Multilocus sequence typing (MLST) analysis of Propionibacterium acnes isolates from radical prostatectomy specimens

BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro‐inflammatory anaerobe, Propion...

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Published inThe Prostate Vol. 73; no. 7; pp. 770 - 777
Main Authors Mak, Tim N., Yu, Shu-Han, De Marzo, Angelo M., Brüggemann, Holger, Sfanos, Karen S.
Format Journal Article
LanguageEnglish
Published Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.05.2013
Wiley Subscription Services, Inc
Subjects
Adult
Aged
Gram-Positive Bacterial Infections - microbiology
Humans
infection
inflammation
Male
Middle Aged
MLST
Multilocus Sequence Typing - methods
Propionibacterium
Propionibacterium - genetics
Propionibacterium - isolation & purification
Propionibacterium acnes
Propionibacterium acnes - genetics
Propionibacterium acnes - isolation & purification
Prostate - microbiology
prostate cancer
Prostatectomy
Prostatic Neoplasms - microbiology
Sequence Analysis, DNA
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Abstract BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro‐inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture‐independent molecular techniques. METHODS Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST). RESULTS Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate‐derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I‐2) and CC53/60 (type II), or are CC53/60‐related singletons. CONCLUSIONS MLST typing results indicated that prostate‐derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy‐derived P. acnes isolates represent contamination from skin flora. Prostate 73: 770–777, 2013. © 2012 Wiley Periodicals, Inc.
AbstractList BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro-inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture-independent molecular techniques. METHODS Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST). RESULTS Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate-derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I-2) and CC53/60 (type II), or are CC53/60-related singletons. CONCLUSIONS MLST typing results indicated that prostate-derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy-derived P. acnes isolates represent contamination from skin flora. Prostate 73: 770-777, 2013. copyright 2012 Wiley Periodicals, Inc.
BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro‐inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture‐independent molecular techniques. METHODS Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST). RESULTS Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate‐derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I‐2) and CC53/60 (type II), or are CC53/60‐related singletons. CONCLUSIONS MLST typing results indicated that prostate‐derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy‐derived P. acnes isolates represent contamination from skin flora. Prostate 73: 770–777, 2013. © 2012 Wiley Periodicals, Inc.
BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro-inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture-independent molecular techniques. METHODS Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST). RESULTS Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate-derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I-2) and CC53/60 (type II), or are CC53/60-related singletons. CONCLUSIONS MLST typing results indicated that prostate-derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy-derived P. acnes isolates represent contamination from skin flora. Prostate 73: 770-777, 2013. © 2012 Wiley Periodicals, Inc.
Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro-inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture-independent molecular techniques. Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST). Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate-derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I-2) and CC53/60 (type II), or are CC53/60-related singletons. MLST typing results indicated that prostate-derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy-derived P. acnes isolates represent contamination from skin flora.
Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro-inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture-independent molecular techniques.BACKGROUNDInflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis. Multiple microorganisms have been implicated in serving as a stimulus for prostatic inflammation. The pro-inflammatory anaerobe, Propionibacterium acnes, is ubiquitously found on human skin and is associated with the skin disease acne vulgaris. Recent studies have shown that P. acnes can be detected in prostatectomy specimens by bacterial culture or by culture-independent molecular techniques.Radical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST).METHODSRadical prostatectomy tissue samples were obtained from 30 prostate cancer patients and subject to both aerobic and anaerobic culture. Cultured species were identified by 16S rDNA gene sequencing. Propionibacterium acnes isolates were typed using multilocus sequence typing (MLST).Our study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate-derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I-2) and CC53/60 (type II), or are CC53/60-related singletons.RESULTSOur study confirmed that P. acnes can be readily cultured from prostatectomy tissues (7 of 30 cases, 23%). In some cases, multiple isolates of P. acnes were cultured as well as other Propionibacterium species, such as P. granulosum and P. avidum. Overall, 9 of 30 cases (30%) were positive for Propionibacterium spp. MLST analyses identified eight different sequence types (STs) among prostate-derived P. acnes isolates. These STs belong to two clonal complexes, namely CC36 (type I-2) and CC53/60 (type II), or are CC53/60-related singletons.MLST typing results indicated that prostate-derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy-derived P. acnes isolates represent contamination from skin flora.CONCLUSIONSMLST typing results indicated that prostate-derived P. acnes isolates do not fall within the typical skin/acne STs, but rather are characteristic of STs associated with opportunistic infections and/or urethral flora. The MLST typing results argue against the likelihood that prostatectomy-derived P. acnes isolates represent contamination from skin flora.
Author Mak, Tim N.
De Marzo, Angelo M.
Sfanos, Karen S.
Brüggemann, Holger
Yu, Shu-Han
AuthorAffiliation 1 Department of Biomedicine, Aarhus University, Aarhus, Denmark
2 Department of Molecular Biology, Max Planck Institute of Infection Biology, Berlin, Germany
3 Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland
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Notes Tim N. Mak and Shu-Han Yu contributed equally to this work.
ArticleID:PROS22621
Disclosure statement: A.M.D. is currently an employee of Predictive Biosciences Inc., who also holds a part-time adjunct appointment at the Johns Hopkins University School of Medicine. However, no funding or other support was provided by the company for any of the work in this manuscript. The terms of the relationship between A.M.D. and Predictive Biosciences are managed by the Johns Hopkins University in accordance with its conflict of interest policies.
Prostate Cancer Foundation (PCF)
The Johns Hopkins University Prostate Cancer SPORE - No. 5P50CA058236
Department of Defense Prostate Cancer Research Program Award - No. W81XWH-11-1-0521
istex:604404DD7953D99958537F717015A7FF5C4D85EA
International Max Planck Research School for Infectious Diseases and Immunology
Prevent Cancer Foundation
ark:/67375/WNG-WSHMG3VF-4
Tim N. Mak and Shu‐Han Yu contributed equally to this work.
Disclosure statement: A.M.D. is currently an employee of Predictive Biosciences Inc., who also holds a part‐time adjunct appointment at the Johns Hopkins University School of Medicine. However, no funding or other support was provided by the company for any of the work in this manuscript. The terms of the relationship between A.M.D. and Predictive Biosciences are managed by the Johns Hopkins University in accordance with its conflict of interest policies.
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Huiying L. Metagenomic study of the human skin microbiome associated with acne. Nat Precedings 2010; http://dx.doi.org/10.1038/npre.2010.5305.1.
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Sfanos KS, Wilson BA, De Marzo AM, Isaacs WB. Acute inflammatory proteins constitute the organic matrix of prostatic corpora amylacea and calculi in men with prostate cancer. Proc Natl Acad Sci USA 2009;106(9):3443-3448.
McDowell A, Valanne S, Ramage G, Tunney MM, Glenn JV, McLorinan GC, Bhatia A, Maisonneuve J-F, Lodes M, Persing DH, Patrick S. Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol 2005;43(1):326-334.
Kilian M, Scholz CFP, Lomholt HB. Multilocus sequence typing and phylogenetic analysis of Propionibacterium acnes. J Clin Microbiol 2012;50(4):1158-1165.
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Cohen RJ, Shannon BA, McNeal JE, Shannon T, Garrett KL. Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: a possible link to cancer evolution? J Urol 2005;173(6):1969-1974.
McDowell A, Perry AL, Lambert PA, Patrick S. A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 2008;57(2):218-224.
Levy PY, Fenollar F, Stein A, Borrione F, Cohen E, Lebail B, Raoult D. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884-1886.
Sapadin AN, Fleischmajer R. Tetracyclines nonantibiotic properties and their clinical implications. Clin Infect Dis 2006;54(2):258-265.
Montagnini Spaine D, Mamizuka EM, Pereira Cedenho A, Srougi M. Microbiologic aerobic studies on normal male urethra. Urology 2000;56(2):207-210.
Alexeyev O, Bergh J, Marklund I, Thellenberg-Karls C, Wiklund F, Gronberg H, Bergh A, Elgh F. Association between the presence of bacterial 16S RNA in prostate specimens taken during transurethral resection of prostate and subsequent risk of prostate cancer (Sweden). Cancer Causes Control 2006;17(9):1127-1133.
Drott J, Alexeyev O, Bergstrom P, Elgh F, Olsson J. Propionibacterium acnes infection induces upregulation of inflammatory genes and cytokine secretion in prostate epithelial cells. BMC Microbiol 2010;10(1):126.
Mak TN, Fischer N, Laube B, Brinkmann V, Metruccio MM, Sfanos KS, Mollenkopf HJ, Meyer TF, Brüggemann H. Propionibacterium acnes host cell tropism contributes to vimentin-mediated invasion and induction of inflammation. Cell Microbiol 2012;14(11):1720-1733.
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Kloos WE, Bannerman TL. Update on clinical significance of coagulase-negative staphylococci. Clin Microbiol Rev 1994;7(1):117-140.
Jakab E, Zbinden R, Gubler J, Ruef C, von Graevenitz A, Krause M. Severe infections caused by Propionibacterium acnes: an underestimated pathogen in late postoperative infections. Yale J Biol Med 1996;69(6):477-482.
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Brook I. Bacteria from, solid tumours. J Med Microbiol 1990;32(3):207-210.
Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P, Lopez J. A molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 2005;28(3):242-264.
Fassi Fehri L, Mak TN, Laube B, Brinkmann V, Ogilvie LA, Mollenkopf H, Lein M, Schmidt T, Meyer TF, Brüggemann H. Prevalence of Propionibacterium acnes in diseased prostates and its inflammatory and transforming activity on prostate epithelial cells. Int J Med Microbiol 2011;301(1):69-78.
McDowell A, Gao A, Barnard E, Fink C, Murray PI, Dowson CG, Nagy I, Lambert PA, Patrick S. A novel multilocus sequence typing scheme for the opportunistic pathogen Propionibacterium acnes and characterization of type I cell surface-associated antigens. Microbiology 2011;157(7):1990-2003.
Nisbet M, Briggs S, Ellis-Pegler R, Thomas M, Holland D. Propionibacterium acnes: an under-appreciated cause of post-neurosurgical infection. J Antimicrob Chemother 2007;60(5):1097-1103.
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Pan SC, Wang JT, Hsueh PR, Chang SC. Endocarditis caused by Propionibacterium acnes: an easily ignored pathogen. J Infect 2005;51(4):e229-e231.
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Sapadin AN (e_1_2_7_26_2) 2006; 54
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– reference: Kilian M, Scholz CFP, Lomholt HB. Multilocus sequence typing and phylogenetic analysis of Propionibacterium acnes. J Clin Microbiol 2012;50(4):1158-1165.
– reference: Shannon BA, Cohen RJ, Garrett KL. Polymerase chain reaction-based identification of Propionibacterium acnes types isolated from the male urinary tract: evaluation of adolescents, normal adults and men with prostatic pathology. BJU Int 2006;98(2):388-392.
– reference: Nickel CJ, Costerton JW. Coagulase-negative Staphylococcus in chronic prostatitis. J Urol 1992;147:389-401.
– reference: Levy PY, Fenollar F, Stein A, Borrione F, Cohen E, Lebail B, Raoult D. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884-1886.
– reference: Kloos WE, Bannerman TL. Update on clinical significance of coagulase-negative staphylococci. Clin Microbiol Rev 1994;7(1):117-140.
– reference: Mak TN, Fischer N, Laube B, Brinkmann V, Metruccio MM, Sfanos KS, Mollenkopf HJ, Meyer TF, Brüggemann H. Propionibacterium acnes host cell tropism contributes to vimentin-mediated invasion and induction of inflammation. Cell Microbiol 2012;14(11):1720-1733.
– reference: Huiying L. Metagenomic study of the human skin microbiome associated with acne. Nat Precedings 2010; http://dx.doi.org/10.1038/npre.2010.5305.1.
– reference: Alexeyev O, Bergh J, Marklund I, Thellenberg-Karls C, Wiklund F, Gronberg H, Bergh A, Elgh F. Association between the presence of bacterial 16S RNA in prostate specimens taken during transurethral resection of prostate and subsequent risk of prostate cancer (Sweden). Cancer Causes Control 2006;17(9):1127-1133.
– reference: Drott J, Alexeyev O, Bergstrom P, Elgh F, Olsson J. Propionibacterium acnes infection induces upregulation of inflammatory genes and cytokine secretion in prostate epithelial cells. BMC Microbiol 2010;10(1):126.
– reference: Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 2004;186(5):1518-1530.
– reference: Galobardes B, Smith GD, Jeffreys M, Kinra S, McCarron P. Acne in adolescence and cause-specific mortality: lower coronary heart disease but higher prostate cancer mortality. Am J Epidemiol 2005;161(12):1094-1101.
– reference: Nelson DE, Van Der Pol B, Dong Q, Revanna KV, Fan B, Easwaran S, Sodergren E, Weinstock GM, Diao L, Fortenberry JD. Characteristic male urine microbiomes associate with asymptomatic sexually transmitted infection. PLoS ONE 2010;5(11):e14116.
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– reference: McDowell A, Perry AL, Lambert PA, Patrick S. A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 2008;57(2):218-224.
– reference: Willen M, Holst E, Myhre EB, Olsson AM. The bacterial flora of the genitourinary tract in healthy fertile men. Scand J Urol Nephrol 1996;30(5):387-393.
– reference: Sutcliffe S, Giovannucci E, Isaacs WB, Willett WC, Platz EA. Acne and risk of prostate cancer. Int J Cancer 2007;121(12):2688-2692.
– reference: Montagnini Spaine D, Mamizuka EM, Pereira Cedenho A, Srougi M. Microbiologic aerobic studies on normal male urethra. Urology 2000;56(2):207-210.
– reference: Sapadin AN, Fleischmajer R. Tetracyclines nonantibiotic properties and their clinical implications. Clin Infect Dis 2006;54(2):258-265.
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– reference: Sfanos KS, Sauvageot J, Fedor HL, Dick JD, De Marzo AM, Isaacs WB. A molecular analysis of prokaryotic and viral DNA sequences in prostate tissue from patients with prostate cancer indicates the presence of multiple and diverse microorganisms. Prostate 2008;68(3):306-320.
– reference: McDowell A, Valanne S, Ramage G, Tunney MM, Glenn JV, McLorinan GC, Bhatia A, Maisonneuve J-F, Lodes M, Persing DH, Patrick S. Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol 2005;43(1):326-334.
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– reference: De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, Drake CG, Nakai Y, Isaacs WB, Nelson WG. Inflammation in prostate carcinogenesis. Nat Rev Cancer 2007;7(4):256-269.
– reference: Sfanos KS, De Marzo AM. Prostate cancer and inflammation: the evidence. Histopathology 2012;60(1):199-215.
– reference: Jakab E, Zbinden R, Gubler J, Ruef C, von Graevenitz A, Krause M. Severe infections caused by Propionibacterium acnes: an underestimated pathogen in late postoperative infections. Yale J Biol Med 1996;69(6):477-482.
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Snippet BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate...
Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate carcinogenesis....
BACKGROUND Inflammation is commonly observed in radical prostatectomy specimens, and evidence suggests that inflammation may contribute to prostate...
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SubjectTerms Adult
Aged
Gram-Positive Bacterial Infections - microbiology
Humans
infection
inflammation
Male
Middle Aged
MLST
Multilocus Sequence Typing - methods
Propionibacterium
Propionibacterium - genetics
Propionibacterium - isolation & purification
Propionibacterium acnes
Propionibacterium acnes - genetics
Propionibacterium acnes - isolation & purification
Prostate - microbiology
prostate cancer
Prostatectomy
Prostatic Neoplasms - microbiology
Sequence Analysis, DNA
Title Multilocus sequence typing (MLST) analysis of Propionibacterium acnes isolates from radical prostatectomy specimens
URI https://api.istex.fr/ark:/67375/WNG-WSHMG3VF-4/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fpros.22621
https://www.ncbi.nlm.nih.gov/pubmed/23184509
https://www.proquest.com/docview/1636453810
https://www.proquest.com/docview/1338399906
https://www.proquest.com/docview/1654674162
https://pubmed.ncbi.nlm.nih.gov/PMC4124636
Volume 73
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