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The relationship between a dolichofacial morphology and bone adaptation of the articular tubercle
Archives of Oral Biology 78 (2017) 20–25
Contents lists available at ScienceDirect
Archives of Oral Biology journal homepage: www.elsevier.com/locate/aob
The relationship between a dolichofacial morphology and bone adaptation of the articular tubercle J.H. Koolstraa,* , M.C.M. Jongenburgera , G.R. Landweera , N.M.B.K. Willemsb a Department of Oral Cell Biology and Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and Vrije Universiteit Amsterdam, MOVE Research Institute Amsterdam, Netherlands b Department of Orthodontics, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and Vrije Universiteit Amsterdam, Gustav Mahlerlaan 3004, 1081 LA, Amsterdam, Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 March 2016 Received in revised form 2 February 2017 Accepted 4 February 2017
Objectives: Against the background of a possibly compromised functional adaptation, the relationship between the height of the articular tubercle was analyzed as a function of the amount of divergence between the maxilla and the mandible. Design: These parameters were obtained retrospectively from orthopantomograms and lateral radiographs produced in a standard procedure before orthodontic treatment. Results: The height of the articular tubercle appeared to be significantly smaller in a group of patients with a dolichofacial morphology, with respect of those with an average (mesofacial) morphology. Furthermore, there was a significant correlation between the height of the articular tubercle and the mandibular angle. Conclusions: These results suggest that bone remodeling in selected parts of the orofacial skeleton can be compromised giving rise to an altered craniofacial morphology. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Functional morphology Anatomy Jaw biomechanics Growth/development Craniofacial anomalies Developmental biology
1. Introduction In orthodontics and oral surgery the problem of relapse is prominent. After the teeth have been positioned correctly by orthodontic treatment often the newly created configuration appears not to be stable. In such a case after some time the teeth migrate to a less favorable configuration. To prevent this unwanted migration a permanent restrain is used. Generally, this restrain does not cause adverse effects, but occasionally allergic reactions can be raised. In oral surgery bilateral split osteotomy is performed for mandibular set-back or advancement when the upper and lower jaw do not occlude normally. Years after this surgical intervention the mandible may have the tendency to remodel towards the original adverse shape. In oral surgery there is presently not a method to prevent the occurrence of this relapse. The problem of relapse seems to be related to craniofacial morphology. Patients with a so-called dolichofacial (long-face) morphology appear to suffer from relapse more than patients with a mesofacial (average) or even brachyfacial (short-face)
* Corresponding author. E-mail address: [email protected] (J.H. Koolstra). http://dx.doi.org/10.1016/j.archoralbio.2017.02.005 0003-9969/© 2017 Elsevier Ltd. All rights reserved.
morphology (Joss & Vassalli, 2008, 2009; Zaher, Bishara, & Jakobsen, 1994). Dolichofacial morphology is characterized by a relatively large lower face height in relation to the upper face height. This relatively strong elongation of the lower face is already developing at the age of 6 years (Ha, Park, & Lee, 2014). From a sagittal perspective the mandibular angle (the angle between the posterior border of the mandibular ramus and the inferior border of the mandibular body) is much wider and, therefore, the mandibular body is rotated forward (clockwise in a right sided view). Herewith, the inclination of the lower border of the mandibular body diverges substantially from the Frankfort horizontal plane (the plane through the infraorbital margins and the roof of the external auditory meatus – Tweed, 1946). This is also indicated as a divergent relationship between upper and lower jaw (Proffit, Fields, & Sarver, 2012). The biological background of a dolichofacial morphology is presently not known. It is associated with reduced strength of the masticatory muscles (van Spronsen, Weijs, Valk, Prahl-Andersen, & van Ginkel, 1992; Weijs & Hillen, 1984). This may indicate that the postnatal development of the area lining the oral cavity has been disturbed. The postnatal growth of the mandible is predominantly performed by bone remodeling (Enlow, 1992; Sperber, 1976). This process normally leads to optimization of bony structures in
J.H. Koolstra et al. / Archives of Oral Biology 78 (2017) 20–25
relation to their functional demands (Huiskes, 2000). If orthodontic treatment or oral surgery is performed in relation to bone from which the remodeling process is not adequately executed, it could give rise to unfavorable effects regarding stabilization of the newly created situation. However, whether the bone remodeling process is compromised or not in the lower facial area of especially subjects with a dolichofacial morphology is not known. It is likely, that when the bone remodeling process of the mandible is compromised this also accounts for other structures in the orofacial region. This could be reflected by alterations of the outgrowth of the lower face which mainly occurs during childhood. In this period also the articular tubercle (or articular eminence) of the temporomandibular joint, which is virtually absent at birth, gets its shape. It comes into existence after birth under influence of the loads of the temporomandibular joints (Iwasaki et al., 2010), to become a prominence of about 7 mm in _ height (Ilgüy et al., 2014). Consequently, if the process of bone remodeling is attenuated in the craniofacial region, it is most likely that also the outgrowth of the articular tubercle will be reduced. If a dolichofacial morphology is (partly) the result of a compromised process of bone remodeling the size of the articular tubercle may be reduced in these subjects. It is, therefore, hypothesized that the size of the articular tubercle will be reduced in subjects with a dolichofacial morphology characterized by a more forwardly rotated mandibular body and divergent relationship between maxilla and mandible. 2. Materials & methods Geometrical data was obtained retrospectively by cephalometry of 94 subjects available from the records present in the department of Orthodontics at ACTA. This material consisted of both orthopantomograms (OPG) and lateral radiographs. They had been produced in a standard procedure before any orthodontic treatment had been performed using a OP100 Orthopantomograph (Instrumentarium, Tuusula, Finland) at a “panorama” setting (70 kV, 16 mA, 17.6 s recording time). For the present study the radiographs were applied anonymously: no other data (except for gender) from the subjects was available. Inclusion criteria were: good visibility of the mandibular condyle, articular tubercle and mandibular fossa on at least one side in the OPG and less than 3 months between production of the OPG and the related lateral radiograph. Selection of the subjects was based upon a variety of mandibular angle by visual inspection of the lateral radiographs. The mandibular angle was determined from the lateral radiographs. It was defined by the angle between the Frankfort horizontal plane (defined by the points Porion and Orbitale) and the line connecting the mandibular angle (point Gonion) and the inferior border of the mandibular symphysis (point Menton). The height of the articular tubercle was determined from the OPG by the vertical distance between the superior-most point of the mandibular fossa and the inferior-most point of the apex of the articular tubercle. The vertical distance was defined perpendicular to the line connecting the superior-most points of both mandibular condyles. Also the posterior slope angle of the articular tubercle was quantified. This angle was defined by the tangent of the posterior aspect of the articular tubercle at the location where it crossed the line connecting the two condyle tops (Fig. 1). All measurements were performed using custom made computer software. Subjects with a mandibular angle less than 32 were considered normal or nearly normal, whereas a dolichofacial morphology was defined by a mandibular angle of 35 and more (Tweed, 1946). Since a mandibular angle between 32 and 35 is considered not so favorable, but neither a mesofacial or dolichofacial morphology, subjects showing this amount were not included in the analysis.
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Fig. 1. Details of the left jaw joint in an orthopantomogram. (A) Superior-most point of the mandibular condyle. (B) Superior-most point of the mandibular fossa. (C) Inferior-most point of the apex of the articular tubercle. Dashed line: line connecting the superior-most points of both mandibular condyles. Solid line: tangent the posterior slope of the articular tubercle.
Unfortunately, for a number of subjects not all relevant structures were unambiguously visible in the OPGs. If this considered one side of a subject, only its other side was included in the analysis. If this considered both sides, the subject was excluded from the analysis. In all other cases the data from the left and right side were averaged (vide infra). All measurements were conducted by two individuals independently. 2.1. Statistical analysis The height of the articular tubercle and its posterior slope angle was correlated to the mandibular angle in a Pearson rank correlation test. A number of tests were performed to analyze the distribution of the various parameters. They included differences between male and female subjects and differences between left and right side. Furthermore, the normality of the distribution of the various parameters were tested with a Shapiro-Wilkinson test. The difference in height and posterior slope angle of the articular tubercle between the two groups (mesofacial and dolichofacial) was tested with an independent sample T-test. Finally, the reliability of the independent observers was tested by the intraclass correlation coefficient. All statistical tests were performed using R version 3.2.2 (www. r-project.org). The level of statistical significance was defined at a probability value of 0.05. 3. Results 3.1. Subjects The records consisted of 46 normal to nearly normal subjects and 32 subjects with a dolichofacial morphology. After exclusion of radiographs where the relevant structures could not be recognized unambiguously, 39 normal or nearly normal subjects (14 male, 25 female) and 26 subjects with a dolichofacial morphology (7 male, 19 female) remained suitable for analysis.
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3.2. Articular tubercle Fig. 2 shows the height of the articular tubercle and its posterior slope angle as a function of the mandibular angle. Both are inversely proportional with a significance level of 0.01 and 0.05, respectively. There was not a significant difference between the relevant parameters on the left or right side for both male and female subjects. For that reason it was considered correct to average the data from the left and right side. Between male and female subjects no significant differences were observed regarding mandibular angle, height and angle of the articular tubercle. Therefore, no correction was applied for gender. Fig. 3 shows the distribution of the relevant morphological parameters. The distributions of tubercular height and slope angle were not significantly different from a normal one. In contrast, the mandibular angle was not normally distributed. Based upon this finding non-parametric tests were used to evaluate the differences in height and angle of the articular tubercle between the two groups. A significant difference (p < 0.03) was observed in the height of the articular tubercle between the mesofacial and dolichofacial subjects (Fig. 4A). The mean difference was about 1.34 mm. In contrast, a significant difference regarding the slope angle was not present (p < 0.194) (Fig. 4B).
The reliability of the observations was tested using the intraclass correlation coefficient. They were 0.99 and 0.98 for height and angle measurements, respectively. 4. Discussion It was demonstrated that the outgrowth of the articular tubercle of the temporomandibular joint is related to the amount of divergence between the maxilla and the mandible. This outgrowth appears to be reduced with an increased (forward) mandibular rotation. This corroborates the consideration that the development of the lower part of the face towards a dolichofacial morphology could be the result of an altered or even disturbed bone remodeling process, which takes place after birth. This is also in agreement with the observations of Ingervall (1974) who presented examples of reduced growth of the mandible in combination with a small articular tubercle and faces with a triangular profile. 4.1. Ramus inclination The present study used the mandibular plane angle as a predictive measure for facial morphology. However, it should be noted that the relationship between the amount of divergence between mandible and maxilla could have been affected by the
Fig. 2. The relationship between the morphology of the articular tubercle and the mandibular angle. (A) Height of the articular tubercle in mm (+) as a function of mandibular angle in degrees. Dashed line: regression line (coefficient = 0.15 (p < 0.01). B: Slope angle of the articular tubercle in degrees (x) as a function of mandibular angle in degrees. Dashed line: regression line (coefficient = 0.42 (p < 0.05).
J.H. Koolstra et al. / Archives of Oral Biology 78 (2017) 20–25
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Fig. 3. Distribution of the morphological parameters in the different groups. Left column: mesofacial group, right column: dolichofacial group. First row: articular tubercle height (mm), second row: slope angle of the articular tubercle (degrees), third row: mandibular angle (degrees).
inclination of the mandibular ramus (the angle between the mandibular ramus and the Frankfort horizontal plane). Since a systemic relationship between this property and the properties under consideration could not be demonstrated, it has not been included in the present study. 4.2. Masticatory muscles Subjects with a divergent relationship between the upper and lower jaw generally have a reduced strength in their masticatory
muscles (van Spronsen et al., 1992; Weijs & Hillen, 1984). It can be argued that, therefore, they apply less loads on their articular tubercle during normal masticatory function. This could explain the reduced height of that structure. However, the mechanical advantage of their muscles is not better than in average subjects (van Spronsen et al., 1997). Furthermore, since the masticatory habits are presumably not different from subjects with a mesofacial craniofacial morphology, habitual loading of the temporomandibular joints can be considered similar (Hylander, 1975). Consequently, the reduced outgrowth of the articular
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J.H. Koolstra et al. / Archives of Oral Biology 78 (2017) 20–25
Fig. 4. Morphological differences of the articular tubercle between the mesofacial and dolichofacial groups. (A) Means and SD of the height of the articular tubercle (mm). (B) Means and SD of the slope angle of the articular tubercle (degrees). * indicates a statistical significance between the means (p < 0.05).
tubercle is not likely to be attributed to reduced masticatory muscle strength.
branchial arches, it is very well possible that both are subjected to similar potential disturbances in the bone remodeling process.
4.3. Subjects
4.6. Clinical implications
The radiographs used in this study were obtained from subjects that visited the department of orthodontics at ACTA for orthodontic treatment. Since this is not necessarily a cross-section of the average population it could have created a bias. However, even if the morphology of the articular tubercle were dependent on the wish to seek orthodontic treatment at all, it would still be unlikely that the relation between the size of this structure would be different from the one in subjects that do not seek orthodontic treatment.
The biological background of the development of a divergence between the maxilla and the mandible is still not unambiguously established. It is also not known why surgical or orthodontic interferences in relevant structures of subjects with a dolichofacial morphology are more prone to a relapse than in subjects with a mesofacial morphology. This process is partly dependent on the process of bone remodeling. The present study indicates that this process is performed differently in subjects with a different facial morphology. Therefore, it could be advantageous if the clinician could be able to predict their effects in relation to the morphology of his/her patient. If underlying mechanisms related to orofacial morphology could be taken into account a better consolidation of the final results may be achieved.
4.4. Statistical analysis To test for a normal distribution of the various parameters a Shapiro-Wilkinson test was applied, while a Kolmogorov Smirnov test has a better power of discernment. However, this becomes applicable when the number of subjects becomes larger. Since the number of subjects was relatively small, the former test was selected. 4.5. Bone remodeling Although the process of bone remodeling is not limited by age, the articular tubercle generally reaches its final thickness around the age of 10 years (Katsavrias, 2002). It is well known that bone remodels under the influence of external loads. It generally results in a structure that is optimized to meet its functional demands (Huiskes, 2000). However, the underlying biological mechanisms are still not completely understood. Apparently, the process may differ per location. For instance, in the appendicular skeleton the loads necessary to maintain bone are larger than in calvarian bone (Schliephake, 2002). Furthermore, vascularisation may play an important role. Mandibular bone has been observed to grow faster in subjects that suffer from festering of blood vessels in adjacent orofacial regions (Mulliken & Young, 1988). Consequently, since the mechanism normally is regulated in a subtle way, it is not impossible that it becomes disturbed by internal or external factors. This is corroborated by the present results. Since the articular tubercle and the mandible both develop from the
4.7. Conclusions The hypothesis that the size of the articular tubercle will be reduced in subjects with a dolichofacial morphology characterized by a more forwardly rotated mandibular body compared to average subjects has been confirmed. This predominantly considered its height. In contrast, a reduction in slope angle could not be confirmed. Acknowledgments The authors wish to thank Dr. G.E.J. Langenbach for his constructive comments on the manuscript. This research was institutionally supported by the Academic Centre for Dentistry Amsterdam (ACTA). The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article. References Enlow, D. H. (1992). The condyle and facial growth, In B. G. Sarnat, & D. M. Laskin (Eds.), The temporomandibular joint (pp. 48–59).4th ed. Philadelphia: W.B. Saunders Company. Ha, Y., Park, Y.-S., & Lee, S.-P. (2014). Do long-faced subjects really have a long anterior face? A longitudinal study. American Journal of Orthodontics and Dentofacial Orthopedics, 145(6), 799–806.
J.H. Koolstra et al. / Archives of Oral Biology 78 (2017) 20–25 Huiskes, R. (2000). If bone is the answer, then what is the question? Journal of Anatomy, 197(2), 145–156. Hylander, W. (1975). Human mandible—Lever or link. American Journal of Physical Anthropology, 43(3), 227–242. _ _ lu, E., Semanur Dölekog lu, S., & Ersan, N. (2014). Ilgüy, D., Ilgüy, M., Fişekçiog Articular eminence inclination, height, and condyle morphology on cone beam computed tomography. Scientific World Journal761714. Ingervall, B. (1974). Relation between height of the articular tubercle of the temporomandibular joint and facial morphology. Angle Orthodontist, 44(1), 15–24. Iwasaki, L. R., Crosby, M. J., Marx, D. B., Gonzalez, Y., McCall, W. D. Jr., Ohrbach, R., et al. (2010). Human temporomandibular joint eminence shape and load minimization. Journal of Dental Research, 89(7), 722–727. Joss, C. U., & Vassalli, I. M. (2008). Stability after bilateral sagittal split osteotomy setback surgery with rigid internal fixation: A systematic review. Journal of Oral and Maxillofacial Surgery, 66(8), 1634–1643. Joss, C. U., & Vassalli, I. M. (2009). Stability after bilateral sagittal split osteotomy advancement surgery with rigid internal fixation: A systematic review. Journal of Oral and Maxillofacial Surgery, 67(2), 301–313. Katsavrias, E. G. (2002). Changes in articular eminence inclination during the craniofacial growth period. Angle Orthodontist, 72(3), 258–264.
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Mulliken, J. B., & Young, A. (1988). Vascular birthmarks: Hemangiomas and malformations. Philadelphia: Saunders. Proffit, W. R., Fields, W., & Sarver, D. M. (2012). Contemporary orthodontics, 5th ed. St. Louis: Mosby. Schliephake, H. (2002). Bone growth factors in maxillofacial skeletal reconstruction. International Journal of Oral and Maxillofacial Surgery, 31, 469–484. Sperber, G. H. (1976). Craniofacial embryology, 2nd ed. Bristol: John Wright & Sons LTD.. Tweed, C. H. (1946). The Frankfort-mandibular plane angle in orthodontic diagnosis, classification, treatment planning, and prognosis. American Journal of Orthodontics and Oral Surgery-Orthodontics, 32(4), 175–230. van Spronsen, P. H., Weijs, W. A., Valk, J., Prahl-Andersen, B., & van Ginkel, F. C. (1992). A comparison of jaw muscle cross-sections of long-face and normal adults. Journal of Dental Research, 71(6), 1279–1285. van Spronsen, P. H., Koolstra, J. H., van Ginkel, F. C., Weijs, W. A., Valk, J., & PrahlAndersen, B. (1997). Relationships between the orientation and moment arms of the human jaw muscles and normal craniofacial morphology. European Journal of Orthodontics, 19(3), 313–328. Weijs, W. A., & Hillen, B. (1984). Relationships between masticatory muscle cross section and skull shape. Journal of Dental Research, 63(9), 1154–1157. Zaher, A. R., Bishara, S. E., & Jakobsen, J. R. (1994). Posttreatment changes in different facial types. Angle Orthodontist, 64(6), 425–436.
Contents lists available at ScienceDirect
Archives of Oral Biology journal homepage: www.elsevier.com/locate/aob
The relationship between a dolichofacial morphology and bone adaptation of the articular tubercle J.H. Koolstraa,* , M.C.M. Jongenburgera , G.R. Landweera , N.M.B.K. Willemsb a Department of Oral Cell Biology and Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and Vrije Universiteit Amsterdam, MOVE Research Institute Amsterdam, Netherlands b Department of Orthodontics, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and Vrije Universiteit Amsterdam, Gustav Mahlerlaan 3004, 1081 LA, Amsterdam, Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 March 2016 Received in revised form 2 February 2017 Accepted 4 February 2017
Objectives: Against the background of a possibly compromised functional adaptation, the relationship between the height of the articular tubercle was analyzed as a function of the amount of divergence between the maxilla and the mandible. Design: These parameters were obtained retrospectively from orthopantomograms and lateral radiographs produced in a standard procedure before orthodontic treatment. Results: The height of the articular tubercle appeared to be significantly smaller in a group of patients with a dolichofacial morphology, with respect of those with an average (mesofacial) morphology. Furthermore, there was a significant correlation between the height of the articular tubercle and the mandibular angle. Conclusions: These results suggest that bone remodeling in selected parts of the orofacial skeleton can be compromised giving rise to an altered craniofacial morphology. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Functional morphology Anatomy Jaw biomechanics Growth/development Craniofacial anomalies Developmental biology
1. Introduction In orthodontics and oral surgery the problem of relapse is prominent. After the teeth have been positioned correctly by orthodontic treatment often the newly created configuration appears not to be stable. In such a case after some time the teeth migrate to a less favorable configuration. To prevent this unwanted migration a permanent restrain is used. Generally, this restrain does not cause adverse effects, but occasionally allergic reactions can be raised. In oral surgery bilateral split osteotomy is performed for mandibular set-back or advancement when the upper and lower jaw do not occlude normally. Years after this surgical intervention the mandible may have the tendency to remodel towards the original adverse shape. In oral surgery there is presently not a method to prevent the occurrence of this relapse. The problem of relapse seems to be related to craniofacial morphology. Patients with a so-called dolichofacial (long-face) morphology appear to suffer from relapse more than patients with a mesofacial (average) or even brachyfacial (short-face)
* Corresponding author. E-mail address: [email protected] (J.H. Koolstra). http://dx.doi.org/10.1016/j.archoralbio.2017.02.005 0003-9969/© 2017 Elsevier Ltd. All rights reserved.
morphology (Joss & Vassalli, 2008, 2009; Zaher, Bishara, & Jakobsen, 1994). Dolichofacial morphology is characterized by a relatively large lower face height in relation to the upper face height. This relatively strong elongation of the lower face is already developing at the age of 6 years (Ha, Park, & Lee, 2014). From a sagittal perspective the mandibular angle (the angle between the posterior border of the mandibular ramus and the inferior border of the mandibular body) is much wider and, therefore, the mandibular body is rotated forward (clockwise in a right sided view). Herewith, the inclination of the lower border of the mandibular body diverges substantially from the Frankfort horizontal plane (the plane through the infraorbital margins and the roof of the external auditory meatus – Tweed, 1946). This is also indicated as a divergent relationship between upper and lower jaw (Proffit, Fields, & Sarver, 2012). The biological background of a dolichofacial morphology is presently not known. It is associated with reduced strength of the masticatory muscles (van Spronsen, Weijs, Valk, Prahl-Andersen, & van Ginkel, 1992; Weijs & Hillen, 1984). This may indicate that the postnatal development of the area lining the oral cavity has been disturbed. The postnatal growth of the mandible is predominantly performed by bone remodeling (Enlow, 1992; Sperber, 1976). This process normally leads to optimization of bony structures in
J.H. Koolstra et al. / Archives of Oral Biology 78 (2017) 20–25
relation to their functional demands (Huiskes, 2000). If orthodontic treatment or oral surgery is performed in relation to bone from which the remodeling process is not adequately executed, it could give rise to unfavorable effects regarding stabilization of the newly created situation. However, whether the bone remodeling process is compromised or not in the lower facial area of especially subjects with a dolichofacial morphology is not known. It is likely, that when the bone remodeling process of the mandible is compromised this also accounts for other structures in the orofacial region. This could be reflected by alterations of the outgrowth of the lower face which mainly occurs during childhood. In this period also the articular tubercle (or articular eminence) of the temporomandibular joint, which is virtually absent at birth, gets its shape. It comes into existence after birth under influence of the loads of the temporomandibular joints (Iwasaki et al., 2010), to become a prominence of about 7 mm in _ height (Ilgüy et al., 2014). Consequently, if the process of bone remodeling is attenuated in the craniofacial region, it is most likely that also the outgrowth of the articular tubercle will be reduced. If a dolichofacial morphology is (partly) the result of a compromised process of bone remodeling the size of the articular tubercle may be reduced in these subjects. It is, therefore, hypothesized that the size of the articular tubercle will be reduced in subjects with a dolichofacial morphology characterized by a more forwardly rotated mandibular body and divergent relationship between maxilla and mandible. 2. Materials & methods Geometrical data was obtained retrospectively by cephalometry of 94 subjects available from the records present in the department of Orthodontics at ACTA. This material consisted of both orthopantomograms (OPG) and lateral radiographs. They had been produced in a standard procedure before any orthodontic treatment had been performed using a OP100 Orthopantomograph (Instrumentarium, Tuusula, Finland) at a “panorama” setting (70 kV, 16 mA, 17.6 s recording time). For the present study the radiographs were applied anonymously: no other data (except for gender) from the subjects was available. Inclusion criteria were: good visibility of the mandibular condyle, articular tubercle and mandibular fossa on at least one side in the OPG and less than 3 months between production of the OPG and the related lateral radiograph. Selection of the subjects was based upon a variety of mandibular angle by visual inspection of the lateral radiographs. The mandibular angle was determined from the lateral radiographs. It was defined by the angle between the Frankfort horizontal plane (defined by the points Porion and Orbitale) and the line connecting the mandibular angle (point Gonion) and the inferior border of the mandibular symphysis (point Menton). The height of the articular tubercle was determined from the OPG by the vertical distance between the superior-most point of the mandibular fossa and the inferior-most point of the apex of the articular tubercle. The vertical distance was defined perpendicular to the line connecting the superior-most points of both mandibular condyles. Also the posterior slope angle of the articular tubercle was quantified. This angle was defined by the tangent of the posterior aspect of the articular tubercle at the location where it crossed the line connecting the two condyle tops (Fig. 1). All measurements were performed using custom made computer software. Subjects with a mandibular angle less than 32 were considered normal or nearly normal, whereas a dolichofacial morphology was defined by a mandibular angle of 35 and more (Tweed, 1946). Since a mandibular angle between 32 and 35 is considered not so favorable, but neither a mesofacial or dolichofacial morphology, subjects showing this amount were not included in the analysis.
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Fig. 1. Details of the left jaw joint in an orthopantomogram. (A) Superior-most point of the mandibular condyle. (B) Superior-most point of the mandibular fossa. (C) Inferior-most point of the apex of the articular tubercle. Dashed line: line connecting the superior-most points of both mandibular condyles. Solid line: tangent the posterior slope of the articular tubercle.
Unfortunately, for a number of subjects not all relevant structures were unambiguously visible in the OPGs. If this considered one side of a subject, only its other side was included in the analysis. If this considered both sides, the subject was excluded from the analysis. In all other cases the data from the left and right side were averaged (vide infra). All measurements were conducted by two individuals independently. 2.1. Statistical analysis The height of the articular tubercle and its posterior slope angle was correlated to the mandibular angle in a Pearson rank correlation test. A number of tests were performed to analyze the distribution of the various parameters. They included differences between male and female subjects and differences between left and right side. Furthermore, the normality of the distribution of the various parameters were tested with a Shapiro-Wilkinson test. The difference in height and posterior slope angle of the articular tubercle between the two groups (mesofacial and dolichofacial) was tested with an independent sample T-test. Finally, the reliability of the independent observers was tested by the intraclass correlation coefficient. All statistical tests were performed using R version 3.2.2 (www. r-project.org). The level of statistical significance was defined at a probability value of 0.05. 3. Results 3.1. Subjects The records consisted of 46 normal to nearly normal subjects and 32 subjects with a dolichofacial morphology. After exclusion of radiographs where the relevant structures could not be recognized unambiguously, 39 normal or nearly normal subjects (14 male, 25 female) and 26 subjects with a dolichofacial morphology (7 male, 19 female) remained suitable for analysis.
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3.2. Articular tubercle Fig. 2 shows the height of the articular tubercle and its posterior slope angle as a function of the mandibular angle. Both are inversely proportional with a significance level of 0.01 and 0.05, respectively. There was not a significant difference between the relevant parameters on the left or right side for both male and female subjects. For that reason it was considered correct to average the data from the left and right side. Between male and female subjects no significant differences were observed regarding mandibular angle, height and angle of the articular tubercle. Therefore, no correction was applied for gender. Fig. 3 shows the distribution of the relevant morphological parameters. The distributions of tubercular height and slope angle were not significantly different from a normal one. In contrast, the mandibular angle was not normally distributed. Based upon this finding non-parametric tests were used to evaluate the differences in height and angle of the articular tubercle between the two groups. A significant difference (p < 0.03) was observed in the height of the articular tubercle between the mesofacial and dolichofacial subjects (Fig. 4A). The mean difference was about 1.34 mm. In contrast, a significant difference regarding the slope angle was not present (p < 0.194) (Fig. 4B).
The reliability of the observations was tested using the intraclass correlation coefficient. They were 0.99 and 0.98 for height and angle measurements, respectively. 4. Discussion It was demonstrated that the outgrowth of the articular tubercle of the temporomandibular joint is related to the amount of divergence between the maxilla and the mandible. This outgrowth appears to be reduced with an increased (forward) mandibular rotation. This corroborates the consideration that the development of the lower part of the face towards a dolichofacial morphology could be the result of an altered or even disturbed bone remodeling process, which takes place after birth. This is also in agreement with the observations of Ingervall (1974) who presented examples of reduced growth of the mandible in combination with a small articular tubercle and faces with a triangular profile. 4.1. Ramus inclination The present study used the mandibular plane angle as a predictive measure for facial morphology. However, it should be noted that the relationship between the amount of divergence between mandible and maxilla could have been affected by the
Fig. 2. The relationship between the morphology of the articular tubercle and the mandibular angle. (A) Height of the articular tubercle in mm (+) as a function of mandibular angle in degrees. Dashed line: regression line (coefficient = 0.15 (p < 0.01). B: Slope angle of the articular tubercle in degrees (x) as a function of mandibular angle in degrees. Dashed line: regression line (coefficient = 0.42 (p < 0.05).
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Fig. 3. Distribution of the morphological parameters in the different groups. Left column: mesofacial group, right column: dolichofacial group. First row: articular tubercle height (mm), second row: slope angle of the articular tubercle (degrees), third row: mandibular angle (degrees).
inclination of the mandibular ramus (the angle between the mandibular ramus and the Frankfort horizontal plane). Since a systemic relationship between this property and the properties under consideration could not be demonstrated, it has not been included in the present study. 4.2. Masticatory muscles Subjects with a divergent relationship between the upper and lower jaw generally have a reduced strength in their masticatory
muscles (van Spronsen et al., 1992; Weijs & Hillen, 1984). It can be argued that, therefore, they apply less loads on their articular tubercle during normal masticatory function. This could explain the reduced height of that structure. However, the mechanical advantage of their muscles is not better than in average subjects (van Spronsen et al., 1997). Furthermore, since the masticatory habits are presumably not different from subjects with a mesofacial craniofacial morphology, habitual loading of the temporomandibular joints can be considered similar (Hylander, 1975). Consequently, the reduced outgrowth of the articular
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Fig. 4. Morphological differences of the articular tubercle between the mesofacial and dolichofacial groups. (A) Means and SD of the height of the articular tubercle (mm). (B) Means and SD of the slope angle of the articular tubercle (degrees). * indicates a statistical significance between the means (p < 0.05).
tubercle is not likely to be attributed to reduced masticatory muscle strength.
branchial arches, it is very well possible that both are subjected to similar potential disturbances in the bone remodeling process.
4.3. Subjects
4.6. Clinical implications
The radiographs used in this study were obtained from subjects that visited the department of orthodontics at ACTA for orthodontic treatment. Since this is not necessarily a cross-section of the average population it could have created a bias. However, even if the morphology of the articular tubercle were dependent on the wish to seek orthodontic treatment at all, it would still be unlikely that the relation between the size of this structure would be different from the one in subjects that do not seek orthodontic treatment.
The biological background of the development of a divergence between the maxilla and the mandible is still not unambiguously established. It is also not known why surgical or orthodontic interferences in relevant structures of subjects with a dolichofacial morphology are more prone to a relapse than in subjects with a mesofacial morphology. This process is partly dependent on the process of bone remodeling. The present study indicates that this process is performed differently in subjects with a different facial morphology. Therefore, it could be advantageous if the clinician could be able to predict their effects in relation to the morphology of his/her patient. If underlying mechanisms related to orofacial morphology could be taken into account a better consolidation of the final results may be achieved.
4.4. Statistical analysis To test for a normal distribution of the various parameters a Shapiro-Wilkinson test was applied, while a Kolmogorov Smirnov test has a better power of discernment. However, this becomes applicable when the number of subjects becomes larger. Since the number of subjects was relatively small, the former test was selected. 4.5. Bone remodeling Although the process of bone remodeling is not limited by age, the articular tubercle generally reaches its final thickness around the age of 10 years (Katsavrias, 2002). It is well known that bone remodels under the influence of external loads. It generally results in a structure that is optimized to meet its functional demands (Huiskes, 2000). However, the underlying biological mechanisms are still not completely understood. Apparently, the process may differ per location. For instance, in the appendicular skeleton the loads necessary to maintain bone are larger than in calvarian bone (Schliephake, 2002). Furthermore, vascularisation may play an important role. Mandibular bone has been observed to grow faster in subjects that suffer from festering of blood vessels in adjacent orofacial regions (Mulliken & Young, 1988). Consequently, since the mechanism normally is regulated in a subtle way, it is not impossible that it becomes disturbed by internal or external factors. This is corroborated by the present results. Since the articular tubercle and the mandible both develop from the
4.7. Conclusions The hypothesis that the size of the articular tubercle will be reduced in subjects with a dolichofacial morphology characterized by a more forwardly rotated mandibular body compared to average subjects has been confirmed. This predominantly considered its height. In contrast, a reduction in slope angle could not be confirmed. Acknowledgments The authors wish to thank Dr. G.E.J. Langenbach for his constructive comments on the manuscript. This research was institutionally supported by the Academic Centre for Dentistry Amsterdam (ACTA). The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article. References Enlow, D. H. (1992). The condyle and facial growth, In B. G. Sarnat, & D. M. Laskin (Eds.), The temporomandibular joint (pp. 48–59).4th ed. Philadelphia: W.B. Saunders Company. Ha, Y., Park, Y.-S., & Lee, S.-P. (2014). Do long-faced subjects really have a long anterior face? A longitudinal study. American Journal of Orthodontics and Dentofacial Orthopedics, 145(6), 799–806.
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