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

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, s...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5378350/
https://www.ncbi.nlm.nih.gov/pubmed/28369127
http://dx.doi.org/10.1371/journal.pone.0174518
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author 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
author_facet 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
author_sort Capoor, Manu N.
collection PubMed
description 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: IA(1), 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.
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spelling pubmed-53783502017-04-07 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 PLoS One Research Article 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: IA(1), 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. Public Library of Science 2017-04-03 /pmc/articles/PMC5378350/ /pubmed/28369127 http://dx.doi.org/10.1371/journal.pone.0174518 Text en © 2017 Capoor et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
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
title Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
title_full Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
title_fullStr Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
title_full_unstemmed Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
title_short Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
title_sort propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5378350/
https://www.ncbi.nlm.nih.gov/pubmed/28369127
http://dx.doi.org/10.1371/journal.pone.0174518
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