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

J 2017

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

MANU NATH CAPOOR, externista, Filip RŮŽIČKA, Jonathan E. SCHMITZ, Garth A. JAMES, Táňa MACHÁČKOVÁ et. al.

Basic information

Original name

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

Authors

MANU NATH CAPOOR, externista (840 United States of America), Filip RŮŽIČKA (203 Czech Republic, belonging to the institution), Jonathan E. SCHMITZ (840 United States of America), Garth A. JAMES (840 United States of America), Táňa MACHÁČKOVÁ (203 Czech Republic, belonging to the institution), Radim JANČÁLEK (203 Czech Republic, belonging to the institution), Martin SMRČKA (203 Czech Republic, belonging to the institution), Radim LIPINA (203 Czech Republic), externista FAHAD AHMED (840 United States of America), Todd F. ALAMIN (840 United States of America), Neel ANAND (840 United States of America), John C. BAIRD (840 United States of America), Nitin BHATIA (840 United States of America), Sibel DEMIR-DEVIREN (840 United States of America), Robert K. EASTLACK (840 United States of America), Steve FISHER (840 United States of America), Steven R. GARFIN (840 United States of America), Jaspaul S. GOGIA (840 United States of America), Ziya L. GOKASLAN (840 United States of America), Calvin C. KUO (840 United States of America), Yu-Po LEE (840 United States of America), Konstantinos MAVROMMATIS (840 United States of America), Elleni PONECHAL MICHU (203 Czech Republic, belonging to the institution), Hana NOSKOVÁ (203 Czech Republic, belonging to the institution), Assaf RAZ (840 United States of America), Jiří ŠÁNA (203 Czech Republic, belonging to the institution), A. Nick SHAMIE (840 United States of America), Philip S. STEWART (840 United States of America), Jerry L. STONEMETZ (840 United States of America), Jeffrey C. WANG (840 United States of America), Timothy F. WITHAM (840 United States of America), Michael F. COSCIA (840 United States of America), Christof BIRKENMAIER (840 United States of America), Vincent A. FISCHETTI (840 United States of America) and Ondřej SLABÝ (203 Czech Republic, guarantor, belonging to the institution)

Edition

Plos one, San Francisco, Public Library of Science, 2017, 1932-6203

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

30102 Immunology

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 2.766

RIV identification code

RIV/00216224:14740/17:00096860

Organization unit

Central European Institute of Technology

DOI

http://dx.doi.org/10.1371/journal.pone.0174518

UT WoS

000399351000019

Keywords in English

LOW-BACK-PAIN; SAPHO SYNDROME; MODIC CHANGES; LUMBAR SPINE; SARCOIDOSIS; INFECTIONS; ASSOCIATION; CONTAMINATION; INVOLVEMENT; DIAGNOSIS

Abstract

V originále

Background In previous studies, Propionibacterium acnes was cultured from intervertebral disc tissue of similar to 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 - similar to 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.

Links

LQ1601, research and development project

Name: CEITEC 2020 (Acronym: CEITEC2020)

Investor: Ministry of Education, Youth and Sports of the CR

Citovat

MANU NATH CAPOOR, externista, Filip RŮŽIČKA, Jonathan E. SCHMITZ, Garth A. JAMES, Táňa MACHÁČKOVÁ, Radim JANČÁLEK, Martin SMRČKA, Radim LIPINA, externista FAHAD 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. KUO, Yu-Po LEE, Konstantinos MAVROMMATIS, Elleni PONECHAL MICHU, Hana NOSKOVÁ, Assaf RAZ, Jiří ŠÁNA, A. Nick SHAMIE, Philip S. STEWART, Jerry L. STONEMETZ, Jeffrey C. WANG, Timothy F. WITHAM, Michael F. COSCIA, Christof BIRKENMAIER, Vincent A. FISCHETTI and Ondřej SLABÝ. Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. Plos one. San Francisco: Public Library of Science, 2017, vol. 12, No 4, p. nestránkováno, 17 pp. ISSN 1932-6203. Available from: https://dx.doi.org/10.1371/journal.pone.0174518.

@article{1382015,
   author = {Manu Nath Capoor, externista and Růžička, Filip and Schmitz, Jonathan E. and James, Garth A. and Macháčková, Táňa and Jančálek, Radim and Smrčka, Martin and Lipina, Radim and Fahad Ahmed, externista and Alamin, Todd F. and Anand, Neel and Baird, John C. and Bhatia, Nitin and DemirandDeviren, Sibel and Eastlack, Robert K. and Fisher, Steve and Garfin, Steven R. and Gogia, Jaspaul S. and Gokaslan, Ziya L. and Kuo, Calvin C. and Lee, YuandPo and Mavrommatis, Konstantinos and Ponechal Michu, Elleni and Nosková, Hana and Raz, Assaf and Šána, Jiří 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 Birkenmaier, Christof and Fischetti, Vincent A. and Slabý, Ondřej},
   article_location = {San Francisco},
   article_number = {4},
   doi = {http://dx.doi.org/10.1371/journal.pone.0174518},
   keywords = {LOW-BACK-PAIN; SAPHO SYNDROME; MODIC CHANGES; LUMBAR SPINE; SARCOIDOSIS; INFECTIONS; ASSOCIATION; CONTAMINATION; INVOLVEMENT; DIAGNOSIS},
   language = {eng},
   issn = {1932-6203},
   journal = {Plos one},
   title = {Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy},
   url = {http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0174518},
   volume = {12},
   year = {2017}
}

TY  - JOUR
ID  - 1382015
AU  - Manu Nath Capoor, externista - Růžička, Filip - Schmitz, Jonathan E. - James, Garth A. - Macháčková, Táňa - Jančálek, Radim - Smrčka, Martin - Lipina, Radim - Fahad Ahmed, externista - 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 - Ponechal Michu, Elleni - Nosková, Hana - Raz, Assaf - Šána, Jiří - Shamie, A. Nick - Stewart, Philip S. - Stonemetz, Jerry L. - Wang, Jeffrey C. - Witham, Timothy F. - Coscia, Michael F. - Birkenmaier, Christof - Fischetti, Vincent A. - Slabý, Ondřej
PY  - 2017
TI  - Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy
JF  - Plos one
VL  - 12
IS  - 4
SP  - nestránkováno
EP  - nestránkováno
PB  - Public Library of Science
SN  - 19326203
KW  - LOW-BACK-PAIN
KW  - SAPHO SYNDROME
KW  - MODIC CHANGES
KW  - LUMBAR SPINE
KW  - SARCOIDOSIS
KW  - INFECTIONS
KW  - ASSOCIATION
KW  - CONTAMINATION
KW  - INVOLVEMENT
KW  - DIAGNOSIS
UR  - http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0174518
L2  - http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0174518
N2  - Background In previous studies, Propionibacterium acnes was cultured from intervertebral disc tissue of similar to 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 - similar to 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.
ER  -

MANU NATH CAPOOR, externista, Filip RŮŽIČKA, Jonathan E. SCHMITZ, Garth A. JAMES, Táňa MACHÁČKOVÁ, Radim JANČÁLEK, Martin SMRČKA, Radim LIPINA, externista FAHAD 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. KUO, Yu-Po LEE, Konstantinos MAVROMMATIS, Elleni PONECHAL MICHU, Hana NOSKOVÁ, Assaf RAZ, Jiří ŠÁNA, A. Nick SHAMIE, Philip S. STEWART, Jerry L. STONEMETZ, Jeffrey C. WANG, Timothy F. WITHAM, Michael F. COSCIA, Christof BIRKENMAIER, Vincent A. FISCHETTI and Ondřej SLABÝ. Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy. \textit{Plos one}. San Francisco: Public Library of Science, 2017, vol.~12, No~4, p.~nestránkováno, 17 pp. ISSN~1932-6203. Available from: https://dx.doi.org/10.1371/journal.pone.0174518.

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