1887

Abstract

Prosthetic joint infections (PJIs) are challenging to treat therapeutically because the infectious agents often are resistant to antibiotics and capable of abundant growth in surface-attached biofilms. Though infection rates are low, ca. 1–2 %, the overall increase in the sheer number of joint replacement surgeries results in an increase in patients at risk.

This study investigates the consensus of microbial species comprising PJI ecology, which is currently lacking.

In this study, PJI populations from seven patients were analysed using combined culturing and whole-genome shotgun sequencing (WGSS) to establish population profiles and compare WGSS and culture methods for detection and identification of the PJI microbiome.

WGSS detected strains when culture did not, notably dormant, culture-resistant and rare microbes. The CosmosID algorithm was used to predict micro-organisms present in the PJI and discriminate contaminants. However, culturing indicated the presence of microbes falling below the WGSS algorithm threshold. In these instances, microbes cultured are believed to be minor species. The two strategies were combined to build a population profile.

Variability between and among PJIs showed that most infections were distinct and unique. Comparative analysis of populations revealed PJIs to form clusters that were related to, but separate from, vaginal, skin and gut microbiomes. Fungi and protists were detected by WGSS, but the role of fungi is just beginning to be understood and for protists it is unknown. These micro-organisms and their novel and strain-specific microbial interactions remain to be determined in current clinical tests.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001068
2019-08-28
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/jmm/68/10/1507.html?itemId=/content/journal/jmm/10.1099/jmm.0.001068&mimeType=html&fmt=ahah

References

  1. Zimmerli W, Trampuz A, Ochsner PE, Infections P-J. Prosthetic-joint infections. N Engl J Med 2004; 351:1645–1654 [View Article]
    [Google Scholar]
  2. Kurtz S, Ong K, Lau E, Mowat F, Halpern M. Projections of primary and revision hip and knee arthroplasty in the United States from 2005 to 2030. J Bone Jt Surg 2007; 89-A:780–785
    [Google Scholar]
  3. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284:1318–1322 [View Article]
    [Google Scholar]
  4. Cunningham DJ, Kavolus JJ, Bolognesi MP, Wellman SS, Seyler TM. Specific infectious organisms associated with poor outcomes in treatment for hip periprosthetic infection. J Arthroplasty 2017; 32:1984–1990 [View Article]
    [Google Scholar]
  5. Wimmer MD, Friedrich MJ, Randau TM, Ploeger MM, Schmolders J et al. Polymicrobial infections reduce the cure rate in prosthetic joint infections: outcome analysis with two-stage exchange and follow-up ≥two years. Int Orthop 2016; 40:1367–1373 [View Article]
    [Google Scholar]
  6. Guren E, Figved W, Frihagen F, Watne LO, Westberg M. Prosthetic joint infection-a devastating complication of hemiarthroplasty for hip fracture. Acta Orthop 2017; 88:383–389 [View Article]
    [Google Scholar]
  7. Elias S, Banin E. Multi-Species biofilms: living with friendly neighbors. FEMS Microbiol Rev 2012; 36:990–1004 [View Article]
    [Google Scholar]
  8. Butler-Wu SM, Burns EM, Pottinger PS, Magaret AS, Rakeman JL et al. Optimization of periprosthetic culture for diagnosis of Propionibacterium acnes prosthetic joint infection. J Clin Microbiol 2011; 49:2490–2495 [View Article]
    [Google Scholar]
  9. Peel TN, Dylla BL, Hughes JG, Lynch DT, Greenwood-Quaintance KE et al. Improved diagnosis of prosthetic joint infection by culturing periprosthetic tissue specimens in blood culture bottles. MBio 2016; 7:1–8 [View Article]
    [Google Scholar]
  10. Larsen LH, Lange J, Xu Y, Schønheyder HC. Optimizing culture methods for diagnosis of prosthetic joint infections: a summary of modifications and improvements reported since 1995. J Med Microbiol 2012; 61:309–316 [View Article]
    [Google Scholar]
  11. Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK et al. Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 2007; 357:654–663 [View Article]
    [Google Scholar]
  12. Penterman J, Nguyen D, Anderson E, Staudinger BJ, Greenberg EP et al. Rapid evolution of culture-impaired bacteria during adaptation to biofilm growth. Cell Rep 2014; 6:293–300 [View Article]
    [Google Scholar]
  13. Cazanave C, Greenwood-Quaintance KE, Hanssen AD, Karau MJ, Schmidt SM et al. Rapid molecular microbiologic diagnosis of prosthetic joint infection. J Clin Microbiol 2013; 51:2280–2287 [View Article]
    [Google Scholar]
  14. Morgenstern C, Cabric S, Perka C, Trampuz A, Renz N. Synovial fluid multiplex PCR is superior to culture for detection of low-virulent pathogens causing periprosthetic joint infection. Diagn Microbiol Infect Dis 2018; 90:115–119 [View Article]
    [Google Scholar]
  15. Swearingen MC, DiBartola AC, Dusane D, Granger J, Stoodley P. 16S rRNA analysis provides evidence of biofilms on all components of three infected periprosthetic knees including permanent braided suture. Pathog Dis 2016; 74:ftw083–11 [View Article]
    [Google Scholar]
  16. Xu Y, Rudkjøbing VB, Simonsen O, Pedersen C, Lorenzen J et al. Bacterial diversity in suspected prosthetic joint infections: an exploratory study using 16S rRNA gene analysis. FEMS Immunol Med Microbiol 2012; 65:291–304 [View Article]
    [Google Scholar]
  17. Ponnusamy D, Kozlova EV, Sha J, Erova TE, Azar SR et al. Cross-talk among flesh-eating Aeromonas hydrophila strains in mixed infection leading to necrotizing fasciitis. Proc Natl Acad Sci U S A 2016; 113:722–727 [View Article]
    [Google Scholar]
  18. Yan Q, Wi M, Thoendel MJ, Raval YS, Greenwood-quaintance KE et al. Evaluation of the CosmosID bioinformatics platform for prosthetic Joint-Associated sonicate fluid shotgun metagenomic data analysis. J Clin Microbiol 2019; 57:1–13
    [Google Scholar]
  19. Arias CA, Murray BE. The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 2012; 10:266–278 [View Article]
    [Google Scholar]
  20. McMullen AR, Anderson N, Wallace MA, Shupe A, Burnham C-AD. When good bugs go bad: epidemiology and antimicrobial resistance profiles of Corynebacterium striatum, an emerging multidrug-resistant, opportunistic pathogen. Antimicrob Agents Chemother 2017; 61:AAC.01111–.01117 [View Article]
    [Google Scholar]
  21. Hellmark B, Söderquist B, Unemo M, Nilsdotter-Augustinsson Åsa. Comparison of Staphylococcus epidermidis isolated from prosthetic joint infections and commensal isolates in regard to antibiotic susceptibility, agr type, biofilm production, and epidemiology. Int J Med Microbiol 2013; 303:32–39 [View Article]
    [Google Scholar]
  22. Thoendel M, Jeraldo P, Greenwood-Quaintance KE, Yao J, Chia N et al. Impact of contaminating DNA in whole-genome amplification kits used for metagenomic shotgun sequencing for infection diagnosis. J Clin Microbiol 2017; 55:1789–1801 [View Article]
    [Google Scholar]
  23. Lewis K, Cells P. Persister cells. Annu Rev Microbiol 2010; 64:357–372 [View Article]
    [Google Scholar]
  24. Street TL, Sanderson ND, Atkins BL, Brent AJ, Cole K et al. Molecular diagnosis of Orthopedic-Device-Related infection directly from sonication fluid by metagenomic sequencing. J Clin Microbiol 2017; 55:2334–2347 [View Article]
    [Google Scholar]
  25. Ivy MI, Thoendel MJ, Jeraldo PR, Greenwood-Quaintance KE, Hanssen AD et al. Direct detection and identification of prosthetic joint infection pathogens in synovial fluid by metagenomic shotgun sequencing. J Clin Microbiol 2018; 56:JCM.00402–.00418 [View Article]
    [Google Scholar]
  26. Ottesen A, Ramachandran P, Reed E, White JR, Hasan N et al. Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak. BMC Microbiol 2016; 16:1–11 [View Article]
    [Google Scholar]
  27. Hasan NA, Young BA, Minard-Smith AT, Saeed K, Li H et al. Microbial community profiling of human saliva using shotgun metagenomic sequencing. PLoS One 2014; 9:e97699 [View Article]
    [Google Scholar]
  28. Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 2014; 345:1048–1052 [View Article]
    [Google Scholar]
  29. Chang Q, Luan Y, Sun F. Variance adjusted weighted UniFrac: a powerful beta diversity measure for comparing communities based on phylogeny. BMC Bioinformatics 2011; 12:118–14 [View Article]
    [Google Scholar]
  30. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article]
    [Google Scholar]
  31. Havelaar AH, Van OM, Drost YC. F-Specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water; 1993; 592956–2962
  32. Armon R, Kott Y. Bacteriophages as indicators of pollution. Crit Rev Environ Sci Technol 1996; 26:299–335 [View Article]
    [Google Scholar]
  33. Jofre J. Indicators of waterborne enteric viruses. In Bosch A. editor Human Viruses in Water Elsevier B.V; 2007 pp 227–249
    [Google Scholar]
  34. Grabow W. Bacteriophages : Update on application as models for viruses in water. Water Res 2001; 27:251–268
    [Google Scholar]
  35. Mesquita MM, Emelko MB. Bacteriophages as surrogates for the fate and transport of pathogens in source water and in drinking water treatment processes. In Kurtboke Ipek. editor Bacteriophages InTech; 2012 p ISBN:978-953-51-0272-4
    [Google Scholar]
  36. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 2015; 12:902–903 [View Article]
    [Google Scholar]
  37. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014; 12:1–12 [View Article]
    [Google Scholar]
  38. Tyner H, Patel R. Propionibacterium acnes biofilm - a sanctuary for Staphylococcus aureus?. Anaerobe 2016; 40:63–67 [View Article]
    [Google Scholar]
  39. Cazanave C, Greenwood-Quaintance KE, Hanssen AD, Patel R. Corynebacterium prosthetic joint infection. J Clin Microbiol 2012; 50:1518–1523 [View Article]
    [Google Scholar]
  40. Shah NB, Tande AJ, Patel R, Berbari EF. Anaerobic prosthetic joint infection. Anaerobe 2015; 36:1–8 [View Article]
    [Google Scholar]
  41. Johnson JL, Moore WEC, Moore LVH. Bacteroides caccae sp. nov., Bacteroides merdae sp. nov., and Bacteroides stercoris sp. nov. isolated from human feces. Int J Syst Bacteriol 1986; 36:499–501 [View Article]
    [Google Scholar]
  42. Hong P-Y, Wu J-H, Liu W-T. Relative abundance of Bacteroides spp. in stools and wastewaters as determined by hierarchical oligonucleotide primer extension. Appl Environ Microbiol 2008; 74:2882–2893 [View Article]
    [Google Scholar]
  43. Ottman N, Smidt H, de Vos WM, Belzer C. The function of our microbiota: who is out there and what do they do?. Front Cell Infect Microbiol 2012; 2:1–11 [View Article]
    [Google Scholar]
  44. Marcy Y, Ouverney C, Bik EM, Lösekann T, Ivanova N et al. Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA 2007; 104:11889–11894 [View Article]
    [Google Scholar]
  45. He X, McLean JS, Edlund A, Yooseph S, Hall AP et al. Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle. Proc Natl Acad Sci USA 2015; 112:244–249 [View Article]
    [Google Scholar]
  46. Marchandin H, Jean-Pierre H, Carrière C, Canovas F, Darbas H et al. Prosthetic joint infection due to Veillonella dispar. EJCMID 2001; 20:340–342 [View Article]
    [Google Scholar]
  47. Gneiding K, Frodl R, Funke G. Identities of Microbacterium spp. encountered in human clinical specimens. J Clin Microbiol 2008; 46:3646–3652 [View Article]
    [Google Scholar]
  48. Boisrenoult P. Cutibacterium acnes prosthetic joint infection: diagnosis and treatment. Orthopaedics & Traumatology: Surgery & Research 2018; 104:S19–S24 [View Article]
    [Google Scholar]
  49. Scholz CFP, Kilian M. The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov. Int J Syst Evol Microbiol 2016; 66:4422–4432 [View Article]
    [Google Scholar]
  50. Brown TS, Petis SM, Osmon DR, Mabry TM, Berry DJ et al. Periprosthetic joint infection with fungal pathogens. J Arthroplasty 2018; 33:2605–2612 [View Article]
    [Google Scholar]
  51. Tornero E, Senneville E, Euba G, Petersdorf S, Rodriguez-Pardo D et al. Characteristics of prosthetic joint infections due to Enterococcus sp. and predictors of failure: a multi-national study. Clin Microbiol Infect 2014; 20:1219–1224 [View Article]
    [Google Scholar]
  52. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol 2000; 30:1217–1258 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001068
Loading
/content/journal/jmm/10.1099/jmm.0.001068
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error