Skin microbiota: Overview and role in the skin diseases acne vulgaris and rosacea

Future Microbiology

Volumn 8, Issue 2, 2013, Pages 209-222

  Murillo, Nathalia ^a   Raoult, Didier ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

acne; antibiotics; culture independent; hygiene; microbiota; rosacea; skin

Indexed keywords

ANTIBIOTIC AGENT;

ACNE VULGARIS; ARCHAEON; ATOPIC DERMATITIS; BACTERIUM; CULTURE MEDIUM; FUNGUS; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; ROSACEA; SKIN FLORA; STAPHYLOCOCCUS AUREUS; VIRUS;

ACNE VULGARIS; BIOTA; HUMANS; ROSACEA; SKIN; SKIN DISEASES, BACTERIAL;

EID: 84873394521     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.12.141     Document Type: Review

References (86)

1. Nakatsuji T, Gallo RL. Antimicrobial peptides: old molecules with new ideas. J. Invest. Dermatol. 132(3 Pt 2), 887-895 (2012).
2. Gallo RL, Nakatsuji T. Microbial symbiosis with the innate immune defense system of the skin. J. Invest. Dermatol. 131(10), 1974-1980 (2011).
3. Kong HH. Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol. Med. 17(6), 320-328 (2011).
4. Rosenthal M, Goldberg D, Aiello A, Larson E, Foxman B. Skin microbiota: microbial community structure and its potential association with health and disease. Infect. Genet. Evol. 11(5), 839-848 (2011).
5. Grice EA, Kong HH, Renaud G et al. A diversity profile of the human skin microbiota. Genome Res. 18(7), 1043-1050 (2008). (Pubitemid 351931155)
6. Kloos WE, Schleifer KH. Simplified scheme for routine identification of human Staphylococcus species. J. Clin. Microbiol. 1(1), 82-88 (1975).
7. Evans CA. Persistent individual differences in the bacterial flora of the skin of the forehead: numbers of Propionibacteria. J. Invest. Dermatol. 64(1), 42-46 (1975).
8. Gao Z, Tseng CH, Pei Z, Blaser MJ. Molecular analysis of human forearm superficial skin bacterial biota. Proc. Natl Acad. Sci. USA 104(8), 2927-2932 (2007). (Pubitemid 46327980)
9. Yuan S, Cohen DB, Ravel J, Abdo Z, Forney LJ. Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS One 7(3), e33865 (2012).
10. Engelbrektson A, Kunin V, Wrighton KC et al. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J. 4(5), 642-647 (2010).
11. Harris JK, Wagner BD. Bacterial identification and analytic challenges in clinical microbiome studies. J. Allergy Clin. Immunol. 129(2), 441-442 (2012).
12. Dekio I, Hayashi H, Sakamoto M et al. Detection of potentially novel bacterial components of the human skin microbiota using culture-independent molecular profiling. J. Med. Microbiol. 54(Pt 12), 1231-1238 (2005). (Pubitemid 41783833)
13. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5(3), 235-237 (2008). (Pubitemid 351325646)
14. Schloss PD, Gevers D, Westcott SL. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6(12), e27310 (2011).
15. Jumpstart Consortium Human Microbiome Project Data Generation Working Group. Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 7(6), e39315 (2012).
16. Huse SM, Ye Y, Zhou Y, Fodor AA. A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One 7(6), e34242 (2012).
17. Hamady M, Knight R. Microbial community profiling for human microbiome projects: Tools, techniques, and challenges. Genome Res. 19(7), 1141-1152 (2009).
18. Turnbaugh PJ, Ley RE, Hamady M, Fraser- Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 449(7164), 804-810 (2007). (Pubitemid 47598620)
19. Lozupone C, Hamady M, Knight R. UniFrac Y an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7, 371 (2006).
20. Lozupone CA, Knight R. Species divergence and the measurement of microbial diversity. FEMS Microbiol. Rev. 32(4), 557-578 (2008). (Pubitemid 351799685)
21. Schloss PD, Westcott SL, Ryabin T et al. Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75(23), 7537-7541 (2009).
22. Leyden JJ, McGinley KJ, Nordstrom KM, Webster GF. Skin microflora. J. Invest. Dermatol. 88(3 Suppl.), 65s-72s (1987). (Pubitemid 17031727)
23. Grice EA, Segre JA. The skin microbiome. Nat. Rev. Microbiol. 9(4), 244-253 (2011).
24. Foulongne V, Sauvage V, Hebert C et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One 7(6), e38499 (2012).
25. Gao Z, Perez-Perez GI, Chen Y, Blaser MJ. Quantitation of major human cutaneous bacterial and fungal populations. J. Clin. Microbiol. 48(10), 3575-3581 (2010).
26. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 326(5960), 1694-1697 (2009).
27. Grice EA, Kong HH, Conlan S et al. Topographical and temporal diversity of the human skin microbiome. Science 324(5931), 1190-1192 (2009).
28. Staudinger T, Pipal A, Redl B Molecular analysis of the prevalent microbiota of human male and female forehead skin compared to forearm skin and the influence of make-up. J. Appl. Microbiol. 110(6), 1381-1389 (2011).
29. Fierer N, Hamady M, Lauber CL, Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc. Natl Acad. Sci. USA 105(46), 17994-17999 (2008).
30. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486(7402), 207-214 (2012).
31. Sugita T, Suzuki M, Goto S et al. Quantitative analysis of the cutaneous Malassezia microbiota in 770 healthy Japanese by age and gender using a real-time PCR assay. Med. Mycol. 48(2), 229-233 (2010).
32. Zhang E, Tanaka T, Tsuboi R, Makimura K, Nishikawa A, Sugita T. Characterization of Malassezia microbiota in the human external auditory canal and on the sole of the foot. Microbiol. Immunol. 56(4), 238-244 (2012).
33. Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin microbiome early in life. J. Invest. Dermatol. 131(10), 2026-2032 (2011).
34. Kligman AM. An overview of acne. J. Invest. Dermatol. 62(3), 268-287 (1974).
35. Leyden JJ, McGinley KJ, Mills OH, Kligman AM. Age-related changes in the resident bacterial flora of the human face. J. Invest. Dermatol. 65(4), 379-381 (1975).
36. Egert M, Schmidt I, Hohne HM, Lachnit T, Schmitz RA, Breves R. rRNA-based profiling of bacteria in the axilla of healthy males suggests rightYleft asymmetry in bacterial activity. FEMS Microbiol. Ecol. 77(1), 146-153 (2011).
37. Sultana B, Cimiotti J, Aiello AE, Sloan D, Larson E. Effects of age and race on skin condition and bacterial counts on hands of neonatal ICU nurses. Heart Lung 32(4), 283-289 (2003). (Pubitemid 36934519)
38. Dotterud LK, Wilsgaard T, Vorland LH, Falk ES. The effect of UVB radiation on skin microbiota in patients with atopic dermatitis and healthy controls. Int. J. Circumpolar Health 67(2-3), 254-260 (2008).
39. Zhang E, Sugita T, Tsuboi R, Yamazaki T, Makimura K. The opportunistic yeast pathogen Trichosporon asahii colonizes the skin of healthy individuals: Analysis of 380 healthy individuals by age and gender using a nested polymerase chain reaction assay. Microbiol. Immunol. 55(7), 483-488 (2011).
40. Plewig G, Holland KT, Nenoff P. Clinical and bacteriological evaluation of nadifloxacin 1% cream in patients with acne vulgaris: A double-blind, Phase III comparison study versus erythromycin 2% cream. Eur. J. Dermatol. 16(1), 48-55 (2006). (Pubitemid 43219405)
41. Basak PY, Cetin ES, Gurses I, Ozseven AG. The effects of systemic isotretinoin and antibiotic therapy on the microbial floras in patients with acne vulgaris. J. Eur. Acad. Dermatol. Venereol. doi:10.1111/j.1468- 3083.2011.04397.x (2012) (Epub ahead of print).
42. Chon SY, Doan HQ, Mays RM, Singh SM, Gordon RA, Tyring SK. Antibiotic overuse and resistance in dermatology. Dermatol. Ther. 25(1), 55-69 (2012).
43. Ishida N, Nakaminami H, Noguchi N, Kurokawa I, Nishijima S, Sasatsu M. Antimicrobial susceptibilities of Propionibacterium acnes isolated from patients with acne vulgaris. Microbiol. Immunol. 52(12), 621-624 (2008).
44. Toyne H, Webber C, Collignon P, Dwan K, Kljakovic M. Propionibacterium acnes (P. acnes) resistance and antibiotic use in patients attending Australian general practice. Australas. J. Dermatol. 53(2), 106-111 (2012).
45. Eriksson G, Nord CE. Impact of topical metronidazole on the skin and colon microflora in patients with rosacea. Infection 15(1), 8-10 (1987). (Pubitemid 17018464)
46. Kampf G, Kramer A. Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin. Microbiol. Rev. 17(4), 863-893, table (2004).
47. de Almeida e Borges LF, Silva BL, Gontijo Filho PP. Hand washing: changes in the skin flora. Am. J. Infect. Control 35(6), 417-420 (2007). (Pubitemid 47103228)
48. Rocha LA, Ferreira de Almeida E Borges, Gontijo Filho PP. Changes in hands microbiota associated with skin damage because of hand hygiene procedures on the health care workers. Am. J. Infect. Control 37(2), 155-159 (2009).
49. Herruzo R, Vizcaino MJ, Herruzo I. In vitroYin vivo sequence studies as a method of selecting the most efficacious alcohol-based solution for hygienic hand disinfection. Clin. Microbiol. Infect. 16(5), 518-523 (2010).
50. Choi JM, Lew VK, Kimball AB. A single-blinded, randomized, controlled clinical trial evaluating the effect of face washing on acne vulgaris. Pediatr. Dermatol. 23(5), 421-427 (2006). (Pubitemid 44434846)
51. Purdy S, de Berker D. Acne. BMJ 333(7575), 949-953 (2006). (Pubitemid 44733770)
52. Bek-Thomsen M, Lomholt HB, Kilian M. Acne is not associated with yet-uncultured bacteria. J. Clin. Microbiol. 46(10), 3355-3360 (2008).
53. Dessinioti C, Katsambas AD. The role of Propionibacterium acnes in acne pathogenesis: facts and controversies. Clin. Dermatol. 28(1), 2-7 (2010).
54. Leyden JJ, McGinley KJ, Mills OH, Kligman AM. Propionibacterium levels in patients with and without acne vulgaris. J. Invest. Dermatol. 65(4), 382-384 (1975).
55. Johnson JL, Cummins CS. Cell wall composition and deoxyribonucleic acid similarities among the anaerobic coryneforms, classical propionibacteria, and strains of Arachnia propionica. J. Bacteriol. 109(3), 1047-1066 (1972).
56. Lomholt HB, Kilian M. Population genetic analysis of Propionibacterium acnes identifies a subpopulation and epidemic clones associated with acne. PLoS One 5(8), e12277 (2010).
57. Valanne S, McDowell A, Ramage G et al CAMP factor homologues in Propionibacterium acnes: A new protein family differentially expressed by types I and II. Microbiology 151(Pt 5), 1369-1379 (2005). (Pubitemid 40711784)
58. Nakatsuji T, Tang DC, Zhang L, Gallo RL, Huang CM. Propionibacterium acnes CAMP factor and host acid sphingomyelinase contribute to bacterial virulence: potential targets for inflammatory acne treatment. PLoS One 6(4), e14797 (2011).
59. Liu PF, Nakatsuji T, Zhu W, Gallo RL, Huang CM. Passive immunoprotection targeting a secreted CAMP factor of Propionibacterium acnes as a novel immunotherapeutic for acne vulgaris. Vaccine 29(17), 3230-3238 (2011).
60. Lazaridou E, Apalla Z, Sotiraki S, Ziakas NG, Fotiadou C, Ioannides D. Clinical and laboratory study of rosacea in northern Greece. J. Eur. Acad. Dermatol. Venereol. 24(4), 410-414 (2010).
61. Crawford GH, Pelle MT, James WD. Rosacea: I. Etiology, pathogenesis, and subtype classification. J. Am. Acad. Dermatol. 51(3), 327-341 (2004). (Pubitemid 39178655)
62. Yamasaki K, Gallo RL. The molecular pathology of rosacea. J. Dermatol. Sci. 55(2), 77-81 (2009).
63. Lazaridou E, Giannopoulou C, Fotiadou C, Vakirlis E, Trigoni A, Ioannides D. The potential role of microorganisms in the development of rosacea. J. Dtsch Dermatol. Ges. 9(1), 21-25 (2011).
64. Ni RS, Bender K, Lacey N, Brennan L, Powell FC. The fatty acid profile of the skin surface lipid layer in papulopustular rosacea. Br. J. Dermatol. 166(2), 279-287 (2012).
65. Dahl MV, Ross AJ, Schlievert PM Temperature regulates bacterial protein production: possible role in rosacea. J. Am. Acad. Dermatol. 50(2), 266-272 (2004). (Pubitemid 38174287)
66. Whitfeld M, Gunasingam N, Leow LJ, Shirato K, Preda V. Staphylococcus epidermidis: A possible role in the pustules of rosacea. J. Am. Acad. Dermatol. 64(1), 49-52 (2011).
67. Roihu T, Kariniemi AL. Demodex mites in acne rosacea. J. Cutan. Pathol. 25(10), 550-552 (1998). (Pubitemid 28552510)
68. Skrlin J, Richter B, Basta-Juzbasic A et al. Demodicosis and rosacea. Lancet 337(8743), 734 (1991).
69. Bonnar E, Eustace P, Powell FC. The Demodex mite population in rosacea. J. Am. Acad. Dermatol. 28(3), 443-448 (1993). (Pubitemid 23075260)
70. Erbagci Z, Ozgoztasi O. The significance of Demodex folliculorum density in rosacea. Int. J. Dermatol. 37(6), 421-425 (1998). (Pubitemid 28284868)
71. Buechner SA. Rosacea: An update. Dermatology 210(2), 100-108 (2005). (Pubitemid 40463198)
72. Georgala S, Katoulis AC, Kylafis GD, Koumantaki-Mathioudaki E, Georgala C, Aroni K. Increased density of Demodex folliculorum and evidence of delayed hypersensitivity reaction in subjects with papulopustular rosacea. J. Eur. Acad. Dermatol. Venereol. 15(5), 441-444 (2001). (Pubitemid 33040117)
73. Zhao YE, Wu LP, Peng Y, Cheng H. Retrospective analysis of the association between Demodex infestation and rosacea. Arch. Dermatol. 146(8), 896-902 (2010).
74. Jing X, Shuling G, Ying L. Environmental scanning electron microscopy observation of the ultrastructure of Demodex. Microsc. Res. Tech. 68(5), 284-289 (2005). (Pubitemid 43003415)
75. Zhao YE, Guo N, Wu LP. The effect of temperature on the viability of Demodex folliculorum and Demodex brevis. Parasitol. Res. 105(6), 1623-1628 (2009).
76. Yamasaki K, Kanada K, Macleod DT et al. TLR2 expression is increased in rosacea and stimulates enhanced serine protease production by keratinocytes. J. Invest. Dermatol. 131(3), 688-697 (2011).
77. Yamasaki K, Di Nardo A, Bardan A et al. Increased serine protease activity and cathelicidin promotes skin inflammation in rosacea. Nat. Med. 13(8), 975-980 (2007). (Pubitemid 47222043)
78. Kimbrell MR, Warshakoon H, Cromer JR et al. Comparison of the immunostimulatory and proinflammatory activities of candidate Gram-positive endotoxins, lipoteichoic acid, peptidoglycan, and lipopeptides, in murine and human cells. Immunol. Lett. 118(2), 132-141 (2008).
79. Shibata M, Katsuyama M, Onodera T, Ehama R, Hosoi J, Tagami H. Glucocorticoids enhance Toll-like receptor 2 expression in human keratinocytes stimulated with Propionibacterium acnes or proinflammatory cytokines. J. Invest. Dermatol. 129(2), 375-382 (2009).
80. Koller B, Muller-Wiefel AS, Rupec R, Korting HC, Ruzicka T. Chitin modulates innate immune responses of keratinocytes. PLoS One 6(2), e16594 (2011).
81. Lacey N, Delaney S, Kavanagh K, Powell FC. Mite-related bacterial antigens stimulate inflammatory cells in rosacea. Br. J. Dermatol. 157(3), 474-481 (2007). (Pubitemid 47256121)
82. Li J, O'Reilly N, Sheha H et al. Correlation between ocular Demodex infestation and serum immunoreactivity to Bacillus proteins in patients with facial rosacea. Ophthalmology 117(5), 870-877 (2010).
83. Fahlen A, Engstrand L, Baker BS, Powles A, Fry L. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch. Dermatol. Res. 304(1), 15-22 (2012).
84. Luk NM, Hui M, Lee HC et al. Antibiotic-resistant Propionibacterium acnes among acne patients in a regional skin centre in Hong Kong. J. Eur. Acad. Dermatol. Venereol. 27(1), 31-36 (2013).
85. van Zuuren EJ, Kramer SF, Carter BR, Graber MA, Fedorowicz Z. Effective and evidence-based management strategies for rosacea: summary of a Cochrane systematic review. Br. J. Dermatol. 165(4), 760-781 (2011).
86. Jarmuda S, O'Reilly N, Zaba R, Jakubowicz O, Szkaradkiewicz A, Kavanagh K. The potential role of Demodex folliculorum mites and bacteria in the induction of rosacea. J. Med. Microbiol. 61(Pt 11), 1504-1510 (2012).