• This record comes from PubMed

Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy

. 2017 ; 12 (4) : e0174518. [epub] 20170403

Language English Country United States Media electronic-ecollection

Document type Journal Article

Grant support
UL1 TR001414 NCATS NIH HHS - United States

BACKGROUND: In previous studies, Propionibacterium acnes was cultured from intervertebral disc tissue of ~25% of patients undergoing microdiscectomy, suggesting a possible link between chronic bacterial infection and disc degeneration. However, given the prominence of P. acnes as a skin commensal, such analyses often struggled to exclude the alternate possibility that these organisms represent perioperative microbiologic contamination. This investigation seeks to validate P. acnes prevalence in resected disc cultures, while providing microscopic evidence of P. acnes biofilm in the intervertebral discs. METHODS: Specimens from 368 patients undergoing microdiscectomy for disc herniation were divided into several fragments, one being homogenized, subjected to quantitative anaerobic culture, and assessed for bacterial growth, and a second fragment frozen for additional analyses. Colonies were identified by MALDI-TOF mass spectrometry and P. acnes phylotyping was conducted by multiplex PCR. For a sub-set of specimens, bacteria localization within the disc was assessed by microscopy using confocal laser scanning and FISH. RESULTS: Bacteria were cultured from 162 discs (44%), including 119 cases (32.3%) with P. acnes. In 89 cases, P. acnes was cultured exclusively; in 30 cases, it was isolated in combination with other bacteria (primarily coagulase-negative Staphylococcus spp.) Among positive specimens, the median P. acnes bacterial burden was 350 CFU/g (12 - ~20,000 CFU/g). Thirty-eight P. acnes isolates were subjected to molecular sub-typing, identifying 4 of 6 defined phylogroups: IA1, IB, IC, and II. Eight culture-positive specimens were evaluated by fluorescence microscopy and revealed P. acnes in situ. Notably, these bacteria demonstrated a biofilm distribution within the disc matrix. P. acnes bacteria were more prevalent in males than females (39% vs. 23%, p = 0.0013). CONCLUSIONS: This study confirms that P. acnes is prevalent in herniated disc tissue. Moreover, it provides the first visual evidence of P. acnes biofilms within such specimens, consistent with infection rather than microbiologic contamination.

Cedars Sinai Institute for Spinal Disorders Los Angeles California United States of America

Celgene Corporation Information Knowledge and Utilization San Francisco California United States of America

Center for Biofilm Engineering Montana State University Bozeman Montana United States of America

Department of Anesthesia The Johns Hopkins Hospital Baltimore Maryland United States of America

Department of Microbiology Faculty of Medicine Masaryk university St Anne's Faculty Hospital Brno Czech Republic

Department of Molecular Oncology Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Neurosurgery St Anne's University Hospital Masaryk University Brno Czech Republic

Department of Neurosurgery The Johns Hopkins Hospital Baltimore Maryland United States of America

Department of Neurosurgery The Warren Alpert Medical School of Brown University Rhode Island Hospital Providence Rhode Island United States of America

Department of Neurosurgery University Hospital Brno Masaryk University Brno Czech Republic

Department of Neurosurgery University Hospital Ostrava Ostrava University Ostrava Czech Republic

Department of Orthopaedic Surgery David Geffen School of Medicine University of California Los Angeles California United States of America

Department of Orthopaedic Surgery University of California Irvine School of Medicine Irvine California United States of America

Department of Orthopaedic Surgery University of California San Diego San Diego California United States of America

Department of Orthopedic Surgery Kaiser Permanente Oakland Medical Center Oakland California United States of America

Department of Orthopedic Surgery Kaiser Permanente San Jose Medical Center San Jose California United States of America

Department of Orthopedic Surgery OrthoIndy Hospital Indianapolis Indiana United States of America

Department of Orthopedic Surgery Stanford University Medical Center Stanford University Stanford California United States of America

Department of Orthopedic Surgery University Southern California Los Angeles California United States of America

Department of Orthopedics Physical Medicine and Rehabilitation University of Munich Munich Germany

Department of Pathology Microbiology and Immunology Vanderbilt University School of Medicine Nashville Tennessee United States of America

Laboratory of Bacterial Pathogenesis and Immunology Rockefeller University New York New York United States of America

Scripps Clinic Division of Orthopedic Surgery San Diego California United States of America

Spine Center UCSF Medical Center San Francisco California United States of America

See more in PubMed

Agarwal V, Golish SR, Alamin TF. Bacteriologic culture of excised intervertebral disc from immunocompetent patients undergoing single level primary lumbar microdiscectomy. J Spinal Disord Tech. 2011;24(6):397–400. 10.1097/BSD.0b013e3182019f3a PubMed DOI

Aghazadeh J, Salehpour F, Ziaeii E, Javanshir N, Samadi A, Sadeghi J, et al. Modic changes in the adjacent vertebrae due to disc material infection with Propionibacterium acnes in patients with lumbar disc herniation. Eur Spine J. 2016. PubMed

Albert HB, Lambert P, Rollason J, Sorensen JS, Worthington T, Pedersen MB, et al. Does nuclear tissue infected with bacteria following disc herniations lead to Modic changes in the adjacent vertebrae? Eur Spine J. 2013;22(4):690–6. PubMed Central PMCID: PMCPMC3631023. 10.1007/s00586-013-2674-z PubMed DOI PMC

Arndt J, Charles YP, Koebel C, Bogorin I, Steib JP. Bacteriology of degenerated lumbar intervertebral disks. J Spinal Disord Tech. 2012;25(7):E211–6. 10.1097/BSD.0b013e318269851a PubMed DOI

Ben-Galim P, Rand N, Giladi M, Schwartz D, Ashkenazi E, Millgram M, et al. Association between sciatica and microbial infection: true infection or culture contamination? Spine (Phila Pa 1976). 2006;31(21):2507–9. PubMed

Carricajo A, Nuti C, Aubert E, Hatem O, Fonsale N, Mallaval FO, et al. Propionibacterium acnes contamination in lumbar disc surgery. J Hosp Infect. 2007;66(3):275–7. 10.1016/j.jhin.2007.04.007 PubMed DOI

Coscia MF, Wack M, Denys G. Low Virulence Bacterial Infections of Intervertebral Discs and the Resultant Spinal Disease Processes. Abstract from Scoliosis Research Society (SRS) Annual Meeting. 2003.

Stirling A, Rafiq M, Mathur K, Elliot TS, Worthington T, Lambert PA. Association Between Sciatica and Skin Commensals. Journal of Bone and Joint Surgery. 2002;84-B(Supplement II):147.

Stirling A, Worthington T, Rafiq M, Lambert PA, Elliott TS. Association between sciatica and Propionibacterium acnes. Lancet. 2001;357(9273):2024–5. 10.1016/S0140-6736(00)05109-6 PubMed DOI

Rigal J, Thelen T, Byrne F, Cogniet A, Boissiere L, Aunoble S, et al. Prospective study using anterior approach did not show association between Modic 1 changes and low grade infection in lumbar spine. Eur Spine J. 2016;25(4):1000–5. 10.1007/s00586-016-4396-5 PubMed DOI

Capoor MN, Ruzicka F, Machackova T, Jancalek R, Smrcka M, Schmitz JE, et al. Prevalence of Propionibacterium acnes in Intervertebral Discs of Patients Undergoing Lumbar Microdiscectomy: A Prospective Cross-Sectional Study. PLoS One. 2016;11(8):e0161676 PubMed Central PMCID: PMCPMC4990245. 10.1371/journal.pone.0161676 PubMed DOI PMC

Lee MJ, Pottinger PS, Butler-Wu S, Bumgarner RE, Russ SM, Matsen FA 3rd. Propionibacterium persists in the skin despite standard surgical preparation. J Bone Joint Surg Am. 2014;96(17):1447–50. 10.2106/JBJS.M.01474 PubMed DOI

Bayston R, Ashraf W, Barker-Davies R, Tucker E, Clement R, Clayton J, et al. Biofilm formation by Propionibacterium acnes on biomaterials in vitro and in vivo: impact on diagnosis and treatment. J Biomed Mater Res A. 2007;81(3):705–9. 10.1002/jbm.a.31145 PubMed DOI

Miles AA, Misra SS, Irwin JO. The estimation of the bactericidal power of the blood. J Hyg (Lond). 1938;38(6):732–49.PubMed Central PMCID: PMCPMC2199673. PubMed PMC

Barnard E, Nagy I, Hunyadkurti J, Patrick S, McDowell A. Multiplex touchdown PCR for rapid typing of the opportunistic pathogen Propionibacterium acnes. J Clin Microbiol. 2015;53(4):1149–55. PubMed Central PMCID: PMCPMC4365214. 10.1128/JCM.02460-14 PubMed DOI PMC

Urquhart DM, Zheng Y, Cheng AC, Rosenfeld JV, Chan P, Liew S, et al. Could low grade bacterial infection contribute to low back pain? A systematic review. BMC Med. 2015;13:13 PubMed Central PMCID: PMCPMC4320560. 10.1186/s12916-015-0267-x PubMed DOI PMC

Dudli S, Liebenberg E, Magnitsky S, Miller S, Demir-Deviren S, Lotz JC. Propionibacterium acnes infected intervertebral discs cause vertebral bone marrow lesions consistent with Modic changes. J Orthop Res. 2016;34(8):1447–55. 10.1002/jor.23265 PubMed DOI

Chen Z, Zheng Y, Yuan Y, Jiao Y, Xiao J, Zhou Z, et al. Modic Changes and Disc Degeneration Caused by Inoculation of Propionibacterium acnes inside Intervertebral Discs of Rabbits: A Pilot Study. Biomed Res Int. 2016;2016:9612437 PubMed Central PMCID: PMCPMC4746301. 10.1155/2016/9612437 PubMed DOI PMC

Han A, Zenilman JM, Melendez JH, Shirtliff ME, Agostinho A, James G, et al. The importance of a multifaceted approach to characterizing the microbial flora of chronic wounds. Wound Repair Regen. 2011;19(5):532–41. PubMed Central PMCID: PMCPMC3227014. 10.1111/j.1524-475X.2011.00720.x PubMed DOI PMC

McDowell A, Valanne S, Ramage G, Tunney MM, Glenn JV, McLorinan GC, et al. Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol. 2005;43(1):326–34. PubMed Central PMCID: PMCPMC540145. 10.1128/JCM.43.1.326-334.2005 PubMed DOI PMC

Rollason J, McDowell A, Albert HB, Barnard E, Worthington T, Hilton AC, et al. Genotypic and antimicrobial characterisation of Propionibacterium acnes isolates from surgically excised lumbar disc herniations. Biomed Res Int. 2013;2013:530382 PubMed Central PMCID: PMCPMC3771251. 10.1155/2013/530382 PubMed DOI PMC

Oliveira F, Lima CA, Bras S, Franca A, Cerca N. Evidence for inter- and intraspecies biofilm formation variability among a small group of coagulase-negative staphylococci. FEMS Microbiol Lett. 2015;362(20). PubMed

Perry A, Lambert P. Propionibacterium acnes: infection beyond the skin. Expert Rev Anti Infect Ther. 2011;9(12):1149–56. 10.1586/eri.11.137 PubMed DOI

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10. 10.1016/S0022-2836(05)80360-2 PubMed DOI

Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2016;44(D1):D67–72. PubMed Central PMCID: PMCPMC4702903. 10.1093/nar/gkv1276 PubMed DOI PMC

Johannes CB, Le TK, Zhou X, Johnston JA, Dworkin RH. The prevalence of chronic pain in United States adults: results of an Internet-based survey. J Pain. 2010;11(11):1230–9. 10.1016/j.jpain.2010.07.002 PubMed DOI

Parker SL, Mendenhall SK, Godil SS, Sivasubramanian P, Cahill K, Ziewacz J, et al. Incidence of Low Back Pain After Lumbar Discectomy for Herniated Disc and Its Effect on Patient-reported Outcomes. Clin Orthop Relat Res. 2015;473(6):1988–99. PubMed Central PMCID: PMCPMC4419014. 10.1007/s11999-015-4193-1 PubMed DOI PMC

Shifflett GD, Bjerke-Kroll BT, Nwachukwu BU, Kueper J, Burket J, Sama AA, et al. Microbiologic profile of infections in presumed aseptic revision spine surgery. Eur Spine J. 2016;25(12):3902–7. 10.1007/s00586-016-4539-8 PubMed DOI

Gausden EB, Villa J, Warner SJ, Redko M, Pearle A, Miller A, et al. Nonunion after clavicle osteosynthesis: High incidence of Propionibacterium acnes. J Orthop Trauma. 2016. PubMed

Gaillard C, Dupond M, Brisou P, Gaillard T. Septic nonunions of lower limb long bones: don't neglect Propionibacterium acnes! Int J Low Extrem Wounds. 2013;12(4):301–5. 10.1177/1534734613489990 PubMed DOI

Singh JA, Sperling JW, Schleck C, Harmsen WS, Cofield RH. Periprosthetic infections after total shoulder arthroplasty: a 33-year perspective. J Shoulder Elbow Surg. 2012;21(11):1534–41. PubMed Central PMCID: PMCPMC3586318. 10.1016/j.jse.2012.01.006 PubMed DOI PMC

Holmberg A, Lood R, Morgelin M, Soderquist B, Holst E, Collin M, et al. Biofilm formation by Propionibacterium acnes is a characteristic of invasive isolates. Clin Microbiol Infect. 2009;15(8):787–95. 10.1111/j.1469-0691.2009.02747.x PubMed DOI

Lutz JA, Otten P, Maestretti G. Late infections after dynamic stabilization of the lumbar spine with Dynesys. Eur Spine J. 2012;21(12):2573–9. PubMed Central PMCID: PMCPMC3508231. 10.1007/s00586-012-2366-0 PubMed DOI PMC

Jakab E, Zbinden R, Gubler J, Ruef C, von Graevenitz A, Krause M. Severe infections caused by Propionibacterium acnes: an underestimated pathogen in late postoperative infections. Yale J Biol Med. 1996;69(6):477–82.PubMed Central PMCID: PMCPMC2589039. PubMed PMC

Amital H, Govoni M, Maya R, Meroni PL, Ori B, Shoenfeld Y, et al. Role of infectious agents in systemic rheumatic diseases. Clin Exp Rheumatol. 2008;26(1 Suppl 48):S27–32. PubMed

Zimmermann P, Curtis N. Synovitis, acne, pustulosis, hyperostosis, and osteitis (SAPHO) syndrome—A challenging diagnosis not to be missed. J Infect. 2016;72 Suppl:S106–14. PubMed

Carneiro S, Sampaio-Barros PD. SAPHO syndrome. Rheum Dis Clin North Am. 2013;39(2):401–18. 10.1016/j.rdc.2013.02.009 PubMed DOI

Omori M, Bito T, Yamada M, Ogura K, Eishi Y, Nishigori C. Systemic sarcoidosis with bone marrow involvement showing Propionibacterium acnes in the lymph nodes. J Eur Acad Dermatol Venereol. 2015;29(10):2059–60. 10.1111/jdv.12594 PubMed DOI

Zhou Y, Hu Y, Li H. Role of Propionibacterium Acnes in Sarcoidosis: A Meta-analysis. Sarcoidosis Vasc Diffuse Lung Dis. 2013;30(4):262–7. PubMed

Satoh F, Morita H, Tayama H, Inoue Y, Eishi Y, Yoshimura A. Renal sarcoidosis with limited lung manifestations expressing Propionibacterium acnes antigens in the affected tubulointerstitium. Am J Med Sci. 2013;346(3):250–2. 10.1097/MAJ.0b013e31828bdf9f PubMed DOI

Eishi Y. Etiologic aspect of sarcoidosis as an allergic endogenous infection caused by Propionibacterium acnes. Biomed Res Int. 2013;2013:935289 PubMed Central PMCID: PMCPMC3697284. 10.1155/2013/935289 PubMed DOI PMC

Asahina A, Miura K, Saito I, Oshikata C, Ishii N, Eishi Y. Cutaneous sarcoidosis with livedoid lesions: evidence of the involvement of Propionibacterium acnes. J Dermatol. 2013;40(6):501–2. 10.1111/1346-8138.12120 PubMed DOI

Bae Y, Ito T, Iida T, Uchida K, Sekine M, Nakajima Y, et al. Intracellular Propionibacterium acnes infection in glandular epithelium and stromal macrophages of the prostate with or without cancer. PLoS One. 2014;9(2):e90324 PubMed Central PMCID: PMCPMC3938683. 10.1371/journal.pone.0090324 PubMed DOI PMC

Fischer N, Mak TN, Shinohara DB, Sfanos KS, Meyer TF, Bruggemann H. Deciphering the intracellular fate of Propionibacterium acnes in macrophages. Biomed Res Int. 2013;2013:603046 PubMed Central PMCID: PMCPMC3687600. 10.1155/2013/603046 PubMed DOI PMC

Newest 20 citations...

See more in
Medvik | PubMed

Sheep as a Potential Model of Intradiscal Infection by the Bacterium Cutibacterium acnes

. 2021 Mar 16 ; 8 (3) : . [epub] 20210316

Pro-Inflammatory and Neurotrophic Factor Responses of Cells Derived from Degenerative Human Intervertebral Discs to the Opportunistic Pathogen Cutibacterium acnes

. 2021 Feb 26 ; 22 (5) : . [epub] 20210226

Letter to the Editor concerning "Bacteria: back pain, leg pain and Modic sign: a surgical multicenter comparative study" by Fritzell, P., Welinder-Olsson, C., Jönsson, B. et al. Eur Spine J (2019)

. 2020 Mar ; 29 (3) : 628-630. [epub] 20191203

A review of microscopy-based evidence for the association of Propionibacterium acnes biofilms in degenerative disc disease and other diseased human tissue

. 2019 Dec ; 28 (12) : 2951-2971. [epub] 20190729

Letter to the Editor concerning "Low virulence bacterial infections in cervical intervertebral discs: a prospective case series" by Chen Y, Wang X, Zhang X, et al. (Eur Spine J; 2018: doi:10.1007/s00586-018-5582-4)

. 2019 May ; 28 (5) : 1242-1245. [epub] 20180623

Intervertebral disc penetration by antibiotics used prophylactically in spinal surgery: implications for the current standards and treatment of disc infections

. 2019 Apr ; 28 (4) : 783-791. [epub] 20181201

Importance of Propionibacterium acnes hemolytic activity in human intervertebral discs: A microbiological study

. 2018 ; 13 (11) : e0208144. [epub] 20181129

Is IL-1β Further Evidence for the Role of Propionibacterium acnes in Degenerative Disc Disease? Lessons From the Study of the Inflammatory Skin Condition Acne Vulgaris

. 2018 ; 8 () : 272. [epub] 20180814

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...