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Published in: Clinical Oral Investigations 8/2016

Open Access 01-11-2016 | Original Article

Isolation of Propionibacterium acnes among the microbiota of primary endodontic infections with and without intraoral communication

Authors: Sadia Ambreen Niazi, Hana Suleiman Al Kharusi, Shanon Patel, Kenneth Bruce, David Beighton, Federico Foschi, Francesco Mannocci

Published in: Clinical Oral Investigations | Issue 8/2016

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Abstract

Objectives

The presence of opportunistic pathogens such as Propionibacterium acnes (P. acnes) may contribute to the endodontic pathology. The presence of P. acnes may be influenced by different endodontic conditions.
The aims of the study were firstly, to identify P. acnes within the whole cultivable microbiota of primary endodontic infections, to investigate which P. acnes phylotypes predominate in such infections and secondly to determine if the presence of an “open” communication (e.g. a sinus) can be associated with the isolation of P. acnes from the root canal.

Material and methods

The predominant cultivable microbiota of 15 primary endodontic lesions (7 without communication with the oral environment and 8 with an open communication) were identified using partial 16S ribosomal RNA (rRNA) gene sequence analysis. The identification of the organism was determined by interrogating the Human Oral Microbiome Database. The P. acnes isolates were typed on the basis of the recA gene sequence comparison. A neighbor-joining tree was constructed using MEGA 4.1 with the inclusion of known recA sequences.

Results

There was no difference in the number of species identified from lesions without communication (5.86 ± 3.7) and those with communication (5.37 ± 3.6) (P > 0.05). PCR-based 16S rRNA gene sequencing revealed P. acnes as the most prevalent isolate recovered from lesions with communication. recA gene sequencing revealed two phylogenetic lineages present in lesion with communication, with mainly type I (further split into type IA and type IB) and type II.

Conclusions

The presence of P. acnes as opportunistic pathogens has been confirmed and may sustain the traits observed in specific clinical presentations.

Clinical relevance

Clinical management of open lesions may require further disinfection to eliminate opportunistic bacteria.
Literature
1.
go back to reference Tancrede C (1992) Role of human microflora in health and disease. Eur J Clin Microbiol Infect Dis 11(11):1012–1015PubMedCrossRef Tancrede C (1992) Role of human microflora in health and disease. Eur J Clin Microbiol Infect Dis 11(11):1012–1015PubMedCrossRef
2.
go back to reference McDowell A, Gao A, Barnard E, Fink C, Murray PI, Dowson CG, Nagy I, Lambert PA, Patrick S (2011) A novel multilocus sequence typing scheme for the opportunistic pathogen Propionibacterium acnes and characterization of type I cell surface-associated antigens. Microbiology 157(Pt 7):1990–2003. doi:10.1099/mic.0.049676-0 PubMedCrossRef McDowell A, Gao A, Barnard E, Fink C, Murray PI, Dowson CG, Nagy I, Lambert PA, Patrick S (2011) A novel multilocus sequence typing scheme for the opportunistic pathogen Propionibacterium acnes and characterization of type I cell surface-associated antigens. Microbiology 157(Pt 7):1990–2003. doi:10.​1099/​mic.​0.​049676-0 PubMedCrossRef
3.
go back to reference Brook I, Frazier EH (1991) Infections caused by Propionibacterium species. Rev Infect Dis 13(5):819–822PubMedCrossRef Brook I, Frazier EH (1991) Infections caused by Propionibacterium species. Rev Infect Dis 13(5):819–822PubMedCrossRef
4.
go back to reference Doyle A, Beigi B, Early A, Blake A, Eustace P, Hone R (1995) Adherence of bacteria to intraocular lenses: a prospective study. Br J Ophthalmol 79(4):347–349PubMedPubMedCentralCrossRef Doyle A, Beigi B, Early A, Blake A, Eustace P, Hone R (1995) Adherence of bacteria to intraocular lenses: a prospective study. Br J Ophthalmol 79(4):347–349PubMedPubMedCentralCrossRef
5.
go back to reference Eady EA, Ingham E (1994) Propionibacterim acnes—friend or foe? Rev Med Microbiol 5:163–173CrossRef Eady EA, Ingham E (1994) Propionibacterim acnes—friend or foe? Rev Med Microbiol 5:163–173CrossRef
6.
go back to reference Leyden JJ (2001) The evolving role of Propionibacterium acnes in acne. Semin Cutan Med Surg 20(3):139–143PubMedCrossRef Leyden JJ (2001) The evolving role of Propionibacterium acnes in acne. Semin Cutan Med Surg 20(3):139–143PubMedCrossRef
7.
go back to reference Eishi Y, Suga M, Ishige I, Kobayashi D, Yamada T, Takemura T, Takizawa T, Koike M, Kudoh S, Costabel U, Guzman J, Rizzato G, Gambacorta M, du Bois R, Nicholson AG, Sharma OP, Ando M (2002) Quantitative analysis of mycobacterial and propionibacterial DNA in lymph nodes of Japanese and European patients with sarcoidosis. J Clin Microbiol 40(1):198–204PubMedPubMedCentralCrossRef Eishi Y, Suga M, Ishige I, Kobayashi D, Yamada T, Takemura T, Takizawa T, Koike M, Kudoh S, Costabel U, Guzman J, Rizzato G, Gambacorta M, du Bois R, Nicholson AG, Sharma OP, Ando M (2002) Quantitative analysis of mycobacterial and propionibacterial DNA in lymph nodes of Japanese and European patients with sarcoidosis. J Clin Microbiol 40(1):198–204PubMedPubMedCentralCrossRef
9.
go back to reference Schaeverbeke T, Lequen L, de Barbeyrac B, Labbe L, Bebear CM, Morrier Y, Bannwarth B, Bebear C, Dehais J (1998) Propionibacterium acnes isolated from synovial tissue and fluid in a patient with oligoarthritis associated with acne and pustulosis. Arthritis Rheum 41(10):1889–1893PubMedCrossRef Schaeverbeke T, Lequen L, de Barbeyrac B, Labbe L, Bebear CM, Morrier Y, Bannwarth B, Bebear C, Dehais J (1998) Propionibacterium acnes isolated from synovial tissue and fluid in a patient with oligoarthritis associated with acne and pustulosis. Arthritis Rheum 41(10):1889–1893PubMedCrossRef
10.
go back to reference Cohen RJ, B.A. S, J.E. MN, Shannon T, K.L. G (2005) Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: a possible link to cancer evolution? J Urol 173:1969–1974PubMedCrossRef Cohen RJ, B.A. S, J.E. MN, Shannon T, K.L. G (2005) Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: a possible link to cancer evolution? J Urol 173:1969–1974PubMedCrossRef
11.
go back to reference Mathisen GE, D. MR, L. GW, M. CD (1984) Brain abscess and cerebritis. Rev Infect Dis 6(Suppl.1):101–106CrossRef Mathisen GE, D. MR, L. GW, M. CD (1984) Brain abscess and cerebritis. Rev Infect Dis 6(Suppl.1):101–106CrossRef
12.
go back to reference Abolnik IZ, Eaton JV, Sexton DJ (1995) Propionibacterium acnes vertebral osteomyelitis following lumbar puncture: case report and review. Clin Infect Dis 21(3):694–695PubMedCrossRef Abolnik IZ, Eaton JV, Sexton DJ (1995) Propionibacterium acnes vertebral osteomyelitis following lumbar puncture: case report and review. Clin Infect Dis 21(3):694–695PubMedCrossRef
13.
go back to reference Harris AE, Hennicke C, Byers K, Welch WC (2005) Postoperative discitis due to Propionibacterium acnes: a case report and review of the literature. Surg Neurol 63(6):538–541 discussion 541PubMedCrossRef Harris AE, Hennicke C, Byers K, Welch WC (2005) Postoperative discitis due to Propionibacterium acnes: a case report and review of the literature. Surg Neurol 63(6):538–541 discussion 541PubMedCrossRef
14.
go back to reference Halkic N, Blanc C, Corthesy ME, Corpataux JM (2001) Lumbar spondylodiscitis after epidural anaesthesia at a distant site. Anaesthesia 56(6):602–603PubMedCrossRef Halkic N, Blanc C, Corthesy ME, Corpataux JM (2001) Lumbar spondylodiscitis after epidural anaesthesia at a distant site. Anaesthesia 56(6):602–603PubMedCrossRef
15.
go back to reference Friberg O, Svedjeholm R, Kallman J, Soderquist B (2007) Incidence, microbiological findings, and clinical presentation of sternal wound infections after cardiac surgery with and without local gentamicin prophylaxis. Eur J Clin Microbiol Infect Dis 26(2):91–97PubMedCrossRef Friberg O, Svedjeholm R, Kallman J, Soderquist B (2007) Incidence, microbiological findings, and clinical presentation of sternal wound infections after cardiac surgery with and without local gentamicin prophylaxis. Eur J Clin Microbiol Infect Dis 26(2):91–97PubMedCrossRef
16.
go back to reference Benz MS, Scott IU, Flynn HW Jr, Unonius N, Miller D (2004) Endophthalmitis isolates and antibiotic sensitivities: a 6-year review of culture-proven cases. Am J Ophthalmol 137(1):38–42 Benz MS, Scott IU, Flynn HW Jr, Unonius N, Miller D (2004) Endophthalmitis isolates and antibiotic sensitivities: a 6-year review of culture-proven cases. Am J Ophthalmol 137(1):38–42
17.
go back to reference Gunthard H, Hany A, Turina M, Wust J (1994) Propionibacterium acnes as a cause of aggressive aortic valve endocarditis and importance of tissue grinding: case report and review. J Clin Microbiol 32(12):3043–3045PubMedPubMedCentral Gunthard H, Hany A, Turina M, Wust J (1994) Propionibacterium acnes as a cause of aggressive aortic valve endocarditis and importance of tissue grinding: case report and review. J Clin Microbiol 32(12):3043–3045PubMedPubMedCentral
18.
go back to reference McDowell A, Valanne S, Ramage G, Tunney MM, Glenn JV, McLorinan GC, Bhatia A, Maisonneuve JF, Lodes M, Persing DH, Patrick S (2005) Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol 43(1):326–334PubMedPubMedCentralCrossRef McDowell A, Valanne S, Ramage G, Tunney MM, Glenn JV, McLorinan GC, Bhatia A, Maisonneuve JF, Lodes M, Persing DH, Patrick S (2005) Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol 43(1):326–334PubMedPubMedCentralCrossRef
19.
go back to reference McDowell A, Perry AL, Lambert PA, Patrick S (2008) A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 57(Pt 2):218–224PubMedCrossRef McDowell A, Perry AL, Lambert PA, Patrick S (2008) A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 57(Pt 2):218–224PubMedCrossRef
20.
go back to reference Valanne S, McDowell A, Ramage G, Tunney MM, Einarsson GG, O’Hagan S, Wisdom GB, Fairley D, Bhatia A, Maisonneuve JF, Lodes M, Persing DH, Patrick S (2005) CAMP factor homologues in Propionibacterium acnes: a new protein family differentially expressed by types I and II. Microbiology 151(Pt 5):1369–1379PubMedCrossRef Valanne S, McDowell A, Ramage G, Tunney MM, Einarsson GG, O’Hagan S, Wisdom GB, Fairley D, Bhatia A, Maisonneuve JF, Lodes M, Persing DH, Patrick S (2005) CAMP factor homologues in Propionibacterium acnes: a new protein family differentially expressed by types I and II. Microbiology 151(Pt 5):1369–1379PubMedCrossRef
21.
go back to reference Lodes MJ, Secrist H, Benson DR, Jen S, Shanebeck KD, Guderian J, Maisonneuve JF, Bhatia A, Persing D, Patrick S, Skeiky YA (2006) Variable expression of immunoreactive surface proteins of Propionibacterium acnes. Microbiology 152(12):3667–3681PubMedCrossRef Lodes MJ, Secrist H, Benson DR, Jen S, Shanebeck KD, Guderian J, Maisonneuve JF, Bhatia A, Persing D, Patrick S, Skeiky YA (2006) Variable expression of immunoreactive surface proteins of Propionibacterium acnes. Microbiology 152(12):3667–3681PubMedCrossRef
22.
go back to reference Nagy I, Pivarcsi A, Kis K, Koreck A, Bodai L, McDowell A, Seltmann H, Patrick S, Zouboulis CC, Kemeny L (2006) Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/chemokines in human sebocytes. Microbes and Infection/Institut Pasteur 8(8):2195–2205. doi:10.1016/j.micinf.2006.04.001 CrossRef Nagy I, Pivarcsi A, Kis K, Koreck A, Bodai L, McDowell A, Seltmann H, Patrick S, Zouboulis CC, Kemeny L (2006) Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/chemokines in human sebocytes. Microbes and Infection/Institut Pasteur 8(8):2195–2205. doi:10.​1016/​j.​micinf.​2006.​04.​001 CrossRef
23.
24.
go back to reference Sampedro MF, Piper KE, McDowell A, Patrick S, Mandrekar JN, Rouse MS, Steckelberg JM, Patel R (2009) Species of Propionibacterium and Propionibacterium acnes phylotypes associated with orthopedic implants. Diagn Microbiol Infect Dis 64(2):138–145 doi:S0732-8893(09)00029–7PubMedCrossRef Sampedro MF, Piper KE, McDowell A, Patrick S, Mandrekar JN, Rouse MS, Steckelberg JM, Patel R (2009) Species of Propionibacterium and Propionibacterium acnes phylotypes associated with orthopedic implants. Diagn Microbiol Infect Dis 64(2):138–145 doi:S0732-8893(09)00029–7PubMedCrossRef
25.
28.
go back to reference Lane DJ (ed) (1991) 16S/23S rRNA sequencing. In nucleic acid techniques in bacterial systematics. Wiley, Chichester Lane DJ (ed) (1991) 16S/23S rRNA sequencing. In nucleic acid techniques in bacterial systematics. Wiley, Chichester
29.
go back to reference Kakehashi S, Stanley HR, Fitzgerald RJ (1965) The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol 20:340–349PubMedCrossRef Kakehashi S, Stanley HR, Fitzgerald RJ (1965) The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol 20:340–349PubMedCrossRef
30.
go back to reference Siqueira JF Jr, Rocas IN (2009) Diversity of endodontic microbiota revisited. J Dent Res 88(11):969–981 Siqueira JF Jr, Rocas IN (2009) Diversity of endodontic microbiota revisited. J Dent Res 88(11):969–981
31.
go back to reference Lee YJ, Kim MK, Hwang HK, Kook JK (2005) Isolation and identification of bacteria from the root canal of the teeth diagnosed as the acute pulpitis and acute periapical abscess. J Korean Acad Conserv Dent 30(5):13CrossRef Lee YJ, Kim MK, Hwang HK, Kook JK (2005) Isolation and identification of bacteria from the root canal of the teeth diagnosed as the acute pulpitis and acute periapical abscess. J Korean Acad Conserv Dent 30(5):13CrossRef
32.
go back to reference Kim SY, Choi HY, Park SH, Choi B (2003) Distribution of oral pathogens in infection of endodontic origin. J Korean Acad Conserv Dent 28(4):303–313CrossRef Kim SY, Choi HY, Park SH, Choi B (2003) Distribution of oral pathogens in infection of endodontic origin. J Korean Acad Conserv Dent 28(4):303–313CrossRef
33.
go back to reference Kum KY, Foud AF (2003) PCR-based identification of Eubacteirum species in endodontic infection. J Korean Acad Conserv Dent 28(3):241–248CrossRef Kum KY, Foud AF (2003) PCR-based identification of Eubacteirum species in endodontic infection. J Korean Acad Conserv Dent 28(3):241–248CrossRef
34.
go back to reference Munson MA, Pitt-Ford T, Chong B, Weightman A, Wade WG (2002) Molecular and cultural analysis of the microflora associated with endodontic infections. J Dent Res 81(11):761–766PubMedCrossRef Munson MA, Pitt-Ford T, Chong B, Weightman A, Wade WG (2002) Molecular and cultural analysis of the microflora associated with endodontic infections. J Dent Res 81(11):761–766PubMedCrossRef
35.
go back to reference van Steenbergen TJ, van Winkelhoff AJ, Mayrand D, Grenier D, de Graaff J (1984) Bacteroides endodontalis sp. nov., an asaccharolytic black-pigmented Bacteroides species from infected dental root canals. Int J Sys Bact 34:118–120CrossRef van Steenbergen TJ, van Winkelhoff AJ, Mayrand D, Grenier D, de Graaff J (1984) Bacteroides endodontalis sp. nov., an asaccharolytic black-pigmented Bacteroides species from infected dental root canals. Int J Sys Bact 34:118–120CrossRef
36.
go back to reference Fouad AF, Barry J, Caimano M, Clawson M, Zhu Q, Carver R, Hazlett K, Radolf JD (2002) PCR-based identification of bacteria associated with endodontic infections. J Clin Microbiol 40(9):3223–3231PubMedPubMedCentralCrossRef Fouad AF, Barry J, Caimano M, Clawson M, Zhu Q, Carver R, Hazlett K, Radolf JD (2002) PCR-based identification of bacteria associated with endodontic infections. J Clin Microbiol 40(9):3223–3231PubMedPubMedCentralCrossRef
37.
go back to reference Siqueira JF Jr, Rocas IN (2002) Dialister pneumosintes can be a suspected endodontic pathogen. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94(4):494–498PubMedCrossRef Siqueira JF Jr, Rocas IN (2002) Dialister pneumosintes can be a suspected endodontic pathogen. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94(4):494–498PubMedCrossRef
38.
go back to reference LE C d PV (2002) Fusobacterium nucleatum in endodontic flare-ups. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 93(2):179–183CrossRef LE C d PV (2002) Fusobacterium nucleatum in endodontic flare-ups. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 93(2):179–183CrossRef
39.
go back to reference Tunney MM, Patrick S, Gorman SP, Nixon JR, Anderson N, Davis RI, Hanna D, Ramage G (1998) Improved detection of infection in hip replacements. A currently underestimated problem. J Bone Joint Surg Br Volume 80(4):568–572CrossRef Tunney MM, Patrick S, Gorman SP, Nixon JR, Anderson N, Davis RI, Hanna D, Ramage G (1998) Improved detection of infection in hip replacements. A currently underestimated problem. J Bone Joint Surg Br Volume 80(4):568–572CrossRef
40.
go back to reference Lazar JM, Schulman DS (1992) Propionibacterium acnes prosthetic valve endocarditis: a case of severe aortic insufficiency. Clin Cardiol 15(4):299–300PubMedCrossRef Lazar JM, Schulman DS (1992) Propionibacterium acnes prosthetic valve endocarditis: a case of severe aortic insufficiency. Clin Cardiol 15(4):299–300PubMedCrossRef
Metadata
Title
Isolation of Propionibacterium acnes among the microbiota of primary endodontic infections with and without intraoral communication
Authors
Sadia Ambreen Niazi
Hana Suleiman Al Kharusi
Shanon Patel
Kenneth Bruce
David Beighton
Federico Foschi
Francesco Mannocci
Publication date
01-11-2016
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 8/2016
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-1739-x

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