouin. 2011. Infection of polarized airway epithelial cells by normal and small-colony variant strains of Staphylococcus aureus is increased in cells with abnormal cystic fibrosis transmembrane conductance regulator function and is influenced by NF-kB. Infect. Immun. 79:3541-3551.
24. Moisan, H., E. Brouillette, C.L. Jacob, P. Langlois-Begin, S. Michaud, and F. Malouin. 2006. Transcription of virulence factors in Staphylococcus aureus small-colony variants isolated from cystic fibrosis patients is influenced by SigB. J. Bacteriol. 188:64-76.
25. Proctor, R.A., B. Kahl, C. von Eiff, P.E. Vaudaux, D.P. Lew, and G. Peters. 1998. Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin. Infect. Dis. 27 Suppl 1:S68-S74.
26. Proctor, R.A., P. van Langevelde, M. Kristjansson, J.N. Maslow, and R.D. Arbeit. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20:95-102.
27. Proctor, R.A., C. von Eiff, B.C. Kahl, K. Becker, P. McNamara, M. Herrmann, and G. Peters. 2006. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4:295-305.
28. Sabat, A., J. Krzyszton-Russjan, W. Strzalka, R. Filipek, K. Kosowska, W. Hryniewicz, J. Travis, and J. Potempa. 2003. New method for typing Staphylococcus aureus strains: multiple-locus variable-number tandem repeat analysis of polymorphism and genetic relationships of clinical isolates. J. Clin. Microbiol. 41:1801-1804.
29. Sadowska, B., A. Bonar, C. von Eiff, R.A. Proctor, M. Chmiela, W. Rudnicka, and B. Rozalska. 2002. Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol. Med. Microbiol. 32:191-197.
30. Seggewiss, J., K. Becker, O. Kotte, M. Eisenacher, M.R. Yazdi, A. Fischer, P. McNamara, N. Al Laham, R. Proctor, G. Peters, and others. 2006. Reporter metabolite analysis of transcriptional profiles of a Staphylococcus aureus strain with normal phenotype and its isogenic hemB mutant displaying the small-colony-variant phenotype. J. Bacteriol. 188: 7765-7777.
31. Smith, G.W., R.L. Lyman, and K.L. Anderson. 2006. Efficacy of vaccination and antimicrobial treatment to eliminate chronic intramammary Staphylococcus aureus infections in dairy cattle. J. Am. Vet. Med. Assoc. 228:422-425.
32. Sommerhäuser, J., B. Kloppert, W. Wolter, M. Zschö ck, A. Sobiraj, and K. Failing. 2003. The epidemiology of Staphylococcus aureus infections from subclinical mastitis in dairy cows during a control programme. Vet. Microbiol. 96: 91-102.
33. Sompolinsky, D., M. Cohen, and G. Ziv. 1974. Epidemiological and biochemical studies on thiamine-less dwarf-colony variants of Staphylococcus aureus as etiological agents of bovine mastitis. Infect. Immun. 9:217-228.
34. Sompolinsky, D., I. Gluskin, and G. Ziv. 1969. Pantothenaterequiring dwarf colony variants of Staphylococcus aureus as the etiological agent in bovine mastitis. J. Hyg. (Lond). 67: 511-516.
35. Tao, W., and B. Mallard. 2007. Differentially expressed genes associated with Staphylococcus aureus mastitis of Canadian Holstein cows. Vet. Immunol. Immunopathol. 120: 201-211.
36. Tuchscherr, L., V. Heitmann, M. Hussain, D. Viemann, J. Roth, C.v. Eiff, G. Peters, K. Becker, and B. Lö ffler. 2010. Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J. Infect. Dis. 202: 1031-1040.
37. von Eiff, C., K. Becker, D. Metze, G. Lubritz, J. Hockmann, T. Schwarz, and G. Peters. 2001. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier's disease. Clin. Infect. Dis. 32:1643-1647.
38. von Eiff, C., D. Bettin, R.A. Proctor, B. Rolauffs, N. Lindner, W. Winkelmann, and G. Peters. 1997. Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin. Infect. Dis. 25:1250-1251.
39. von Eiff, C., C. Heilmann, R.A. Proctor, C. Woltz, G. Peters, and F. Gotz. 1997. A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J. Bacteriol. 179:4706-4712.
40. von Eiff, C., P. McNamara, K. Becker, D. Bates, X.H. Lei, M. Ziman, B.R. Bochner, G. Peters, and R.A. Proctor. 2006. Phenotype microarray profiling of Staphylococcus aureus menD and hemB mutants with the small-colony-variant phenotype. J. Bacteriol. 188:687-693.
41. von Eiff, C., R.A. Proctor, and G. Peters. 2000. Staphylococcus aureus small colony variants: formation and clinical impact. Int. J. Clin. Pract. Suppl. 44-49.
42. Wise, R.I., and W.W. Spink. 1954. The influence of antibiotics on the origin of small colonies (G variants) of Micrococcus pyogenes var. aureus. J. Clin. Invest. 33:1611-1622.
43. Woo, P.C., A.S. Leung, K.W. Leung, and K.Y. Yuen. 2001. Identification of slide coagulase positive, tube coagulase negative Staphylococcus aureus by 16S ribosomal RNA gene sequencing. Mol. Pathol. 54:244-247.
44. Yagci, S., G. Hascelik, D. Dogru, U. Ozcelik, and B. Sener. Prevalence and genetic diversity of Staphylococcus aureus small-colony variants in cystic fibrosis patients. Clin. Microbiol. Infect. [Epub ahead of print]; DOI:10.1111/j.1469- 0691.2011.03742.x.
45. Yegian, D., G. Gallo, and M.W. Toll. 1959. Kanamycin resistant staphylococcus mutant requiring heme for growth J. Bacteriol. 78:10-12.