Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy

A prospective cross-sectional study

Manu N. Capoor, Filip Ruzicka, Tana Machackova, Radim Jancalek, Martin Smrcka, Jonathan E. Schmitz, Marketa Hermanova, Jiri Sana, Elleni Michu, John C. Baird, Fahad S. Ahmed, Karel MacA, Radim Lipina, Todd F. Alamin, Michael F. Coscia, Jerry L. Stonemetz, Timothy F Witham, Garth D. Ehrlich, Ziya L. Gokaslan, Konstantinos Mavrommatis & 3 others Christof Birkenmaier, Vincent A. Fischetti, Ondrej Slaby

Research output: Contribution to journalArticle

Abstract

Background The relationship between intervertebral disc degeneration and chronic infection by Propionibacterium acnes is controversial with contradictory evidence available in the literature. Previous studies investigating these relationships were under-powered and fraught with methodical differences; moreover, they have not taken into consideration P. acnes' ability to form biofilms or attempted to quantitate the bioburden with regard to determining bacterial counts/genome equivalents as criteria to differentiate true infection from contamination. Theaim of this prospective cross-sectional study was to determine the prevalence of P. acnes in patients undergoing lumbar disc microdiscectomy. Methods and Findings The sample consisted of 290 adult patients undergoing lumbar microdiscectomy for symptomatic lumbar disc herniation. An intraoperative biopsy and pre-operative clinical data were taken in all cases. One biopsy fragment was homogenized and used for quantitative anaerobic culture and a second was frozen and used for real-time PCR-based quantification of P. acnes genomes. P. acnes was identified in 115 cases (40%), coagulase-negative staphylococci in 31 cases (11%) and alpha-hemolytic streptococci in 8 cases (3%). P. acnes counts ranged from 100 to 9000 CFU/ml with a median of 400 CFU/ml. The prevalence of intervertebral discs with abundant P. acnes (≥ 1x103 CFU/ml) was 11% (39 cases). There was significant correlation between the bacterial counts obtained by culture and the number of P. acnes genomes detected by real-time PCR (r = 0.4363, p<0.0001). Conclusions In a large series of patients, the prevalence of discs with abundant P. acnes was 11%. We believe, disc tissue homogenization releases P. acnes from the biofilm so that they can then potentially be cultured, reducing the rate of false-negative cultures. Further, quantification study revealing significant bioburden based on both culture and real-time PCR minimize the likelihood that observed findings are due to contamination and supports the hypothesis P. acnes acts as a pathogen in these cases of degenerative disc disease.

Original languageEnglish (US)
Article numbere0161676
JournalPLoS One
Volume11
Issue number8
DOIs
StatePublished - Aug 1 2016

Fingerprint

Propionibacterium acnes
intervertebral disks
Intervertebral Disc
cross-sectional studies
Biopsy
Cross-Sectional Studies
Genes
Biofilms
Contamination
Coagulase
Pathogens
Cell culture
Real-Time Polymerase Chain Reaction
Tissue
quantitative polymerase chain reaction
microbial load
Bacterial Load
plate count
biofilm
genome

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Capoor, M. N., Ruzicka, F., Machackova, T., Jancalek, R., Smrcka, M., Schmitz, J. E., ... Slaby, O. (2016). Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy: A prospective cross-sectional study. PLoS One, 11(8), [e0161676]. https://doi.org/10.1371/journal.pone.0161676

Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy : A prospective cross-sectional study. / Capoor, Manu N.; Ruzicka, Filip; Machackova, Tana; Jancalek, Radim; Smrcka, Martin; Schmitz, Jonathan E.; Hermanova, Marketa; Sana, Jiri; Michu, Elleni; Baird, John C.; Ahmed, Fahad S.; MacA, Karel; Lipina, Radim; Alamin, Todd F.; Coscia, Michael F.; Stonemetz, Jerry L.; Witham, Timothy F; Ehrlich, Garth D.; Gokaslan, Ziya L.; Mavrommatis, Konstantinos; Birkenmaier, Christof; Fischetti, Vincent A.; Slaby, Ondrej.

In: PLoS One, Vol. 11, No. 8, e0161676, 01.08.2016.

Research output: Contribution to journalArticle

Capoor, MN, Ruzicka, F, Machackova, T, Jancalek, R, Smrcka, M, Schmitz, JE, Hermanova, M, Sana, J, Michu, E, Baird, JC, Ahmed, FS, MacA, K, Lipina, R, Alamin, TF, Coscia, MF, Stonemetz, JL, Witham, TF, Ehrlich, GD, Gokaslan, ZL, Mavrommatis, K, Birkenmaier, C, Fischetti, VA & Slaby, O 2016, 'Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy: A prospective cross-sectional study', PLoS One, vol. 11, no. 8, e0161676. https://doi.org/10.1371/journal.pone.0161676
Capoor, Manu N. ; Ruzicka, Filip ; Machackova, Tana ; Jancalek, Radim ; Smrcka, Martin ; Schmitz, Jonathan E. ; Hermanova, Marketa ; Sana, Jiri ; Michu, Elleni ; Baird, John C. ; Ahmed, Fahad S. ; MacA, Karel ; Lipina, Radim ; Alamin, Todd F. ; Coscia, Michael F. ; Stonemetz, Jerry L. ; Witham, Timothy F ; Ehrlich, Garth D. ; Gokaslan, Ziya L. ; Mavrommatis, Konstantinos ; Birkenmaier, Christof ; Fischetti, Vincent A. ; Slaby, Ondrej. / Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy : A prospective cross-sectional study. In: PLoS One. 2016 ; Vol. 11, No. 8.
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abstract = "Background The relationship between intervertebral disc degeneration and chronic infection by Propionibacterium acnes is controversial with contradictory evidence available in the literature. Previous studies investigating these relationships were under-powered and fraught with methodical differences; moreover, they have not taken into consideration P. acnes' ability to form biofilms or attempted to quantitate the bioburden with regard to determining bacterial counts/genome equivalents as criteria to differentiate true infection from contamination. Theaim of this prospective cross-sectional study was to determine the prevalence of P. acnes in patients undergoing lumbar disc microdiscectomy. Methods and Findings The sample consisted of 290 adult patients undergoing lumbar microdiscectomy for symptomatic lumbar disc herniation. An intraoperative biopsy and pre-operative clinical data were taken in all cases. One biopsy fragment was homogenized and used for quantitative anaerobic culture and a second was frozen and used for real-time PCR-based quantification of P. acnes genomes. P. acnes was identified in 115 cases (40{\%}), coagulase-negative staphylococci in 31 cases (11{\%}) and alpha-hemolytic streptococci in 8 cases (3{\%}). P. acnes counts ranged from 100 to 9000 CFU/ml with a median of 400 CFU/ml. The prevalence of intervertebral discs with abundant P. acnes (≥ 1x103 CFU/ml) was 11{\%} (39 cases). There was significant correlation between the bacterial counts obtained by culture and the number of P. acnes genomes detected by real-time PCR (r = 0.4363, p<0.0001). Conclusions In a large series of patients, the prevalence of discs with abundant P. acnes was 11{\%}. We believe, disc tissue homogenization releases P. acnes from the biofilm so that they can then potentially be cultured, reducing the rate of false-negative cultures. Further, quantification study revealing significant bioburden based on both culture and real-time PCR minimize the likelihood that observed findings are due to contamination and supports the hypothesis P. acnes acts as a pathogen in these cases of degenerative disc disease.",
author = "Capoor, {Manu N.} and Filip Ruzicka and Tana Machackova and Radim Jancalek and Martin Smrcka and Schmitz, {Jonathan E.} and Marketa Hermanova and Jiri Sana and Elleni Michu and Baird, {John C.} and Ahmed, {Fahad S.} and Karel MacA and Radim Lipina and Alamin, {Todd F.} and Coscia, {Michael F.} and Stonemetz, {Jerry L.} and Witham, {Timothy F} and Ehrlich, {Garth D.} and Gokaslan, {Ziya L.} and Konstantinos Mavrommatis and Christof Birkenmaier and Fischetti, {Vincent A.} and Ondrej Slaby",
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T1 - Prevalence of propionibacterium acnes in intervertebral discs of patients undergoing lumbar microdiscectomy

T2 - A prospective cross-sectional study

AU - Capoor, Manu N.

AU - Ruzicka, Filip

AU - Machackova, Tana

AU - Jancalek, Radim

AU - Smrcka, Martin

AU - Schmitz, Jonathan E.

AU - Hermanova, Marketa

AU - Sana, Jiri

AU - Michu, Elleni

AU - Baird, John C.

AU - Ahmed, Fahad S.

AU - MacA, Karel

AU - Lipina, Radim

AU - Alamin, Todd F.

AU - Coscia, Michael F.

AU - Stonemetz, Jerry L.

AU - Witham, Timothy F

AU - Ehrlich, Garth D.

AU - Gokaslan, Ziya L.

AU - Mavrommatis, Konstantinos

AU - Birkenmaier, Christof

AU - Fischetti, Vincent A.

AU - Slaby, Ondrej

PY - 2016/8/1

Y1 - 2016/8/1

N2 - Background The relationship between intervertebral disc degeneration and chronic infection by Propionibacterium acnes is controversial with contradictory evidence available in the literature. Previous studies investigating these relationships were under-powered and fraught with methodical differences; moreover, they have not taken into consideration P. acnes' ability to form biofilms or attempted to quantitate the bioburden with regard to determining bacterial counts/genome equivalents as criteria to differentiate true infection from contamination. Theaim of this prospective cross-sectional study was to determine the prevalence of P. acnes in patients undergoing lumbar disc microdiscectomy. Methods and Findings The sample consisted of 290 adult patients undergoing lumbar microdiscectomy for symptomatic lumbar disc herniation. An intraoperative biopsy and pre-operative clinical data were taken in all cases. One biopsy fragment was homogenized and used for quantitative anaerobic culture and a second was frozen and used for real-time PCR-based quantification of P. acnes genomes. P. acnes was identified in 115 cases (40%), coagulase-negative staphylococci in 31 cases (11%) and alpha-hemolytic streptococci in 8 cases (3%). P. acnes counts ranged from 100 to 9000 CFU/ml with a median of 400 CFU/ml. The prevalence of intervertebral discs with abundant P. acnes (≥ 1x103 CFU/ml) was 11% (39 cases). There was significant correlation between the bacterial counts obtained by culture and the number of P. acnes genomes detected by real-time PCR (r = 0.4363, p<0.0001). Conclusions In a large series of patients, the prevalence of discs with abundant P. acnes was 11%. We believe, disc tissue homogenization releases P. acnes from the biofilm so that they can then potentially be cultured, reducing the rate of false-negative cultures. Further, quantification study revealing significant bioburden based on both culture and real-time PCR minimize the likelihood that observed findings are due to contamination and supports the hypothesis P. acnes acts as a pathogen in these cases of degenerative disc disease.

AB - Background The relationship between intervertebral disc degeneration and chronic infection by Propionibacterium acnes is controversial with contradictory evidence available in the literature. Previous studies investigating these relationships were under-powered and fraught with methodical differences; moreover, they have not taken into consideration P. acnes' ability to form biofilms or attempted to quantitate the bioburden with regard to determining bacterial counts/genome equivalents as criteria to differentiate true infection from contamination. Theaim of this prospective cross-sectional study was to determine the prevalence of P. acnes in patients undergoing lumbar disc microdiscectomy. Methods and Findings The sample consisted of 290 adult patients undergoing lumbar microdiscectomy for symptomatic lumbar disc herniation. An intraoperative biopsy and pre-operative clinical data were taken in all cases. One biopsy fragment was homogenized and used for quantitative anaerobic culture and a second was frozen and used for real-time PCR-based quantification of P. acnes genomes. P. acnes was identified in 115 cases (40%), coagulase-negative staphylococci in 31 cases (11%) and alpha-hemolytic streptococci in 8 cases (3%). P. acnes counts ranged from 100 to 9000 CFU/ml with a median of 400 CFU/ml. The prevalence of intervertebral discs with abundant P. acnes (≥ 1x103 CFU/ml) was 11% (39 cases). There was significant correlation between the bacterial counts obtained by culture and the number of P. acnes genomes detected by real-time PCR (r = 0.4363, p<0.0001). Conclusions In a large series of patients, the prevalence of discs with abundant P. acnes was 11%. We believe, disc tissue homogenization releases P. acnes from the biofilm so that they can then potentially be cultured, reducing the rate of false-negative cultures. Further, quantification study revealing significant bioburden based on both culture and real-time PCR minimize the likelihood that observed findings are due to contamination and supports the hypothesis P. acnes acts as a pathogen in these cases of degenerative disc disease.

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