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

Manu N Capoor; Filip Ruzicka; Gurpreet Sandhu; Jess Rollason; Konstantinos Mavrommatis; Fahad S Ahmed; Jonathan E Schmitz; Assaf Raz; Holger Brüggemann; Peter A Lambert; Vincent A Fischetti; Ondrej Slaby

doi:10.1371/journal.pone.0208144

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

Manu N Capoor^*, Filip Ruzicka, Gurpreet Sandhu, Jess Rollason, Konstantinos Mavrommatis, Fahad S Ahmed, Jonathan E Schmitz, Assaf Raz, Holger Brüggemann, Peter A Lambert, Vincent A Fischetti, Ondrej Slaby^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Most patients with chronic lower back pain (CLBP) exhibit degenerative disc disease. Disc specimens obtained during initial therapeutic discectomies are often infected/colonized with Propionibacterium acnes, a Gram-positive commensal of the human skin. Although pain associated with infection is typically ascribed to the body's inflammatory response, the Gram-positive bacterium Staphylococcus aureus was recently observed to directly activate nociceptors by secreting pore-forming α-hemolysins that disrupt neuronal cell membranes. The hemolytic activity of P. acnes in cultured disc specimens obtained during routine therapeutic discectomies was assessed through incubation on sheep-blood agar. The β-hemolysis pattern displayed by P. acnes on sheep-blood agar was variable and phylogroup-dependent. Their molecular phylogroups were correlated with their hemolytic patterns. Our findings raise the possibility that pore-forming proteins contribute to the pathogenesis and/or symptomology of chronic P. acnes disc infections and CLBP, at least in a subset of cases.

Original language	English
Article number	e0208144
Journal	PLoS ONE
Volume	13
Issue number	11
DOIs	https://doi.org/10.1371/journal.pone.0208144
Publication status	Published - 29 Nov 2018

Bibliographical note

© 2018 Capoor et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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10.1371/journal.pone.0208144Licence: CC BY 3.0

Importance of Propionibacterium acnes hemolytic activity in human intervertebral discs: A microbiological study
© 2018 Capoor et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Final published version, 1.38 MBLicence: CC BY 3.0

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Capoor, M. N., Ruzicka, F., Sandhu, G., Rollason, J., Mavrommatis, K., Ahmed, F. S., Schmitz, J. E., Raz, A., Brüggemann, H., Lambert, P. A., Fischetti, V. A., & Slaby, O. (2018). Importance of Propionibacterium acnes hemolytic activity in human intervertebral discs: A microbiological study. PLoS ONE, 13(11), Article e0208144. https://doi.org/10.1371/journal.pone.0208144

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title = "Importance of Propionibacterium acnes hemolytic activity in human intervertebral discs: A microbiological study",

abstract = "Most patients with chronic lower back pain (CLBP) exhibit degenerative disc disease. Disc specimens obtained during initial therapeutic discectomies are often infected/colonized with Propionibacterium acnes, a Gram-positive commensal of the human skin. Although pain associated with infection is typically ascribed to the body's inflammatory response, the Gram-positive bacterium Staphylococcus aureus was recently observed to directly activate nociceptors by secreting pore-forming α-hemolysins that disrupt neuronal cell membranes. The hemolytic activity of P. acnes in cultured disc specimens obtained during routine therapeutic discectomies was assessed through incubation on sheep-blood agar. The β-hemolysis pattern displayed by P. acnes on sheep-blood agar was variable and phylogroup-dependent. Their molecular phylogroups were correlated with their hemolytic patterns. Our findings raise the possibility that pore-forming proteins contribute to the pathogenesis and/or symptomology of chronic P. acnes disc infections and CLBP, at least in a subset of cases.",

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AU - Rollason, Jess

AU - Mavrommatis, Konstantinos

AU - Ahmed, Fahad S

AU - Schmitz, Jonathan E

AU - Raz, Assaf

AU - Brüggemann, Holger

AU - Lambert, Peter A

AU - Fischetti, Vincent A

AU - Slaby, Ondrej

N1 - © 2018 Capoor et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Y1 - 2018/11/29

N2 - Most patients with chronic lower back pain (CLBP) exhibit degenerative disc disease. Disc specimens obtained during initial therapeutic discectomies are often infected/colonized with Propionibacterium acnes, a Gram-positive commensal of the human skin. Although pain associated with infection is typically ascribed to the body's inflammatory response, the Gram-positive bacterium Staphylococcus aureus was recently observed to directly activate nociceptors by secreting pore-forming α-hemolysins that disrupt neuronal cell membranes. The hemolytic activity of P. acnes in cultured disc specimens obtained during routine therapeutic discectomies was assessed through incubation on sheep-blood agar. The β-hemolysis pattern displayed by P. acnes on sheep-blood agar was variable and phylogroup-dependent. Their molecular phylogroups were correlated with their hemolytic patterns. Our findings raise the possibility that pore-forming proteins contribute to the pathogenesis and/or symptomology of chronic P. acnes disc infections and CLBP, at least in a subset of cases.

AB - Most patients with chronic lower back pain (CLBP) exhibit degenerative disc disease. Disc specimens obtained during initial therapeutic discectomies are often infected/colonized with Propionibacterium acnes, a Gram-positive commensal of the human skin. Although pain associated with infection is typically ascribed to the body's inflammatory response, the Gram-positive bacterium Staphylococcus aureus was recently observed to directly activate nociceptors by secreting pore-forming α-hemolysins that disrupt neuronal cell membranes. The hemolytic activity of P. acnes in cultured disc specimens obtained during routine therapeutic discectomies was assessed through incubation on sheep-blood agar. The β-hemolysis pattern displayed by P. acnes on sheep-blood agar was variable and phylogroup-dependent. Their molecular phylogroups were correlated with their hemolytic patterns. Our findings raise the possibility that pore-forming proteins contribute to the pathogenesis and/or symptomology of chronic P. acnes disc infections and CLBP, at least in a subset of cases.

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

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