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

Manu N. Capoor, Filip Ruzicka, Jonathan E. Schmitz, Garth A. James, Tana Machackova, Radim Jancalek, Martin Smrcka, Radim Lipina, Fahad S. Ahmed, Todd F. Alamin, Neel Anand, John C. Baird, Nitin Bhatia, Sibel Demir-Deviren, Robert K. Eastlack, Steve Fisher, Steven R. Garfin, Jaspaul S. Gogia, Ziya L. Gokaslan, Calvin C. KuoYu Po Lee, Konstantinos Mavrommatis, Elleni Michu, Hana Noskova, Assaf Raz, Jiri Sana, A. Nick Shamie, Philip S. Stewart, Jerry L. Stonemetz, Jeffrey C. Wang, Timothy F Witham, Michael F. Coscia, Christof Birkenmaier, Vincent A. Fischetti, Ondrej Slaby

Research output: Contribution to journalArticle

Abstract

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). Thirtyeight 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.

Original languageEnglish (US)
Article numbere0174518
JournalPLoS One
Volume12
Issue number4
DOIs
StatePublished - Mar 1 2017

Fingerprint

Propionibacterium acnes
intervertebral disks
Intervertebral Disc
Biofilms
biofilm
Bacteria
Contamination
Tissue
Confocal microscopy
Coagulase
Fluorescence microscopy
bacteria
Mass spectrometry
Skin
Scanning
Lasers
Intervertebral Disc Degeneration
Molecular Typing
Intervertebral Disc Displacement
coagulase negative staphylococci

ASJC Scopus subject areas

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

Cite this

Capoor, M. N., Ruzicka, F., Schmitz, J. E., James, G. A., Machackova, T., Jancalek, R., ... Slaby, O. (2017). Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. PLoS One, 12(4), [e0174518]. https://doi.org/10.1371/journal.pone.0174518

Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. / Capoor, Manu N.; Ruzicka, Filip; Schmitz, Jonathan E.; James, Garth A.; Machackova, Tana; Jancalek, Radim; Smrcka, Martin; Lipina, Radim; Ahmed, Fahad S.; Alamin, Todd F.; Anand, Neel; Baird, John C.; Bhatia, Nitin; Demir-Deviren, Sibel; Eastlack, Robert K.; Fisher, Steve; Garfin, Steven R.; Gogia, Jaspaul S.; Gokaslan, Ziya L.; Kuo, Calvin C.; Lee, Yu Po; Mavrommatis, Konstantinos; Michu, Elleni; Noskova, Hana; Raz, Assaf; Sana, Jiri; Shamie, A. Nick; Stewart, Philip S.; Stonemetz, Jerry L.; Wang, Jeffrey C.; Witham, Timothy F; Coscia, Michael F.; Birkenmaier, Christof; Fischetti, Vincent A.; Slaby, Ondrej.

In: PLoS One, Vol. 12, No. 4, e0174518, 01.03.2017.

Research output: Contribution to journalArticle

Capoor, MN, Ruzicka, F, Schmitz, JE, James, GA, Machackova, T, Jancalek, R, Smrcka, M, Lipina, R, Ahmed, FS, Alamin, TF, Anand, N, Baird, JC, Bhatia, N, Demir-Deviren, S, Eastlack, RK, Fisher, S, Garfin, SR, Gogia, JS, Gokaslan, ZL, Kuo, CC, Lee, YP, Mavrommatis, K, Michu, E, Noskova, H, Raz, A, Sana, J, Shamie, AN, Stewart, PS, Stonemetz, JL, Wang, JC, Witham, TF, Coscia, MF, Birkenmaier, C, Fischetti, VA & Slaby, O 2017, 'Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy', PLoS One, vol. 12, no. 4, e0174518. https://doi.org/10.1371/journal.pone.0174518
Capoor MN, Ruzicka F, Schmitz JE, James GA, Machackova T, Jancalek R et al. Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. PLoS One. 2017 Mar 1;12(4). e0174518. https://doi.org/10.1371/journal.pone.0174518
Capoor, Manu N. ; Ruzicka, Filip ; Schmitz, Jonathan E. ; James, Garth A. ; Machackova, Tana ; Jancalek, Radim ; Smrcka, Martin ; Lipina, Radim ; Ahmed, Fahad S. ; Alamin, Todd F. ; Anand, Neel ; Baird, John C. ; Bhatia, Nitin ; Demir-Deviren, Sibel ; Eastlack, Robert K. ; Fisher, Steve ; Garfin, Steven R. ; Gogia, Jaspaul S. ; Gokaslan, Ziya L. ; Kuo, Calvin C. ; Lee, Yu Po ; Mavrommatis, Konstantinos ; Michu, Elleni ; Noskova, Hana ; Raz, Assaf ; Sana, Jiri ; Shamie, A. Nick ; Stewart, Philip S. ; Stonemetz, Jerry L. ; Wang, Jeffrey C. ; Witham, Timothy F ; Coscia, Michael F. ; Birkenmaier, Christof ; Fischetti, Vincent A. ; Slaby, Ondrej. / Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. In: PLoS One. 2017 ; Vol. 12, No. 4.
@article{9c79dba7b3144606ac4751ad6688ac4d,
title = "Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy",
abstract = "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). Thirtyeight 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.",
author = "Capoor, {Manu N.} and Filip Ruzicka and Schmitz, {Jonathan E.} and James, {Garth A.} and Tana Machackova and Radim Jancalek and Martin Smrcka and Radim Lipina and Ahmed, {Fahad S.} and Alamin, {Todd F.} and Neel Anand and Baird, {John C.} and Nitin Bhatia and Sibel Demir-Deviren and Eastlack, {Robert K.} and Steve Fisher and Garfin, {Steven R.} and Gogia, {Jaspaul S.} and Gokaslan, {Ziya L.} and Kuo, {Calvin C.} and Lee, {Yu Po} and Konstantinos Mavrommatis and Elleni Michu and Hana Noskova and Assaf Raz and Jiri Sana and Shamie, {A. Nick} and Stewart, {Philip S.} and Stonemetz, {Jerry L.} and Wang, {Jeffrey C.} and Witham, {Timothy F} and Coscia, {Michael F.} and Christof Birkenmaier and Fischetti, {Vincent A.} and Ondrej Slaby",
year = "2017",
month = "3",
day = "1",
doi = "10.1371/journal.pone.0174518",
language = "English (US)",
volume = "12",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "4",

}

TY - JOUR

T1 - Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy

AU - Capoor, Manu N.

AU - Ruzicka, Filip

AU - Schmitz, Jonathan E.

AU - James, Garth A.

AU - Machackova, Tana

AU - Jancalek, Radim

AU - Smrcka, Martin

AU - Lipina, Radim

AU - Ahmed, Fahad S.

AU - Alamin, Todd F.

AU - Anand, Neel

AU - Baird, John C.

AU - Bhatia, Nitin

AU - Demir-Deviren, Sibel

AU - Eastlack, Robert K.

AU - Fisher, Steve

AU - Garfin, Steven R.

AU - Gogia, Jaspaul S.

AU - Gokaslan, Ziya L.

AU - Kuo, Calvin C.

AU - Lee, Yu Po

AU - Mavrommatis, Konstantinos

AU - Michu, Elleni

AU - Noskova, Hana

AU - Raz, Assaf

AU - Sana, Jiri

AU - Shamie, A. Nick

AU - Stewart, Philip S.

AU - Stonemetz, Jerry L.

AU - Wang, Jeffrey C.

AU - Witham, Timothy F

AU - Coscia, Michael F.

AU - Birkenmaier, Christof

AU - Fischetti, Vincent A.

AU - Slaby, Ondrej

PY - 2017/3/1

Y1 - 2017/3/1

N2 - 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). Thirtyeight 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.

AB - 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). Thirtyeight 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.

UR - http://www.scopus.com/inward/record.url?scp=85016602260&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85016602260&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0174518

DO - 10.1371/journal.pone.0174518

M3 - Article

C2 - 28369127

AN - SCOPUS:85016602260

VL - 12

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 4

M1 - e0174518

ER -