Small Colony Variants of Staphylococcus aureus - review

Folia Microbiologica

Volumn 55, Issue 6, 2010, Pages 548-558

  Melter, O ^a   Radojevic B ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; VIRULENCE;

GENETIC VARIATION; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MUTATION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS; STRAWBERRY CRINKLE VIRUS;

EID: 78751604875     PISSN: 00155632     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12223-010-0089-3     Document Type: Review

References (72)

1. Abu-qatouseh L. F., Chinni S. V., Seggewiss J., Proctor R. A., Brosius J., Rozhdestvensky T. S., Peters G., VON Eiff C., Becker K.: Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J. Mol. Med. 88, 565-575 (2010).
2. Anderson S. W., Stapp J. R., Burns J. L., Qin X.: Characterization of small-colony-variant Stenotrophomonas maltophilia isolated from the sputum specimens of five patients with cystic fibrosis. J. Clin. Microbiol. 45, 529-535 (2007).
3. Balwit J. M., VAN Langevelde P., Vann J. M., Proctor R. A.: Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170, 1033-1037 (1994).
4. Becker K., Friedrich A. W., Lubritz G., Weilert M., Peters G., VON Eiff C.: Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J. Clin. Microbiol. 41, 1434-1439 (2003).
5. Becker K., Harmsen D., Mellmann A., Meier C., Schumann P., Peters G., VON Eiff C.: Development and evaluation of a qualitycontrolled ribosomal sequence database for 16S ribosomal DNA-based identification of Staphylococcus species. J. Clin. Microbiol. 42, 4988-4995 (2004).
6. Becker K., Laham N. A., Fegeler W., Proctor R. A., Peters G., VON Eiff C.: Fourier-transform infrared spectroscopic analysis is a powerful tool for studying the dynamic changes in Staphylococcus aureus small-colony variants. J. Clin. Microbiol. 44, 3274-3278 (2006).
7. Bentley R., Meganathan R.: Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 46, 241-280 (1982).
8. Besier B., Smaczny C., Mallinckrodt C., Krahl A., Ackerman H., Brade V., Wichelhaus T. A.: Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J. Clin. Microbiol. 45, 168-172 (2007).
9. Besier S., Zander J., Siegel E., Saum S. H., Hunfeld K. P., Ehrhart A., Brade V., Wichelhaus T. A.: Thymidine-dependent Staphylococcus aureus small-colony variants: human pathogens that are relevant not only in cases of cystic fibrosis lung disease. J. Clin. Microbiol. 46, 3829-3832 (2008).
10. Borderon E., Horodniceanu T.: Metabolically deficient dwarf-colony mutants of Escherichia coli: deficiency and resistance to antibiotics of strains isolated from urine culture. J. Clin. Microbiol. 8, 629-634 (1978).
11. Browning C. H., Adamson H. S.: Stable dwarf-colony forms produced Staphylococcus pyogenes. J. Pathol. Bacteriol. 62, 499-500 (1950).
12. Chambers H. F., Miller M. M.: Emergence of resistance to cephalothin and gentamicin during combination therapy for methicillin-resistant Staphylococcus aureus endocarditis in rabbits. J. Infect. Dis. 155, 581-585 (1987).
13. Chatterjee I., Herrmann M., Proctor R. A., Peters G., Kahl B. C.: 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 (2007).
14. Chatterjee I., Kriegeskorte A., Fischer A., Deiwick S., Theimann N., Proctor R. A., Peters G., Herrmann M., Kahl B. C.: 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 (2008).
15. Devriese L. A.: Hemin-dependent mutants isolated from methicillin-resistant Staphylococcus aureus strains. Antoine van Leeuwenhoek39, 33-40 (1973).
16. von Eiff C.: Staphylococcus aureus small colony variants: a challenge to microbiologist and clinicians. Internat. J. Antimicrob. Agents31, 507-510 (2008).
17. von Eiff C., Becker K.: Small-colony variants (SCVs) of staphylococci: a role in foreign body-associated infections. Internat. J. Artur. Organs30, 778-785 (2007).
18. von Eiff C., Bettin D., Proctor R. A., Rolauffs B., Lindner N., Winkelmann W., Peters G.: Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin. Infect. Dis. 25, 1250-1251 (1997a).
19. von Eiff C., Heilmann C., Proctor R. A., Woltz C., Peters G., Gotz F.: A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persist intracellulary. J. Bacteriol. 179, 4706-4712 (1997b).
20. von Eiff C., Vaudaux P., Kahl B. C., Lew D., Emler S., Schmidt A., Peters G., Proctor R. A.: Bloodstream infections caused by small colony variants of coagulase negative staphylococci following pacemaker implantation. Clin. Infect. Dis. 29, 932-934 (1999).
21. von Eiff C., Becker K., Metze D., Lubritz G., Hockmann J., Scwartz T., Peters G.: 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 (2001).
22. von Eiff C., McNamara P., Becker K., Bates D., Lei X. H., Ziman M., Bochner B. R., Peters G., Proctor R. A.: Phenotype microarray profilig of Staphylococcus aureus menD and hemB mutants with small-colony-variant phenotype. J. Bacteriol. 188, 687-693 (2006).
23. Enright M. C., Day N. P. J., Davies C. E., Peacock S. J., Spratt B. G.: Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38, 1008-1015 (2000).
24. Fischer A., VON Eiff C., Kuczius T., Omoe K., Peters G., Becker K.: A quantitative real-time immuno-PCR approach for detection of staphylococcal enterotoxins. J. Mol. Med. 85, 461-469 (2007).
25. Garzoni C., Kelley W. L.: Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 17, 59-65 (2009).
26. Goudie J. G., Goudie R. B.: Recurrent infections by a stable dwarf-colony variant of Staphylococcus aureus. J. Clin. Pathol. 8, 284-287 (1955).
27. Häussler S., Tümmler B., Weissbrodt H., Rohde M., Steinmetz I.: Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin. Infect. Dis. 29, 621-625 (1999).
28. Häussler S., Ziegler I., Löttel A., VON Götz F., Rohde M., Wehmhöhner D., Saravanamuthu S., Tümmler B., Steinmetz I.: Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J. Med. Microbiol. 22, 295-301 (2003).
29. Høiby N., Krogh Johansen H., Moser C., Song Z., Ciofu O., Kharazmi A.: Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect. 3, 23-35 (2001).
30. Johnson W. M., Tyler S. D., Ewan E. P., Ashton F. E., Pollard D. R., Rozee K. R.: Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J. Clin. Microbiol. 29, 426-430 (1991).
31. Kahl B., Herrmann M., Everding A. S., Koch H. G., Becker K., Harms E., Proctor R. A., Peters G.: Persistent infection with small colony variant strains of Staphylococcus aureus in patient with cystic fibrosis. J. Infect. Dis. 177, 1023-1029 (1998).
32. Kahl B., Duebbers A., Lubritz G., Haeberle J., Koch H. G., Ritzerfeld B., Reilly M., Harms E., Proctor R. A., Herrmann M., Peters G.: Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J. Clin. Microbiol. 41, 4424-4427 (2003a).
33. Kahl B., Belling G., Reichelt R., Herrmann M., Proctor R. A., Peters G.: Thymidine-dependent small-colony variants of Staphylococcus aureus exhibit gross morphological and ultrastructural changes consistent with impaired cell separation. J. Clin. Microbiol. 41, 410-413 (2003b).
34. Kaplan M. L., Dye W.: Growth requirements of some small-colony-forming variants of Staphylococcus aureus. J. Clin. Microbiol. 4, 343-348 (1976).
35. Kipp F., Becker K., Peters G., VON Eiff C.: Evaluation of different methods to detect methicillin resistance in small-colony variants of Staphylococcus aureus. J. Clin. Microbiol. 42, 1277-1279 (2004).
36. Kipp F., Kahl B., Becker K., Baron E. J., Proctor R. A., Peters G., VON Eiff C.: Evaluation of two chromogenic agar media for recovery and identification of Staphylococcus aureus small-colony variants. J. Clin. Microbiol. 43, 1956-1959 (2005).
37. Koh K. S., Lam K. W., Alhede M., Queck S. Y., Labbate M., Kjelleberg S., Rice S. A.: Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes. J. Bacteriol. 189, 119-130 (2007).
38. Kohler C., VON Eiff C., Peters G., Proctor R. A., Hecker M., Engelmann S.: Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J. Bacteriol. 185, 6928-6937 (2003).
39. Lacey R. W.: Dwarf-colony variants of Staphylococcus aureus resistant to aminoglycoside antibiotics and to fatty acids. J. Med. Microbiol. 2, 187-197 (1969).
40. Lacey R. W., Mitchell A. B.: Gentamicin-resistant Staphylococcus aureus. Lancet2, 1425-1426 (1969).
41. Lånnergård J., VON Eiff C., Sander G., Cordes T., Seggewiss J., Peters G., Proctor R. A., Becker K., Hughes D.: Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of S. aureus. Antimicrob. Agents Chemother. 52, 4017-4022 (2008).
42. Lina G., Piémont Y., Godail-Gamot F., Bes M., Peter M. O., Gauduchon V., Vandenesch F., Etienne J.: Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29, 1128-1132 (1999).
43. Lyczak J. B., Cannon C. L., Pier G. B.: Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15, 194-222 (2002).
44. Malone J. G., Jaeger T., Spangler C., Ritz D., Spang A., Arrieumerlou C., Kaever V., Landmann R., Jenal U.: YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathogens12, e1000804 (2010).
45. Massey R. C., Buckling A., Peacock S. J.: Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus. Curr. Biol. 11, 1810-1814 (2001).
46. Menzies B. E., Kernodle D. S.: Site-directed mutagenesis of the α-toxin gene of Staphylococcus aureus: role of histidines in toxin activity in vitro and in a murine model. Infect. Immun. 62, 1843-1847 (1994).
47. Morton H. E., Shoemaker J.: The identification of Neisseria gonorrhoeae by means of bacterial variation and the detection of small colony forms in clinical material. J Bacteriol. 50, 585-587 (1945).
48. National Food Institute, Technical University of Denmark: Multiplex PCR for the detection of the mecA gene; http://www. eurlar. eu/data/images/meca-pcr_protocol%2006. 02. 08. pdf (2008).
49. Oliver A., Cantón R., Campo P., Baquero F., Blázquez J.: High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science288, 1251-1254 (2000).
50. Proctor R. A., VAN Langevelde P., Kristjansson M., Maslow J. N., Arbeit R. D.: Persistent and relapsing infections associated with small colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20, 95-102 (1995).
51. Proctor R. A., Kah B., VON Eiff C., Vaudaux P. E., Lew D. P., Peters G.: Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin. Inf. Dis. 27, S68-S74 (1998).
52. Proctor R. A., VON Eiff C., Kahl B. C., Becker K., McNamara P., Herrmann M., Peters G.: Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4, 295-305 (2006).
53. Quie P. G.: Microcolonies (G variants) of Staphylococcus aureus. Yale J. Biol. Med. 41, 394-403 (1969).
54. Sabat A., Malachova N., Miedzobrodzki J., Hryniewicz W.: Comparison of PCR-based methods for typing Staphylococcus aureus isolates. J. Clin. Microbiol. 44, 3804-3807 (2006).
55. Sadowska B., Bonar A., VON Eiff C., Proctor R. A., Chmiela M., Rudnicka W., Róźalska B.: Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol. Med. Microbiol. 32, 191-197 (2002).
56. Schaaff F., Bierbaum G., Baumert N., Bartmann P., Sahl H. G.: Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus. Internat. J. Med. Microbiol. 293, 427-435 (2003).
57. Schneider M., Mühlemann K., Droz S., Couzinet S., Casaulta C., Zimmerli S.: Clinical characteristics associated with isolation of small-colony variants of Staphylococcus aureus and Pseudomonas aeruginosa from respiratory secretions of patients with cystic fibrosis. J. Clin. Microbiol. 46, 1832-1834 (2008).
58. Schnitzer R. J., Canagni L. J., Back M.: Resistence of small colony variants (G forms) of a Staphylococcus toward the bacteriostatic activity of penicillin. Proc. Soc. Exp. Biol. Med. 53, 75-78 (1943).
59. Seggewiss J., Becker K., Kotte O., Eisenacher M., Yazdi M. R., Fischer A., McNamara P., AL Laham N., Proctor R. A., Peters G., Heinemann M., VON Eiff C.: Reporter metabolite analysis of a trancriptional 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 (2006).
60. Seifert H., VON Eiff C., Fätkenheuer G.: Fatal case due to methicillin-resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg. Infect. Dis. 5, 450-453 (1999).
61. Seifert H., Oltmanns D., Becker K., Wisplinghoff H, VON Eiff C.: Staphylococcus lugdunensis pacemaker-related infection. Emerg. Infect. Dis. 11, 1283-1286 (2005).
62. Sendi P., Proctor R. A.: Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol. 17, 54-58 (2009).
63. Sherris J. C.: Two small colony variants of Staphylococcus aureus isolated in pure culture from closed infected lesions and their carbon dioxide requirements. J. Clin. Pathol. 5, 354-355 (1952).
64. Sinha B., Fraunholz M.: Staphylococcus aureus host cell invasion and post-invasion events. Internat. J. Med. Microbiol. 300, 170-175 (2010).
65. Sinha B., Herrmann M.: Mechanism and consequences of invasion of endothelial cells by S. aureus. Tromb. Haemost. 94, 266-277 (2005).
66. Stokes J. L., Bayne H. G.: Dwarf colony mutant of Salmonellae. J. Bacteriol. 76, 136-141 (1958).
67. Tebbutt T. M., Coleman D. J.: Evaluation of some methods for the laboratory examination of sputum. J. Clin. Pathol. 31, 724-729 (1978).
68. 2-dependent Staphylococcus. J. Clin. Pathol. 8, 288-291 (1955).
69. Tuchscherr L., Heitmann V., Hussain M., Viemann D., Roth J., VON Eiff C., Peters G., Becker K., Löffler B.: Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J. Infect. Dis. 202, 1031-1040 (2010).
70. Vesga O., Groeschel M. C., Otten M. F., Brar D. W., Vann J. M., Proctor R. A.: Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis. 173, 739-742 (1996).
71. Wise R. I., Spink W. W.: The influence of antibiotics on the origin of small colonies (G variants) of Micrococcus pyogenes var. aureus. 45th Annual Meet. American Society for Clinical Investigation (1953).
72. Youmans G. P., Delves E.: The effect of inorganic salts on the production of small colony variants by Staphylococcus aureus. J. Bacteriol. 44, 127-136 (1942).