Molecular diagnosis of orthopedic-device-related infection directly from sonication fluid by metagenomic sequencing

Journal of Clinical Microbiology

Volumn 55, Issue 8, 2017, Pages 2334-2347

  Street, Teresa L ^a   Sanderson, Nicholas D ^a   Atkins, Bridget L ^b,c   Brent, Andrew J ^a,b   Cole, Kevin ^d   Foster, Dona ^a   McNally, Martin A ^b   Oakley, Sarah ^c   Peto, Leon ^a   Taylor, Adrian ^b   Peto, Tim E A ^a,e   Crook, Derrick W ^a,e   Eyre, David W ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NUFFIELD ORTHOPAEDIC CENTRE   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d ROYAL SUSSEX COUNTY HOSPITAL   (United Kingdom)

^e NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

Author keywords

Diagnosis; Metagenomic sequencing; Orthopedic device infection; Prosthetic joint infection

Indexed keywords

BACTERIAL DNA;

AEROBIC BACTERIUM; ANAEROBIC BACTERIUM; ARTICLE; BACTERIUM CULTURE; CAUSAL ATTRIBUTION; CONTROLLED STUDY; CORYNEBACTERIUM; DEVICE INFECTION; DNA CONTAMINATION; DNA EXTRACTION; DNA SEQUENCE; ENTEROBACTERIACEAE; ENTEROCOCCUS; GENE SEQUENCE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; METAGENOMICS; MOLECULAR DIAGNOSIS; NONHUMAN; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; PROSTHESIS INFECTION; SENSITIVITY AND SPECIFICITY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS; ULTRASOUND; COMPARATIVE STUDY; EVALUATION STUDY; INFECTION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PROCEDURES; PROSTHESES AND ORTHOSES; SPECIMEN HANDLING; TIME FACTOR;

BACTERIOLOGICAL TECHNIQUES; HUMANS; METAGENOMICS; MOLECULAR DIAGNOSTIC TECHNIQUES; PROSTHESES AND IMPLANTS; PROSTHESIS-RELATED INFECTIONS; SENSITIVITY AND SPECIFICITY; SONICATION; SPECIMEN HANDLING; TIME FACTORS;

EID: 85026215329     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00462-17     Document Type: Article

References (40)

1. Lamagni T. 2014. Epidemiology and burden of prosthetic joint infections. J Antimicrob Chemother 69(Suppl 1):i5-i10. https://doi.org/10 .1093/jac/dku247.
2. Atkins BL, Athanasou N, Deeks JJ, Crook DW, Simpson H, Peto TE, McLardy-Smith P, Berendt AR. 1998. Prospective evaluation of criteria for microbiological diagnosis of prosthetic-joint infection at revision arthroplasty. The OSIRIS Collaborative Study Group. J Clin Microbiol 36:2932-2939.
3. Parvizi J, Zmistowski B, Berbari EF, Bauer TW, Springer BD, Della Valle CJ, Garvin KL, Mont MA, Wongworawat MD, Zalavras CG. 2011. New definition for periprosthetic joint infection: from the Workgroup of the Musculoskeletal Infection Society. Clin Orthop Relat Res 469:2992-2994. https://doi.org/10.1007/s11999-011-2102-9.
4. Osmon DR, Berbari EF, Berendt AR, Lew D, Zimmerli W, Steckelberg JM, Rao N, Hanssen A, Wilson WR. 2013. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 56:e1-e25. https://doi.org/ 10.1093/cid/cis803.
5. Bejon P, Berendt A, Atkins BL, Green N, Parry H, Masters S, McLardy-Smith P, Gundle R, Byren I. 2010. Two-stage revision for prosthetic joint infection: predictors of outcome and the role of reimplantation microbiology. J Antimicrob Chemother 65:569-575. https://doi.org/10.1093/ jac/dkp469.
6. 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 80:568-572. https://doi.org/10.1302/0301-620X.80B4.8473.
7. Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R. 2007. Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 357:654-663. https://doi.org/10.1056/NEJMoa061588.
8. Piper KE, Jacobson MJ, Cofield RH, Sperling JW, Sanchez-Sotelo J, Osmon DR, McDowell A, Patrick S, Steckelberg JM, Mandrekar JN, Sampedro MF, Patel R. 2009. Microbiologic diagnosis of prosthetic shoulder infection by use of implant sonication. J Clin Microbiol 47:1878-1884. https://doi .org/10.1128/JCM.01686-08.
9. Achermann Y, Vogt M, Leunig M, Wust J, Trampuz A. 2010. Improved diagnosis of periprosthetic joint infection by multiplex PCR of sonication fluid from removed implants. J Clin Microbiol 48:1208-1214. https://doi .org/10.1128/JCM.00006-10.
10. Gomez E, Cazanave C, Cunningham SA, Greenwood-Quaintance KE, Steckelberg JM, Uhl JR, Hanssen AD, Karau MJ, Schmidt SM, Osmon DR, Berbari EF, Mandrekar J, Patel R. 2012. Prosthetic joint infection diagnosis using broad-range PCR of biofilms dislodged from knee and hip arthroplasty surfaces using sonication. J Clin Microbiol 50:3501-3508. https://doi.org/10.1128/JCM.00834-12.
11. Cazanave C, Greenwood-Quaintance KE, Hanssen AD, Karau MJ, Schmidt SM, Gomez Urena EO, Mandrekar JN, Osmon DR, Lough LE, Pritt BS, Steckelberg JM, Patel R. 2013. Rapid molecular microbiologic diagnosis of prosthetic joint infection. J Clin Microbiol 51:2280-2287. https://doi .org/10.1128/JCM.00335-13.
12. Ryu SY, Greenwood-Quaintance KE, Hanssen AD, Mandrekar JN, Patel R. 2014. Low sensitivity of periprosthetic tissue PCR for prosthetic knee infection diagnosis. Diagn Microbiol Infect Dis 79:448-453. https://doi .org/10.1016/j.diagmicrobio.2014.03.021.
13. Fenollar F, Roux V, Stein A, Drancourt M, Raoult D. 2006. Analysis of 525 samples to determine the usefulness of PCR amplification and sequencing of the 16S rRNA gene for diagnosis of bone and joint infections. J Clin Microbiol 44:1018-1028. https://doi.org/10.1128/JCM.44.3.1018-1028.2006.
14. Tunney MM, Patrick S, Curran MD, Ramage G, Hanna D, Nixon JR, Gorman SP, Davis RI, Anderson N. 1999. Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene. J Clin Microbiol 37:3281-3290.
15. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW. 2012. Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 13:601-612. https://doi.org/10.1038/nrg3226.
16. Lefterova MI, Suarez CJ, Banaei N, Pinsky BA. 2015. Next-generation sequencing for infectious disease diagnosis and management: a report of the Association for Molecular Pathology. J Mol Diagn 17:623-634. https://doi.org/10.1016/j.jmoldx.2015.07.004.
17. Goldberg B, Sichtig H, Geyer C, Ledeboer N, Weinstock GM. 2015. Making the leap from research laboratory to clinic: challenges and opportunities for next-generation sequencing in infectious disease diagnostics. mBio 6:e01888-15. https://doi.org/10.1128/mBio.01888-15.
18. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. https://doi.org/10.1186/s12915-014-0087-z.
19. Laurence M, Hatzis C, Brash DE. 2014. Common contaminants in nextgeneration sequencing that hinder discovery of low-abundance microbes. PLoS One 9:e97876. https://doi.org/10.1371/journal.pone .0097876.
20. Eyre DW, Golubchik T, Gordon NC, Bowden R, Piazza P, Batty EM, Ip CLC, Wilson DJ, Didelot X, O'Connor L, Lay R, Buck D, Kearns AM, Shaw A, Paul J, Wilcox MH, Donnelly PJ, Peto TEA, Walker AS, Crook DW. 2012. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2:e001124. https://doi.org/10.1136/bmjopen-2012-001124.
21. Reuter S, Ellington MJ, Cartwright EJ, Koser CU, Torok ME, Gouliouris T, Harris SR, Brown NM, Holden MT, Quail M, Parkhill J, Smith GP, Bentley SD, Peacock SJ. 2013. Rapid bacterial whole-genome sequencing to enhance diagnostic and public health microbiology. JAMA Intern Med 173:1397-1404. https://doi.org/10.1001/jamainternmed.2013.7734.
22. Didelot X, Eyre DW, Cule M, Ip CLC, Ansari MA, Griffiths D, Vaughan A, O'Connor L, Golubchik T, Batty EM, Piazza P, Wilson DJ, Bowden R, Donnelly PJ, Dingle KE, Wilcox M, Walker AS, Crook DW, Peto TEA, Harding RM. 2012. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 13:R118. https://doi .org/10.1186/gb-2012-13-12-r118.
23. Eyre DW, Fawley WN, Best EL, Griffiths D, Stoesser NE, Crook DW, Peto TE, Walker AS, Wilcox MH. 2013. Comparison of multilocus variable-number tandem-repeat analysis and whole-genome sequencing for investigation of Clostridium difficile transmission. J Clin Microbiol 51:4141-4149. https://doi.org/10.1128/JCM.01095-13.
24. Walker TM, Lalor MK, Broda A, Ortega LS, Morgan M, Parker L, Churchill S, Bennett K, Golubchik T, Giess AP, Elias CD, Jeffery KJ, Bowler ICJW, Laurenson IF, Barrett A, Drobniewski F, McCarthy ND, Anderson LF, Abubakar I, Thomas HL, Monk P, Smith EG, Walker AS, Crook DW, Peto TEA, Conlon CP. 2014. Assessment of Mycobacterium tuberculosis transmission in Oxfordshire, UK, 2007-12, with whole pathogen genome sequences: an observational study. Lancet Respir Med 2:285-292. https://doi.org/10.1016/S2213-2600(14)70027-X.
25. Stoesser N, Batty EM, Eyre DW, Morgan M, Wyllie DH, Del Ojo Elias C, Johnson JR, Walker AS, Peto TE, Crook DW. 2013. Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J Antimicrob Chemother 68: 2234-2244. https://doi.org/10.1093/jac/dkt180.
26. Gordon NC, Price JR, Cole K, Everitt R, Morgan M, Finney J, Kearns AM, Pichon B, Young B, Wilson DJ, Llewelyn MJ, Paul J, Peto TEA, Crook DW, Walker AS, Golubchik T. 2014. Prediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencing. J Clin Microbiol 52:1182-1191. https://doi.org/10.1128/JCM.03117-13.
27. Walker TM, Kohl TA, Omar SV, Hedge J, Del Oji Elias C, Bradley P, Iqbal Z, Feverriegel S, Niehaus KE, Wilson DJ, Clifton DA, Kapatai G, Ip CL, Bowden R, Drobniewski FA, Allix-Beguec C, Gaudin C, Parkhill J, Diet R, Supply P, Crook DW, Smith EG, Walker AS, Ismail N, Niemann S, Petot TEA, Modernizing Medical Microbiology (MMM) Informatics Group. 2015. Wholegenome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis 15:1193-1202. https://doi.org/10.1016/S1473-3099(15)00062-6.
28. Li Y, Metcalf BJ, Chochua S, Li Z, Gertz RE, Jr, Walker H, Hawkins PA, Tran T, Whitney CG, McGee L, Beall BW. 2016. Penicillin-binding protein transpeptidase signatures for tracking and predicting beta-lactam resistance levels in Streptococcus pneumoniae. mBio 7:e00756-16. https://doi .org/10.1128/mBio.00756-16.
29. Pankhurst LJ, Del Ojo Elias C, Votintseva AA, Walker TM, Cole K, Davies J, Fermont JM, Gascoyne-Binzi DM, Kohl TA, Kong C, Lemaitre N, Niemann S, Paul J, Rogers TR, Roycroft E, Smith EG, Supply P, Tang P, Wilcox MH, Wordsworth S, Wyllie D, Xu L, Crook DW, Compass-TB Study Group. 2016. Rapid, comprehensive, and affordable mycobacterial diagnosis with whole-genome sequencing: a prospective study. Lancet Respir Med 4:49-58. https://doi.org/10.1016/S2213-2600(15)00466-X.
30. Hasman H, Saputra D, Sicheritz-Ponten T, Lund O, Svendsen CA, Frimodt-Moller N, Aarestrup FM. 2014. Rapid whole-genome sequencing for detection and characterization of microorganisms directly from clinical samples. J Clin Microbiol 52:139-146. https://doi.org/10.1128/JCM .02452-13.
31. Wilson MR, Naccache SN, Samayoa E, Biagtan M, Bashir H, Yu G, Salamat SM, Somasekar S, Federman S, Miller S, Sokolic R, Garabedian E, Candotti F, Buckley RH, Reed KD, Meyer TL, Seroogy CM, Galloway R, Henderson SL, Gern JE, DeRisi JL, Chiu CY. 2014. Actionable diagnosis of neuroleptospirosis by next-generation sequencing. N Engl J Med 370:2408-2417. https://doi.org/10.1056/NEJMoa1401268.
32. Naccache SN, Peggs KS, Mattes FM, Phadke R, Garson JA, Grant P, Samayoa E, Federman S, Miller S, Lunn MP, Gant V, Chiu CY. 2015. Diagnosis of neuroinvasive astrovirus infection in an immunocompromised adult with encephalitis by unbiased next-generation sequencing. Clin Infect Dis 60:919-923. https://doi.org/10.1093/cid/ ciu912.
33. Wilson MR, Shanbhag NM, Reid MJ, Singhal NS, Gelfand JM, Sample HA, Benkli B, O'Donovan BD, Ali IK, Keating MK, Dunnebacke TH, Wood MD, Bollen A, DeRisi JL. 2015. Diagnosing Balamuthia mandrillaris encephalitis with metagenomic deep sequencing. Ann Neurol 78:722-730. https://doi.org/10.1002/ana.24499.
34. Kearney MF, Spindler J, Wiegand A, Shao W, Anderson EM, Maldarelli F, Ruscetti FW, Mellors JW, Hughes SH, Le Grice SF, Coffin JM. 2012. Multiple sources of contamination in samples from patients reported to have XMRV infection. PLoS One 7:e30889. https://doi.org/10.1371/ journal.pone.0030889.
35. Naccache SN, Greninger AL, Lee D, Coffey LL, Phan T, Rein-Weston A, Aronsohn A, Hackett J, Jr, Delwart EL, Chiu CY. 2013. The perils of pathogen discovery: origin of a novel parvovirus-like hybrid genome traced to nucleic acid extraction spin columns. J Virol 87:11966-11977. https://doi.org/10.1128/JVI.02323-13.
36. Votintseva AA, Pankhurst LJ, Anson LW, Morgan MR, Gascoyne-Binzi D, Walker TM, Quan TP, Wyllie DH, Del Ojo Elias C, Wilcox M, Walker AS, Peto TE, Crook DW. 2015. Mycobacterial DNA extraction for wholegenome sequencing from early positive liquid (MGIT) cultures. J Clin Microbiol 53:1137-1143. https://doi.org/10.1128/JCM.03073-14.
37. Wood DE, Salzberg SL. 2014. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46. https://doi .org/10.1186/gb-2014-15-3-r46.
38. Ondov BD, Bergman NH, Phillippy AM. 2011. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12:385. https://doi .org/10.1186/1471-2105-12-385.
39. Youden WJ. 1950. Index for rating diagnostic tests. Cancer 3:32-35. https://doi.org/10.1002/1097-0142(1950)3:1-32::AID-CNCR282 0030106-3.0.CO;2-3.
40. Portillo ME, Salvadó M, Sorli L, Alier A, Martinez S, Trampuz A, Gómez J, Puig L, Horcajada JP. 2012. Multiplex PCR of sonication fluid accurately differentiates between prosthetic joint infection and aseptic failure. J Infect 65:541-548. https://doi.org/10.1016/j.jinf.2012.08.018.