This review aims to establish current knowledge of the shoulder skin microbiome and how to manage the bacteria that reside within it.
Methods
A review was undertaken of the current literature through OvidSP. All abstracts were reviewed by three independent researchers.
Results
Thirty-five studies met the inclusion criteria. With forward referencing an additional 14 were included. None commented on organisms specific to the shoulder microbiome other than Cutibacterium acnes. Therefore, this review is focussed on the current knowledge of C. acnes.
Discussion
C. acnes is a skin commensal within the pilo-sebaceous glands reported to be the primary pathogen in up to 86% of shoulder joint infections. Pre-operative culture of unprepared skin can be indicative of underlying joint infection in shoulder arthroplasty revision. Intra-articular biopsies may have a high false positive due to skin contamination. Correlating the number of positive samples and certain associated signs can give a greater than 90% probability of a true infection. Standard surgical skin preparation, peri-surgical intravenous antibiotics and oral pre-operative antibiotics do not reduce bacterial load within the skin. However, topical benzoyl peroxide and clindamycin have both demonstrated significantly reduced bacteria load. Phylogenetically there are six main types. Patients may have more than one phenotype present during infection.
BookerSJBoydMGallacherS., et al.The colonisation of the glenohumeral joint by Propionibacterium acnes is not associated with frozen shoulder but is more likely to occur after an injection into the joint. Bone Joint J2017; 99-B: 1067–1072.
3.
BelkJWKraeutlerMJSmithJR., et al.Prevention of Cutibacterium acnes in arthroscopic shoulder surgery: a systematic review. J Shoulder Elbow Surg2020; 29: 867–873.
4.
BrookIFrazierEH.Infections caused by Propionibacterium species. Rev Infect Dis1991; 13: 819–822.
5.
HsuJENeradilekMBRussSM.Preoperative skin cultures are predictive of Propionibacterium load in deep cultures obtained at revision shoulder arthroplasty. J Shoulder Elbow Surg2018; 27: 765–770.
6.
MoherDLiberatiATetzlaffJ., et al.PRISMA – review guidelines. PLoS Med2009; 6: e1000097–e1000097.
7.
OuzzaniMHammadyHFedorowiczZ., et al.Rayyan – a web and mobile app for systematic reviews. Syst Rev2016; 5: 210–210.
AchermannYGoldsteinEJCoenyeT., et al.Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen. Clin Microbiol Rev2014; 27: 419–440.
10.
CogenALNizetVGalloR.Skin microbiota: a source of disease or defence?Br J Dermatol2008; 158: 442–455.
11.
Fitz-GibbonSTomidaSChiuBH., et al.Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol2013; 133: 2152–2160.
12.
EishiYSugaMIshigeI., et al.Quantitative analysis of mycobacterial and propionibacterial DNA in lymph nodes of Japanese and European patients with sarcoidosis. J Clin Microbiol2002; 40: 198–204.
13.
Fassi FehriLMakTNLaubeB., et al.Prevalence of Propionibacterium acnes in diseased prostates and its inflammatory and transforming activity on prostate epithelial cells. Int J Med Microbiol2011; 301: 69–78.
14.
PerryALambertP.Propionibacterium acnes: infection beyond the skin. Expert Rev Anti Infect Ther2011; 9: 1149–1156.
15.
LevyOIyerSAtounE., et al.Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis?J Shoulder Elbow Surg2013; 22: 505–511.
16.
AthwalGSSperlingJWRispoliDM., et al.Deep infection after rotator cuff repair. J Shoulder Elbow Surg2007; 16: 306–311.
17.
LeemingJPHollandKTCunliffeWJ.The microbial ecology of pilosebaceous units isolated from human skin. J Gen Microbiol1984; 130: 803–807.
18.
KohKMarshJPDrinkovicD.Propionibacterium acnes in primary shoulder arthroplasty: rates of colonisation, patient risk factors, and efficacy of perioperative prophylaxis. J Shoulder Elbow Surg2016; 25: 846–852.
19.
HudekRSommerFAbdelkawiAF.Propionibacterium acnes in shoulder surgery: is loss of hair protective for infection?J Shoulder Elbow Surg2016; 25: 973–980.
20.
SampedroMFPiperKEMcDowellA., et al.Species of Cutibacterium and Cutibacterium acnes phylotypes associated with orthopedic implants. Diagn Microbiol Infect Dis2009; 64: 138–145.
21.
QiuBAlKPena-DiazAM., et al.Cutibacterium acnes and the shoulder microbiome. J Shoulder Elbow Surg2018; 27: 1734–1739.
22.
Sethi PM, Sabetta JR, Stuek SJ, et al. Incidence of culture positive Propionibacterium acnes in shoulder arthroscopy. Orthop J Sports Med 2014; 2(2 Suppl): 2325967114S00094.
23.
KimSSongHWeon-JuL.Antimicrobial susceptibility and characterisation of Propionibacterium acnes by multilocus sequence typing and repetitive-sequence-based PCR. J Bacterial Virol2016; 46: 135–141.
24.
JohnsonTKangDBarnardE., et al.Strain-level differences in porphyrin production and regulation in Propionibacterium acnes elucidate disease associations. mSphere2016; 1: e00023–15.
25.
NodzoSRHohmanDWCraneJK., et al.Hemolysis as a clinical marker for Propionibacterium acnes orthopedic infection. Am J Orthop2014; 43: E93–E97.
26.
BumgarnerRHarrisonDHsuJ.Cutibacterium acnes isolates from deep tissue specimens retrieved during revision shoulder arthroplasty: similar colony morphology does not indicate clonality. J Clin Microbiol2020; 58: 121–119.
27.
MaccioniCBWoodbridgeABBalestroJCY., et al.Low rate of Propionibacterium acnes in arthritic shoulders undergoing primary total shoulder replacement surgery using a strict specimen collection technique. J Shoulder Elbow Surg2015; 24: 1206–1211.
28.
HorneffJGIIIHsuJEVoletiPB., et al.Propionibacterium acnes infection in shoulder arthroscopy patients with postoperative pain. J Shoulder Elbow Surg2015; 24: 838–843.
29.
MookWRKlementMRGreenCL., et al.The incidence of Propionibacterium acnes in open shoulder surgery: a controlled diagnostic study. J Bone Joint Surg Am2015; 97: 957–963.
30.
AtkinsBLAthanasouNDeeksJJ., et al.Prospective evaluation of criteria for microbiological diagnosis of prosthetic-joint infection at revision arthroplasty. J Clin Microbiol1998; 36: 2932–2939.
31.
KolakowskiLLaiJKDuvallG., et al.Benzoyl peroxide effectively decreases pre-operative Propionibacterium acnes shoulder burden: a randomised trial. J Shoulder Elbow Surg2017; 27: 131–132.
32.
LeeMJMatsenFAIIIPottingerP., et al.Propionibacterium persists in the skin in spite of standard surgical preparation. J Bone Joint Surg Am2014; 96: 1447–1450.
33.
PhadnisJGordonDKrishnanJ., et al.Frequent isolation of Propionibacterium acnes from the shoulder dermis despite skin preparation and prophylactic antibiotics. J Shoulder Elbow Surg2016; 25: 304–310.
34.
NumdariSNicholsonTParviziJ.Propionibacterium acnes from the skin of the shoulder: a randomised controlled trial. J Shoulder Elbow Surg2017; 26: 1495–1499.
35.
FalconerTMBabaMKruseLM., et al.Contamination of the surgical field with Propionibacterium acnes in primary shoulder arthroplasty. J Bone Joint Surg2016; 98: 1722–1728.
36.
ChuangMJJancoskoJJMendozaV., et al.The incidence of Propionibacterium acnes in shoulder arthroscopy. Arthroscopy2015; 31: 1702–1707.
37.
DizayHHLauDGNottageW.Benzoyl peroxide and clindamycin topical skin preparation decreases Propionibacterium acnes colonisation in shoulder arthroscopy. J Shoulder Elbow Surg2017; 26: 1190–1195.
38.
HernandezPSagerBWLiangT., et al.Bactericidal efficacy of hydrogen peroxide on Propionibacterium acnes. Bone Joint Res2019; 8: 3–10.
39.
MatsenFARussSMBertelsenA., et al.Propionibacterium can be isolated from deep cultures obtained at primary arthroplasty despite intravenous antimicrobial prophylaxis. J Shoulder Elbow Surg2015; 24: 844–847.
40.
ZellerVGhorbaniAStradyC., et al.Cutibacterium acnes: an agent of prosthetic joint infection and colonization. J Infect2007; 55: 119–124.
41.
LutzMFBerthelotPFresardA., et al.Arthro-plastic and osteosynthetic infections due to Cutibacterium acnes: a retrospective study of 52 cases, 1995–2002. Eur J Clin Microbiol Infect Dis2005; 24: 739–744.
42.
AchermannYSahinFSchwyzerH-K., et al.Characteristics and outcome of 16 periprosthetic shoulder joint infections. Infection2013; 41: 613–620.
43.
DohertyCFurnessNFBattenT., et al.Arthroscopy of the symptomatic shoulder arthroplasty. J Shoulder Elbow Surg2019; 28: 1971–1976.
44.
FrangiamoreSJSalehAGrossoMJ., et al.α-Defensin as a predictor of periprosthetic shoulder infection. J Shoulder Elbow Surg2015; 24: 1021–1027.
SaperDCapiroNNaR., et al.Management of Propionibacterium acnes infection after shoulder surgery. Curr Rev Musculoskelet Med2015; 8: 67–74.
47.
BarreauMPagnierILa ScolaB.Improving the identification of anaerobes in the clinical microbiology laboratory through MALDI-TOF mass spectrometry. Anaerobe2013; 22: 123–125.
48.
AsserayNPapinCTouchaisS., et al.Improving diagnostic criteria for Cutibacterium acnes osteomyelitis: a retrospective analysis. Scand J Infect Dis2010; 42: 421–425.
49.
SchaferFFichFLamM., et al.Antimicrobial susceptibility and genetic characteristics of Propionibacterium acnes isolated from patients with acne. Int J Dermatol2013; 52: 418–425.
50.
LeydenJ.New developments in topical antimicrobial therapy for acne. J Drugs Dermatol2008; 7: s8–s11.
51.
TsukayamaDTEstradaRGustiloRB.Infection after total hip arthroplasty. A study of the treatment of one hundred and six infections. J Bone Joint Surg Am1996; 78: 512–523.
52.
HsuJEGorbatyJDWhitneyIJ., et al.Single-stage revision is effective for failed shoulder arthroplasty with positive cultures for Propionibacterium. J Bone Joint Surg Am2016; 98: 2047–2051.
53.
JacobsAMVan HooffMLMeisJF., et al.Treatment of prosthetic joint infections due to Cutibacterium. Similar results in 60 patients treated with and without rifampicin. Acta Orthop2016; 87: 60–66.
