Small colony variants (SCVs) of Staphylococcus aureus – A bacterial survival strategy

Kahl, Barbara C.

doi:10.1016/j.meegid.2013.05.016

Cited by 118Antimicrobial Resistance in StaphylococcusBacterial Genetics and BiotechnologyBacterial biofilms and quorum sensing

Small colony variants (SCVs) of Staphylococcus aureus – A bacterial survival strategy

Kahl, Barbara C.·2014·Infection, Genetics and Evolution

DOI 10.1016/j.meegid.2013.05.016

Open this paper in CoChat — free account

Abstract

Small colony variants (SCVs) of Staphylococcus aureus have been implicated in chronic recurrent infections and have therefore gained renewed interest during the last decade. Moreover, SCVs have been shown to be part of the regular growth cycle, are highly dynamic or stable and can be selected during various harsh conditions. As such, the emergence of SCVs has been described not only in human, but also in veterinary medicine as well as in food microbiology. SCVs are characterized by impaired growth, down-regulation of genes for metabolism and virulence, while sigB and genes important for persistence and biofilm formation are up-regulated. Furthermore, SCVs are resistant to various antibiotics such as aminoglycosides, trimethoprim-sulfamethoxazole, fluorquinolones, fusidic acid or even to antiseptics such as triclosan. An underlying mechanism has been determined for hemin-, menadione- and thymidine-dependent SCVs as well as for SCVs which are impaired in their stress response. SCVs are optimized for persistence in the host. They are able to reverse and thereby constitute a highly dynamic subpopulation of S. aureus. Such phenotype switching constitutes an integral part of the infection process enabling the bacteria to hide inside the host cell without eliciting a strong host response.

Integrity signals

Registry

Crossref · 10.1016/j.meegid.2013.05.016

Cites

100 of 100 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

This correlates with the clinical evidence that SCVs are able to persist in host tissues, resisting clearance by immune cells that expose the pathogen to the oxidative burst.
“This correlates with the clinical evidence that SCVs are able to persist in host tissues, resisting clearance by immune cells that expose the pathogen to the oxidative burst (1–14, 36, 37).”
From Staphylococcus aureus Adapts to Oxidative Stress by Producing H 2 O 2 -Resistant Small-Colony Variants via the SOS Response (2015) · cites this paper as [6]

High Frequency of Hypermutable Pseudomonas aeruginosa in Cystic Fibrosis Lung Infection
Oliver, A., Cantón, R., Campo, P., Baquero, F., & Blázquez, J. (2000) · Science · doi:10.1126/science.288.5469.1251 · Cited by 1,466 · see citing works
Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections
Proctor, R. A., von Eiff, C., Kahl, B. C., Becker, K., McNamara, P., Herrmann, M., & Peters, G. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1384 · Cited by 1,175 · see citing works
Self-citation
Self-generated diversity produces “insurance effects” in biofilm communities
Boles, B. R., Thoendel, M., & Singh, P. K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407460101 · Cited by 665 · see citing works
Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa
Hoffman, L. R., Déziel, É., D’Argenio, D. A., Lepine, F. L., Emerson, J., McNamara, S., Gibson, R. L., Ramsey, B. W., & Miller, S. I. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606756104 · Cited by 470 · see citing works
Treatment of lung infection in patients with cystic fibrosis: Current and future strategies
Döring, G., Flume, P. A., Heijerman, H. G. M., & Elborn, J. S. (2012) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2012.10.004 · Cited by 468 · see citing works
Persistent and Relapsing Infections Associated with Small-Colony Variants of Staphylococcus aureus
Proctor, R. A., van Langevelde, P., Kristjansson, M., Maslow, J. N., & Arbeit, R. D. (1995) · Clinical Infectious Diseases · doi:10.1093/clinids/20.1.95 · Cited by 437 · see citing works
Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection
Tuchscherr, L., Medina, E., Hussain, M., Völker, W., Heitmann, V., Niemann, S., Holzinger, D., Roth, J., Proctor, R. A., Becker, K., et al. (2011) · EMBO Molecular Medicine · doi:10.1002/emmm.201000115 · Cited by 437 · see citing works
Persistent Infection with Small Colony Variant Strains of Staphylococcus aureus in Patients with Cystic Fibrosis
Kahl, B., Herrmann, M., Everding, A. S., Koch, H. G., Becker, K., Harms, E., Proctor, R. A., & Peters, G. (1998) · Journal of Infectious Diseases · doi:10.1086/515238 · Cited by 357 · see citing works
Self-citation
Whole-Genome Sequencing of Staphylococcus haemolyticus Uncovers the Extreme Plasticity of Its Genome and the Evolution of Human-Colonizing Staphylococcal Species
Takeuchi, F., Watanabe, S., Baba, T., Yuzawa, H., Ito, T., Morimoto, Y., Kuroda, M., Cui, L., Takahashi, M., Ankai, A., et al. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.21.7292-7308.2005 · Cited by 331 · see citing works
A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly
von Eiff, C., Heilmann, C., Proctor, R. A., Woltz, C., Peters, G., & Götz, F. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.15.4706-4712.1997 · Cited by 310 · see citing works
Staphylococcus aureus as an intracellular pathogen: the role of small colony variants
Sendi, P., & Proctor, R. A. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2008.11.004 · Cited by 281 · see citing works
Staphylococcus aureus Small‐Colony Variants Are Adapted Phenotypes for Intracellular Persistence
Tuchscherr, L., Heitmann, V., Hussain, M., Viemann, D., Roth, J., von Eiff, C., Peters, G., Becker, K., & Löffler, B. (2010) · The Journal of Infectious Diseases · doi:10.1086/656047 · Cited by 275 · see citing works
Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study
Singh, R., Ray, P., Das, A., & Sharma, M. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.009720-0 · Cited by 262 · see citing works
Genome-wide antisense transcription drives mRNA processing in bacteria
Lasa, Í., Toledo‐Arana, A., Dobin, A., Villanueva, M., Mozos, I. R. D. L., Vergara-Irigaray, M., Segura, V., Fagegaltier, D., Penadés, J. R., Valle, J., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113521108 · Cited by 249 · see citing works
Small-Colony Variants of Pseudomonas aeruginosa in Cystic Fibrosis
Rohde, M. (1999) · Clinical Infectious Diseases · doi:10.1086/598644 · Cited by 239 · see citing works
Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells
Balwit, J. M., Langevelde, P. V., Vann, J. M., & Proctor, R. A. (1994) · Journal of Infectious Diseases · doi:10.1093/infdis/170.4.1033 · Cited by 237 · see citing works
Antibacterial Household Products: Cause for Concern
Levy, S. B. (2001) · Emerging infectious diseases · doi:10.3201/eid0707.017705 · Cited by 231 · see citing works
Two Novel Point Mutations in Clinical Staphylococcus aureus Reduce Linezolid Susceptibility and Switch on the Stringent Response to Promote Persistent Infection
Gao, W., Chua, K., Davies, J. K., Newton, H. J., Seemann, T., Harrison, P. F., Holmes, N. E., Rhee, H., Hong, J., Hartland, E. L., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000944 · Cited by 218 · see citing works
High Rate of Macrolide Resistance in Staphylococcus aureus Strains from Patients with Cystic Fibrosis Reveals High Proportions of Hypermutable Strains
Prunier, A., Malbruny, B., Laurans, M., Brouard, J., Duhamel, J.-F., & Leclercq, R. (2003) · The Journal of Infectious Diseases · doi:10.1086/374937 · Cited by 198 · see citing works
Small-Colony Variant Selection as a Survival Strategy for Staphylococcus aureus in the Presence of Pseudomonas aeruginosa
Biswas, L., Biswas, R., Schlag, M., Bertram, R., & Götz, F. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01211-09 · Cited by 182 · see citing works
Staphylococcus aureus Small Colony Variants Are Induced by the Endothelial Cell Intracellular Milieu
Vesga, Ó., Groeschel, M., Otten, M. F., Brar, D. W., Vann, J. M., & Proctor, R. A. (1996) · The Journal of Infectious Diseases · doi:10.1093/infdis/173.3.739 · Cited by 178 · see citing works
Antibiotic activity against small-colony variants of Staphylococcus aureus: review of in vitro, animal and clinical data
Garcia, L. G., Lemaire, S., Kahl, B. C., Becker, K., Proctor, R. A., Denis, O., Tulkens, P. M., & Van Bambeke, F. (2013) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkt072 · Cited by 177 · see citing works
Self-citation
Activation of Hypoxia Inducible Factor 1 Is a General Phenomenon in Infections with Human Pathogens
Werth, N., Beerlage, C., Rosenberger, C., Yazdi, A. S., Edelmann, M., Amr, A., Bernhardt, W. M., von Eiff, C., Becker, K., Schäfer, A., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011576 · Cited by 173 · see citing works
Staphylococcus aureus sigma B-dependent emergence of small-colony variants and biofilm production following exposure to Pseudomonas aeruginosa 4-hydroxy-2-heptylquinoline-N-oxide
Mitchell, G., Séguin, D. L., Asselin, A.-E., Déziel, E., Cantin, A. M., Frost, E. H., Michaud, S., & Malouin, F. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-33 · Cited by 165 · see citing works
Prevalence and Clinical Significance of Staphylococcus aureus Small-Colony Variants in Cystic Fibrosis Lung Disease
Besier, S. M., Smaczny, C., von Mallinckrodt, C., Krahl, A., Ackermann, H., Brade, V., & Wichelhaus, T. A. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.01510-06 · Cited by 164 · see citing works
Intraoperative Handling and Wound Healing: Controlled Clinical Trial Comparing Coated VICRYL® Plus Antibacterial Suture (Coated Polyglactin 910 Suture with Triclosan) with Coated VICRYL® Suture (Coated Polyglactin 910 Suture)
Ford, H. R., Jones, P., Gaines, B. A., et al. (2005) · Surgical Infections · doi:10.1089/sur.2005.6.313 · Cited by 144 · see citing works
Variant subpopulations of Staphylococcus aureus as cause of persistent and recurrent infections.
Proctor, R. A., Balwit, J. M., & Vesga, Ó. (1994) · PubMed · Cited by 139 · see citing works
Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus
Massey, R. C., Buckling, A. G. J., & Peacock, S. J. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00507-3 · Cited by 138 · see citing works
Physiological Characterization of a Heme-Deficient Mutant of Staphylococcus aureus by a Proteomic Approach
Köhler, C., von Eiff, C., Peters, G., Proctor, R. A., Hecker, M., & Engelmann, S. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.23.6928-6937.2003 · Cited by 133 · see citing works
Small colony variants of Staphylococcus aureus — review
Melter, O., & Radojevič, B. (2010) · Folia Microbiologica · doi:10.1007/s12223-010-0089-3 · Cited by 132 · see citing works
Physiology and Antibiotic Susceptibility of Staphylococcus aureus Small Colony Variants
Baumert, N., von Eiff, C., Schaaff, F., Peters, G., Proctor, R. A., & Sahl, H.-G. (2002) · Microbial Drug Resistance · doi:10.1089/10766290260469507 · Cited by 130 · see citing works
Phenotype Microarray Profiling of Staphylococcus aureus menD and hemB Mutants with the Small-Colony-Variant Phenotype
von Eiff, C., McNamara, P. J., Becker, K., Bates, D. M., Lei, X.-H., Ziman, M., Bochner, B. R., Peters, G., & Proctor, R. A. (2005) · Journal of Bacteriology · doi:10.1128/jb.188.2.687-693.2006 · Cited by 129 · see citing works
In Vivo Mutations of Thymidylate Synthase (Encoded by thyA ) Are Responsible for Thymidine Dependency in Clinical Small-Colony Variants of Staphylococcus aureus
Chatterjee, I., Kriegeskorte, A., Fischer, A., Deiwick, S., Theimann, N., Proctor, R. A., Peters, G., Herrmann, M., & Kahl, B. C. (2007) · Journal of Bacteriology · doi:10.1128/jb.00912-07 · Cited by 126 · see citing works
Self-citation
Transcription of Virulence Factors in Staphylococcus aureus Small-Colony Variants Isolated from Cystic Fibrosis Patients Is Influenced by SigB
Moisan, H., Brouillette, E., Jacob, C. L., Langlois-Bégin, P., Michaud, S., & Malouin, F. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.1.64-76.2006 · Cited by 116 · see citing works
Genetic and Phenotypic Identification of Fusidic Acid-Resistant Mutants with the Small-Colony-Variant Phenotype in Staphylococcus aureus
Norström, T., Lannergård, J., & Hughes, D. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00328-07 · Cited by 108 · see citing works
Identification of the Genetic Basis for Clinical Menadione-Auxotrophic Small-Colony Variant Isolates of Staphylococcus aureus
Lannergård, J., von Eiff, C., Sander, G., Cordes, T., Seggewiβ, J., Peters, G., Proctor, R. A., Becker, K., & Hughes, D. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00668-08 · Cited by 108 · see citing works
Thymidine-Dependent Staphylococcus aureus Small-Colony Variants Are Associated with Extensive Alterations in Regulator and Virulence Gene Expression Profiles
Kahl, B. C., Belling, G., Becker, P., Chatterjee, I., Wardecki, K., Hilgert, K., Cheung, A. L., Peters, G., & Herrmann, M. (2005) · Infection and Immunity · doi:10.1128/iai.73.7.4119-4126.2005 · Cited by 102 · see citing works
Self-citation
Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus
Schaaff, F., Bierbaum, G., Baumert, N., Bartmann, P., & Sahl, H. (2003) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00282 · Cited by 98 · see citing works
Biosynthesis of Nucleotides
Ross, C. W. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-675406-3.50010-4 · Cited by 97 · see citing works
Molecular analysis of the thymidine-auxotrophic small colony variant phenotype of Staphylococcus aureus
Besier, S., Ludwig, A., Ohlsen, K., Brade, V., & Wichelhaus, T. A. (2007) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2007.02.003 · Cited by 94 · see citing works
Thymidine-Dependent Small-Colony Variants of Staphylococcus aureus Exhibit Gross Morphological and Ultrastructural Changes Consistent with Impaired Cell Separation
Kahl, B. C., Belling, G., Reichelt, R., Herrmann, M., Proctor, R. A., & Peters, G. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.1.410-413.2003 · Cited by 92 · see citing works
Self-citation
Small colony variants of Staphylococcus aureus reveal distinct protein profiles
Kriegeskorte, A., König, S., Sander, G., Pirkl, A., Mahabir, E., Proctor, R. A., von Eiff, C., Peters, G., & Becker, K. (2011) · PROTEOMICS · doi:10.1002/pmic.201000796 · Cited by 89 · see citing works
Prevalence of thymidine-dependent Staphylococcus aureus in patients with cystic fibrosis
Gilligan, P. H., Gage, P. A., Welch, D. F., Muszynski, M. J., & Wait, K. J. (1987) · Journal of Clinical Microbiology · doi:10.1128/jcm.25.7.1258-1261.1987 · Cited by 87 · see citing works
Single and Combination Antibiotic Therapy of Staphylococcus aureus Experimental Endocarditis: Emergence of Gentamicin-Resistant Mutants
Miller, M. H., Wexler, M. A., & Steigbigel, N. H. (1978) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.14.3.336 · Cited by 85 · see citing works
The Thymidine-Dependent Small-Colony-Variant Phenotype Is Associated with Hypermutability and Antibiotic Resistance in Clinical Staphylococcus aureus Isolates
Besier, S. M., Zander, J., Kahl, B. C., Kraiczy, P., Brade, V., & Wichelhaus, T. A. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01395-07 · Cited by 85 · see citing works
Self-citation
Small Colony Variants of Staphylococcus aureus and Pacemaker-related Infection
Seifert, H., Wisplinghoff, H., Schnabel, P., & von Eiff, C. (2003) · Emerging infectious diseases · doi:10.3201/eid0910.0302000 · Cited by 84 · see citing works
Phenotype Switching Is a Natural Consequence of Staphylococcus aureus Replication
Edwards, A. M. (2012) · Journal of Bacteriology · doi:10.1128/jb.00948-12 · Cited by 83 · see citing works
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
Seggewiß, J., Becker, K., Kotte, O., Eisenacher, M., Yazdi, M. R. K., Fischer, A., McNamara, P. J., Laham, N. A., Proctor, R. A., Peters, G., et al. (2006) · Journal of Bacteriology · doi:10.1128/jb.00774-06 · Cited by 83 · see citing works
Staphylocidal action of thrombin-induced platelet microbicidal protein is not solely dependent on transmembrane potential
Koo, S.-P., Bayer, A. S., Sahl, H., Proctor, R. A., & Yeaman, M. R. (1996) · Infection and Immunity · doi:10.1128/iai.64.3.1070-1074.1996 · Cited by 80 · see citing works
Chronic Prosthetic Hip Infection Caused by a Small-Colony Variant of Escherichia coli
Roggenkamp, A., Sing, A., Hornef, M. W., Brunner, U. H., Autenrieth, I. B., & Heesemann, J. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.9.2530-2534.1998 · Cited by 76 · see citing works
Effect of Low Temperature on Growth and Ultra-Structure of Staphylococcus spp
Onyango, L. A., Dunstan, R. H., Gottfries, J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029031 · Cited by 72 · see citing works
A role for sigma factor B in the emergence of Staphylococcus aureus small-colony variants and elevated biofilm production resulting from an exposure to aminoglycosides
Mitchell, G., Brouillette, É., Séguin, D. L., Asselin, A.-E., Jacob, C. L., & Malouin, F. (2009) · Microbial Pathogenesis · doi:10.1016/j.micpath.2009.10.003 · Cited by 71 · see citing works
Fatal Outcome of Lung Transplantation in Cystic Fibrosis Patients due to Small-Colony Variants of the Burkholderia cepacia Complex
Häußler, S., Lehmann, C., Breselge, C., et al. (2003) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-003-0901-y · Cited by 70 · see citing works
The Effect of Environmental Conditions on Biofilm Formation of Burkholderia pseudomallei Clinical Isolates
Ramli, N. S. K., Chua, E. G., Nathan, S., & Vadivelu, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044104 · Cited by 69 · see citing works
Fatal Case Due to Methicillin-Resistant Staphylococcus aureus Small Colony Variants in an AIDS Patient
Seifert, H., von Eiff, C., & Fätkenheuer, G. (1999) · Emerging infectious diseases · doi:10.3201/eid0503.990319 · Cited by 68 · see citing works
Tomatidine Inhibits Replication of Staphylococcus aureus Small-Colony Variants in Cystic Fibrosis Airway Epithelial Cells
Mitchell, G., Gattuso, M., Grondin, G., Marsault, É., Bouarab, K., & Malouin, F. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01468-10 · Cited by 67 · see citing works
Prevalence and genetic diversity of Staphylococcus aureus small-colony variants in cystic fibrosis patients
Yağcı, S., Hasçelik, G., Doğru, D., Özçelik, U., & Şener, B. (2011) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2011.03742.x · Cited by 64 · see citing works
Enhanced production of exopolysaccharide matrix and biofilm by a menadione-auxotrophic Staphylococcus aureus small-colony variant
Singh, R., Ray, P., Das, A., & Sharma, M. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.017046-0 · Cited by 64 · see citing works
Intracellular Activity of Antibiotics in a Model of Human THP-1 Macrophages Infected by a Staphylococcus aureus Small-Colony Variant Strain Isolated from a Cystic Fibrosis Patient: Pharmacodynamic Evaluation and Comparison with Isogenic Normal-Phenotype and Revertant Strains
Nguyen, H. A., Denis, O., Vergison, A., Theunis, A., Tulkens, P. M., Struelens, M. J., & Françoise Van Bambeke, A. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01145-08 · Cited by 62 · see citing works
Genetic Determinants of Resistance to Fusidic Acid among Clinical Bacteremia Isolates of Staphylococcus aureus
Lannergård, J., Norström, T., & Hughes, D. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00871-08 · Cited by 60 · see citing works
Characterization of a Staphylococcus aureus Small Colony Variant (SCV) Associated with Persistent Bovine Mastitis
Atalla, H., Gyles, C. L., Jacob, C. L., Moisan, H., Malouin, F., & Mallard, B. A. (2008) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2008.0110 · Cited by 59 · see citing works
Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antiseptics
Bayston, R., Ashraf, W., & Smith, T. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm031 · Cited by 59 · see citing works
Staphylococcus aureus small colony variants are resistant to the antimicrobial peptide lactoferricin B
Samuelsen, Ø., Haukland, H. H., Kahl, B. C., von Eiff, C., Proctor, R. A., Ulvatne, H., Sandvik, K., & Vorland, L. H. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki385 · Cited by 58 · see citing works
Self-citation
Evaluation of Different Methods To Detect Methicillin Resistance in Small-Colony Variants of Staphylococcus aureus
Kipp, F., Becker, K., Peters, G., & von Eiff, C. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.3.1277-1279.2004 · Cited by 58 · see citing works
Staphylococcus aureus SigB activity promotes a strong fibronectin–bacterium interaction which may sustain host tissue colonization by small‐colony variants isolated from cystic fibrosis patients
Mitchell, G., Lamontagne, C., Brouillette, É., Grondin, G., Talbot, B. G., Grandbois, M., & Malouin, F. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06511.x · Cited by 58 · see citing works
Characterization of Clinical Enterococcus faecalis Small-Colony Variants
Wellinghausen, N., Chatterjee, I., Berger, A., et al. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.00485-09 · Cited by 56 · see citing works
Highly resistant Burkholderia pseudomallei small colony variants isolated in vitro and in experimental melioidosis
Häußler, S., Rohde, M., & Steinmetz, I. (1999) · Medical Microbiology and Immunology · doi:10.1007/s004300050110 · Cited by 55 · see citing works
Recurrent Ventriculoperitoneal Shunt Infection Caused by Small-Colony Variants of Staphylococcus aureus
Spanu, T., Romano, L., D’Inzeo, T., Masucci, L., Albanese, A., Papacci, F., Marchese, E., Sanguinetti, M., & Fadda, G. (2005) · Clinical Infectious Diseases · doi:10.1086/432577 · Cited by 54 · see citing works
Staphylococcus aureussmall colony variants (SCVs) and their role in disease
Atalla, H., Gyles, C. L., & Mallard, B. A. (2011) · Animal Health Research Reviews · doi:10.1017/s1466252311000065 · Cited by 53 · see citing works
Evaluation of Two Chromogenic Agar Media for Recovery and Identification of Staphylococcus aureus Small-Colony Variants
Kipp, F., Kahl, B. C., Becker, K., Baron, E. J., Proctor, R. A., Peters, G., & von Eiff, C. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.4.1956-1959.2005 · Cited by 53 · see citing works
Self-citation
Small-colony variants: a novel mechanism for triclosan resistance in methicillin-resistant Staphylococcus aureus
Seaman, P. F., Ochs, D., & Day, M. J. (2006) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkl450 · Cited by 51 · see citing works
Clinical and Molecular Characteristics of Infections with CO 2 -Dependent Small-Colony Variants of Staphylococcus aureus
Gómez-González, C., Acosta, J., Villa, J., Barrado, L., Sanz, F., Orellana, M. Á., Otero, J. R., & Cháves, F. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.00520-10 · Cited by 49 · see citing works
Studies on Small Colony Variants of Staphylococcus aureus
Swingle, E. L. (1935) · Journal of Bacteriology · doi:10.1128/jb.29.5.467-489.1935 · Cited by 48 · see citing works
Detection of Staphylococcus aureus by 16S rRNA directed in situ hybridisation in a patient with a brain abscess caused by small colony variants
Kipp, F. (2003) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.74.7.1000 · Cited by 48 · see citing works
Small-Colony Mutants of Staphylococcus aureus Allow Selection of Gyrase-Mediated Resistance to Dual-Target Fluoroquinolones
Pan, X.-S., Hamlyn, P. J., Taléns‐Visconti, R., Alovero, F. L., Manzo, R. H., & Fisher, L. M. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.8.2498-2506.2002 · Cited by 47 · see citing works
Virulent gentamicin-induced small colony variants of Staphylococcus aureus.
Ll, P., Richardson, M. D., & Feist, M. D. (1979) · PubMed · Cited by 46 · see citing works
The development of high hydrostatic pressure processes as an alternative to other pathogen reduction methods
Demazeau, G., & Rivalain, N. (2011) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2011.05000.x · Cited by 45 · see citing works
Pharmacodynamic Evaluation of the Activity of Antibiotics against Hemin- and Menadione-Dependent Small-Colony Variants of Staphylococcus aureus in Models of Extracellular (Broth) and Intracellular (THP-1 Monocytes) Infections
Garcia, L. G., Lemaire, S., Kahl, B. C., Becker, K., Proctor, R. A., Denis, O., Tulkens, P. M., & Françoise Van Bambeke, A. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00285-12 · Cited by 44 · see citing works
Self-citation
Osteopetrosis, femoral fracture, and chronic osteomyelitis caused by Staphylococcus aureus small colony variants (SCV) treated by girdlestone resection – 6-year follow-up
Rolauffs, B., Bernhardt, T. M., von Eiff, C., Hart, M. L., & Bettin, D. (2002) · Archives of Orthopaedic and Trauma Surgery · doi:10.1007/s00402-002-0435-2 · Cited by 43 · see citing works
National survey of molecular epidemiology of Staphylococcus aureus colonization in Belgian cystic fibrosis patients
Vergison, A., Denis, O., Deplano, A., Casimir, G. E., Claeys, G., DeBaets, F., DeBoeck, K., Douat, N., Franckx, H., Gigi, J., et al. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm037 · Cited by 42 · see citing works
Orientation and expression of methicillin-resistant Staphylococcus aureus small RNAs by direct multiplexed measurements using the nCounter of NanoString technology
Beaume, M. G., Hernández, D., Docquier, M., et al. (2011) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2010.12.025 · Cited by 41 · see citing works
Growth requirements of some small-colony-forming variants of Staphylococcus aureus
Kaplan, M., & Dye, W. E. (1976) · Journal of Clinical Microbiology · doi:10.1128/jcm.4.4.343-348.1976 · Cited by 41 · see citing works
Altered Growth, Pigmentation, and Antimicrobial Susceptibility Properties of Staphylococcus aureus Due to Loss of the Major Cold Shock Gene cspB
Duval, B. D., Mathew, A., Satola, S. W., & Shafer, W. M. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01786-09 · Cited by 40 · see citing works
Thymidine Auxotrophic Staphylococcus aureus Small-Colony Variant Endocarditis and Left Ventricular Assist Device Infection
Maduka-Ezeh, A. N., Seville, M. T., Kusne, S., Vikram, H. R., Blair, J. E., Greenwood‐Quaintance, K. E., Arabía, F. A., & Patel, R. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.01170-11 · Cited by 39 · see citing works
Intracellular Activity of Antibiotics in a Model of Human THP-1 Macrophages Infected by a Staphylococcus aureus Small-Colony Variant Strain Isolated from a Cystic Fibrosis Patient: Study of Antibiotic Combinations
Nguyen, H. A., Denis, O., Vergison, A., Tulkens, P. M., Struelens, M. J., & Françoise Van Bambeke, A. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01146-08 · Cited by 39 · see citing works
Fusidic acid in bone and joint infections
Atkins, B. L., & Gottlieb, T. (1999) · International Journal of Antimicrobial Agents · doi:10.1016/s0924-8579(98)00077-6 · Cited by 38 · see citing works
Thymidine-Dependent Staphylococcus aureus Small-Colony Variants: Human Pathogens That Are Relevant Not Only in Cases of Cystic Fibrosis Lung Disease
Besier, S. M., Zander, J., Siegel, E., Saum, S. H., Hunfeld, K., Ehrhart, A., Brade, V., & Wichelhaus, T. A. (2008) · Journal of Clinical Microbiology · doi:10.1128/jcm.01440-08 · Cited by 35 · see citing works
Genetic Complexity of Fusidic Acid-Resistant Small Colony Variants (SCV) in Staphylococcus aureus
Lannergård, J., Cao, S., Norström, T., Delgado, A., Gustafson, J. E., & Hughes, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028366 · Cited by 30 · see citing works
Piezotolerant Small-Colony Variants with Increased Thermotolerance, Antibiotic Susceptibility, and Low Invasiveness in a Clonal Staphylococcus aureus Population
Karatzas, K. A. G., Zervos, A., Tassou, C. C., Mallidis, C. G., & Humphrey, T. J. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01801-06 · Cited by 30 · see citing works
Characteristics of quinolone-induced small colony variants in Staphylococcus aureus
Mitsuyama, J., Yamada, H., Maehana, J., et al. (1997) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/39.6.697 · Cited by 28 · see citing works
The characteristics of intramucosal bacteria in chronic rhinosinusitis: a prospective cross‐sectional analysis
Kim, R., Freeman, J. T., Waldvogel‐Thurlow, S., et al. (2012) · International Forum of Allergy & Rhinology · doi:10.1002/alr.21117 · Cited by 24 · see citing works
Comparative in vitro activity of finafloxacin against staphylococci displaying normal and small colony variant phenotypes
Idelevich, E. A., Kriegeskorte, A., Stubbings, W. J., Kahl, B. C., Peters, G., & Becker, K. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkr393 · Cited by 24 · see citing works
Self-citation
Antibody and cell-mediated immune responses to Staphylococcus aureus small colony variants and their parental strains associated with bovine mastitis
Atalla, H., Wilkie, B. N., Gyles, C. L., et al. (2010) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2010.07.005 · Cited by 21 · see citing works
Characteristics of Staphylococcus aureus Small Colony Variant and Its Parent Strain Isolated from Chronic Mastitis at a Dairy Farm in Beijing, China
Alkasir, R., Liu, X., Zahra, M., Ferreri, M., Su, J., & Han, B. R. (2012) · Microbial Drug Resistance · doi:10.1089/mdr.2012.0086 · Cited by 21 · see citing works
Extracellular and intracellular bactericidal activities of XF-70 against small-colony variant hemB mutants of meticillin-susceptible and meticillin-resistant Staphylococcus aureus
Vaudaux, P. E., Huggler, E., Rhys‐Williams, W., Love, W. G., & Lew, D. P. (2011) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2011.01.015 · Cited by 9 · see citing works
Thymidine-dependent Strain ofSalmonella osloSelected by Trimethoprim–Sulfamethoxazole Therapy
McCarthy, L. R., Chmel, H., Bell, G., et al. (1977) · American Journal of Clinical Pathology · doi:10.1093/ajcp/68.2.307 · Cited by 9 · see citing works
Drug‐eluting biomaterials in urology: the time is ripe
Knudsen, B. E., Chew, B. H., & Denstedt, J. D. (2005) · British Journal of Urology · doi:10.1111/j.1464-410x.2005.05388.x · Cited by 6 · see citing works
The Biosynthesis of Nucleotides
Cohen, G. N. (2014) · Springer eBooks · doi:10.1007/978-94-017-8908-0_33 · Cited by 6 · see citing works
Thymidine-dependent meticillin-resistant Staphylococcus aureus: a potentially unrecognized reservoir of MRSA in hospital patients?
Cleeve, V., Perry, J. D., Cresswell, G., et al. (2006) · Journal of Hospital Infection · doi:10.1016/j.jhin.2005.11.009 · Cited by 5 · see citing works
Characterization of Staphylococcus aureus strains isolated from cystic fibrosis patients by conventional and molecular typing.
Sadowska, B., Cochard, T., Poutrel, B., et al. (2001) · PubMed · Cited by 4 · see citing works

Flagged first, then by citations

Sorted by citations

Staphylococcus aureus Adapts to Oxidative Stress by Producing H 2 O 2 -Resistant Small-Colony Variants via the SOS Response
Painter, K. L., Strange, E., Parkhill, J., Bamford, K. B., Armstrong-James, D., & Edwards, A. M. (2015) · Infection and Immunity · doi:10.1128/iai.03016-14 · Cited by 153 · see citing works
Inactivation of thyA in Staphylococcus aureus Attenuates Virulence and Has a Strong Impact on Metabolism and Virulence Gene Expression
Kriegeskorte, A., Block, D., Drescher, M., Windmüller, N., Mellmann, A., Baum, C., Neumann, C., Lorè, N. I., Bragonzi, A., Liebau, E., et al. (2014) · mBio · doi:10.1128/mbio.01447-14 · Cited by 89 · see citing works
Self-citation
The Agr Quorum-Sensing System Regulates Fibronectin Binding but Not Hemolysis in the Absence of a Functional Electron Transport Chain
Pader, V., James, E. H., Painter, K. L., Wigneshweraraj, S., & Edwards, A. M. (2014) · Infection and Immunity · doi:10.1128/iai.02254-14 · Cited by 32 · see citing works

Binding and accumulation of hemin in Porphyromonas gingivalis are induced by hemin
Genco, C. A., Odusanya, B. M., & Brown, G. (1994) · Infection and Immunity · doi:10.1128/iai.62.7.2885-2892.1994 · Cited by 77 · see citing works
Hemin uptake in Porphyromonas gingivalis: Omp26 is a hemin-binding surface protein
Bramanti, T. E., & Holt, S. C. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.22.7413-7420.1993 · Cited by 59 · see citing works
Hemin pretreatment inhibits hepatic fibrosis induced by carbon tetrachloride on rat liver
Narita, T., Akamatsu, Y., Moriya, T., et al. (2004) · Kanzo · doi:10.2957/kanzo.45.463
Determination of incorporation of 59fe in hemin of peripheral red blood cells and of red cells in bone marrow cultures
Thunell, S. (1965) · Clinica Chimica Acta · doi:10.1016/0009-8981(65)90222-6 · Cited by 56 · see citing works
Study on the new technology for extracting hemin
Min, L. (2005) · Food Science and Technology International

Authors: Kahl, B. C.
Affiliations: University Hospital Münster (DE)
Corresponding author: Kahl, Barbara C.
ORCID: Kahl, Barbara C.
Venue: Infection, Genetics and Evolution
Publisher: Elsevier BV
Published: 2014-01
Volume: 21
Pages: 515-522
ISSN: 1567-1348 (ISSN-L)
DOI: 10.1016/j.meegid.2013.05.016
OpenAlex: W2078268465
Cited by: 118
References: 100
Citations by year: 2026: 5 · 2025: 7 · 2024: 8 · 2023: 5 · 2022: 8 · 2021: 9 · 2020: 9 · 2019: 11 · 2018: 11 · 2017: 14 · 2016: 10 · 2015: 11 · 2014: 7 · 2013: 3
FWCI: 7.54
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Infection Genetics and Evolution (publishedVersion)
PubMed (publishedVersion)
Funders: Bundesministerium für Bildung und Forschung (0315829B)
Interdisziplinäres Zentrum für Klinische Forschung, Universitätsklinikum Würzburg (Kah2/024/09, SFTR34C7)
Topics: Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Keywords: small colony variants, Staphylococcus aureus, bacterial persistence, antibiotic resistance, phenotypic switching, SigB, biofilm formation, stress response, host cell survival, triclosan resistance, veterinary infections, food microbiology
MeSH terms: Anti-Bacterial Agents, Humans, Phenotype, Staphylococcal Infections, Staphylococcus aureus, Genetic Variation, Virulence, Gene Expression Regulation, Bacterial, Drug Resistance, Bacterial

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Small colony variants (SCVs) of Staphylococcus aureus – A bacterial survival strategy

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks