Propionibacterium avidum as an Etiological Agent of Prosthetic Hip Joint Infection

Peter Wildeman, Holger Brüggemann, Christian F P Scholz, Andreas Leimbach, Bo Söderquist, Peter Wildeman, Holger Brüggemann, Christian F P Scholz, Andreas Leimbach, Bo Söderquist

Abstract

Propionibacterium acnes is well-established as a possible etiologic agent of prosthetic joint infections (PJIs). Other Propionibacterium spp. have occasionally been described as a cause of PJIs, but this has not previously been the case for P. avidum despite its capacity to form biofilm. We describe two patients with prosthetic hip joint infections caused by P. avidum. Both patients were primarily operated with an anteriorly curved skin incision close to the skin crease of the groin, and both were obese. Initial treatment was performed according to the DAIR procedure (debridement, antibiotics, and implant retention). In case 1, the outcome was successful, but in case 2, a loosening of the cup was present 18 months post debridement. The P. avidum isolate from case 1 and two isolates from case 2 (obtained 18 months apart) were selected for whole genome sequencing. The genome of P. avidum obtained from case 1 was approximately 60 kb larger than the genomes of the two isolates of case 2. These latter isolates were clonal with the exception of SNPs in the genome. All three strains possessed the gene cluster encoding exopolysaccharide synthesis. P. avidum has a pathogenic potential and the ability to cause clinically relevant infections, including abscess formation, in the presence of foreign bodies such as prosthetic joint components. Skin incision in close proximity to the groin or deep skin crease, such as the anteriorly curved skin incision approach, might pose a risk of PJIs by P. avidum, especially in obese patients.

Conflict of interest statement

Competing Interests: Co-author Holger Brüggemann is a PLOS ONE Editorial Board member. This does not alter the authors’ adherence to PLOS ONE Editorial policies and criteria.

Figures

Fig 1. Anteriorly curved skin incision approach.
Fig 1. Anteriorly curved skin incision approach.
Case 1 left hip and. Red line indicates the anterior skin incision.
Fig 2. Anteriorly curved skin incision approach.
Fig 2. Anteriorly curved skin incision approach.
Case 2 right hip. Red line indicates the anterior skin incision.
Fig 3. Genome comparison of P .…
Fig 3. Genome comparison of P. avidum and other cutaneous Propionibacteria.
P. avidum strain T13 was used as the reference genome. The most inner rings represent GC content and GC skew variation. Other P. avidum genomes (rings from inside to outside) are added according to their similarity to the reference genomes, i.e. T15 is most similar and HGH0353 is most dissimilar to T13. The comparison of P. avidum genomes with representative genomes of P. acnes/P. humerusii/P. granulosum shows overall genome synteny but also revealed P. avidum-specific genomic regions. These islands are numbered (1–20); gene content of the islands is shown in Table A1 in S1 File. Island 14 is the locus encoding EPS biosynthesis. The BRIG program was used to generate the figure.
Fig 4. A phylogenetic analysis of sequenced…
Fig 4. A phylogenetic analysis of sequenced P. avidum strains and their relation to other cutaneous Propionibacteria.
The analysis is based on the shared core genome of the depicted organisms. T13, T14, and T15 cluster closely not only with each other, but also with strain 44067 (14), another clinical isolate from an abscess. Some strains (KPL2000, KPL2005, KPL1852, KPL1838) are currently not correctly assigned to P. avidum in the public databases. The population of P. avidum can be divided into three (phylogenetic) clusters: cluster A: T13, T14, T15, 44067; cluster B: ATCC25577, KPL2000, KPL2005, TM16; cluster C: KPL1852, KPL1838). Their gene content differences are shown in Table B1-3 in S2 File.

References

    1. Learmonth ID, Young C, Rorabeck C. The operation of the century: total hip replacement. Lancet. 2007;370(9597):1508–19.
    1. Tande AJ, Patel R. Prosthetic joint infection. Clin Microbiol Rev. 2014;27(2):302–45. 10.1128/CMR.00111-13
    1. Perry AL, Lambert PA. Propionibacterium acnes. Lett Appl Microbiol. 2006;42(3):185–8.
    1. Perry A, Lambert P. Propionibacterium acnes: infection beyond the skin. Expert Rev Anti Infect Ther. 2011;9(12):1149–56. 10.1586/eri.11.137
    1. Zimmerli W, Trampuz A, Ochsner PE. Prosthetic-joint infections. N Engl J Med. 2004;351(16):1645–54.
    1. Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol. 2012;65(2):158–68. 10.1111/j.1574-695X.2012.00938.x
    1. Lutz MF, Berthelot P, Fresard A, Cazorla C, Carricajo A, Vautrin AC, et al. Arthroplastic and osteosynthetic infections due to Propionibacterium acnes: a retrospective study of 52 cases, 1995–2002. Eur J Clin Microbiol Infect Dis. 2005;24(11):739–44.
    1. Zeller V, Ghorbani A, Strady C, Leonard P, Mamoudy P, Desplaces N. Propionibacterium acnes: an agent of prosthetic joint infection and colonization. J Infect. 2007;55(2):119–24.
    1. Piper KE, Jacobson MJ, Cofield RH, Sperling JW, Sanchez-Sotelo J, Osmon DR, et al. Microbiologic diagnosis of prosthetic shoulder infection by use of implant sonication. J Clin Microbiol. 2009;47(6):1878–84. 10.1128/JCM.01686-08
    1. Nystrom LM, Wyatt CM, Noiseux NO. Arthroplasty infection by Priopionibacterium granulosum treated with reimplantation despite ongoing purulent-appearing fluid collection. J Arthroplasty. 2013;28(1):198 e5–8. 10.1016/j.arth.2012.03.004
    1. Panagea S, Corkill JE, Hershman MJ, Parry CM. Breast abscess caused by Propionibacterium avidum following breast reduction surgery: case report and review of the literature. J Infect. 2005;51(5):e253–5.
    1. Vohra A, Saiz E, Chan J, Castro J, Amaro R, Barkin J. Splenic abscess caused by Propionibacterium avidum as a complication of cardiac catheterization. Clin Infect Dis. 1998;26(3):770–1.
    1. Janvier F, Delacour H, Larreche S, Abdalla S, Aubert P, Merens A. Abdominal wall and intra-peritoneal abscess by Propionibacterium avidum as a complication of abdominal parietoplasty. Pathol Biol (Paris). 2013;61(5):223–5.
    1. Million M, Roux F, Cohen Solal J, Breville P, Desplaces N, Barthas J, et al. Septic arthritis of the hip with Propionibacterium avidum bacteremia after intraarticular treatment for hip osteoarthritis. Joint Bone Spine. 2008;75(3):356–8. 10.1016/j.jbspin.2007.06.012
    1. Mak TN, Schmid M, Brzuszkiewicz E, Zeng G, Meyer R, Sfanos KS, et al. Comparative genomics reveals distinct host-interacting traits of three major human-associated propionibacteria. BMC Genomics. 2013;14:640 10.1186/1471-2164-14-640
    1. Bertin KC, Rottinger H. Anterolateral mini-incision hip replacement surgery: a modified Watson-Jones approach. Clin Orthop Relat Res. 2004(429):248–55.
    1. Muller M, Tohtz S, Springer I, Dewey M, Perka C. Randomized controlled trial of abductor muscle damage in relation to the surgical approach for primary total hip replacement: minimally invasive anterolateral versus modified direct lateral approach. Arch Orthop Trauma Surg. 2011;131(2):179–89. 10.1007/s00402-010-1117-0
    1. Paprosky WG, Perona PG, Lawrence JM. Acetabular defect classification and surgical reconstruction in revision arthroplasty. A 6-year follow-up evaluation. J Arthroplasty. 1994;9(1):33–44.
    1. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75 10.1186/1471-2164-9-75
    1. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics. 2011;12:124 10.1186/1471-2105-12-124
    1. Ordogh L, Hunyadkurti J, Voros A, Horvath B, Szucs A, Urban E, et al. Complete Genome Sequence of Propionibacterium avidum Strain 44067, Isolated from a Human Skin Abscess. Genome announcements. 2013;1(3).
    1. Parvizi J, Zmistowski B, Adeli B. Periprosthetic joint infection: treatment options. Orthopedics. 2010;33(9):659 10.3928/01477447-20100722-42
    1. Chechik O, Khashan M, Lador R, Salai M, Amar E. Surgical approach and prosthesis fixation in hip arthroplasty world wide. Arch Orthop Trauma Surg. 2013;133(11):1595–600. 10.1007/s00402-013-1828-0
    1. Petis S, Howard JL, Lanting BL, Vasarhelyi EM. Surgical approach in primary total hip arthroplasty: anatomy, technique and clinical outcomes. Can J Surg. 2015;58(2):128–39.
    1. Leunig M, Faas M, von Knoch F, Naal FD. Skin crease 'bikini' incision for anterior approach total hip arthroplasty: surgical technique and preliminary results. Clin Orthop Relat Res. 2013;471(7):2245–52. 10.1007/s11999-013-2806-0
    1. Alecci V, Valente M, Crucil M, Minerva M, Pellegrino CM, Sabbadini DD. Comparison of primary total hip replacements performed with a direct anterior approach versus the standard lateral approach: perioperative findings. J Orthop Traumatol. 2011;12(3):123–9. 10.1007/s10195-011-0144-0
    1. Woo RY, Morrey BF. Dislocations after total hip arthroplasty. J Bone Joint Surg Am. 1982;64(9):1295–306.
    1. Masonis JL, Bourne RB. Surgical approach, abductor function, and total hip arthroplasty dislocation. Clin Orthop Relat Res. 2002(405):46–53.
    1. Lindgren V, Garellick G, Karrholm J, Wretenberg P. The type of surgical approach influences the risk of revision in total hip arthroplasty: a study from the Swedish Hip Arthroplasty Register of 90,662 total hipreplacements with 3 different cemented prostheses. Acta Orthop. 2012;83(6):559–65. 10.3109/17453674.2012.742394
    1. Tsukada S, Wakui M. Lower Dislocation Rate Following Total Hip Arthroplasty via Direct Anterior Approach than via Posterior Approach: Five-Year-Average Follow-Up Results. Open Orthop J. 2015;9:157–62. 10.2174/1874325001509010157
    1. Connolly KP, Kamath AF. Direct anterior total hip arthroplasty: Comparative outcomes and contemporary results. World Journal of Orthopedics. 2016;7(2):94–101. 10.5312/wjo.v7.i2.94
    1. Bergin PF, Doppelt JD, Kephart CJ, Benke MT, Graeter JH, Holmes AS, et al. Comparison of minimally invasive direct anterior versus posterior total hip arthroplasty based on inflammation and muscle damage markers. J Bone Joint Surg Am. 2011;93(15):1392–8. 10.2106/JBJS.J.00557
    1. Xu CP, Li X, Song JQ, Cui Z, Yu B. Mini-Incision versus Standard Incision Total Hip Arthroplasty Regarding Surgical Outcomes: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. PLoS One. 2013;8(11).
    1. McGinley KJ, Webster GF, Leyden JJ. Regional variations of cutaneous propionibacteria. Appl Environ Microbiol. 1978;35(1):62–6.
    1. Khassebaf J, Hellmark B, Davidsson S, Unemo M, Nilsdotter-Augustinsson A, Soderquist B. Antibiotic susceptibility of Propionibacterium acnes isolated from orthopaedic implant-associated infections. Anaerobe. 2015;32:57–62. 10.1016/j.anaerobe.2014.12.006
    1. Wang B, Jessamine P, Desjardins M, Toye B, Ramotar K. Direct mecA polymerase chain reaction testing of blood culture bottles growing Gram-positive cocci and the clinical potential in optimizing antibiotic therapy for staphylococcal bacteremia. Diagn Microbiol Infect Dis. 2013;75(1):37–41. 10.1016/j.diagmicrobio.2012.09.014
    1. Wang WL, Everett ED, Johnson M, Dean E. Susceptibility of Propionibacterium acnes to seventeen antibiotics. Antimicrob Agents Chemother. 1977;11(1):171–3.
    1. Stefansdottir A, Robertsson O, A WD, Kiernan S, Gustafson P, Lidgren L. Inadequate timing of prophylactic antibiotics in orthopedic surgery. We can do better. Acta Orthop. 2009;80(6):633–8. 10.3109/17453670903316868
    1. Bayston R, Nuradeen B, Ashraf W, Freeman BJ. Antibiotics for the eradication of Propionibacterium acnes biofilms in surgical infection. J Antimicrob Chemother. 2007;60(6):1298–301.
    1. Sendi P, Zimmerli W. Antimicrobial treatment concepts for orthopaedic device-related infection. Clin Microbiol Infect. 2012;18(12):1176–84. 10.1111/1469-0691.12003
    1. Furustrand Tafin U, Corvec S, Betrisey B, Zimmerli W, Trampuz A. Role of rifampin against Propionibacterium acnes biofilm in vitro and in an experimental foreign-body infection model. Antimicrob Agents Chemother. 2012;56(4):1885–91. 10.1128/AAC.05552-11
    1. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421 10.1186/1471-2105-10-421
    1. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7.
    1. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. 10.1093/molbev/mst197
    1. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77. 10.1089/cmb.2012.0021
    1. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12:402 10.1186/1471-2164-12-402
    1. Moreno-Hagelsieb G, Latimer K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics. 2008;24(3):319–24.

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