Abstract
Objectives
Magnetic resonance imaging (MRI) is a standardized method for assisting joint diagnosis. To validate the reliability of different imaging-based grading systems, this study examined (1) the associations between grading systems for osseous change, joint effusion, and the Wilkes classification of temporomandibular joint (TMJ) disorders and (2) the correlation between cytokines in synovial fluid and imaging-based joint scores.
Materials and methods
Twenty-seven patients, who routinely received numeric rating scale (NRS) and MRI assessment before TMJ arthrocentesis, were enrolled. Each joint was evaluated through the grading criteria for severity of osseous change and joint effusion by blinded observers using MRI. ImageJ was employed for classifying joint effusion. Joint synovial fluid, collected through arthrocentesis, was examined for cytokine expression by using a Luminex multiplex assay. All data were analyzed using the Pearson correlation analysis.
Results
The Wilkes classification was strongly correlated with osseous change scores, but not with joint effusion scores. Joint effusion scores significantly correlated with NRS scores, but not with the Wilkes classification and osseous change scores. Compared with osseous change scores, joint effusion scores had a higher correlation with the levels of inflammatory cytokines (interleukin (IL)-8 and soluble IL-6 receptor (sIL-6R)) and with anti-inflammatory cytokines (soluble tumor necrosis factor receptors I and II (sTNF-RI/II)).
Conclusions
In patients with TMJ disorders, MRI grades are strongly correlated with NRS scores and levels of cytokines (IL-8, sIL-6R, and sTNF-RI/II) in the synovial fluid.
Clinical relevance
Joint effusion scoring can be a reliable and valid indicator for pathological assessment of TMJ disorders.
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References
Dashnyam K, Lee JH, Mandakhbayar N, Jin GZ, Lee HH, Kim HW (2018) Intra-articular biomaterials-assisted delivery to treat temporomandibular joint disorders. J Tissue Eng 9:2041731418776514
Seifi M, Ebadifar A, Kabiri S, Badiee MR, Abdolazimi Z, Amdjadi P (2017) Comparative effectiveness of low level laser therapy and transcutaneous electric nerve stimulation on temporomandibular joint disorders. J Lasers Med Sci 8:S27–S31
Atsu SS, Ayhan-Ardic F (2006) Temporomandibular disorders seen in rheumatology practices: a review. Rheumatol Int 26:781–787
Shahidi S, Salehi P, Abedi P, Dehbozorgi M, Hamedani S, Berahman N (2018) Comparison of the bony changes of TMJ in patients with and without TMD complaints using CBCT. J Dent (Shiraz) 19:142–149
Bristela M, Schmid-Schwap M, Eder J, Reichenberg G, Kundi M, Piehslinger E, Robinson S (2017) Magnetic resonance imaging of temporomandibular joint with anterior disk dislocation without reposition—long-term results. Clin Oral Investig 21:237–245
Larheim TA (2005) Role of magnetic resonance imaging in the clinical diagnosis of the temporomandibular joint. Cells Tissues Organs 180:6–21
Dimitroulis G (2013) A new surgical classification for temporomandibular joint disorders. Int J Oral Maxillofac Surg 42:218–222
Wilkes CH (1989) Internal derangements of the temporomandibular joint. Pathological variations. Arch Otolaryngol Head Neck Surg 115:469–477
Ahmad M, Hollender L, Anderson Q, Kartha K, Ohrbach R, Truelove EL, John MT, Schiffman EL (2009) Research diagnostic criteria for temporomandibular disorders (RDC/TMD): development of image analysis criteria and examiner reliability for image analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107:844–860
Yano K, Sano T, Okano T (2004) A longitudinal study of magnetic resonance (MR) evidence of temporomandibular joint (TMJ) fluid in patients with TMJ disorders. Cranio 22:64–71
Vangsness CT Jr, Burke WS, Narvy SJ, MacPhee RD, Fedenko AN (2011) Human knee synovial fluid cytokines correlated with grade of knee osteoarthritis—a pilot study. Bull NYU Hosp Jt Dis 69:122–127
Park HN, Kim KA, Koh KJ (2014) Relationship between pain and effusion on magnetic resonance imaging in temporomandibular disorder patients. Imaging Sci Dent 44:293–299
Swan A, Amer H, Dieppe P (2002) The value of synovial fluid assays in the diagnosis of joint disease: a literature survey. Ann Rheum Dis 61:493–498
Bouloux GF (2009) Temporomandibular joint pain and synovial fluid analysis: a review of the literature. J Oral Maxillofac Surg 67:2497–2504
MIG Campos PC, SRP Line (2006) Inflammatory cytokines activity in temporomandibular joint disorders: a review of literature. Braz J Oral Sci 5:1054–1062
Kristensen KD, Alstergren P, Stoustrup P, Kuseler A, Herlin T, Pedersen TK (2014) Cytokines in healthy temporomandibular joint synovial fluid. J Oral Rehabil 41:250–256
Wojdasiewicz P, Poniatowski ŁA, Szukiewicz D (2014) The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediat Inflamm 2014:561459
González-García R (2015) The current role and the future of minimally invasive temporomandibular joint surgery. Oral Maxillofac Surg Clin North Am 27:69–84
Ahmed N, Mustafa HM, Catrina AI, Alstergren P (2013) Impact of temporomandibular joint pain in rheumatoid arthritis. Mediat Inflamm 2013:597419
De Riu G, Stimolo M, Meloni SM et al (2013) Arthrocentesis and temporomandibular joint disorders: clinical and radiological results of a prospective study. Int J Dent 2013:790648
Paniagua B, Pascal L, Prieto J, et al (2017) Diagnostic index: an open-source tool to classify TMJ OA condyles. Proc SPIE Int Soc Opt Eng 10137. https://doi.org/10.1117/12.2254070
Al-Hashmi A, Al-Azri A, Al-Ismaily M, Goss AN (2011) Temporomandibular disorders in patients with mandibular fractures: a preliminary comparative case-control study between South Australia and Oman. Int J Oral Maxillofac Surg 40:1369–1372
Suenaga S, Nagayama K, Nagasawa T, Indo H, Majima HJ (2016) The usefulness of diagnostic imaging for the assessment of pain symptoms in temporomandibular disorders. Jpn Dent Sci Rev 52:93–106
Fu KY, Li YW, Zhang ZK, Ma XC (2009) Osteonecrosis of the mandibular condyle as a precursor to osteoarthrosis: a case report. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107:e34–e38
Saini A, Saifuddin A (2004) MRI of osteonecrosis. Clin Radiol 59:1079–1093
Larheim TA, Katzberg RW, Westesson PL, Tallents RH, Moss ME (2001) MR evidence of temporomandibular joint fluid and condyle marrow alterations: occurrence in asymptomatic volunteers and symptomatic patients. Int J Oral Maxillofac Surg 30:113–117
Segami N, Nishimura M, Kaneyama K, Miyamaru M, Sato J, Murakami KI (2001) Does joint effusion on T2 magnetic resonance images reflect synovitis? Comparison of arthroscopic findings in internal derangements of the temporomandibular joint. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92:341–345
Oliveira JX, Rosa JA, Dutra ME, Santos KC, Gil C (2013) Assessing joint effusion and bone changes of the head of the mandible in MR images of symptomatic patients. Braz Oral Res 27:37–41
Nogami S, Takahashi T, Ariyoshi W, Yoshiga D, Morimoto Y, Yamauchi K (2013) Increased levels of interleukin-6 in synovial lavage fluid from patients with mandibular condyle fractures: correlation with magnetic resonance evidence of joint effusion. J Oral Maxillofac Surg 71:1050–1058
Wakita T, Mogi M, Kurita K, Kuzushima M, Togari A (2006) Increase in RANKL: OPG ratio in synovia of patients with temporomandibular joint disorder. J Dent Res 85:627–632
Vernal R, Velásquez E, Gamonal J, Garcia-Sanz JA, Silva A, Sanz M (2008) Expression of proinflammatory cytokines in osteoarthritis of the temporomandibular joint. Arch Oral Biol 53:910–915
Monasterio G, Castillo F, Rojas L et al (2018) Th1/Th17/Th22 immune response and their association with joint pain, imagenological bone loss, RANKL expression and osteoclast activity in temporomandibular joint osteoarthritis: a preliminary report. J Oral Rehabil 45:589–597
Kaneyama K, Segami N, Sun W, Sato J, Fujimura K (2005) Levels of soluble cytokine factors in temporomandibular joint effusions seen on magnetic resonance images. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 99:411–418
Kaneyama K, Segami N, Sun W, Sato J, Fujimura K (2005) Analysis of tumor necrosis factor-alpha, interleukin-6, interleukin-1beta, soluble tumor necrosis factor receptors I and II, interleukin-6 soluble receptor, interleukin-1 soluble receptor type II, interleukin-1 receptor antagonist, and protein in the synovial fluid of patients with temporomandibular joint disorders. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 99:276–284
Bendre MS, Montague DC, Peery T, Akel NS, Gaddy D, Suva LJ (2003) Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease. Bone 33:28–37
Nishimura M, Segami N, Kaneyama K, Suzuki T, Miyamaru M (2002) Proinflammatory cytokines and arthroscopic findings of patients with internal derangement and osteoarthritis of the temporomandibular joint. Br J Oral Maxillofac Surg 40:68–71
Rose-John S, Scheller J, Elson G, Jones SA (2006) Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 80:227–236
N Ogura TK (2015) Molecular aspects in inflammatory events of temporomandibular joint: microarray-based identification of mediators. Jpn Dent Sci Rev 51:10–24
Walker HK, Hall WD, Hurst JW (1990) Clinical methods: the history, physical, and laboratory examinations, 3rd edn. Butterworths, Boston
Funding
This research was supported by a grant from the Ministry of Science and Technology, Taiwan (MOST105-2314-B-010-031-MY2).
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Figure S1
No significant correlation between expression of cytokines and the Wilkes classification. TNF-α, IL-6, IFN-γ, MMP 3, MMP 12, MMP 13, IL-1β, IL-1ra, sIL-1RII, IL-4, IL-10, and IL-13 exhibited no significant correlations with the Wilkes classification. Tumor necrosis factor-α (TNF-α); Interleukin (IL); Interferon (IFN)-γ; Matrix metalloproteinase (MMP); IL-1 receptor antagonist (IL-1ra); Soluble IL-1 receptor II (sIL-1RII). (PDF 158 kb)
Figure S2
No significant correlation between expression of cytokines and the osseous change score. TNF-α, IL-6, IFN-γ, MMP 3, MMP 12, MMP 13, IL-1β, IL-1ra, sIL-1RII, IL-4, IL-10, and IL-13exhibited no significant correlations with the osseous change score. (PDF 157 kb)
Figure S3
No significant correlation between expression of cytokines and joint effusion score. TNF-α, IL-6, IFN-γ, MMP 3, MMP 12, MMP 13, IL-1β, IL-1ra, sIL-1RII, IL-4, IL-10, and IL-13 exhibited no significant correlations with the joint effusion score. (PDF 158 kb)
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Yang, MC., Wang, DH., Wu, HT. et al. Correlation of magnetic resonance imaging grades with cytokine levels of synovial fluid of patients with temporomandibular joint disorders: a cross-sectional study. Clin Oral Invest 23, 3871–3878 (2019). https://doi.org/10.1007/s00784-019-02817-z
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DOI: https://doi.org/10.1007/s00784-019-02817-z