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Published in: BMC Infectious Diseases 1/2020

01-12-2020 | Antibiotic | Research article

Staphylococcal species less frequently isolated from human clinical specimens - are they a threat for hospital patients?

Authors: Magdalena Szemraj, Magdalena Grazul, Ewa Balcerczak, Eligia M. Szewczyk

Published in: BMC Infectious Diseases | Issue 1/2020

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Abstract

Background

Coagulase-negative staphylococci belonging to S. haemolyticus, S. hominis subsp. hominis, S. simulans, and S. warneri are often described as etiological factors of infections. Staphylococci are a phylogenetically coherent group; nevertheless, there are differences among the species which may be important to clinicians.

Methods

We investigated selected virulence factors and antibiotic resistance that were phenotypically demonstrated, the presence and expression of genes encoding the virulence factors, and the type of the SCCmec cassette.

Results

The differences between the tested species were revealed. A great number of isolates produced a biofilm and many of them contained single icaADBC operon genes. Clear differences between species in the lipolytic activity spectrum could be related to their ability to cause various types of infections. Our studies also revealed the presence of genes encoding virulence factors homologous to S. aureus in the analysed species such as enterotoxin and pvl genes, which were also expressed in single isolates of S. simulans and S. warneri. S. haemolyticus and S. hominis subsp. hominis isolates were resistant to all clinically important antibiotics including ß-lactams. The identified SCCmec cassettes belonged to IV, V, VII, and IX type but most of the detected cassettes were non-typeable. Among the investigated species, S. hominis subsp. hominis isolates accumulated virulence genes typical for S. aureus in the most efficient way and were widely resistant to antibiotics.

Conclusions

Our results clearly indicated significant differences between the tested species, which might be a result of the horizontal gene transfer (HGT) and can lead to the formation and selection of multi-drug resistant strains as well as strains with new virulence features. Such strains can have a new clinical relevance.
Literature
1.
go back to reference Lamers RP, Muthukrishnan G, Castoe TA, Tafur S, Cole AM, Parkinson CL. Phylogenetic relationships among Staphylococcus species and refinement of cluster groups based on multilocus data. BMC Evol Biol. 2012;12:171.PubMedPubMedCentralCrossRef Lamers RP, Muthukrishnan G, Castoe TA, Tafur S, Cole AM, Parkinson CL. Phylogenetic relationships among Staphylococcus species and refinement of cluster groups based on multilocus data. BMC Evol Biol. 2012;12:171.PubMedPubMedCentralCrossRef
2.
go back to reference Barros EM, Lemos M. Souto-Padro’n T, Giambiagi-deMarval M. phenotypic and genotypic characterization of biofilm formation in Staphylococcus haemolyticus. Curr Microbiol. 2015;70(6):829–34.PubMedCrossRef Barros EM, Lemos M. Souto-Padro’n T, Giambiagi-deMarval M. phenotypic and genotypic characterization of biofilm formation in Staphylococcus haemolyticus. Curr Microbiol. 2015;70(6):829–34.PubMedCrossRef
3.
go back to reference Hitzenbichler F, Simon M, Salzberger B, Hanses F. Clinical significance of coagulase-negative staphylococci other than S. epidermidis blood stream isolates at a tertiary care hospital. Infection. 2017;45(2):179–86.PubMedCrossRef Hitzenbichler F, Simon M, Salzberger B, Hanses F. Clinical significance of coagulase-negative staphylococci other than S. epidermidis blood stream isolates at a tertiary care hospital. Infection. 2017;45(2):179–86.PubMedCrossRef
5.
go back to reference Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y, et al. Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol. 2005;187(21):7292–308.PubMedPubMedCentralCrossRef Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y, et al. Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol. 2005;187(21):7292–308.PubMedPubMedCentralCrossRef
6.
go back to reference Barros EM, Ceotto H, Bastos MCF, Dos Santos KRN, Giambiagi-Demarval M. Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol. 2012;50(1):166–8.PubMedPubMedCentralCrossRef Barros EM, Ceotto H, Bastos MCF, Dos Santos KRN, Giambiagi-Demarval M. Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol. 2012;50(1):166–8.PubMedPubMedCentralCrossRef
7.
go back to reference Czekaj T, Ciszewski M, Szewczyk EM. Staphylococcus haemolyticus - an emerging threat in the twilight of the antibiotics age. Microbiology. 2015;161(11):2061–8.PubMedCrossRef Czekaj T, Ciszewski M, Szewczyk EM. Staphylococcus haemolyticus - an emerging threat in the twilight of the antibiotics age. Microbiology. 2015;161(11):2061–8.PubMedCrossRef
8.
go back to reference Al Wohoush I, Rivera J, Cairo J, Hachem R, Raad I. Comparing clinical and microbiological methods for the diagnosis of true bacteraemia among patients with multiple blood cultures positive for coagulase-negative staphylococci. Clin Microbiol Infect. 2011;17(4):569–71.PubMedCrossRef Al Wohoush I, Rivera J, Cairo J, Hachem R, Raad I. Comparing clinical and microbiological methods for the diagnosis of true bacteraemia among patients with multiple blood cultures positive for coagulase-negative staphylococci. Clin Microbiol Infect. 2011;17(4):569–71.PubMedCrossRef
9.
go back to reference Mendoza-Olazarán S, Morfin-Otero R, Rodríguez-Noriega E, Llaca-Díaz J, Flores-Treviño S, González-González GM, Villarreal-Treviño L, Garza-González E. Microbiological and molecular characterization of Staphylococcus hominis isolates from blood. PLoS One. 2013;8(4):e61161.PubMedPubMedCentralCrossRef Mendoza-Olazarán S, Morfin-Otero R, Rodríguez-Noriega E, Llaca-Díaz J, Flores-Treviño S, González-González GM, Villarreal-Treviño L, Garza-González E. Microbiological and molecular characterization of Staphylococcus hominis isolates from blood. PLoS One. 2013;8(4):e61161.PubMedPubMedCentralCrossRef
10.
go back to reference Frickmann H, Hahn A, Skusa R, Mund N, Viehweger V, Köller T, et al. Comparison of the etiological relevance of Staphylococcus haemolyticus and Staphylococcus hominis. Eur J Clin Microbiol Infect Dis. 2018;37(8):1539–45.PubMedCrossRef Frickmann H, Hahn A, Skusa R, Mund N, Viehweger V, Köller T, et al. Comparison of the etiological relevance of Staphylococcus haemolyticus and Staphylococcus hominis. Eur J Clin Microbiol Infect Dis. 2018;37(8):1539–45.PubMedCrossRef
11.
go back to reference Peel TN, Cheng AC, Buising KL, Choong PF. Microbiological aetiology, epidemiology, and clinical profile of prosthetic joint infections: are current antibiotic prophylaxis guidelines effective? Antimicrob Agents Chemother. 2012;56(5):2386–91.PubMedPubMedCentralCrossRef Peel TN, Cheng AC, Buising KL, Choong PF. Microbiological aetiology, epidemiology, and clinical profile of prosthetic joint infections: are current antibiotic prophylaxis guidelines effective? Antimicrob Agents Chemother. 2012;56(5):2386–91.PubMedPubMedCentralCrossRef
12.
go back to reference von Eiff C, Arciola CR, Montanaro L, Becker K, Campoccia D. Emerging Staphylococcus species as new pathogens in implant infections. Int J Artif Organs. 2006;29(4):360–7.CrossRef von Eiff C, Arciola CR, Montanaro L, Becker K, Campoccia D. Emerging Staphylococcus species as new pathogens in implant infections. Int J Artif Organs. 2006;29(4):360–7.CrossRef
13.
14.
go back to reference Mohan N, Iyer MN, Wirostko WJ, Kim SH, Simons KB. Staphylococcus hominis endophthalmitis associated with a capsular hypopyon. Am J Ophthalmol. 2005;139(5:930–2. Mohan N, Iyer MN, Wirostko WJ, Kim SH, Simons KB. Staphylococcus hominis endophthalmitis associated with a capsular hypopyon. Am J Ophthalmol. 2005;139(5:930–2.
15.
go back to reference Kline DA. Staphylococcus simulans osteomyelitis of the foot: a case report. Foot Ankle Online J. 2010;3(1):4.CrossRef Kline DA. Staphylococcus simulans osteomyelitis of the foot: a case report. Foot Ankle Online J. 2010;3(1):4.CrossRef
16.
go back to reference Marrie TJ, Kwan C, Noble MA, West A, Duffield L. Staphylococcus saprophyticus as a cause of urinary tract infections. J Clin Microbiol. 1982;16(3):4.CrossRef Marrie TJ, Kwan C, Noble MA, West A, Duffield L. Staphylococcus saprophyticus as a cause of urinary tract infections. J Clin Microbiol. 1982;16(3):4.CrossRef
18.
go back to reference Vallianou N, Evangelopoulos A, Makri P, Zacharias G, Stefanitsi P, Karachalios A, Avgerinos PC. Vertebral osteomyelitis and native valve endocarditis due to Staphylococcus simulans: a case report. J Med Case Rep. 2008;2:183.PubMedPubMedCentralCrossRef Vallianou N, Evangelopoulos A, Makri P, Zacharias G, Stefanitsi P, Karachalios A, Avgerinos PC. Vertebral osteomyelitis and native valve endocarditis due to Staphylococcus simulans: a case report. J Med Case Rep. 2008;2:183.PubMedPubMedCentralCrossRef
19.
go back to reference Barnham M, Horton R, Smith JMP, Richardson J, Marples RR, Reith S. Methicillin-resistant Staphylococcus simulans masquerading as MRSA in a nursing home. J Hosp Infect. 1996;34(4):331–7.PubMedCrossRef Barnham M, Horton R, Smith JMP, Richardson J, Marples RR, Reith S. Methicillin-resistant Staphylococcus simulans masquerading as MRSA in a nursing home. J Hosp Infect. 1996;34(4):331–7.PubMedCrossRef
20.
go back to reference Torre D, Ferraro G, Fiori GP, Martegani R, Speranza F, Tambini R, Zeroli C. Ventriculatrial shunt infection caused by Staphylococcus warneri: case report and review. Clin Infect Dis. 1992;14(1):49–52.PubMedCrossRef Torre D, Ferraro G, Fiori GP, Martegani R, Speranza F, Tambini R, Zeroli C. Ventriculatrial shunt infection caused by Staphylococcus warneri: case report and review. Clin Infect Dis. 1992;14(1):49–52.PubMedCrossRef
21.
go back to reference Ivić I, Karanović J, Pavičić-Ivelja M. Sepsis with multiple abscesses caused by Staphylococcus warneri: a case report. Cent Eur J Med. 2013;8(1):45–7. Ivić I, Karanović J, Pavičić-Ivelja M. Sepsis with multiple abscesses caused by Staphylococcus warneri: a case report. Cent Eur J Med. 2013;8(1):45–7.
22.
go back to reference Campoccia D, Montanaro L, Visai L, Corazzari T, Poggio C, Pegreffi F, et al. Characterization of 26 Staphylococcus warneri isolates from orthopedic infections. Int J Artif Organs. 2010;33(9):575–81.PubMedCrossRef Campoccia D, Montanaro L, Visai L, Corazzari T, Poggio C, Pegreffi F, et al. Characterization of 26 Staphylococcus warneri isolates from orthopedic infections. Int J Artif Organs. 2010;33(9):575–81.PubMedCrossRef
23.
go back to reference Cimiotti JP, Haas JP, Della-Latta P, Wu F, Saiman L, Larson EL. Prevalence and clinical relevance of Staphylococcus warneri in the neonatal intensive care unit. Infect Control Hosp Epidemiol. 2007;28(3):326–30.PubMedPubMedCentralCrossRef Cimiotti JP, Haas JP, Della-Latta P, Wu F, Saiman L, Larson EL. Prevalence and clinical relevance of Staphylococcus warneri in the neonatal intensive care unit. Infect Control Hosp Epidemiol. 2007;28(3):326–30.PubMedPubMedCentralCrossRef
24.
go back to reference Ohara-Nemoto Y, Haraga H, Kimura S, Nemoto TK. Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. J Med Microbiol. 2008;57(1):95–9.PubMedCrossRef Ohara-Nemoto Y, Haraga H, Kimura S, Nemoto TK. Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. J Med Microbiol. 2008;57(1):95–9.PubMedCrossRef
25.
go back to reference Shin JH, Kim SH, Jeong HS, Oh SH, Kim HR, Lee JN, Yoon YC, Kim YW, Kim YH. Identification of coagulase-negative staphylococci isolated from continuous ambulatory peritoneal dialysis fluid using 16S ribosomal RNA, tuf, and sodA gene sequencing. Perit Dial Int. 2011;31(3):340–6.PubMedCrossRef Shin JH, Kim SH, Jeong HS, Oh SH, Kim HR, Lee JN, Yoon YC, Kim YW, Kim YH. Identification of coagulase-negative staphylococci isolated from continuous ambulatory peritoneal dialysis fluid using 16S ribosomal RNA, tuf, and sodA gene sequencing. Perit Dial Int. 2011;31(3):340–6.PubMedCrossRef
26.
go back to reference Spanu T, Sanguinetti M, Ciccaglione D, D’Inzeo T, Romano L, Leone F, Fadda G. Use of the VITEK 2 system for rapid identification of clinical isolates of staphylococci from bloodstream infections. J Clin Microbiol. 2003;41(9):4259–63.PubMedPubMedCentralCrossRef Spanu T, Sanguinetti M, Ciccaglione D, D’Inzeo T, Romano L, Leone F, Fadda G. Use of the VITEK 2 system for rapid identification of clinical isolates of staphylococci from bloodstream infections. J Clin Microbiol. 2003;41(9):4259–63.PubMedPubMedCentralCrossRef
27.
go back to reference Blaiotta G, Casaburi A, Villani F. Identification and differentiation of Staphylococcus carnosus and Staphylococcus simulans by species-specific PCR assays of sodA genes. Syst Appl Microbiol. 2005;28(6):519–26.PubMedCrossRef Blaiotta G, Casaburi A, Villani F. Identification and differentiation of Staphylococcus carnosus and Staphylococcus simulans by species-specific PCR assays of sodA genes. Syst Appl Microbiol. 2005;28(6):519–26.PubMedCrossRef
28.
go back to reference Hirotaki S, Sasaki T, Kuwahara-Arai K, Hiramatsu K. Rapid and accurate identification of human-associated staphylococci by use of multiplex PCR. J Clin Microbiol. 2011;49(10):3627–31.PubMedPubMedCentralCrossRef Hirotaki S, Sasaki T, Kuwahara-Arai K, Hiramatsu K. Rapid and accurate identification of human-associated staphylococci by use of multiplex PCR. J Clin Microbiol. 2011;49(10):3627–31.PubMedPubMedCentralCrossRef
29.
go back to reference Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF. Melton, Beachey EH. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol. 1985;22(6):996–1006.PubMedPubMedCentralCrossRef Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF. Melton, Beachey EH. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol. 1985;22(6):996–1006.PubMedPubMedCentralCrossRef
31.
go back to reference Zhang K, Mcclure J, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome. Microbiology. 2005;43(10):5026–33. Zhang K, Mcclure J, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome. Microbiology. 2005;43(10):5026–33.
32.
go back to reference Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother. 2007;51(1):264–74.PubMedCrossRef Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother. 2007;51(1):264–74.PubMedCrossRef
33.
go back to reference Oliveira DC, Milheiriço C, De Lencastre H. Redefining a structural variant of staphylococcal cassette chromosome mec, SCCmec type VI. Antimicrob Agents Chemother. 2006;50(10):3457–9.PubMedPubMedCentralCrossRef Oliveira DC, Milheiriço C, De Lencastre H. Redefining a structural variant of staphylococcal cassette chromosome mec, SCCmec type VI. Antimicrob Agents Chemother. 2006;50(10):3457–9.PubMedPubMedCentralCrossRef
34.
go back to reference Zhang L, Thomas JC, Miragaia M, Bouchami O, Chaves F, d'Azevedo PA, et al. Multilocus sequence typing and further genetic characterization of the enigmatic pathogen, Staphylococcus hominis. 2013;8(6):PLoS One, e66496 2013. Zhang L, Thomas JC, Miragaia M, Bouchami O, Chaves F, d'Azevedo PA, et al. Multilocus sequence typing and further genetic characterization of the enigmatic pathogen, Staphylococcus hominis. 2013;8(6):PLoS One, e66496 2013.
35.
go back to reference International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother. 2009;53(12):4961–7. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother. 2009;53(12):4961–7.
36.
go back to reference Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70(2):631–41.PubMedPubMedCentralCrossRef Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70(2):631–41.PubMedPubMedCentralCrossRef
37.
go back to reference Ünal N, Çinar OD. Detection of stapylococcal enterotoxin, methicillin-resistant and Panton–valentine leukocidin genes in coagulase-negative staphylococci isolated from cows and ewes with subclinical mastitis. Trop Anim Health Prod. 2012;44(2):369–75.PubMedCrossRef Ünal N, Çinar OD. Detection of stapylococcal enterotoxin, methicillin-resistant and Panton–valentine leukocidin genes in coagulase-negative staphylococci isolated from cows and ewes with subclinical mastitis. Trop Anim Health Prod. 2012;44(2):369–75.PubMedCrossRef
38.
go back to reference Arciola CR, Gamberini S, Campoccia D, Visai L, Speziale P, Baldassarri L, Montanaro L. A multiplex PCR method for the detection of all five individual genes of Ica locus in Staphylococcus epidermidis. A survey of 400 clinical isolates from prosthesis-associated infections. J Biomed Mater Res. 2005;75(2):408–13.CrossRef Arciola CR, Gamberini S, Campoccia D, Visai L, Speziale P, Baldassarri L, Montanaro L. A multiplex PCR method for the detection of all five individual genes of Ica locus in Staphylococcus epidermidis. A survey of 400 clinical isolates from prosthesis-associated infections. J Biomed Mater Res. 2005;75(2):408–13.CrossRef
39.
go back to reference de Vos P, Garrity G, Jones D, Krieg N, Ludwig W, Rainey F, Whitman SK, W. Berge’s manual of determinative bacteriology. The Firmicutes. Dordrecgt Heidelberg, New York: Springer; 2009. de Vos P, Garrity G, Jones D, Krieg N, Ludwig W, Rainey F, Whitman SK, W. Berge’s manual of determinative bacteriology. The Firmicutes. Dordrecgt Heidelberg, New York: Springer; 2009.
40.
go back to reference Naushad S, Barkema HW, Luby C, Condas LAZ, Nobrega DB, Carson DA, DeBuck J. Comprehensive phylogenetic analysis of bovine non-aureus staphylococci species basedon whole-genome sequencing. Front Microbiol. 2016;7:1990.PubMedPubMedCentralCrossRef Naushad S, Barkema HW, Luby C, Condas LAZ, Nobrega DB, Carson DA, DeBuck J. Comprehensive phylogenetic analysis of bovine non-aureus staphylococci species basedon whole-genome sequencing. Front Microbiol. 2016;7:1990.PubMedPubMedCentralCrossRef
41.
go back to reference Even S, Leroy S, Charlier C, Zakour NB, Chacornac JP, Lebert I, et al. Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented food stuffs. Int J Food Microbiol. 2010;139(1–2):87–95.PubMedCrossRef Even S, Leroy S, Charlier C, Zakour NB, Chacornac JP, Lebert I, et al. Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented food stuffs. Int J Food Microbiol. 2010;139(1–2):87–95.PubMedCrossRef
42.
go back to reference Gao P, Wang Y, Villanueva I, Ho PL, Davies J, Kao RYT. Construction of a multiplex promoter reporter platform to monitor Staphylococcus aureus virulence gene expression and the identification of usnic acid as a potent suppressor of psm gene expression. Front Microbiol. 2016;7:1344.PubMedPubMedCentral Gao P, Wang Y, Villanueva I, Ho PL, Davies J, Kao RYT. Construction of a multiplex promoter reporter platform to monitor Staphylococcus aureus virulence gene expression and the identification of usnic acid as a potent suppressor of psm gene expression. Front Microbiol. 2016;7:1344.PubMedPubMedCentral
43.
go back to reference Pinheiro L, Brito CI, de Oliveira A, Martins PY, Pereira VC, da Cunha Mde L. Staphylococcus epidermidis and Staphylococcus haemolyticus: molecular detection of cytotoxin and enterotoxin genes. Toxins. 2015;7(9):3688–99.PubMedPubMedCentralCrossRef Pinheiro L, Brito CI, de Oliveira A, Martins PY, Pereira VC, da Cunha Mde L. Staphylococcus epidermidis and Staphylococcus haemolyticus: molecular detection of cytotoxin and enterotoxin genes. Toxins. 2015;7(9):3688–99.PubMedPubMedCentralCrossRef
44.
go back to reference Darouiche R. Device-associated infections: a macroproblem that starts with microadher- ence. Clin Infect Dis. 2001;33(9):1567–72.PubMedCrossRef Darouiche R. Device-associated infections: a macroproblem that starts with microadher- ence. Clin Infect Dis. 2001;33(9):1567–72.PubMedCrossRef
45.
go back to reference Jain A, Agarwal A. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J Microbiol Methods. 2009;76(1):88–92.PubMedCrossRef Jain A, Agarwal A. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J Microbiol Methods. 2009;76(1):88–92.PubMedCrossRef
46.
go back to reference Cardile AP, Sanchez CJ, Samberg ME Jr, Romano DR, Hardy SK, Wenke JC, Murray CK, Akers KS. Human plasma enhances the expression of staphylococcal microbial surface components recognizing adhesive matrix molecules promoting biofilm formation and increases antimicrobial tolerance in vitro. BMC Res Notes. 2014;7:457.PubMedPubMedCentralCrossRef Cardile AP, Sanchez CJ, Samberg ME Jr, Romano DR, Hardy SK, Wenke JC, Murray CK, Akers KS. Human plasma enhances the expression of staphylococcal microbial surface components recognizing adhesive matrix molecules promoting biofilm formation and increases antimicrobial tolerance in vitro. BMC Res Notes. 2014;7:457.PubMedPubMedCentralCrossRef
47.
48.
go back to reference Mertens A, Ghebremedhin B. Genetic determinants and biofilm formation of clinical Staphylococcus epidermidis isolates from blood cultures and indwelling devises. Eur J Microbiol Immunol. 2013;3(2):111–9.CrossRef Mertens A, Ghebremedhin B. Genetic determinants and biofilm formation of clinical Staphylococcus epidermidis isolates from blood cultures and indwelling devises. Eur J Microbiol Immunol. 2013;3(2):111–9.CrossRef
49.
go back to reference Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, Otto M. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem. 2004;279:54881–6.PubMedCrossRef Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, Otto M. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem. 2004;279:54881–6.PubMedCrossRef
50.
go back to reference Ziebuhr W, Heilmann C, Geotz F, Meyer P, Wilms K, Straube E, Hacker J. Detection of the intercellular adhesion gene cluster (Ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun. 1997;65(3):890–6.PubMedPubMedCentralCrossRef Ziebuhr W, Heilmann C, Geotz F, Meyer P, Wilms K, Straube E, Hacker J. Detection of the intercellular adhesion gene cluster (Ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun. 1997;65(3):890–6.PubMedPubMedCentralCrossRef
51.
go back to reference Bowden MG, Visai L, Longshaw CM, Holland KT, Speziale P, Hook M. Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin? J Biol Chem. 2002;8(45):43017–23.CrossRef Bowden MG, Visai L, Longshaw CM, Holland KT, Speziale P, Hook M. Is the GehD lipase from Staphylococcus epidermidis a collagen binding adhesin? J Biol Chem. 2002;8(45):43017–23.CrossRef
52.
go back to reference Coenye T, Peeters E, Nelis HJ. Biofilm formation by Propionibacterium acnes is associated with increased resistance to antimicrobial agents and increased production of putative virulence factors. Res Microbiol. 2007;158(4):386–92.PubMedCrossRef Coenye T, Peeters E, Nelis HJ. Biofilm formation by Propionibacterium acnes is associated with increased resistance to antimicrobial agents and increased production of putative virulence factors. Res Microbiol. 2007;158(4):386–92.PubMedCrossRef
53.
go back to reference Burkhart CG. Clinical assessment of acne pathogenesis with treatment implications. Int Pediatr. 2003;18:14–9. Burkhart CG. Clinical assessment of acne pathogenesis with treatment implications. Int Pediatr. 2003;18:14–9.
54.
go back to reference Bojar RA, Holland KT. Review: the human cutaneous microflora and factors controlling colonization. World J Microbiol Biotechnol. 2002;18(9):889–903.CrossRef Bojar RA, Holland KT. Review: the human cutaneous microflora and factors controlling colonization. World J Microbiol Biotechnol. 2002;18(9):889–903.CrossRef
55.
go back to reference Delekta PC, Shook JC, Lydic TA, Mulks MH, Hammer ND. Staphylococcus aureus utilizes host-derived lipoprotein particles as sources of exogenous fatty acids. J Bacteriol. 2018;200(11):e00728–17.PubMedPubMedCentralCrossRef Delekta PC, Shook JC, Lydic TA, Mulks MH, Hammer ND. Staphylococcus aureus utilizes host-derived lipoprotein particles as sources of exogenous fatty acids. J Bacteriol. 2018;200(11):e00728–17.PubMedPubMedCentralCrossRef
56.
go back to reference Rollof J, Hedström SA, Nilsson-Ehle P. Lipolytic activity of Staphylococcus aureus strains from disseminated and localized infections. Acta Pathol Microbiol Immunol Scand B. 1987;95(2):109–13.PubMed Rollof J, Hedström SA, Nilsson-Ehle P. Lipolytic activity of Staphylococcus aureus strains from disseminated and localized infections. Acta Pathol Microbiol Immunol Scand B. 1987;95(2):109–13.PubMed
57.
go back to reference Parsons JB, Frank MW, Subramanian C, Saenkham P, Rock CO. Metabolic basis for the differential susceptibility of gram-positive pathogens to fatty acid synthesis inhibitors. Proc Natl Acad Sci U S A. 2011;108(37):15378–83.PubMedPubMedCentralCrossRef Parsons JB, Frank MW, Subramanian C, Saenkham P, Rock CO. Metabolic basis for the differential susceptibility of gram-positive pathogens to fatty acid synthesis inhibitors. Proc Natl Acad Sci U S A. 2011;108(37):15378–83.PubMedPubMedCentralCrossRef
58.
go back to reference van Kampen MD, Rosenstein R, Götz F, Egmond MR. Cloning, purification and characterisation of Staphylococcus warneri lipase 2. Biochim Biophys Acta. 2001;1544(1–2):229–41.PubMedCrossRef van Kampen MD, Rosenstein R, Götz F, Egmond MR. Cloning, purification and characterisation of Staphylococcus warneri lipase 2. Biochim Biophys Acta. 2001;1544(1–2):229–41.PubMedCrossRef
59.
go back to reference Rosenstein R, Götz F. Staphylococcal lipases: biochemical and molecular characterization. Biochimie. 2000;82(11):1005–14.PubMedCrossRef Rosenstein R, Götz F. Staphylococcal lipases: biochemical and molecular characterization. Biochimie. 2000;82(11):1005–14.PubMedCrossRef
60.
go back to reference Simons JW, van Kampen MD, Riel S, Götz F, Egmond MR, Verheij HM. Cloning, purification and characterisation of the lipase from Staphylococcus epidermidis-comparison of the substrate selectivity with those of other microbial lipases. Eur J Biochem. 1998;253(3):675–83.PubMedCrossRef Simons JW, van Kampen MD, Riel S, Götz F, Egmond MR, Verheij HM. Cloning, purification and characterisation of the lipase from Staphylococcus epidermidis-comparison of the substrate selectivity with those of other microbial lipases. Eur J Biochem. 1998;253(3):675–83.PubMedCrossRef
61.
go back to reference Lina G, Bohach GA, Nair SP, Hiramatsu K, Jouvin-Marche E, Mariuzza R. International nomenclature Committee for Staphylococcal Superantigens. Standard nomenclature for the superantigens expressed by staphylococcus. J Infect Dis. 2004;189(12):2334–6.PubMedCrossRef Lina G, Bohach GA, Nair SP, Hiramatsu K, Jouvin-Marche E, Mariuzza R. International nomenclature Committee for Staphylococcal Superantigens. Standard nomenclature for the superantigens expressed by staphylococcus. J Infect Dis. 2004;189(12):2334–6.PubMedCrossRef
62.
go back to reference Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J. Involvement of Pan ton-valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis. 1999;29(5):1128–32.PubMedCrossRef Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J. Involvement of Pan ton-valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis. 1999;29(5):1128–32.PubMedCrossRef
63.
go back to reference Prevost G, Couppie P, Prevost P, Gayet S, Petiau P, Cribier B, Monteil H, Piemont Y. Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J Med Microbiol. 1995;42(4):237–45.PubMedCrossRef Prevost G, Couppie P, Prevost P, Gayet S, Petiau P, Cribier B, Monteil H, Piemont Y. Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J Med Microbiol. 1995;42(4):237–45.PubMedCrossRef
64.
go back to reference Gonzalez BE, Teruya J, Mahoney DH Jr, Hulten KG, Edwards R, Lamberth LB, Hammerman WA, Mason EO Jr, Kaplan SL. Venous thrombosis associated with staphylococcal osteomyelitis in children. Pediatrics. 2006;117(5):1673–9.PubMedCrossRef Gonzalez BE, Teruya J, Mahoney DH Jr, Hulten KG, Edwards R, Lamberth LB, Hammerman WA, Mason EO Jr, Kaplan SL. Venous thrombosis associated with staphylococcal osteomyelitis in children. Pediatrics. 2006;117(5):1673–9.PubMedCrossRef
65.
go back to reference Sheikh HQ, Aqil A, Kirby A, Hossain FS. Panton-valentine leukocidin osteomyelitis in children: a growing threat. Br J Hosp Med (Lond). 2015;76(1):18–24.CrossRef Sheikh HQ, Aqil A, Kirby A, Hossain FS. Panton-valentine leukocidin osteomyelitis in children: a growing threat. Br J Hosp Med (Lond). 2015;76(1):18–24.CrossRef
66.
go back to reference Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, et al. Association between Staphylococcus aureus strains carrying gene for Panton-valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet. 2002;359(9308):753–9.PubMedCrossRef Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, et al. Association between Staphylococcus aureus strains carrying gene for Panton-valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet. 2002;359(9308):753–9.PubMedCrossRef
67.
go back to reference Shallcross LJ, Fragaszy E, Johnson AM, Hayward AC. Te role of the Panton-valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. Lancet Infect Dis. 2013;13(1):43–54.PubMedPubMedCentralCrossRef Shallcross LJ, Fragaszy E, Johnson AM, Hayward AC. Te role of the Panton-valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. Lancet Infect Dis. 2013;13(1):43–54.PubMedPubMedCentralCrossRef
68.
go back to reference David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616–87.PubMedPubMedCentralCrossRef David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616–87.PubMedPubMedCentralCrossRef
69.
go back to reference Schmitz FJ, MacKenzie CR, Geisel R, Wagner S, Idel H, Verhoef J, Hadding U, Heinz HP. Enterotoxin and toxic shock syndrome toxin-1 production of methicillin resistant and methicillin sensitive Staphylococcus aureus strains. Eur J Epidemiol. 1997;13(6):699–708.PubMedCrossRef Schmitz FJ, MacKenzie CR, Geisel R, Wagner S, Idel H, Verhoef J, Hadding U, Heinz HP. Enterotoxin and toxic shock syndrome toxin-1 production of methicillin resistant and methicillin sensitive Staphylococcus aureus strains. Eur J Epidemiol. 1997;13(6):699–708.PubMedCrossRef
70.
go back to reference Tremaine MT, Brockman DK, Betley MJ. Staphylococcal enterotoxin a gene (sea) expression is not affected by the accessory gene regulator (agr). Infect Immun. 1993;61(1):356–9.PubMedPubMedCentralCrossRef Tremaine MT, Brockman DK, Betley MJ. Staphylococcal enterotoxin a gene (sea) expression is not affected by the accessory gene regulator (agr). Infect Immun. 1993;61(1):356–9.PubMedPubMedCentralCrossRef
71.
go back to reference Omoe K, Hu DL, Takahashi-Omoe H, Hanane A, Shinagawa K. Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett. 2005;246(2):191–8.PubMedCrossRef Omoe K, Hu DL, Takahashi-Omoe H, Hanane A, Shinagawa K. Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett. 2005;246(2):191–8.PubMedCrossRef
73.
go back to reference Fluit AC, Carpaij N, Majoor EA, Bonten MJM, Willems RJL. Shared reservoir of ccrB gene sequences between coagulase-negative staphylococci and methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother. 2013;68(8):1707–13.PubMedCrossRef Fluit AC, Carpaij N, Majoor EA, Bonten MJM, Willems RJL. Shared reservoir of ccrB gene sequences between coagulase-negative staphylococci and methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother. 2013;68(8):1707–13.PubMedCrossRef
74.
go back to reference Kloos WE, George CG, Olgiate JS, Van Pelt L, McKinnon ML, Zimmer BL, Muller E, Weinstein MP, Mirrett S. Staphylococcus hominis subsp. novobiosepticus subsp. nov. a novel trehaloseand N-acetyl-D-glucosamine-negative, novobiocin-and multiple-antibiotic-resistant subspecies isolated from human blood cultures. Int J Syst Bacteriol. 1998;48(3):799–812.PubMedCrossRef Kloos WE, George CG, Olgiate JS, Van Pelt L, McKinnon ML, Zimmer BL, Muller E, Weinstein MP, Mirrett S. Staphylococcus hominis subsp. novobiosepticus subsp. nov. a novel trehaloseand N-acetyl-D-glucosamine-negative, novobiocin-and multiple-antibiotic-resistant subspecies isolated from human blood cultures. Int J Syst Bacteriol. 1998;48(3):799–812.PubMedCrossRef
75.
go back to reference Szemraj M, Czekaj T, Kalisz J, Szewczyk EM. Differences in distribution of MLS antibiotics resistance genes in clinical isolates of staphylococci belonging to species: S. epidermidis, S. hominis, S. haemolyticus, S. simulans and S. warneri. BMC Microbiol. 2019;19:124.PubMedPubMedCentralCrossRef Szemraj M, Czekaj T, Kalisz J, Szewczyk EM. Differences in distribution of MLS antibiotics resistance genes in clinical isolates of staphylococci belonging to species: S. epidermidis, S. hominis, S. haemolyticus, S. simulans and S. warneri. BMC Microbiol. 2019;19:124.PubMedPubMedCentralCrossRef
76.
go back to reference Soumya K, Roopashree S, Balasubrahmanya HV. Prevalence and antibiogram of methicillin resistant Staphylococcus aureus in a tertiary care Centre in Tumkur. India Int J Curr Microbiol App Sci. 2017;6(9):2236–43. Soumya K, Roopashree S, Balasubrahmanya HV. Prevalence and antibiogram of methicillin resistant Staphylococcus aureus in a tertiary care Centre in Tumkur. India Int J Curr Microbiol App Sci. 2017;6(9):2236–43.
77.
go back to reference Martínez-Meléndez A, Morfín-Otero R, Villarreal-Treviño L, González-González G, Llaca-Díaz J, Rodríguez-Noriega E, Camacho-Ortíze A, Garza-González E. Staphylococcal cassette chromosome mec (SCCmec) in coagulase negative staphylococci. Med Univ. 2015;17(69):229–33. Martínez-Meléndez A, Morfín-Otero R, Villarreal-Treviño L, González-González G, Llaca-Díaz J, Rodríguez-Noriega E, Camacho-Ortíze A, Garza-González E. Staphylococcal cassette chromosome mec (SCCmec) in coagulase negative staphylococci. Med Univ. 2015;17(69):229–33.
78.
go back to reference Panda S, Kar S, Sharma S, Singh DV. Multidrug-resistant Staphylococcus haemolyticus isolates from infected eyes and healthy conjunctivae in India. J Glob Antimicrob Resist. 2016;6:154–9.PubMedCrossRef Panda S, Kar S, Sharma S, Singh DV. Multidrug-resistant Staphylococcus haemolyticus isolates from infected eyes and healthy conjunctivae in India. J Glob Antimicrob Resist. 2016;6:154–9.PubMedCrossRef
79.
go back to reference Szczuka E, Kaznowski A. Zróżnicowanie kaset SCCmec u metycylinoopornych gronkowców koagulazo-ujemnych. Postępy Mikrobiol. 2014;53(3):223–8. Szczuka E, Kaznowski A. Zróżnicowanie kaset SCCmec u metycylinoopornych gronkowców koagulazo-ujemnych. Postępy Mikrobiol. 2014;53(3):223–8.
80.
go back to reference Mendoza-Olazarán S, Morfin-Otero R, Villarreal-Trevino L, Rodriguez-Noriega E, Llaca-Diaz J, Camacho-Ortiz A, González GM, Casillas-Vega N, Garza-González E. Antibiotic susceptibility of biofilm cells and molecular characterisation of staphylococcus hominis isolates from blood. PLoS One. 2015;10(12):1–13.CrossRef Mendoza-Olazarán S, Morfin-Otero R, Villarreal-Trevino L, Rodriguez-Noriega E, Llaca-Diaz J, Camacho-Ortiz A, González GM, Casillas-Vega N, Garza-González E. Antibiotic susceptibility of biofilm cells and molecular characterisation of staphylococcus hominis isolates from blood. PLoS One. 2015;10(12):1–13.CrossRef
81.
go back to reference Silva NCC, Guimarães FF, Manzi MDP, Gómez-Sanz E, Gómez P, Araújo JP, Langoni H, Rall VL, Torres C. Characterization of methicillin-resistant coagulase-negative staphylococci in milk from cows with mastitis in Brazil. Antonie Van Leeuwenhoek. 2014;106(2):227–33.PubMedCrossRef Silva NCC, Guimarães FF, Manzi MDP, Gómez-Sanz E, Gómez P, Araújo JP, Langoni H, Rall VL, Torres C. Characterization of methicillin-resistant coagulase-negative staphylococci in milk from cows with mastitis in Brazil. Antonie Van Leeuwenhoek. 2014;106(2):227–33.PubMedCrossRef
82.
go back to reference Zong Z, Peng C, Lü X. Diversity of SCCmec elements in methicillin-resistant coagulase-negative staphylococci clinical isolates. PLoS One. 2011;6(5):1–6.CrossRef Zong Z, Peng C, Lü X. Diversity of SCCmec elements in methicillin-resistant coagulase-negative staphylococci clinical isolates. PLoS One. 2011;6(5):1–6.CrossRef
Metadata
Title
Staphylococcal species less frequently isolated from human clinical specimens - are they a threat for hospital patients?
Authors
Magdalena Szemraj
Magdalena Grazul
Ewa Balcerczak
Eligia M. Szewczyk
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Antibiotic
Published in
BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-020-4841-2

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