Sheep as a Potential Model of Intradiscal Infection by the Bacterium Cutibacterium acnes
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
N/A
Indiana Orthopaedic Hospital
PubMed
33809558
PubMed Central
PMC8002071
DOI
10.3390/vetsci8030048
PII: vetsci8030048
Knihovny.cz E-zdroje
- Klíčová slova
- Cutibacterium acnes, bacterial discitis, percutaneous injections, sheep model, spinal intervertebral discs,
- Publikační typ
- časopisecké články MeSH
The anaerobic bacterium Cutibacterium acnes has been increasingly linked to the development of degenerative disc disease (DDD), although causality is yet to be conclusively proven. To better study how this organism could contribute to the aetiology of DDD, improved animal models that are more reflective of human disc anatomy, biology and mechanical properties are required. Against this background, our proof-of concept study aimed to be the first demonstration that C. acnes could be safely administered percutaneously into sheep intervertebral discs (IVDs) for in vivo study. Following our protocol, two sheep were successfully injected with a strain of C. acnes (8.3 × 106 CFU/disc) previously recovered from a human degenerative disc. No adverse reactions were noted, and at one-month post inoculation all triplicate infected discs in our first animal grew C. acnes, albeit at a reduced load (5.12 × 104 to 6.67 × 104 CFU/disc). At six months, no growth was detected in discs from our second animal indicating bacterial clearance. This pilot study has demonstrated the feasibility of safe percutaneous injection of C. acnes into sheep IVDs under fluoroscopic guidance. The design of follow-up sheep studies to investigate the potential of C. acnes to drive pathological changes within infected discs should now be pursued.
Center for Diagnostic Imaging Carmel IN 46032 USA
Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic
College of Osteopathic Medicine Marian University Indianapolis IN 46222 USA
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Institute for Health Metrics and Evaluation (IHME) Findings from the Global Burden of Disease Study. IHME; Seattle, WA, USA: 2018.
Urban J., Roberts S. Degeneration of the intervertebral disc. Arthritis Res. 2003;5:120–130. doi: 10.1186/ar629. PubMed DOI PMC
Luoma K., Riihimäki H., Luukkonen R., Raininko R., Viikari-Juntura E., Lamminen A. Low back pain in relation to lumbar disc degeneration. Spine. 2000;25:487–492. doi: 10.1097/00007632-200002150-00016. PubMed DOI
Stirling A., Worthington T., Rafiq M., Lambert P.A., Elliot T.S. Association between sciatica and Propionibacterium acnes. Lancet. 2001;357:2024–2025. doi: 10.1016/S0140-6736(00)05109-6. PubMed DOI
Coscia M., Denys G., Wack M. Propionibacterium acnes, coagulase-negative staphylococcus, and the “biofilm-like” intervertebral disc. Spine. 2016;41:1860–1865. doi: 10.1097/BRS.0000000000001909. PubMed DOI PMC
Salehpour F., Aghazadeh J., Mirzaei F., Ziaeii E., Alavi S.A.N. Propionibacterium acnes infection in disc material and different antibiotic susceptibility in patients with lumbar disc herniation. Int. J. Spine Surg. 2019;13:146–152. doi: 10.14444/6019. PubMed DOI PMC
Rajasekaran S., Tangavel C., Aiyer S.N., Nayagam S.M., Raveendran M., Demonte N.L., Subbaiah P., Kanna R., Shetty A.P., Dharmalingam K. ISSLS PRIZE IN CLINICAL SCIENCE 2017: Is infection the possible initiator of disc disease? An insight from proteomic analysis. Eur. Spine J. 2017;26:1384–1400. PubMed
Bivona L.J., Camacho J.E., Usmani F., Nash A., Bruckner J.J., Hughes M., Bhandutia A.K., Koh E.Y., Banagan K.E., Gelb D.E., et al. The prevalence of bacterial infection in patients undergoing elective ACDF for degenerative cervical spine conditions: A prospective cohort study with contaminant control. Glob. Spine J. 2021;11:13–20. doi: 10.1177/2192568219888179. PubMed DOI PMC
Lin Y., Jiao Y., Yuan Y., Zhou Z., Zheng Y., Xiao J., Li C., Chen Z., Cao P. Propionibacterium acnes induces intervertebral disc degeneration by promoting nucleus pulposus cell apoptosis via the TLR2/JNK/mitochondrial-mediated pathway. Emerg. Microbes Infect. 2018;7:1. doi: 10.1038/s41426-017-0002-0. PubMed DOI PMC
Yuan Y., Chen Y., Zhou Z., Jiao Y., Li C., Zheng Y., Lin Y., Xiao J., Chen Z., Cao P. Association between chronic inflammation and latent infection of Propionibacterium acnes in non-pyogenic degenerated intervertebral discs: A pilot study. Eur. Spine J. 2018;27:2506–2517. doi: 10.1007/s00586-017-5363-5. PubMed DOI
Tang G., Wang Z., Chen J., Zhang Z., Qian H., Chen Y. Latent infection of low-virulence anaerobic bacteria in degenerated lumbar intervertebral discs. BMC Musculoskelet. Disord. 2018;19:445. doi: 10.1186/s12891-018-2373-3. PubMed DOI PMC
Rollason J., McDowell A., Albert H.B., Barnard E., Worthington T., Hilton A.C., Vernallis A., Patrick S., Elliott T., Lambert P. Genotypic and antimicrobial characterization of Propionibacterium acnes isolates from surgically excised lumbar disc herniations. BioMed Res. Int. 2013;2013:530382. doi: 10.1155/2013/530382. PubMed DOI PMC
Tang G., Chen Y., Chen J., Wang Z., Jiang W. Higher proportion of low-virulence anaerobic bacterial infection in young patients with intervertebral disc herniation. Exp. Ther. Med. 2019;18:3085–3089. doi: 10.3892/etm.2019.7910. PubMed DOI PMC
Dudli S., Liebenberg E., Magnitsky S., Miller S., Demir-Deviren S., Lotz J.C. Propionibacterium acnes infected intervertebral discs cause vertebral bone marrow lesions consistent with modic changes. J. Orthop. Res. 2016;34:1447–1455. doi: 10.1002/jor.23265. PubMed DOI
McLaughlin J., Watterson S., Layton A.M., Bjourson A.J., Barnard E., McDowell A. Propionibacterium acnes and acne vulgaris: New insights from the integration of population genetic, multi-omic, biochemical and host-microbe studies. Microorganisms. 2019;7:128. doi: 10.3390/microorganisms7050128. PubMed DOI PMC
Cole K.A., Banerjee A., Dipreta J.A. Propionibacterium acnes osteomyelitis after intraosseous cannulation in a child. Case Rep. Orthop. 2019:7170154. doi: 10.1155/2019/7170154. PubMed DOI PMC
Ely A.L., Neely K. Propionibacterium acnes endophthalmitis following Baerveldt glaucoma device implantation. J. Glaucoma. 2020;29:e71–e73. doi: 10.1097/IJG.0000000000001526. PubMed DOI
Niazi S.A., Clarke D., Do T., Gilbert S.C., Mannocci F., Beighton D. Propionibacterium acnes and Staphylococcus epidermidis isolated from refractory endodontic lesions are opportunistic pathogens. J. Clin. Microbiol. 2010;48:3859–3869. doi: 10.1128/JCM.01326-10. PubMed DOI PMC
Piper K.E., Jacobson M.J., Cofield R.H., Sperling J.W., Sanchez-Sotelo J., Osmon D.R., McDowell A., Patrick S., Steckelberg J.M., Mandrekar J.N., et al. Microbiologic diagnosis of prosthetic shoulder infection by use of implant sonication. J. Clin. Microbiol. 2009;47:1878–1884. doi: 10.1128/JCM.01686-08. PubMed DOI PMC
Beaver M., Lagundzin D., Thapa I., Lee J., Ali H., Kielian T., Skar G.L. C. acnes central nervous system catheter infection induces long-term changes in the CSF proteome. Infect. Immun. 2020:IAI.00531-20. doi: 10.1128/IAI.00531-20. PubMed DOI PMC
Cohen R.J., Shannon B.A., McNeal J.E., Shannon T., Garrett K.L. Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: A possible link to cancer evolution? J. Urol. 2005;173:1969–1974. doi: 10.1097/01.ju.0000158161.15277.78. PubMed DOI
Eishi Y. Etiologic link between sarcoidosis and Propionibacterium acnes. Respir. Investig. 2013;51:56–68. doi: 10.1016/j.resinv.2013.01.001. PubMed DOI
Capoor M.N., Ruzicka F., Schmitz J.E., James G.A., Machackova T., Jancalek R., Smrcka M., Lipina R., Ahmed F.S., Alamin T.F., et al. Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. PLoS ONE. 2017;12:e0174518. PubMed PMC
Ohrt-Nissen S., Fritz B.G., Walbom J., Kragh K.N., Bjarnsholt T., Dahl B., Manniche C. Bacterial biofilms: A possible mechanism for chronic infection in patients with lumbar disc herniation—A prospective proof-of-concept study using fluorescence in situ hybridization. APMIS. 2018;126:440–447. doi: 10.1111/apm.12841. PubMed DOI
Georgy M.M., Vaida F., Stern M., Murphy K. Association between type I modic changes and Propionibacterium acnes infection in the cervical spine: An observational study. AJNR. 2018;39:1764–1767. doi: 10.3174/ajnr.A5741. PubMed DOI PMC
Albert H.B., Lambert P., Rollason J., Sorensen J.S., Worthington T., Pedersen M.B., Nørgaard H.S., Vernallis A., Busch F., Manniche C., et al. Does nuclear tissue infected with bacteria following disc herniations lead to modic changes in the adjacent vertebrae? Eur. Spine J. 2013;22:690–696. doi: 10.1007/s00586-013-2674-z. PubMed DOI PMC
Aghazadeh J., Salehpour F., Ziaeii E., Javanshir N., Samadi A., Sadeghi J., Mirzaei F., Naseri Alavi S.A. Modic changes in the adjacent vertebrae due to disc material infection with Propionibacterium acnes in patients with lumbar disc herniation. Eur. Spine J. 2017;26:3129–3134. doi: 10.1007/s00586-016-4887-4. PubMed DOI
Shan Z., Zhang X., Li S., Yu T., Liu J., Zhao F. Propionibacterium acnes incubation in the discs can result in time-dependent modic changes: A long-term rabbit model. Spine (Phila Pa 1976) 2017;42:1595–1603. doi: 10.1097/BRS.0000000000002192. PubMed DOI
Chen Z., Zheng Y., Yuan Y., Jiao Y., Xiao J., Zhou Z., Cao P. 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 PMC
Daly C., Ghosh P., Jenkin G., Oehme D., Goldschlager T. A review of animal models of intervertebral disc degeneration: Pathophysiology, regeneration, and translation to the clinic. Biomed. Res. Int. 2016;2016:5952165. doi: 10.1155/2016/5952165. PubMed DOI PMC
O’Connell G.D., Vresilovic E.J., Elliott D.M. Comparison of animals used in disc research to human lumbar disc geometry. Spine (Phila Pa 1976) 2007;32:328–333. doi: 10.1097/01.brs.0000253961.40910.c1. PubMed DOI
Cappello R., Bird J.L., Pfeiffer D., Bayliss M.T., Dudhia J. Notochordal cell produce and assemble extracellular matrix in a distinct manner, which may be responsible for the maintenance of healthy nucleus pulposus. Spine (Phila Pa 1976) 2006;31:873–882; discussion 883. doi: 10.1097/01.brs.0000209302.00820.fd. PubMed DOI
Jin L., Balian G., Li X.J. Animal models for disc degeneration-an update. Histol. Histopathol. 2018;33:543–554. PubMed PMC
Wilke H.J., Kettler A., Wenger K.H., Claes L.E. Anatomy of the sheep spine and its comparison to the human spine. Anat. Rec. 1997;247:542–555. doi: 10.1002/(SICI)1097-0185(199704)247:4<542::AID-AR13>3.0.CO;2-P. PubMed DOI
Lipp C., Kirker K., Agostinho A., James G., Stewart P. Testing wound dressings using an in vitro wound model. J. Wound Care. 2010;19:220–226. doi: 10.12968/jowc.2010.19.6.48468. PubMed DOI PMC
AVMA Guidelines for the Euthanasia of Animals: 2020 Edition. [(accessed on 1 December 2020)]; Available online: https://www.avma.org/KB/Policies/Documents/euthanasia.pdf.
Elliott D.M., Yerramalli C.S., Beckstein J.C., Boxberger J.I., Johannessen W., Vresilovic E.J. The effect of relative needle diameter in puncture and sham injection animal models of degeneration. Spine (Phila Pa 1976) 2008;33:588–596. doi: 10.1097/BRS.0b013e318166e0a2. PubMed DOI
Zamora T., Palma J., Andia M., Garcia P., Wozniak A., Solar A., Campos M. Effect of Propionibacterium acnes (PA) injection on intervertebral disc degeneration in a rat model: Does it mimic modic changes? Orthop. Traumatol. Surg. Res. 2017;103:795–799. doi: 10.1016/j.otsr.2017.04.005. PubMed DOI
Shinohara D.B., Vaghasia A.M., Yu S.H., Mak T.N., Brüggemann H., Nelson W.G., De Marzo A.M., Yegnasubramanian S., Sfanos K.S. A mouse model of chronic prostatic inflammation using a human prostate cancer-derived isolate of Propionibacterium acnes. Prostate. 2013;73:1007–1105. PubMed PMC
Olsson J., Drott J.B., Laurantzon L., Laurantzon O., Bergh A., Elgh F. Chronic prostatic infection and inflammation by Propionibacterium acnes in a rat prostate infection model. PLoS ONE. 2012;7:e51434. doi: 10.1371/journal.pone.0051434. Erratum in: PLoS ONE2013, 8. PubMed DOI PMC