Abstract
Purpose
Even though effective techniques in diagnosis of periprosthetic joint infections (PJIs) have been developed, the optimal modality has yet to be determined. The present meta-analysis aimed to compare the diagnostic accuracy of dithiothreitol (DTT) and sonication against the Musculoskeletal Infection Society criteria in patients undergoing revision joint surgery.
Methods
We searched the PubMed, Scopus, and Central Cochrane register of controlled trials as well as gray literature until the 9th of November, 2021. We included articles considering the comparative diagnostic accuracy of sonication and DTT in adult patients having revision hip and knee arthroplasty for septic or aseptic reasons. We calculated pooled sensitivity, specificity, and diagnostic accuracy of the above diagnostic techniques against the Musculoskeletal Infection Society (MSIS) criteria and created receiver operating characteristics (ROC) curves to enable comparisons between each other. The quality of included papers was evaluated utilizing QUADAS-2 and QUADAS-C tools.
Results
Data from five comparative studies totaling 726 implants were pooled together. The diagnostic accuracy of DTT and sonication were 86.7% (95% CI 82.7 to 90.1) and 83.9% (95% CI 79.7 to 87.5), respectively. Pooled sensitivity and specificity showed no statistically significant differences between DTT and sonication (0.7 [95% CI 0.62 to 0.77] vs 0.72 [95% CI 0.65 to 0.78], p = 0.14; and 0.99 [95% CI 0.97 to 1] vs 0.97 [95% CI 0.93 to 0.99], p = 5.5, respectively).
Conclusions
This meta-analysis did not identify any clinically meaningful difference between the diagnostic potential of sonication and the chemical-based biofilm dislodgment methods. This finding remained robust after adjusting for the administration of antibiotics prophylaxis, implementation of the polymerase chain reaction of sonicated fluid, and study quality.
Similar content being viewed by others
Data Availability
Not applicable.
Change history
24 March 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00264-022-05363-8
References
Tsang STJ, Gwynne PJ, Gallagher MP, Simpson AHRW (2018) The biofilm eradication activity of acetic acid in the management of periprosthetic joint infection. Bone Joint Res 7(8):517–523. https://doi.org/10.1302/2046-3758.78.BJR-2018-0045.R1
Ahmed SS, Haddad FS (2019) Prosthetic joint infection. Bone Joint Res 8(11):570–572. https://doi.org/10.1302/2046-3758.812.BJR-2019-0340
Springer BD, Cahue S, Etkin CD, Lewallen DG, McGrory BJ (2017) Infection burden in total hip and knee arthroplasties: an international registry-based perspective. Arthroplasty Today 3(2):137–140. https://doi.org/10.1016/j.artd.2017.05.003
Parvizi J, Tan TL, Goswami K, Higuera C, Della Valle C, Chen AF, Shohat N (2018) The 2018 definition of periprosthetic hip and knee infection: an evidence-based and validated criteria. J Arthroplasty 33(5):1309-1314.e2. https://doi.org/10.1016/j.arth.2018.02.078
Kurtz SM, Ong KL, Lau E, Bozic KJ, Berry D, Parvizi J (2010) Prosthetic joint infection risk after TKA in the Medicare population. Clin Orthop Relat Res 468(1):52–56. https://doi.org/10.1007/s11999-009-1013-5
Rasouli MR, Harandi AA, Adeli B, Purtill JJ, Parvizi J (2012) Revision total knee arthroplasty: infection should be ruled out in all cases. J Arthroplasty 27(6):1239-43.e1–2. https://doi.org/10.1016/j.arth.2011.01.019
Sambri A, Cadossi M, Giannini S, Pignatti G, Marcacci M, Neri MP, Maso A, Storni E, Gamberini S, Naldi S, Torri A, Zannoli S, Tassinari M, Fantini M, Bianchi G, Donati D, Sambri V (2018) Is treatment with dithiothreitol more effective than sonication for the diagnosis of prosthetic joint infection? Clin Orthop Relat Res 76(1):137–145. https://doi.org/10.1007/s11999.0000000000000060
Aggarwal VK, Bakhshi H, Ecker NU, Parvizi J, Gehrke T, Kendoff D (2014) Organism profile in periprosthetic joint infection: pathogens differ at two arthroplasty infection referral centers in Europe and in the United States. J Knee Surg 27(5):399–406. https://doi.org/10.1055/s-0033-1364102
Schinsky MF, Della Valle CJ, Sporer SM, Paprosky WG (2008) Perioperative testing for joint infection in patients undergoing revision total hip arthroplasty. J Bone Joint Surg Am 90(9):1869–1875. https://doi.org/10.2106/JBJS.G.01255
Holinka J, Bauer L, Hirschl AM, Graninger W, Windhager R, Presterl E (2011) Sonication cultures of explanted components as an add-on test to routinely conducted microbiological diagnostics improve pathogen detection. J Orthop Res 29(4):617–622. https://doi.org/10.1002/jor.21286
Trampuz A, Osmon DR, Hanssen AD, Steckelberg JM, Patel R (2003) Molecular and antibiofilm approaches to prosthetic joint infection. Clin Orthop Relat Res 414:69–88. https://doi.org/10.1097/01.blo.0000087324.60612.93
Costerton JW, Post JC, Ehrlich GD, Hu FZ, Kreft R, Nistico L, Kathju S, Stoodley P, Hall-Stoodley L, Maale G, James G, Sotereanos N, DeMeo P (2011) New methods for the detection of orthopedic and other biofilm infections. FEMS Immunol Med Microbiol 61(2):133–140. https://doi.org/10.1111/j.1574-695X.2010.00766.x
Evangelopoulos DS, Stathopoulos IP, Morassi GP, Koufos S, Albarni A, Karampinas PK, Stylianakis A, Kohl S, Pneumaticos S, Vlamis J (2013) Sonication: a valuable technique for diagnosis and treatment of periprosthetic joint infections. Scientific World Journal 2013:375140https://doi.org/10.1155/2013/375140
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(7):654–663. https://doi.org/10.1056/NEJMoa061588
Ahmed EA, Almutairi MK, Alkaseb AT (2021) Accuracy of tissue and sonication fluid sampling for the diagnosis of fracture-related infection: diagnostic meta-analysis. Cureus 13(5):e14925. https://doi.org/10.7759/cureus.14925
Drago L (2018) CORR Insights®: is treatment with dithiothreitol more effective than sonication for the diagnosis of prosthetic joint infection? Clin Orthop Relat Res 476(2):439–440. https://doi.org/10.1007/s11999.0000000000000135
Trampuz A, Piper KE, Hanssen AD, Osmon DR, Cockerill FR, Steckelberg JM, Patel R (2006) Sonication of explanted prosthetic components in bags for diagnosis of prosthetic joint infection is associated with risk of contamination. J Clin Microbiol 44(2):628–631. https://doi.org/10.1128/JCM.44.2.628-631.2006
Drago L, Romanò CL, Mattina R, Signori V, De Vecchi E (2012) Does dithiothreitol improve bacterial detection from infected prostheses? A pilot study infection. Clin Orthop Relat Res 470(10):2915–2925. https://doi.org/10.1007/s11999-012-2415-3
Parvizi J, Gehrke T, International Consensus Group on Periprosthetic Joint Infection (2014) Definition of periprosthetic joint infection. J Arthroplasty 29(7):1331. https://doi.org/10.1016/j.arth.2014.03.009
Gamie Z, Karthikappallil D, Gamie E, Stamiris S, Kenanidis E, Tsiridis E (2021) Molecular sequencing technologies in the diagnosis and management of prosthetic joint infections. Expert Rev Mol Diagn 1-21https://doi.org/10.1080/14737159.2021.1894929
Hawass NE. (1997) Comparing the sensitivities and specificities of two diagnostic procedures performed on the same group of patients Br J Radiol (832):360–6. https://doi.org/10.1259/bjr.70.832.9166071
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155(8):529–36. https://doi.org/10.7326/0003-4819-155-8-201110180-00009
Yang B, Mallett S, Takwoingi Y, Davenport CF, Hyde CJ, Whiting PF, Deeks JJ, Leeflang MMG (2021) QUADAS-C Group. QUADAS-C: a tool for assessing risk of bias in comparative diagnostic accuracy studies. Ann Intern Med 4(11):1592–1599. https://doi.org/10.7326/M21-2234
Drago L, Signori V, De Vecchi E, Vassena C, Palazzi E, Cappelletti L, Romanò D, Romanò CL (2013) Use of dithiothreitol to improve the diagnosis of prosthetic joint infections. J Orthop Res 31(11):1694–1699. https://doi.org/10.1002/jor.22423
Randau TM, Molitor E, Fröschen FS, Hörauf A, Kohlhof H, Scheidt S, Gravius S, Hischebeth GT (2021) The performance of a dithiothreitol-based diagnostic system in diagnosing periprosthetic joint infection compared to sonication fluid cultures and tissue biopsies. Z Orthop Unfall 159(4):447–453. https://doi.org/10.1055/a-1150-8396
Karbysheva S, Renz N, Yermak K, Cabric S, Trampuz A (2019) New methods in the diagnosis of prosthetic joint infection. Traumatol Orthop Russ 25(4):56–63. https://doi.org/10.21823/2311-2905-2019-25-4-56-63
Fang X, Zhang L, Cai Y, Huang Z, Li W, Zhang C, Yang B, Lin J, Wahl P, Zhang W (2021) Effects of different tissue specimen pretreatment methods on microbial culture results in the diagnosis of periprosthetic joint infection. Bone Joint Res 10(2):96–104. https://doi.org/10.1302/2046-3758.102.BJR-2020-0104.R3
Sebastian S, Malhotra R, Sreenivas V, Kapil A, Dhawan B (2021) The utility of dithiothreitol treatment of periprosthetic tissues and explanted implants in the diagnosis of prosthetic joint infection. Indian J Med Microbiol 39(2):179–183. https://doi.org/10.1016/j.ijmmb.2020.12.004
Sambri A, Maso A, Storni E, Donati ME, Pederzoli A, Dallari D, Bianchi G, Donati DM (2019). Is sonication of antibiotic-loaded cement spacers useful in two-stage revision of prosthetic joint infection? J Microbiol Methods 81-84https://doi.org/10.1016/j.mimet.2018.12.006
Parvizi J, Pawasarat IM, Azzam KA, Joshi A, Hansen EN, Bozic KJ (2010) Periprosthetic joint infection: the economic impact of methicillin-resistant infections. J Arthroplasty 25(SUPPL. 6):103–107. https://doi.org/10.1016/j.arth.2010.04.011
Walls RJ, Roche SJ, O’Rourke A, McCabe JP (2008) Surgical site infection with methicillin-resistant Staphylococcus aureus after primary total hip replacement. J Bone Joint Surg Br 90(3):292–298. https://doi.org/10.1302/0301-620X.90B3.20155
Ting NT, Della Valle CJ (2017) Diagnosis of periprosthetic joint infection-an algorithm-based approach. J Arthroplasty 32(7):2047–2050. https://doi.org/10.1016/j.arth.2017.02.070
Morgenstern C, Cabric S, Perka C, Trampuz A, Renz N (2018) Synovial fluid multiplex PCR is superior to culture for detection of low-virulent pathogens causing periprosthetic joint infection. Diagn Microbiol Infect Dis 90(2):115–119. https://doi.org/10.1016/j.diagmicrobio.2017.10.016
Nelson CL, Jones RB, Wingert NC, Foltzer M, Bowen TR (2014) Sonication of antibiotic spacers predicts failure during two-stage revision for prosthetic knee and hip infections. Clin Orthop Relat Res 472(7):2208–2214. https://doi.org/10.1007/s11999-014-3571-4
Van Cauter M, Cornu O, Yombi JC, Rodriguez-Villalobos H, Kaminski L (2018) The effect of storage delay and storage temperature on orthopaedic surgical samples contaminated by Staphylococcus Epidermidis. PLoS One 13(3):e0192048. https://doi.org/10.1371/journal.pone.0192048
Kamineni S, Huang C (2019) The antibacterial effect of sonication and its potential medical application. SICOT J 5:19. https://doi.org/10.1051/sicotj/2019017
De Vecchi E, Bortolin M, Signori V, Romanò CL, Drago L (2016) Treatment with dithiothreitol improves bacterial recovery from tissue samples in osteoarticular and joint infections. J Arthroplasty 31(12):2867–2870. https://doi.org/10.1016/j.arth.2016.05.008
Stephan A, Thürmer A, Glauche I, Nowotny J, Zwingenberger S, Stiehler M (2021) Does preoperative antibiotic prophylaxis affect sonication-based diagnosis in implant-associated infection? J Orthop Res:1–7. https://doi.org/10.1002/jor.25015
Li C, Renz N, Trampuz A, Ojeda-Thies C (2020) Twenty common errors in the diagnosis and treatment of periprosthetic joint infection. Int Orthop 44(1):3–14. https://doi.org/10.1007/s00264-019-04426-7
Prieto-Borja L, Rodriguez-Sevilla G, Auñon A, Pérez-Jorge C, Sandoval E, Garcia-Cañete J, Gadea I, Fernandez-Roblas R, Blanco A, Esteban J (2017) Evaluation of a commercial multiplex PCR (Unyvero i60®) designed for the diagnosis of bone and joint infections using prosthetic-joint sonication. Enferm Infect Microbiol Clin 35(4):236–242. https://doi.org/10.1016/j.eimc.2016.09.007
Tan TL, Maltenfort MG, Chen AF, Shahi A, Higuera CA, Siqueira M, Parvizi J (2018) Development and evaluation of a preoperative risk calculator for periprosthetic joint infection following total joint arthroplasty. J Bone Joint Surg Am 100(9):777–785. https://doi.org/10.2106/JBJS.16.01435
Indelli PF, Ghirardelli S, Violante B, Amanatullah DF (2021) Next generation sequencing for pathogen detection in periprosthetic joint infections. EFORT Open Rev 6(4):236–244. https://doi.org/10.1302/2058-5241.6.200099
Flurin L, Wolf MJ, Greenwood-Quaintance KE, Sanchez-Sotelo J, Patel R (2021) Targeted next generation sequencing for elbow periprosthetic joint infection diagnosis. Diagn Microbiol Infect Dis 101(2):115448. https://doi.org/10.1016/j.diagmicrobio.2021.115448
Dudek P, Grajek A, Kowalczewski J, Madycki G, Marczak D (2020) Ultrasound frequency of sonication applied in microbiological diagnostics has a major impact on viability of bacteria causing PJI. Int J Infect Dis 100:158–163. https://doi.org/10.1016/j.ijid.2020.08.038
Kheir MM, Tan TL, Ackerman CT, Modi R, Foltz C, Parvizi J (2010) Culturing periprosthetic joint infection: number of samples, growth duration, and organisms. J Arthroplasty 33(11):3531-3536.e1. https://doi.org/10.1016/j.arth.2018.06.018
Bozhkova S, Suardi V, Sharma HK, Tsuchiya H, Del Sel H, Hafez MA, Benzakour T, Drago L, Romanò CL (2020) The W A.I.O.T. definition of peri-prosthetic joint infection: a multi-center, retrospective validation study. J Clin Med 9(6):1965. https://doi.org/10.3390/jcm9061965
Osmon DR, Berbari EF, Berendt AR, Lew D, Zimmerli W, Steckelberg JM, Rao N, Hanssen A, Wilson WR (2013) Infectious Diseases Society of America. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 56(1):e1–e25. https://doi.org/10.1093/cid/cis803
Nelson GN, Davis DE, Namdari S (2006) Outcomes in the treatment of periprosthetic joint infection after shoulder arthroplasty: a systematic review. J Shoulder Elbow Surg 25(8):1337–1345. https://doi.org/10.1016/j.jse.2015.11.064
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
Author information
Authors and Affiliations
Contributions
Mr. Tsikopoulos conceptualized the idea before conducting this study, handled the statistical software, and drafted the original manuscript. Mr. Christofilos and Mr. Gravalidis contributed to the data extraction and drafting of this meta-analysis. Mr. Sidiropoulos contributed to the literature search and quality assessment. Mr. Kitridis assessed the methodological quality of the papers and contributed to the literature search. Mr. Stoikos contributed to the data extraction and editing of the article. Professor Givissis and Professor Papaioannidou supervised and reviewed the paper. All authors have read and agreed to the current version of the manuscript. Mr Christofilos participated in this study while he was an intern at Professor Maniatis’s group at the University College London.
Corresponding author
Ethics declarations
Ethics approval
We declare that ethical approval was not required for this study.
Consent to participate
Patients’ consent to participate was not applicable.
Consent for publication
Patients’ consent to publish was not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Prospective registration: We have registered this study to PROSPERO (CRD42021290099), and PRISMA 2020 guidelines have been followed [49].
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original version of this article was revised. Check erratum for the changes.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tsikopoulos, K., Christofilos, S.I., Kitridis, D. et al. Is sonication superior to dithiothreitol in diagnosis of periprosthetic joint infections? A meta-analysis. International Orthopaedics (SICOT) 46, 1215–1224 (2022). https://doi.org/10.1007/s00264-022-05350-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00264-022-05350-z