- Email: [email protected]
Longitudinal study of temporomandibular joint disc status and craniofacial growth
ORIGINAL ARTICLE
Longitudinal study of temporomandibular joint disc status and craniofacial growth Carlos Flores-Mir,a Brian Nebbe,b Giseon Heo,c and Paul W. Majord Edmonton, Alberta, Canada Introduction: The objective of this retrospective cohort study was to assess the association of temporomandibular joint (TMJ) disc status and craniofacial growth. Methods: Seventy-nine subjects (52 female, 27 male) with and without TMJ disc abnormalities were followed for a mean time of 3 years 8 months. Of this sample, 40 subjects (21 female, 19 male) received orthodontic treatment. Disc displacement and disc length measurements from magnetic resonance imaging of the jaw joints were used to evaluate TMJ disc status. A principal component analysis was used to produce a single disc status score per subject. Horizontal and vertical growth changes were obtained from cephalometric radiographs. The Fishman skeletal maturation index system was used to obtain the percentage of the total craniofacial growth attained. In addition, previous orthodontic treatment and time frames between the follow-up cephalometric radiographs were considered. Results: A stepwise multiple linear regression analysis was used to evaluate the influence of TMJ disc status and orthodontic treatment on the displacement vectors between initial records (T1) and final records (T2) for each cephalometric point. Less horizontal and vertical growth was found in specific regions of the maxilla and the mandible in subjects with TMJ disc abnormalities, although their respective determination coefficients were mild (R2 ⬍11.2%). Conclusions: TMJ disc abnormality was associated with reduced forward growth of the maxillary and mandibular bodies. TMJ disc abnormality was associated with reduced downward growth of the mandibular ramus. (Am J Orthod Dentofacial Orthop 2006;130:324-30)
T
he prevalence of temporomandibular joint (TMJ) disorders varies considerably depending on sample origin, sample selection, diagnostic criteria, and study type.1-20 Until recently, the principal diagnostic criteria for defining a TMJ internal derangement were the clinical evaluation of TMJ sounds and the movement pattern of the joints. Based on these diagnostic criteria, the prevalence ranged from 3%1 to 27%2 (without aided listening), and from 10% in children3 to 44% in late adolescents4 (with aided listening). A trend of increased TMJ sounds and age has been reported in cross-sectional studies4-11 but not confirmed in longitudinal studies.12-14 With the use of noninvasive imaging techniques such as magnetic resonance imaging (MRI), the recorded prevalence values of TMJ disc disorders have increased in asymptomatic adult populations from 30% From the Department of Dentistry, University of Alberta, Edmonton, Alberta, Canada. a Clinical associate professor, Orthodontic Graduate Program. b Clinical assistant professor, Orthodontic Graduate Program. c Assistant professor, Statistics. d Professor, Director of Orthodontic Graduate Program. Reprint requests to: Dr Carlos Flores-Mir, Faculty of Medicine and Dentistry, Room 4051A, Dentistry/Pharmacy Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2N8; e-mail, [email protected]. Submitted, October 2004; revised and accepted, January 2005. 0889-5406/$32.00 Copyright © 2006 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2005.01.024
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to 75%15-19 and in symptomatic groups from 12% to 82%.15,17-20 Differences in the recruitment process and sample characteristics might explain this broad range. The prevalences, recorded by MRI, of TMJ disc displacement were approximately 50% in preorthodontic adolescent boys and 75% in preorthodontic adolescent girls.16 Several studies evaluated the association between TMJ disorders and occlusal features3,4,10,21 or craniofacial characteristics.22-26 In general, these studies reported that TMJ internal derangement was associated with reduced ramus height,7,23-27 decreased mandibular body length,7,25,26 reduced posterior total facial height without associated increases in anterior facial height,24-26 palatal24,25 and mandibular24-26 planes more convergent in the posterior region, vertically reduced maxillary molar position,24,25 reduced size of the anterior25,26 and posterior cranial bases,25 and uprighting of the mandibular incisor relative to the mandibular plane.25 To our knowledge, no previous longitudinal study has evaluated the association between TMJ disc status and craniofacial growth. Because TMJ disc status seems to be associated with altered craniofacial characteristics, this study was designed to evaluate the influence between TMJ disc status and craniofacial growth in a longitudinal sample of adolescents.
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Table I.
Descriptive statistics Subjects Minimum Maximum Range Mean (n) (y) (y) (y) (y)
T1 (total) T1 (girls) T1 (boys) T2 T2 (girls) T2 (boys) T1-T2 T1-T2 (girls) T1-T2 (boys)
79 52 27 79 52 27 79 52 27
9.06 9.06 9.58 10.14 10.14 12.19 1.08 1.08 1.16
16.86 16.64 16.86 20.64 20.64 19.86 5.75 5.75 5.00
7.80 7.58 7.28 10.50 10.50 7.67 4.67 4.67 3.84
12.93 12.94 12.90 16.57 16.64 16.42 3.64 3.70 3.51
SD (y) 1.79 1.70 1.99 2.10 1.98 2.33 1.12 1.14 1.10
n, Number; y, years; SD, standard deviation.
MATERIAL AND METHODS
This longitudinal study was a follow-up from a previously reported sample of 194 adolescents (119 girls, 75 boys) that was used to evaluate the association of TMJ disc status with craniofacial morphology.24 Subjects from the original sample were contacted by telephone and mail to participate in this study. Of the original sample, 42 (21.7%) could not be contacted (lost in follow-up), 58 (29.9%) declined to participate, and 6 (3.1%) could not participate (active orthodontic treatment, pregnancy, or rheumatoid arthritis). From the remaining 88 subjects (45.4%), only 79 (52 girls, 27 boys) had all the required records and fulfilled the inclusion criteria. From this sample of 79 subjects, 40 (21 girls, 19 boys) had undergone orthodontic treatment between initial records (T1) and final records (T2). Mean follow-up time between T1 and T2 was 43.68 months (Table I). MRIs of the TMJs were performed at T1 without sedation by using a 1.0 T magnet (Shimadzu Corporation 3, Tokyo, Japan) and a unilateral 3-in surface receiver coil. Axial scout images were obtained to identify the condyles. Bilateral closed-mouth sagittal sections were obtained perpendicular to the long axis of the condylar axis, and coronal images were obtained parallel to the condylar long axis. Closed-mouth images were taken with polyvinylsiloxane (President Jet-Bite, Coltene/Whaladent, Mahwah, NJ) centric-occlusion bite registration. To prevent muscle fatigue, bilateral open-mouth sagittal images were produced with a Burnett caliper (Medrad, Pittsburgh, Pa) set at 10 mm below the maximum voluntary interincisal mouth opening. Subjects were instructed to rest the anterior teeth on the blades of the caliper. T1-weighted 500/20 (TR ms: TE ms) pulse sequences were performed on all subjects by using 3-mm slice thickness, 140-mm field of view, NEX of 2, and image matrix of 204-204 pixels. The technique for quantitative analysis of MRI disc
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status used in this study was reported and validated by Nebbe et al.28 All sagittal MRI slices of the joint were traced by a previously calibrated researcher (B.N.),28 and perpendiculars were drawn from an established condylar load point, a discal midpoint, and posterior and anterior bands of the disc to the eminence plane. The eminence reference plane was previously determined at an angle of 50° to the transferred Frankfort horizontal. Disc length (DL) was measured in millimeters as the total linear distance between the perpendicular representing the posterior band of the articular disc and the perpendicular representing the anterior band of the disc along the eminence reference plane. Disc displacement (DD) was measured in millimeters as the total linear displacement of the discal midpoint from the condylar load point (closest joint space between head of the condyle and the posterior surface of the articular eminence) along the eminence reference plane.28 To reduce the number of independent variables, a principal component analysis (SPSS for Windows, SPSS, Chicago, Ill) was used that assigned a single weighted score based on the variability of all DD and DL measurements for each joint.28 Previously, a negative relationship between DD and DL was shown.28 It was considered prudent to allow these variables to proceed in the same relative direction. Therefore, measurements of DL were subtracted from what was considered to be a normal disc length (10 mm) to produce a reciprocal DL measurement.28 Several assumptions were made for this model. It was assumed that varying degrees of DD were associated with varying degrees of facial alteration, that unilateral DD is less severe than bilateral DD, and that the effects of DD in either TMJ were additive. These assumptions allowed a single additive score of DD to be assigned to each subject from the measurements of DD made from the right and left joints.28 Closed-mouth lateral cephalometric radiographs were obtained for each subject with a Siemens OP 10 (Siemens, Bensheim, Germany) radiographic machine with the mandible stabilized with the same polyvinylsiloxane habitual occlusion bite registration. Openmouth lateral cephalometric radiographs were also acquired to accurately determine the shape of the head of the condyle. The radiographs were coded for examiner blinding. Representative cephalometric points were traced twice with a month difference for T1 and T2 on acetate tracing film by a single researcher (C.F.) (Fig). An accurate outline of the condylar head was obtained from the open-mouth image by superimposing the closed-mouth tracing of the symphysis, the lower bor-
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Fig. Cephalometric points: PNS, posterior nasal spine; ANS, anterior nasal spine; Pg, pogonion; Gn, gnathion; Me, menton; Go, gonion.
der of the mandible, developing dental follicles, and enamel organ when present. An average measurement was used to represent bilateral structures identified on lateral cephalometric films. A customized computer program was developed in Microsoft Visual Basic for Windows (Microsoft, Redmond, Wash) that permitted the superimposition of the T1 and T2 tracings. For each time point, the 2 tracings were scanned into the computer and the necessary cephalometric points marked. The best fits of the anterior wall of sella turcica and the base of the sphenoid bone were selected as the superimposition reference structures.29 The composite image from the T2 cephalometric tracing was rotated over the composite image from the T1 cephalometric tracing on the computer screen. The superimposition reference structures changed color from red to green as superimposition of the images was obtained. When optimum superimposition was achieved, the computer program automatically calculated changes (X and Y coordinates) in positions of the cephalometric points between T1 and T2. The difference between the location of the cephalometric points between T1 and T2 was considered the amount of growth during that time period. T1 hand-wrist radiographs were analyzed by using the Fishman maturation prediction method30 (GrowthTek, Skaneateles, NY) to determine skeletal maturation
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level (advanced, normal, or delayed) and stage (relative position of the subject in the pubertal growth curve). With this information, the percentage of growth at T1 was determined for the maxilla and the mandible. Age and sex differences were factored out by using this method. Previous orthodontic treatment was determined as a dichotomous variable. Intraexaminer reliability (B.N.) for DL measurements and DD degree was evaluated with the coefficient of intrarater reliability. They were 1.00 and 0.98, respectively, based on retracings of 20 MRIs with mean variabilities of 1.041 mm for DL and 0.972 mm for DD.31 Intraexaminer reliability (C.F.) for the cephalometric measurements was calculated by retracing 8 randomly selected radiographs 8 times and measuring the horizontal and vertical vectors for each cephalometric point. The intraclass correlation coefficient was 0.99 (0.99, 1.00). The mean variability for repeated measurement of the cephalometric points was 0.442 mm (0.068, 0.887). Skeletal evaluation with the Fishman maturation prediction method was completed independently by a calibrated technician at the GrowthTek Company. Intraexaminer reliability was also evaluated with the intraclass correlation coefficient by using 10 triplicate hand-wrist x-rays; a coefficient of 0.99 (0.98, 0.99) was obtained. Efforts were made to make the research process as blind as possible. The examiner (B.N.) who completed the MRI analysis of disc status was blinded to growth measurements, and the examiner (C.F.) who made the growth measurement was blinded to disc status. The technician who completed the Fishman normal growth prediction was blinded to disc status and actual growth A statistician (G.H.) completed the initial statistical analysis without specific knowledge of the relevance or clinical significance of the variable interaction effects. Statistical analysis
An initial analysis was made at T1 to determine whether sex was associated with skeletal maturation level and stage with the Mann-Whitney U test and independent samples t test, respectively. Percentage of attained growth at T1 according to the Fishman method was factored out with a stepwise multiple linear regression analysis by calculating the horizontal and vertical unstandarized residuals of the measurements of the selected cephalometric points. Then stepwise multiple linear regression analysis was used to evaluate the effect of TMJ disc status and previous orthodontic treatment on the horizontal and vertical changes of the
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selected cephalometric points. The attained growth was factored out. RESULTS
The sample distribution according to classification of TMJ disc status at T1 is shown in Table I. No differences were found between boys and girls for T1 maturational level (P ⫽ .271; Mann-Whitney U test); however, differences were found between boys and girls for maturational stage (P ⬍.001; independent samples t test). Less horizontal mandibular body and maxillary growth was found in subjects with TMJ disc abnormality: (PNS [R2 ⫽ 8.3%], ANS [R2 ⫽ 5.3%], Pg [R2 ⫽ 9.9%], Gn [R2 ⫽ 10.5%], and Me [R2 ⫽ 10.6%]), but not for Go (see Fig for definitions). Subjects with TMJ disc abnormalities also had less vertical mandibular ramus growth: Go (R2 ⫽ 11.2%). No other vertical mandibular or maxillary growth alteration was found, except for ANS when previous orthodontic treatment significantly increased the amount of vertical growth (R2 ⫽ 5.0%). DISCUSSION
This is the only published longitudinal cephalometric growth study for an adolescent sample with disc status established by MRI. Our sample was a follow-up (mean, 3 years 8 months between T1 and T2) of all available subjects from the Edmonton TMJ sample. This sample was the basis for previous reports on diagnostic tools for determination of TMJ status28,31-36 and the associations between TMJ disc status and craniofacial morphology.24-26,37 In this discussion, TMJ disc abnormality refers to TMJ disc displacement and length alterations. In this study, we used a previously validated approach that allowed analysis of disc status (length and displacement) as a continuous variable.28 This facilitates regression analysis to identify the potential contribution of disc status to craniofacial growth and avoids the potential error associated with subjective classification of partial disc displacement.34 For these reasons, the conventional TMJ disc position classification was not used. The Fishman maturation prediction method was selected to factor out initial (at T1) skeletal maturation stage and level differences from the measured changes between T1 and T2.30 A previous systematic review by Flores-Mir et al38 concluded that the overall horizontal and vertical facial growth velocity is related to skeletal maturity indicators determined by analysis of handwrist radiographs and that skeletal maturity analysis of hand-wrist radiographs should include bone staging
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and ossification events for prediction of facial growth velocity. The Fishman method was therefore suitable for this study because it considered skeletal age and skeletal level at the same time. This methodology gives an estimate of the amount of growth completed in the maxilla and the mandible based on the skeletal age and level evaluated from a hand-wrist x-ray. Differences in the potential for normal growth changes were statistically factored out from the measured changes between T1 and T2. In a joint with a chronically displaced disc, there is an alteration in its normal functional environment. The disc is displaced and unable to provide load dissipation, lubrication, and nutrition to functional joint surfaces.39,40 As function continues, damage occurs to tissues that are usually not loaded or exposed to compressive and shear stresses of mastication. Retrodiscal tissues interposed between the articular surfaces are loaded, and tissue breakdown occurs. Fibrocartilage is damaged due to excessive point application of loads between incongruous osseous articular surfaces. Interleukin 1 released during acute inflammation is a potent inhibitor of matrix synthesis and proliferation and induces proteases, resulting in cartilage resorption.41Damaged tissue responds with acute inflammation and fluid exudate that, with continued function and tissue breakdown, is converted to a chronic inflammation with fibrosis.41,42 Disc displacement results in synovial intimal cell damage; the intimal cells are less able to prevent large macromolecular proteins from entering the joint space and, in addition, show reduced production of hyaluronic acid and proteoglycans. Loss of these synovial fluid constituents leads to less efficient joint lubrication, whereas the addition of macromolecules to synovial fluid alters the viscosity of the fluid and its lubrication properties.40 The production of inflammatory exudate and inflammatory products increases the viscosity of synovial fluid and raises intra-articular pressure, reducing joint perfusion.43 Reduced perfusion affects the delivery of nutrients and oxygen to articular surfaces and results in a build-up of metabolic waste products in the joint. Continued joint function and hypoxia create a gradient for oxygen diffusion that results in joint damage by hypoxic reperfusion.43-45 TMJ disc abnormality was related in the maxilla to a decrease in the horizontal growth of PNS and ANS. Although the horizontal position of ANS appears to be significantly associated to TMJ disc abnormality, the statistical value was barely significant (P ⫽ .041) and most likely not clinically significant. Even though a significant tracing error was possible for PNS (possible superimposition of third molars) and ANS (difficult to locate), it would theoretically camouflage the effects
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(random bias). Previous studies that have reported the association of craniofacial morphology with disc status have not reported shorter maxillary lengths with disc abnormalities.23-25 In a previous cross-sectional study, Brandt7 reported reduced maxillary length, but that study used different sample selection criteria and different TMJ status diagnostic criteria (continuous against dichotomic classification, respectively). TMJ disc abnormality was significantly related to a decrease in the horizontal growth of the anterior portion of the mandibular body (Pg, Gn, and Me). TMJ disc abnormality was associated with reduced vertical growth of the mandibular ramus (Go). Vertical growth in the anterior region of the mandible was not influenced by TMJ disc status. The results of our study demonstrate that the craniofacial pattern associated with disc abnormality previously reported by Nebbe et al23-26 became more pronounced with growth. The mandible became relatively more retrognathic. Reduced posterior face height (vertical ramus growth) without altered anterior facial growth produced a clockwise mandibular growth rotation. Nebbe et al23 identified sex differences associated with craniofacial morphology and TMJ disc status. Girls with disc abnormalities had more pronounced differences in ramus height. In this study, we did not analyze sex differences in craniofacial growth associated with disc status because the use of the Fishman methodology automatically factored out maturation and sex differences. Future research could evaluate sex differences in facial growth in this sample. Previous orthodontic treatment had a limited association with craniofacial growth. Orthodontic treatment was associated only with a more downward vertical position of ANS. When more specific details of the orthodontic treatment were considered— eg, type of extraction pattern, headgear, or elastic use—they were not significantly associated with the vertical position of ANS. Orthodontic treatment was not associated with mandibular growth differences or horizontal maxillary growth. We did not evaluate changes in disc status over the study duration. Progressive disc abnormality might be accompanied by altered condylar growth, whereas stable disc displacement and length alterations would have no further influence. It is also possible that there is a threshold of disc abnormality below which craniofacial growth is not affected. We did not include clinical signs of TMJ abnormality, such as pain on movement and joint tenderness. Joint pain might be clinical evidence of chronic inflammation, but this might be questionable because of the wide variation in reported pain among adolescents, as well as asymptomatic displacements.
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Persistent inflammation with secondary disc abnormality might result in altered craniofacial growth. Resolution of inflammation regardless of disc status could allow resumption of normal growth. Furthermore, biomechanical and biochemical alterations might be more significant than disc position alone. We did not evaluate TMJ osseous morphology. However, previous research regarding condyle shape and condyle position showed a relatively low predictive value of disc status,32 and radiographic evidence of degenerative joint disease is a relatively uncommon finding in adolescents. Careful consideration should be given to the use of the Fishman methodology. Although it is an analysis that considers skeletal level and stage, it gives only a general percentage of attained growth for the maxilla and the mandible at any given skeletal maturation. In our study, the evaluated cephalometric points under consideration were from various regions of the craniofacial complex. The obtained percentages might not be identical for every part of the maxilla or the mandible because of differences in the growth rates in vertical or anteroposterior dimensions of various regions At the same time, there is no reason to assume that any potential bias attributed to this methodology would be biased in any direction. The percentage of patients with TMJ internal derangements in asymptomatic samples is substantial15-19; therefore, orthodontists should be cognizant that many adolescent orthodontic patients have undiagnosed disc abnormalities. The influence of disc status on facial growth identified in this study was significant, but only a relatively small percentage (⬍11.2%) of the total variability in facial growth can be explained on the basis of TMJ disc status alone. The specific growth pattern for each patient cannot be accurately predicted from the results of this study. Although our results suggest that TMJ disc status should be considered in orthodontic treatment planning, the contributions of muscle function, hormonal influences, environmental factors, and genetic potential must all be considered for a complete picture of the possible implications of disc displacement over craniofacial growth. Further studies with an improved methodology are required to substantiate these findings. MRI has no known health risk, and the primary limitations for obtaining MRI of the TMJ as part of normal records are cost and availability. Health care providers have a responsibility to seek balance between treatment costs and probable patient benefit. At this time, there is insufficient evidence to recommend MRI of the TMJ as a screening protocol for all orthodontic patients.
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CONCLUSIONS
Based on the characteristics of our sample, the following conclusions were made. 1. TMJ disc abnormality was associated with reduced forward growth of the maxillary and mandibular bodies. 2. TMJ disc abnormality was associated with reduced downward growth of the mandibular ramus. We thank Edmonton Diagnostic Imaging, Magnetic Resonance Imaging Centre of Edmonton, and the McIntyre Memorial Research Fund, University of Alberta. REFERENCES 1. Dworkin SF, Huggins KH, LeResche L, Von Korff M, Howard J, Truelove E, et al. Epidemiology of signs and symptoms in temporomandibular disorders: clinical signs in cases and controls. J Am Dent Assoc 1990;120:273-81. 2. Mohlin B, Pilley JR, Shaw WC. A survey of craniomandibular disorders in 1000 12-year-olds. Study design and baseline data in a follow-up study. Eur J Orthod 1991;13:111-23. 3. Keeling SD, McGorray S, Wheeler TT, King GJ. Risk factors associated with temporomandibular joint sounds in children 6 to 12 years of age. Am J Orthod Dentofacial Orthop 1994; 105:279-87. 4. Gazit E, Lieberman M, Eini R, Hirsch N, Serfaty V, Fuchs C, et al. Prevalence of mandibular dysfunction in 10-18 year old Israeli schoolchildren. J Oral Rehabil 1984;11:307-17. 5. Egermark-Eriksson I, Carlsson GE, Ingervall B. Prevalence of mandibular dysfunction and orofacial parafunction in 7-, 11- and 15-year-old Swedish children. Eur J Orthod 1981;3:163-72. 6. Nilner M, Kopp S. Distribution by age and sex of functional disturbances and diseases of the stomatognathic system in 7-18 year olds. Swed Dent J 1983;7:191-8. 7. Brandt D. Temporomandibular disorders and their association with morphologic malocclusion in children. In: Carlson DS, McNamara JA Jr, Ribbens KA, editors. Developmental aspects of temporomandibular joint disorders. Monograph 16. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 1985. p. 279-98. 8. Ogura T, Morinushi T, Ohno H, Sumi K, Hatada K. An epidemiological study of TMJ dysfunction syndrome in adolescents. J Pedod 1985;10:22-35. 9. de Boever JA, van den Berghe L. Longitudinal study of functional conditions in the masticatory system in Flemish children. Community Dent Oral Epidemiol 1987;15:100-3. 10. Riolo ML, Brandt D, TenHave TR. Associations between occlusal characteristics and signs and symptoms of TMJ dysfunction in children and young adults. Am J Orthod Dentofacial Orthop 1987;92:467-77. 11. Runge ME, Sadowsky C, Sakols EI, BeGole EA. The relationship between temporomandibular joint sounds and malocclusion. Am J Orthod Dentofacial Orthop 1989;96:36-42. 12. Magnusson T, Egermark-Eriksson I, Carlsson GE. Four-year longitudinal study of mandibular dysfunction in children. Community Dent Oral Epidemiol 1985;13:117-20. 13. Wanman A, Agerberg G. Temporomandibular joint sounds in adolescents: a longitudinal study. Oral Surg Oral Med Oral Pathol 1990;69:2-9.
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31. Nebbe B, Brooks SL, Hatcher D, Hollender LG, Prasad NG, Major PW. Interobserver reliability in quantitative MRI assessment of temporomandibular joint disk status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:746-50. 32. Kamelchuk L, Nebbe B, Baker C, Major P. Adolescent TMJ tomography and magnetic resonance imaging: a comparative analysis. J Orofac Pain 1997;11:321-7. 33. Williamson PC, Major PW, Nebbe B, Glover KE, Prasad NG. Horizontal condylar angulation and condyle position associated with adolescent TMJ disk status. Cranio 1999;17:101-8. 34. Nebbe B, Brooks SL, Hatcher D, Hollender LG, Prasad NG, Major PW. Magnetic resonance imaging of the temporomandibular joint: interobserver agreement in subjective classification of disk status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;90:102-7. 35. Kinniburgh RD, Major PW, Nebbe B, West K, Glover KE. Osseous morphology and spatial relationships of the temporomandibular joint: comparisons of normal and anterior disc positions. Angle Orthod 2000;70:70-80. 36. Major PW, Kinniburgh RD, Nebbe B, Prasad NG, Glover KE. Tomographic assessment of temporomandibular joint osseous articular surface contour and spatial relationships associated with disc displacement and disc length. Am J Orthod Dentofacial Orthop 2002;121:152-61. 37. Trpkova B, Major P, Nebbe B, Prasad N. Craniofacial asymmetry and temporomandibular joint internal derangement in female adolescents: a posteroanterior cephalometric study. Angle Orthod 2000; 70:81-8.
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38. Flores-Mir C, Nebbe B, Major PW. Use of skeletal maturation based on hand-wrist radiographic analysis as a predictor of facial growth: a systematic review. Angle Orthod 2004;74: 119-24. 39. Hou JS, Mow VC, Lai WM, Holmes MH. An analysis of the squeeze-film lubrication mechanism for articular cartilage. J Biomech 1992;25:247-59. 40. Stegenga B, de Bont LG, Boering G, van Willigen JD. Tissue responses to degenerative changes in the temporomandibular joint: a review. J Oral Maxillofac Surg 1991;49:1079-88. 41. Lotz M, Blanco FJ, von Kempis J, Dudler J, Maier R, Villiger PM, et al. Cytokine regulation of chondrocyte functions. J Rheumatol 1995;43(Suppl):104-8. 42. Pelletier JP, McCollum R, Cloutier JM, Martel-Pelletier J. Synthesis of metalloproteases and interleukin 6 (IL-6) in human osteoarthritic synovial membrane is an IL-1 mediated process. J Rheumatol 1995;43(Suppl):109-14. 43. Merry P, Williams R, Cox N, King JB, Blake DR. Comparative study of intra-articular pressure dynamics in joints with acute traumatic and chronic inflammatory effusions: potential implications for hypoxic-reperfusion injury. Ann Rheum Dis 1991;50: 917-20. 44. Allen RE, Blake DR, Nazhat NB, Jones P. Superoxide radical generation by inflamed human synovium after hypoxia. Lancet 1989;2:282-3. 45. Blake DR, Merry P, Unsworth J, Kidd BL, Outhwaite JM, Ballard R, et al. Hypoxic-reperfusion injury in the inflamed human joint. Lancet 1989;1:289-93.
Longitudinal study of temporomandibular joint disc status and craniofacial growth Carlos Flores-Mir,a Brian Nebbe,b Giseon Heo,c and Paul W. Majord Edmonton, Alberta, Canada Introduction: The objective of this retrospective cohort study was to assess the association of temporomandibular joint (TMJ) disc status and craniofacial growth. Methods: Seventy-nine subjects (52 female, 27 male) with and without TMJ disc abnormalities were followed for a mean time of 3 years 8 months. Of this sample, 40 subjects (21 female, 19 male) received orthodontic treatment. Disc displacement and disc length measurements from magnetic resonance imaging of the jaw joints were used to evaluate TMJ disc status. A principal component analysis was used to produce a single disc status score per subject. Horizontal and vertical growth changes were obtained from cephalometric radiographs. The Fishman skeletal maturation index system was used to obtain the percentage of the total craniofacial growth attained. In addition, previous orthodontic treatment and time frames between the follow-up cephalometric radiographs were considered. Results: A stepwise multiple linear regression analysis was used to evaluate the influence of TMJ disc status and orthodontic treatment on the displacement vectors between initial records (T1) and final records (T2) for each cephalometric point. Less horizontal and vertical growth was found in specific regions of the maxilla and the mandible in subjects with TMJ disc abnormalities, although their respective determination coefficients were mild (R2 ⬍11.2%). Conclusions: TMJ disc abnormality was associated with reduced forward growth of the maxillary and mandibular bodies. TMJ disc abnormality was associated with reduced downward growth of the mandibular ramus. (Am J Orthod Dentofacial Orthop 2006;130:324-30)
T
he prevalence of temporomandibular joint (TMJ) disorders varies considerably depending on sample origin, sample selection, diagnostic criteria, and study type.1-20 Until recently, the principal diagnostic criteria for defining a TMJ internal derangement were the clinical evaluation of TMJ sounds and the movement pattern of the joints. Based on these diagnostic criteria, the prevalence ranged from 3%1 to 27%2 (without aided listening), and from 10% in children3 to 44% in late adolescents4 (with aided listening). A trend of increased TMJ sounds and age has been reported in cross-sectional studies4-11 but not confirmed in longitudinal studies.12-14 With the use of noninvasive imaging techniques such as magnetic resonance imaging (MRI), the recorded prevalence values of TMJ disc disorders have increased in asymptomatic adult populations from 30% From the Department of Dentistry, University of Alberta, Edmonton, Alberta, Canada. a Clinical associate professor, Orthodontic Graduate Program. b Clinical assistant professor, Orthodontic Graduate Program. c Assistant professor, Statistics. d Professor, Director of Orthodontic Graduate Program. Reprint requests to: Dr Carlos Flores-Mir, Faculty of Medicine and Dentistry, Room 4051A, Dentistry/Pharmacy Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2N8; e-mail, [email protected]. Submitted, October 2004; revised and accepted, January 2005. 0889-5406/$32.00 Copyright © 2006 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2005.01.024
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to 75%15-19 and in symptomatic groups from 12% to 82%.15,17-20 Differences in the recruitment process and sample characteristics might explain this broad range. The prevalences, recorded by MRI, of TMJ disc displacement were approximately 50% in preorthodontic adolescent boys and 75% in preorthodontic adolescent girls.16 Several studies evaluated the association between TMJ disorders and occlusal features3,4,10,21 or craniofacial characteristics.22-26 In general, these studies reported that TMJ internal derangement was associated with reduced ramus height,7,23-27 decreased mandibular body length,7,25,26 reduced posterior total facial height without associated increases in anterior facial height,24-26 palatal24,25 and mandibular24-26 planes more convergent in the posterior region, vertically reduced maxillary molar position,24,25 reduced size of the anterior25,26 and posterior cranial bases,25 and uprighting of the mandibular incisor relative to the mandibular plane.25 To our knowledge, no previous longitudinal study has evaluated the association between TMJ disc status and craniofacial growth. Because TMJ disc status seems to be associated with altered craniofacial characteristics, this study was designed to evaluate the influence between TMJ disc status and craniofacial growth in a longitudinal sample of adolescents.
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Table I.
Descriptive statistics Subjects Minimum Maximum Range Mean (n) (y) (y) (y) (y)
T1 (total) T1 (girls) T1 (boys) T2 T2 (girls) T2 (boys) T1-T2 T1-T2 (girls) T1-T2 (boys)
79 52 27 79 52 27 79 52 27
9.06 9.06 9.58 10.14 10.14 12.19 1.08 1.08 1.16
16.86 16.64 16.86 20.64 20.64 19.86 5.75 5.75 5.00
7.80 7.58 7.28 10.50 10.50 7.67 4.67 4.67 3.84
12.93 12.94 12.90 16.57 16.64 16.42 3.64 3.70 3.51
SD (y) 1.79 1.70 1.99 2.10 1.98 2.33 1.12 1.14 1.10
n, Number; y, years; SD, standard deviation.
MATERIAL AND METHODS
This longitudinal study was a follow-up from a previously reported sample of 194 adolescents (119 girls, 75 boys) that was used to evaluate the association of TMJ disc status with craniofacial morphology.24 Subjects from the original sample were contacted by telephone and mail to participate in this study. Of the original sample, 42 (21.7%) could not be contacted (lost in follow-up), 58 (29.9%) declined to participate, and 6 (3.1%) could not participate (active orthodontic treatment, pregnancy, or rheumatoid arthritis). From the remaining 88 subjects (45.4%), only 79 (52 girls, 27 boys) had all the required records and fulfilled the inclusion criteria. From this sample of 79 subjects, 40 (21 girls, 19 boys) had undergone orthodontic treatment between initial records (T1) and final records (T2). Mean follow-up time between T1 and T2 was 43.68 months (Table I). MRIs of the TMJs were performed at T1 without sedation by using a 1.0 T magnet (Shimadzu Corporation 3, Tokyo, Japan) and a unilateral 3-in surface receiver coil. Axial scout images were obtained to identify the condyles. Bilateral closed-mouth sagittal sections were obtained perpendicular to the long axis of the condylar axis, and coronal images were obtained parallel to the condylar long axis. Closed-mouth images were taken with polyvinylsiloxane (President Jet-Bite, Coltene/Whaladent, Mahwah, NJ) centric-occlusion bite registration. To prevent muscle fatigue, bilateral open-mouth sagittal images were produced with a Burnett caliper (Medrad, Pittsburgh, Pa) set at 10 mm below the maximum voluntary interincisal mouth opening. Subjects were instructed to rest the anterior teeth on the blades of the caliper. T1-weighted 500/20 (TR ms: TE ms) pulse sequences were performed on all subjects by using 3-mm slice thickness, 140-mm field of view, NEX of 2, and image matrix of 204-204 pixels. The technique for quantitative analysis of MRI disc
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status used in this study was reported and validated by Nebbe et al.28 All sagittal MRI slices of the joint were traced by a previously calibrated researcher (B.N.),28 and perpendiculars were drawn from an established condylar load point, a discal midpoint, and posterior and anterior bands of the disc to the eminence plane. The eminence reference plane was previously determined at an angle of 50° to the transferred Frankfort horizontal. Disc length (DL) was measured in millimeters as the total linear distance between the perpendicular representing the posterior band of the articular disc and the perpendicular representing the anterior band of the disc along the eminence reference plane. Disc displacement (DD) was measured in millimeters as the total linear displacement of the discal midpoint from the condylar load point (closest joint space between head of the condyle and the posterior surface of the articular eminence) along the eminence reference plane.28 To reduce the number of independent variables, a principal component analysis (SPSS for Windows, SPSS, Chicago, Ill) was used that assigned a single weighted score based on the variability of all DD and DL measurements for each joint.28 Previously, a negative relationship between DD and DL was shown.28 It was considered prudent to allow these variables to proceed in the same relative direction. Therefore, measurements of DL were subtracted from what was considered to be a normal disc length (10 mm) to produce a reciprocal DL measurement.28 Several assumptions were made for this model. It was assumed that varying degrees of DD were associated with varying degrees of facial alteration, that unilateral DD is less severe than bilateral DD, and that the effects of DD in either TMJ were additive. These assumptions allowed a single additive score of DD to be assigned to each subject from the measurements of DD made from the right and left joints.28 Closed-mouth lateral cephalometric radiographs were obtained for each subject with a Siemens OP 10 (Siemens, Bensheim, Germany) radiographic machine with the mandible stabilized with the same polyvinylsiloxane habitual occlusion bite registration. Openmouth lateral cephalometric radiographs were also acquired to accurately determine the shape of the head of the condyle. The radiographs were coded for examiner blinding. Representative cephalometric points were traced twice with a month difference for T1 and T2 on acetate tracing film by a single researcher (C.F.) (Fig). An accurate outline of the condylar head was obtained from the open-mouth image by superimposing the closed-mouth tracing of the symphysis, the lower bor-
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Fig. Cephalometric points: PNS, posterior nasal spine; ANS, anterior nasal spine; Pg, pogonion; Gn, gnathion; Me, menton; Go, gonion.
der of the mandible, developing dental follicles, and enamel organ when present. An average measurement was used to represent bilateral structures identified on lateral cephalometric films. A customized computer program was developed in Microsoft Visual Basic for Windows (Microsoft, Redmond, Wash) that permitted the superimposition of the T1 and T2 tracings. For each time point, the 2 tracings were scanned into the computer and the necessary cephalometric points marked. The best fits of the anterior wall of sella turcica and the base of the sphenoid bone were selected as the superimposition reference structures.29 The composite image from the T2 cephalometric tracing was rotated over the composite image from the T1 cephalometric tracing on the computer screen. The superimposition reference structures changed color from red to green as superimposition of the images was obtained. When optimum superimposition was achieved, the computer program automatically calculated changes (X and Y coordinates) in positions of the cephalometric points between T1 and T2. The difference between the location of the cephalometric points between T1 and T2 was considered the amount of growth during that time period. T1 hand-wrist radiographs were analyzed by using the Fishman maturation prediction method30 (GrowthTek, Skaneateles, NY) to determine skeletal maturation
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level (advanced, normal, or delayed) and stage (relative position of the subject in the pubertal growth curve). With this information, the percentage of growth at T1 was determined for the maxilla and the mandible. Age and sex differences were factored out by using this method. Previous orthodontic treatment was determined as a dichotomous variable. Intraexaminer reliability (B.N.) for DL measurements and DD degree was evaluated with the coefficient of intrarater reliability. They were 1.00 and 0.98, respectively, based on retracings of 20 MRIs with mean variabilities of 1.041 mm for DL and 0.972 mm for DD.31 Intraexaminer reliability (C.F.) for the cephalometric measurements was calculated by retracing 8 randomly selected radiographs 8 times and measuring the horizontal and vertical vectors for each cephalometric point. The intraclass correlation coefficient was 0.99 (0.99, 1.00). The mean variability for repeated measurement of the cephalometric points was 0.442 mm (0.068, 0.887). Skeletal evaluation with the Fishman maturation prediction method was completed independently by a calibrated technician at the GrowthTek Company. Intraexaminer reliability was also evaluated with the intraclass correlation coefficient by using 10 triplicate hand-wrist x-rays; a coefficient of 0.99 (0.98, 0.99) was obtained. Efforts were made to make the research process as blind as possible. The examiner (B.N.) who completed the MRI analysis of disc status was blinded to growth measurements, and the examiner (C.F.) who made the growth measurement was blinded to disc status. The technician who completed the Fishman normal growth prediction was blinded to disc status and actual growth A statistician (G.H.) completed the initial statistical analysis without specific knowledge of the relevance or clinical significance of the variable interaction effects. Statistical analysis
An initial analysis was made at T1 to determine whether sex was associated with skeletal maturation level and stage with the Mann-Whitney U test and independent samples t test, respectively. Percentage of attained growth at T1 according to the Fishman method was factored out with a stepwise multiple linear regression analysis by calculating the horizontal and vertical unstandarized residuals of the measurements of the selected cephalometric points. Then stepwise multiple linear regression analysis was used to evaluate the effect of TMJ disc status and previous orthodontic treatment on the horizontal and vertical changes of the
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selected cephalometric points. The attained growth was factored out. RESULTS
The sample distribution according to classification of TMJ disc status at T1 is shown in Table I. No differences were found between boys and girls for T1 maturational level (P ⫽ .271; Mann-Whitney U test); however, differences were found between boys and girls for maturational stage (P ⬍.001; independent samples t test). Less horizontal mandibular body and maxillary growth was found in subjects with TMJ disc abnormality: (PNS [R2 ⫽ 8.3%], ANS [R2 ⫽ 5.3%], Pg [R2 ⫽ 9.9%], Gn [R2 ⫽ 10.5%], and Me [R2 ⫽ 10.6%]), but not for Go (see Fig for definitions). Subjects with TMJ disc abnormalities also had less vertical mandibular ramus growth: Go (R2 ⫽ 11.2%). No other vertical mandibular or maxillary growth alteration was found, except for ANS when previous orthodontic treatment significantly increased the amount of vertical growth (R2 ⫽ 5.0%). DISCUSSION
This is the only published longitudinal cephalometric growth study for an adolescent sample with disc status established by MRI. Our sample was a follow-up (mean, 3 years 8 months between T1 and T2) of all available subjects from the Edmonton TMJ sample. This sample was the basis for previous reports on diagnostic tools for determination of TMJ status28,31-36 and the associations between TMJ disc status and craniofacial morphology.24-26,37 In this discussion, TMJ disc abnormality refers to TMJ disc displacement and length alterations. In this study, we used a previously validated approach that allowed analysis of disc status (length and displacement) as a continuous variable.28 This facilitates regression analysis to identify the potential contribution of disc status to craniofacial growth and avoids the potential error associated with subjective classification of partial disc displacement.34 For these reasons, the conventional TMJ disc position classification was not used. The Fishman maturation prediction method was selected to factor out initial (at T1) skeletal maturation stage and level differences from the measured changes between T1 and T2.30 A previous systematic review by Flores-Mir et al38 concluded that the overall horizontal and vertical facial growth velocity is related to skeletal maturity indicators determined by analysis of handwrist radiographs and that skeletal maturity analysis of hand-wrist radiographs should include bone staging
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and ossification events for prediction of facial growth velocity. The Fishman method was therefore suitable for this study because it considered skeletal age and skeletal level at the same time. This methodology gives an estimate of the amount of growth completed in the maxilla and the mandible based on the skeletal age and level evaluated from a hand-wrist x-ray. Differences in the potential for normal growth changes were statistically factored out from the measured changes between T1 and T2. In a joint with a chronically displaced disc, there is an alteration in its normal functional environment. The disc is displaced and unable to provide load dissipation, lubrication, and nutrition to functional joint surfaces.39,40 As function continues, damage occurs to tissues that are usually not loaded or exposed to compressive and shear stresses of mastication. Retrodiscal tissues interposed between the articular surfaces are loaded, and tissue breakdown occurs. Fibrocartilage is damaged due to excessive point application of loads between incongruous osseous articular surfaces. Interleukin 1 released during acute inflammation is a potent inhibitor of matrix synthesis and proliferation and induces proteases, resulting in cartilage resorption.41Damaged tissue responds with acute inflammation and fluid exudate that, with continued function and tissue breakdown, is converted to a chronic inflammation with fibrosis.41,42 Disc displacement results in synovial intimal cell damage; the intimal cells are less able to prevent large macromolecular proteins from entering the joint space and, in addition, show reduced production of hyaluronic acid and proteoglycans. Loss of these synovial fluid constituents leads to less efficient joint lubrication, whereas the addition of macromolecules to synovial fluid alters the viscosity of the fluid and its lubrication properties.40 The production of inflammatory exudate and inflammatory products increases the viscosity of synovial fluid and raises intra-articular pressure, reducing joint perfusion.43 Reduced perfusion affects the delivery of nutrients and oxygen to articular surfaces and results in a build-up of metabolic waste products in the joint. Continued joint function and hypoxia create a gradient for oxygen diffusion that results in joint damage by hypoxic reperfusion.43-45 TMJ disc abnormality was related in the maxilla to a decrease in the horizontal growth of PNS and ANS. Although the horizontal position of ANS appears to be significantly associated to TMJ disc abnormality, the statistical value was barely significant (P ⫽ .041) and most likely not clinically significant. Even though a significant tracing error was possible for PNS (possible superimposition of third molars) and ANS (difficult to locate), it would theoretically camouflage the effects
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(random bias). Previous studies that have reported the association of craniofacial morphology with disc status have not reported shorter maxillary lengths with disc abnormalities.23-25 In a previous cross-sectional study, Brandt7 reported reduced maxillary length, but that study used different sample selection criteria and different TMJ status diagnostic criteria (continuous against dichotomic classification, respectively). TMJ disc abnormality was significantly related to a decrease in the horizontal growth of the anterior portion of the mandibular body (Pg, Gn, and Me). TMJ disc abnormality was associated with reduced vertical growth of the mandibular ramus (Go). Vertical growth in the anterior region of the mandible was not influenced by TMJ disc status. The results of our study demonstrate that the craniofacial pattern associated with disc abnormality previously reported by Nebbe et al23-26 became more pronounced with growth. The mandible became relatively more retrognathic. Reduced posterior face height (vertical ramus growth) without altered anterior facial growth produced a clockwise mandibular growth rotation. Nebbe et al23 identified sex differences associated with craniofacial morphology and TMJ disc status. Girls with disc abnormalities had more pronounced differences in ramus height. In this study, we did not analyze sex differences in craniofacial growth associated with disc status because the use of the Fishman methodology automatically factored out maturation and sex differences. Future research could evaluate sex differences in facial growth in this sample. Previous orthodontic treatment had a limited association with craniofacial growth. Orthodontic treatment was associated only with a more downward vertical position of ANS. When more specific details of the orthodontic treatment were considered— eg, type of extraction pattern, headgear, or elastic use—they were not significantly associated with the vertical position of ANS. Orthodontic treatment was not associated with mandibular growth differences or horizontal maxillary growth. We did not evaluate changes in disc status over the study duration. Progressive disc abnormality might be accompanied by altered condylar growth, whereas stable disc displacement and length alterations would have no further influence. It is also possible that there is a threshold of disc abnormality below which craniofacial growth is not affected. We did not include clinical signs of TMJ abnormality, such as pain on movement and joint tenderness. Joint pain might be clinical evidence of chronic inflammation, but this might be questionable because of the wide variation in reported pain among adolescents, as well as asymptomatic displacements.
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Persistent inflammation with secondary disc abnormality might result in altered craniofacial growth. Resolution of inflammation regardless of disc status could allow resumption of normal growth. Furthermore, biomechanical and biochemical alterations might be more significant than disc position alone. We did not evaluate TMJ osseous morphology. However, previous research regarding condyle shape and condyle position showed a relatively low predictive value of disc status,32 and radiographic evidence of degenerative joint disease is a relatively uncommon finding in adolescents. Careful consideration should be given to the use of the Fishman methodology. Although it is an analysis that considers skeletal level and stage, it gives only a general percentage of attained growth for the maxilla and the mandible at any given skeletal maturation. In our study, the evaluated cephalometric points under consideration were from various regions of the craniofacial complex. The obtained percentages might not be identical for every part of the maxilla or the mandible because of differences in the growth rates in vertical or anteroposterior dimensions of various regions At the same time, there is no reason to assume that any potential bias attributed to this methodology would be biased in any direction. The percentage of patients with TMJ internal derangements in asymptomatic samples is substantial15-19; therefore, orthodontists should be cognizant that many adolescent orthodontic patients have undiagnosed disc abnormalities. The influence of disc status on facial growth identified in this study was significant, but only a relatively small percentage (⬍11.2%) of the total variability in facial growth can be explained on the basis of TMJ disc status alone. The specific growth pattern for each patient cannot be accurately predicted from the results of this study. Although our results suggest that TMJ disc status should be considered in orthodontic treatment planning, the contributions of muscle function, hormonal influences, environmental factors, and genetic potential must all be considered for a complete picture of the possible implications of disc displacement over craniofacial growth. Further studies with an improved methodology are required to substantiate these findings. MRI has no known health risk, and the primary limitations for obtaining MRI of the TMJ as part of normal records are cost and availability. Health care providers have a responsibility to seek balance between treatment costs and probable patient benefit. At this time, there is insufficient evidence to recommend MRI of the TMJ as a screening protocol for all orthodontic patients.
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CONCLUSIONS
Based on the characteristics of our sample, the following conclusions were made. 1. TMJ disc abnormality was associated with reduced forward growth of the maxillary and mandibular bodies. 2. TMJ disc abnormality was associated with reduced downward growth of the mandibular ramus. We thank Edmonton Diagnostic Imaging, Magnetic Resonance Imaging Centre of Edmonton, and the McIntyre Memorial Research Fund, University of Alberta. REFERENCES 1. Dworkin SF, Huggins KH, LeResche L, Von Korff M, Howard J, Truelove E, et al. Epidemiology of signs and symptoms in temporomandibular disorders: clinical signs in cases and controls. J Am Dent Assoc 1990;120:273-81. 2. Mohlin B, Pilley JR, Shaw WC. A survey of craniomandibular disorders in 1000 12-year-olds. Study design and baseline data in a follow-up study. Eur J Orthod 1991;13:111-23. 3. Keeling SD, McGorray S, Wheeler TT, King GJ. Risk factors associated with temporomandibular joint sounds in children 6 to 12 years of age. Am J Orthod Dentofacial Orthop 1994; 105:279-87. 4. Gazit E, Lieberman M, Eini R, Hirsch N, Serfaty V, Fuchs C, et al. Prevalence of mandibular dysfunction in 10-18 year old Israeli schoolchildren. J Oral Rehabil 1984;11:307-17. 5. Egermark-Eriksson I, Carlsson GE, Ingervall B. Prevalence of mandibular dysfunction and orofacial parafunction in 7-, 11- and 15-year-old Swedish children. Eur J Orthod 1981;3:163-72. 6. Nilner M, Kopp S. Distribution by age and sex of functional disturbances and diseases of the stomatognathic system in 7-18 year olds. Swed Dent J 1983;7:191-8. 7. Brandt D. Temporomandibular disorders and their association with morphologic malocclusion in children. In: Carlson DS, McNamara JA Jr, Ribbens KA, editors. Developmental aspects of temporomandibular joint disorders. Monograph 16. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 1985. p. 279-98. 8. Ogura T, Morinushi T, Ohno H, Sumi K, Hatada K. An epidemiological study of TMJ dysfunction syndrome in adolescents. J Pedod 1985;10:22-35. 9. de Boever JA, van den Berghe L. Longitudinal study of functional conditions in the masticatory system in Flemish children. Community Dent Oral Epidemiol 1987;15:100-3. 10. Riolo ML, Brandt D, TenHave TR. Associations between occlusal characteristics and signs and symptoms of TMJ dysfunction in children and young adults. Am J Orthod Dentofacial Orthop 1987;92:467-77. 11. Runge ME, Sadowsky C, Sakols EI, BeGole EA. The relationship between temporomandibular joint sounds and malocclusion. Am J Orthod Dentofacial Orthop 1989;96:36-42. 12. Magnusson T, Egermark-Eriksson I, Carlsson GE. Four-year longitudinal study of mandibular dysfunction in children. Community Dent Oral Epidemiol 1985;13:117-20. 13. Wanman A, Agerberg G. Temporomandibular joint sounds in adolescents: a longitudinal study. Oral Surg Oral Med Oral Pathol 1990;69:2-9.
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14. Egermark I, Magnusson T, Carlsson GE. A 20-year follow-up of signs and symptoms of temporomandibular disorders and malocclusions in subjects with and without orthodontic treatment in childhood. Angle Orthod 2003;73:109-15. 15. Nebbe B, Major PW. Prevalence of TMJ disc displacement in a pre-orthodontic adolescent sample. Angle Orthod 2000;70: 454-63. 16. Kircos LT, Ortendahl DA, Mark AS, Arakawa M. Magnetic resonance imaging of the TMJ disc in asymptomatic volunteers. J Oral Maxillofac Surg 1987;45:852-4. 17. Katzberg RW, Westesson PL, Tallents RH, Drake CM. Anatomic disorders of the temporomandibular joint disc in asymptomatic subjects. J Oral Maxillofac Surg 1996;54:147-53. 18. Tasaki MM, Westesson PL, Isberg AM, Ren YF, Tallents RH. Classification and prevalence of temporomandibular joint disk displacement in patients and symptom-free volunteers. Am J Orthod Dentofacial Orthop 1996;109:249-62. 19. Ribeiro RF, Tallents RH, Katzberg RW, Murphy WC, Moss ME, Magalhaes AC, et al. The prevalence of disc displacement in symptomatic and asymptomatic volunteers aged 6 to 25 years. J Orofac Pain 1997;11:37-47. 20. Hans MG, Lieberman J, Goldberg J, Rozencweig G, Bellon E. A comparison of clinical examination, history, and magnetic resonance imaging for identifying orthodontic patients with temporomandibular joint disorders. Am J Orthod Dentofacial Orthop 1992;101:54-9. 21. Egermark-Eriksson I, Ingervall B, Carlsson GE. The dependence of mandibular dysfunction in children on functional and morphologic malocclusion. Am J Orthod 1983;83:187-94. 22. Brand JW, Nielson KJ, Tallents RH, Nanda RS, Currier GF, Owen WL. Lateral cephalometric analysis of skeletal pattern in patients with or without internal derangment of the temporomandibular joint. Am J Orthod Dentofacial Orthop 1995;107:121-8. 23. Nebbe B, Major PW, Prasad NG, Grace M, Kamelchuk LS. TMJ internal derangement and adolescent craniofacial morphology: a pilot study. Angle Orthod 1997;67:407-14. 24. Nebbe B, Major PW, Prasad NG. Adolescent female craniofacial morphology associated with advanced bilateral TMJ disc displacement. Eur J Orthod 1998;20:701-12. 25. Nebbe B, Major PW, Prasad N. Female adolescent facial pattern associated with TMJ disk displacement and reduction in disk length: part I. Am J Orthod Dentofacial Orthop 1999; 116:168-76. 26. Nebbe B, Major PW, Prasad NG. Male adolescent facial pattern associated with TMJ disk displacement and reduction in disk length: part II. Am J Orthod Dentofacial Orthop 1999;116:301-7. 27. Dibbets JMH, van der Weele LT, Boering G. Craniofacial morphology and temporomandibular joint disfunction in children. In: Carlson DS, McNamara JA Jr, Ribbens KA, editors. Developmental aspects of temporormandibular joint disorders. Monograph 16. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 1985. p. 151-82. 28. Nebbe B, Major PW, Prasad NG, Hatcher D. Quantitative assessment of temporomandibular joint disk status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:598-607. 29. Athanasiou AE. Orthodontic cephalometry. Baltimore: MosbyWolfe; 1995. 30. Fishman LS. Maturational development and facial form relative to treatment timing. In: Subtelny JD, editor. Early orthodontic treatment. Chicago: Quintessence Publishing; 2000.
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31. Nebbe B, Brooks SL, Hatcher D, Hollender LG, Prasad NG, Major PW. Interobserver reliability in quantitative MRI assessment of temporomandibular joint disk status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:746-50. 32. Kamelchuk L, Nebbe B, Baker C, Major P. Adolescent TMJ tomography and magnetic resonance imaging: a comparative analysis. J Orofac Pain 1997;11:321-7. 33. Williamson PC, Major PW, Nebbe B, Glover KE, Prasad NG. Horizontal condylar angulation and condyle position associated with adolescent TMJ disk status. Cranio 1999;17:101-8. 34. Nebbe B, Brooks SL, Hatcher D, Hollender LG, Prasad NG, Major PW. Magnetic resonance imaging of the temporomandibular joint: interobserver agreement in subjective classification of disk status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;90:102-7. 35. Kinniburgh RD, Major PW, Nebbe B, West K, Glover KE. Osseous morphology and spatial relationships of the temporomandibular joint: comparisons of normal and anterior disc positions. Angle Orthod 2000;70:70-80. 36. Major PW, Kinniburgh RD, Nebbe B, Prasad NG, Glover KE. Tomographic assessment of temporomandibular joint osseous articular surface contour and spatial relationships associated with disc displacement and disc length. Am J Orthod Dentofacial Orthop 2002;121:152-61. 37. Trpkova B, Major P, Nebbe B, Prasad N. Craniofacial asymmetry and temporomandibular joint internal derangement in female adolescents: a posteroanterior cephalometric study. Angle Orthod 2000; 70:81-8.
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