Clin Oral Invest DOI 10.1007/s00784-014-1246-x
ORIGINAL ARTICLE
Comparative evaluation of thickness of jaw-closing muscles in patients with long-standing bilateral temporomandibular joint ankylosis: a retrospective case-controlled study Vinay V. Kumar & Neelima A. Malik & Corine M. Visscher & Supriya Ebenezer & Keyvan Sagheb & Frank Lobbezoo
Received: 13 May 2013 / Accepted: 24 April 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Objectives The aim of the study was to compare the thickness and cross-sectional area (CSA) of masseter and medial pterygoid muscles in young patients with long-standing bilateral temporomandibular joint ankylosis (bTMJA) in relation to controls. Methods Axial sections of computed tomography scans of patients with bTMJA from two tertiary care university hospitals were reviewed from 1995 to 2010 and compared to ageand sex-matched controls. The outlines of masseter and medial pterygoid muscles corresponding to a predefined reference plane were traced onto acetate paper. The thickness and CSA of the muscles were calculated using an image-analyzing
Vinay V. Kumar and Neelima A. Malik contributed equally to the paper. V. V. Kumar : C. M. Visscher : F. Lobbezoo Department of Oral Kinesiology, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and VU University Amsterdam, MOVE Research Institute Amsterdam, Amsterdam, The Netherlands V. V. Kumar : K. Sagheb Department of Maxillofacial and Plastic Surgery, University Medical Center of Johannes Gutenberg University, Mainz, Germany V. V. Kumar (*) Department of Oral and Maxillofacial Surgery, M R Ambedkar Dental College and Hospital, 37 Lazar Layout, Frazer Town, Bangalore 560005, India e-mail: [email protected]
software and calibrated according to the scale provided in the CT scan slides. Results Out of a total of 167 cases of temporomandibular joint ankylosis (TMJA), 15 fulfilled the inclusion criteria. The mean thickness and CSA of masseter and medial pterygoid muscles in cases of bTMJA were 19.4 mm (SD 2.3), 734.9 mm 2 (SD 156.7), 11.53 mm (SD 1.35), and 267.4 mm2 (SD 65.35), respectively. For the control group, respective values were 10.5 mm (SD 1.8), 430.1 mm2 (SD 66.8), 9.2 mm (SD 1.2), and 254.6 mm2 (SD 45.7). There was a statistically significant increased thickness and CSA of the muscles in cases of bTMJA as compared to control as evaluated by Mann-Whitney U test. Conclusions The results show that thickness and CSA of masseter and medial pterygoid muscles in patients with bTMJA were larger as compared to controls. This may suggest that, muscular hyperactivity, may be a cofactor in the pathogenesis of TMJA. Clinical significance Although temporomandibular joint ankylosis is one of the most restrictive musculoskeletal disorder in the maxillofacial region, there is little information on the form and function of jaw muscles in this condition. This study evaluates thickness and cross-sectional areas of jaw elevator muscles and indicates that muscle hyperactivity might be associated with ankylosis, thereby providing a probable hypothesis on the etiopathogenesis of this condition. Keywords Temporomandibular joint ankylosis . Muscles of mastication . Masseter . Medial pterygoid . Bilateral
N. A. Malik Department of Oral and Maxillofacial Surgery, School of Dental Sciences, Krishna Institute of Medical Sciences University, Karad, Maharashtra, India
Introduction
S. Ebenezer Department of Periodontics, M R Ambedkar Dental College and Hospital, Bangalore, India
Temporomandibular joint ankylosis (TMJA) is a condition of restricted mouth opening caused due to the bony or fibrous
Clin Oral Invest
fusion of the condyle to the temporal bone. Although there have been no reports on the exact prevalence of this condition, it has been described as being rare in developed countries and more common in developing countries, especially in the South Asian region [1–7]. Among the various etiologic factors, such as local or systemic infection and neoplasms of the condyle, traumatic injury to the mandibular condyle has been suggested to be the most common cause [5, 8, 9]. TMJA exists in both unilateral and bilateral forms. TMJA is an incapacitating condition with the afflicted individuals having difficulty in normal mandibular movement, mastication, speech, and maintenance of oral hygiene. This may yield severe psychosocial handicap. Due to decreased mouth opening and occlusal irregularities in this patient population, maintenance of adequate oral hygiene is a problem, leading to widespread dental caries and periodontal disease. When manifested in young patients, there are severe growth disturbances of the mandible and face. Patients with unilateral TMJA have facial asymmetry with a flatness and elongation on the unaffected side, and fullness and roundness of the face on the affected side. There is deviation of the chin towards the affected side. In bilateral cases, there is a pronounced decrease in chin prominence as well as shortness in the length and height of the mandible. Also in patients with this condition, there is a pronounced antegonial notch, which is more prominent on the affected side of the mandible (in cases of unilateral TMJA) [10]. The treatment of TMJA is very challenging, not only in achieving adequate facial aesthetics and oral rehabilitation, but also in preventing re-ankylosis. Although the treatment of TMJA is mainly surgical, the role of post-operative physiotherapy cannot be underestimated. It has been widely accepted that the high recurrence rates in developing countries are related to the unavailability of adequate post-operative physiotherapy in these patients [9, 11, 12]. Various hypotheses and theories have been suggested as to explain the etiopathogenesis of TMJA, with the majority of them focusing solely on articular and bony causes [7]. The concept of TMJA is that it occurs due to the discontinuity of the condylar surface, followed by the formation of an intracapsular hematoma that subsequently organizes and ossifies, thus forming the ankylotic mass [13–15]. It has also been postulated that in addition to condylar injury, damage of the meniscal disk as well as medial dislocation of the condylar neck predisposes towards the formation of TMJA [16]. This possibly would occur by osteogenesis caused due to traction of the lateral pterygoid muscle on the bone after sagittal fracture of the mandibular condyle [17]. However, in spite of the many theories trying to explain the etiopathogenesis of the disease, none of them completely explain the formation of TMJA. Recently, extra-articular factors have been suggested as possible important predisposing, initiating, and/or perpetuating
factors that could play a role in the pathogenesis of this condition [18]. One of the most important extra-articular factors is the activity of the masticatory muscles. It has been suggested that chronic arthralgia inhibits the normal use of the joint, inducing reflex muscle splinting to protect the joint [19]; thus, the patients themselves tend to immobilize the joint. The masticatory muscles in these conditions adapt to a restricted range of mouth opening by shortening [20]. Thus, these muscles could become an additional, extraarticular cause of mandibular movement restriction. These effects are generally more evident when joint pathology exists for a longer period. Based on this concept, it has been shown clinically that injection of Botulinum toxin, as an adjunct to surgical therapy, in the masseter muscles of patients operated for TMJA has improved outcomes [18]. Botulinum toxin works by blocking the presynaptic cholinergic nerve endings, thus causing relaxation of the voluntary muscle [21]. Hence, it is seen that there is clinical benefit in the treatment of TMJA by reducing the activity of elevator muscles of the mandible. Studies regarding the characteristics of masticatory muscles in TMJA patients have not been carried out so far. To understand muscular contributions to the etiopathogenesis of TMJA, it is important to know the muscular response of the elevator muscles of the mandible in this condition. Muscle thickness and cross-sectional areas have been used as indirect measures of muscle activity [22]. Muscle thickness is a linear measurement of the thickest region of the muscle, and crosssectional area is the measurement of the circumference of the muscle. The aim of this study was to investigate if there is a difference in the thickness of the elevator muscles of the mandible in patients suffering from bilateral TMJA as compared to an unaffected population. The objective of the study was to measure the thickness and cross-sectional areas of masseter and medial pterygoid muscles in young patients suffering from long-standing bilateral temporomandibular joint ankylosis (bTMJA) in comparison to sex- and agematched controls.
Materials and methods Patient selection Records of patient files from two, tertiary care, teaching university hospitals (Unit NAM, Nair Hospital Dental College, Mumbai, India; and Maharaja Agrasen Medical College, Agroha, India) were reviewed from the year 1995 to 2010 for cases of bTMJA. As the study consisted of evaluating retrospective patient records, no additional examinations were performed. Furthermore, the information was analyzed
Clin Oral Invest
anonymously, and considering these factors, a formal ethical committee clearance was not required. Inclusion criteria All patients diagnosed with bilateral temporomandibular joint ankylosis due to traumatic etiology, in the age range of 16– 20 years on presentation, with increased severity of the disease (defined by the authors as: having the disease for more than 6 years duration; and presenting with less than 8 mm of interincisal distance on maximal mouth opening) were included in the study. None of the chosen patients had documented evidence of any other temporomandibular joint disorders or bruxism. Such narrowly defined inclusion criteria were taken to have as homogenous a patient population as possible. All included cases had to be with adequate documentation, using computed tomography (CT) scans with axial section CT cuts of at least 3 mm thickness, and representation of the appropriate axial slice containing the lingula for measurement. The lingula is a bony prominence that is seen at the plane of mandibular foramen, the region where the inferior alveolar nerve runs into the ramus of the mandible [23]. As the control population, age- and sex-matched individuals were chosen, who were documented with adequate CT scans. The chosen control subject included patients in the age range of 16–19 years, with cystic/pathologic lesions of the maxilla that did not affect the musculoskeletal structures of the masticatory system. The diagnoses of the control group of patients were as follows: dentigerous cyst (four cases), ameloblastoma (three cases), keratinizing cystic odontogenic tumor (three cases), adenomatoid odontogenic tumor (two cases), and one case each of mucoepidermoid carcinoma, aneurysmal bone cyst, and juvenile ossifying fibroma. None of the control subjects had documented histories or findings of any form of temporomandibular joint disease/disorders or bruxism. The CT scans were obtained using Siemens Somatom Sensation 4-slice CT scanner (Siemens AG, Forchheim, Germany), with settings of 140 kVp, 300 mA, 3 mm slice thickness, and no gantry tilt. According to the imaging protocol, the patients were instructed to keep their mouth gently closed and relaxed during the scanning period.
Fig. 1 Representative examples of axial cross sections of CT scans of the patients included in this study. The masseter muscles are outlined in red, and the medial pterygoid muscles are outlined in blue. Axial sections showing the mandibular foramen at the lingula (green arrow) were chosen. The calibration scale can be seen at the right-hand side of the scan. a Example of a bTMJA patient. b Example of a control subject
The images of the chosen axial section were traced onto an acetate paper, and outlines of the masseter and medial pterygoid muscles were drawn (Fig. 1). From this, the thickness and the cross-sectional areas of the muscles were calculated using an image-analyzing software (Image J 1.4q, National Institute of Health, USA) and calibrated according to the scale provided in the CT scan slides. The measurements made were: masseter muscle thickness (M-Th) (in mm), masseter muscle cross-sectional area (M-CSA) (in mm2), medial pterygoid thickness (mP-Th) (in mm), and medial pterygoid crosssectional area (mP-CSA) (in mm2). Two rough working tables were made with the characteristics entered separately corresponding to two different groups of patients: bTMJA and control. The values of the muscle thickness and CSA were presented for the corresponding groups and entered as right and left sides. The tables also contained the following patient characteristics: age, sex, age at onset of TMJA, duration of the condition, and maximal mouth opening. To improve the accuracy of the measurements, the thickness and CSA measurements were performed by two examiners (VVK, KS) working together. They worked together on the tracings and came to an agreement on the outline of the muscles. The same two examiners also evaluated the TH and CSA values. Statistical analysis
Measurements Axial sections of the CT scans were assessed for masseter as well as the medial pterygoid muscles (Fig. 1). A standard reproducible plane was chosen for all the patients to avoid variations in the measurements of muscle thickness and cross sections, because the thickness and cross-sectional area of the muscles differ at different planes. The reproducible axial plane was chosen corresponding to the section containing the lingulae bilaterally.
For both the bTMJA and the control group, first a Wilcoxon test was done to evaluate if there is a difference in masseter and medial pterygoid muscle (thickness and cross-sectional area) between the right and left sides. It was seen that there were no differences in the left and right sides, so the mean of the left and right values for each patient was used to make subsequent analyses between the groups. To analyze the difference in the muscle thickness between the control group and the bTMJA patients (for the masseter
Clin Oral Invest
data as well as for the medial pterygoid data), Mann-Whitney U tests were used. To correct for multiple testing, the Holm’s Bonferroni procedure was used (Holland and Copenhaver, Psychol Bull 1988; 104: 145–149). p values less than or equal to 0.05 were considered statistically significant.
Bonferroni- Holm’s correction of p values yielded similar outcomes. A column to Table 2 presents the corrected p values.
Discussion
Results A total of 167 cases of TMJA (age range from 3 to 45 years) were identified, out of which 69 were cases of bTMJA and 98 cases of unilateral TMJA. Out of the 69 cases of bTMJA, 54 cases had to be excluded as they either did not have adequate documentation or did not fit the inclusion criteria. This resulted in only 15 cases chosen as the test group of study. Fifteen CT scans (sample size matched to the number of bTMJA patients) were chosen randomly from the pool of general patients that had the same age range, who were evaluated at the hospitals, served as the matched controls. Table 1 shows the mean age of the included patients, mean age of onset, the mean duration of complaint, and the mean maximal inter-incisal distance along with the standard deviation and range. In the evaluation of differences between the right and left sides of the masseter and medial pterygoid (thickness and cross-sectional areas) within the groups of bTMJA and controls (using Wilcoxon test), it was seen that there were no statistically significant differences (p>0.05) between the groups. Table 2 shows the mean thickness and cross-sectional areas of the masseter and medial pterygoid muscles in control as well as bilateral TMJA patient groups. When comparing the mean thickness and cross-sectional areas of the masseter muscles between the bTMJA and the control group, statistically significant differences were found. The masseter muscle thickness and its CSA were larger in the group of bTMJA as compared to controls (Table 2). The thickness of medial pterygoid muscles was larger in the group of bTMJA as compared to controls, but there were no statistically different values for the CSA of medial pterygoid muscle.
TMJA is an extensively described entity with many articles describing the bony maxillomandibular and cephalometric characteristics [24–27]. However, the thickness of elevator muscles in this patient population has not been reported so far. Ultrasound [24–27], CT scans, as well as MRI are methods that have been consistently documented to measure muscle thickness. Ultrasound is a cost effective and noninvasive method whereby one can measure the muscle thickness both in contraction as well as relaxation. However, it is technique sensitive, and reproducibility may often be an issue. Moreover, although it is useful to evaluate masseter muscle, it is not possible to evaluate medial pterygoid muscle using ultrasound. MRI is considered as the gold standard for measuring soft tissue thickness. Although superior, it is expensive and not routinely carried out for patients with TMJA. CT scans are routinely carried out for preoperative assessment of TMJA patients. Various studies have used CT scans for measurement of masseter and medial pterygoid muscle thickness, hence a reliable method [28, 29]. Since it was a retrospective study, and CT scan records were readily available, we chose this method of measurement. Slice thickness of 3 mm, although not as accurate as 1-mm slice thickness, has been reported to be sufficient for the evaluation of muscle properties as measured in this study [30]. TMJA is usually seen in young patients [11, 31–33]. The reason for choosing the age group of 16 to 19 years was to find a comparable group of sufficient numbers of patients with the condition. Including patients with a larger age group variation would mean that, due to the difference in the age, it would not have been possible to meaningfully compare muscle parameters of the patients (and controls). The stringent inclusion criteria in our study ensured that only small groups of patients with very similar characteristics were chosen. None of the patients included in the study were operated previously, which
Table 1 Characteristics of the study population
bTMJA (15 subjects) Control (15 patients)
Age of presentation (in years)
Age of onset (in years)
Duration of restricted mouth opening (in years)
Maximal inter incisal distance at presentation (in millimeters)
17.5 (SD: 1.1; range: 16–19) 17.8 (SD: 1.1; range: 16–19)
8.8 (SD: 1.9; range: 5–12) N.A.
8.8 (SD: 1.7; range: 6–12) N.A.
2.5 (SD: 2.0; range: 0–8) W.N.L.
The mean age of the included patients (in years), mean age of onset (in years), the mean duration of complaint (in years), and the mean maximal interincisal distance (in millimeters) are listed. The standard deviation and range of the values are presented in parenthesis bTMJA bilateral temporomandibular joint ankylosis, SD Standard deviation, N.A. not applicable, W.N.L. within normal limits (exact mouth opening was not measured in the control group)
Clin Oral Invest Table 2 Mean thickness and cross-sectional areas of the masseter and medial pterygoid muscles in control as well as bilateral TMJA patient groups Muscle parameter
Side
Number of observations
Mean
SD
p value
Corrected p valuea
M-Th (in mm)
CONTROL bTMJA CONTROL bTMJA CONTROL bTMJA CONTROL bTMJA
15 15 15 15 15 15 15 15
10.58 19.41 430.14 734.89 9.15 11.53 254.59 267.47
1.76 2.37 66.80 156.75 1.15 1.35 45.68 65.35
ORIGINAL ARTICLE
Comparative evaluation of thickness of jaw-closing muscles in patients with long-standing bilateral temporomandibular joint ankylosis: a retrospective case-controlled study Vinay V. Kumar & Neelima A. Malik & Corine M. Visscher & Supriya Ebenezer & Keyvan Sagheb & Frank Lobbezoo
Received: 13 May 2013 / Accepted: 24 April 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Objectives The aim of the study was to compare the thickness and cross-sectional area (CSA) of masseter and medial pterygoid muscles in young patients with long-standing bilateral temporomandibular joint ankylosis (bTMJA) in relation to controls. Methods Axial sections of computed tomography scans of patients with bTMJA from two tertiary care university hospitals were reviewed from 1995 to 2010 and compared to ageand sex-matched controls. The outlines of masseter and medial pterygoid muscles corresponding to a predefined reference plane were traced onto acetate paper. The thickness and CSA of the muscles were calculated using an image-analyzing
Vinay V. Kumar and Neelima A. Malik contributed equally to the paper. V. V. Kumar : C. M. Visscher : F. Lobbezoo Department of Oral Kinesiology, Academic Centre for Dentistry Amsterdam (ACTA), University of Amsterdam and VU University Amsterdam, MOVE Research Institute Amsterdam, Amsterdam, The Netherlands V. V. Kumar : K. Sagheb Department of Maxillofacial and Plastic Surgery, University Medical Center of Johannes Gutenberg University, Mainz, Germany V. V. Kumar (*) Department of Oral and Maxillofacial Surgery, M R Ambedkar Dental College and Hospital, 37 Lazar Layout, Frazer Town, Bangalore 560005, India e-mail: [email protected]
software and calibrated according to the scale provided in the CT scan slides. Results Out of a total of 167 cases of temporomandibular joint ankylosis (TMJA), 15 fulfilled the inclusion criteria. The mean thickness and CSA of masseter and medial pterygoid muscles in cases of bTMJA were 19.4 mm (SD 2.3), 734.9 mm 2 (SD 156.7), 11.53 mm (SD 1.35), and 267.4 mm2 (SD 65.35), respectively. For the control group, respective values were 10.5 mm (SD 1.8), 430.1 mm2 (SD 66.8), 9.2 mm (SD 1.2), and 254.6 mm2 (SD 45.7). There was a statistically significant increased thickness and CSA of the muscles in cases of bTMJA as compared to control as evaluated by Mann-Whitney U test. Conclusions The results show that thickness and CSA of masseter and medial pterygoid muscles in patients with bTMJA were larger as compared to controls. This may suggest that, muscular hyperactivity, may be a cofactor in the pathogenesis of TMJA. Clinical significance Although temporomandibular joint ankylosis is one of the most restrictive musculoskeletal disorder in the maxillofacial region, there is little information on the form and function of jaw muscles in this condition. This study evaluates thickness and cross-sectional areas of jaw elevator muscles and indicates that muscle hyperactivity might be associated with ankylosis, thereby providing a probable hypothesis on the etiopathogenesis of this condition. Keywords Temporomandibular joint ankylosis . Muscles of mastication . Masseter . Medial pterygoid . Bilateral
N. A. Malik Department of Oral and Maxillofacial Surgery, School of Dental Sciences, Krishna Institute of Medical Sciences University, Karad, Maharashtra, India
Introduction
S. Ebenezer Department of Periodontics, M R Ambedkar Dental College and Hospital, Bangalore, India
Temporomandibular joint ankylosis (TMJA) is a condition of restricted mouth opening caused due to the bony or fibrous
Clin Oral Invest
fusion of the condyle to the temporal bone. Although there have been no reports on the exact prevalence of this condition, it has been described as being rare in developed countries and more common in developing countries, especially in the South Asian region [1–7]. Among the various etiologic factors, such as local or systemic infection and neoplasms of the condyle, traumatic injury to the mandibular condyle has been suggested to be the most common cause [5, 8, 9]. TMJA exists in both unilateral and bilateral forms. TMJA is an incapacitating condition with the afflicted individuals having difficulty in normal mandibular movement, mastication, speech, and maintenance of oral hygiene. This may yield severe psychosocial handicap. Due to decreased mouth opening and occlusal irregularities in this patient population, maintenance of adequate oral hygiene is a problem, leading to widespread dental caries and periodontal disease. When manifested in young patients, there are severe growth disturbances of the mandible and face. Patients with unilateral TMJA have facial asymmetry with a flatness and elongation on the unaffected side, and fullness and roundness of the face on the affected side. There is deviation of the chin towards the affected side. In bilateral cases, there is a pronounced decrease in chin prominence as well as shortness in the length and height of the mandible. Also in patients with this condition, there is a pronounced antegonial notch, which is more prominent on the affected side of the mandible (in cases of unilateral TMJA) [10]. The treatment of TMJA is very challenging, not only in achieving adequate facial aesthetics and oral rehabilitation, but also in preventing re-ankylosis. Although the treatment of TMJA is mainly surgical, the role of post-operative physiotherapy cannot be underestimated. It has been widely accepted that the high recurrence rates in developing countries are related to the unavailability of adequate post-operative physiotherapy in these patients [9, 11, 12]. Various hypotheses and theories have been suggested as to explain the etiopathogenesis of TMJA, with the majority of them focusing solely on articular and bony causes [7]. The concept of TMJA is that it occurs due to the discontinuity of the condylar surface, followed by the formation of an intracapsular hematoma that subsequently organizes and ossifies, thus forming the ankylotic mass [13–15]. It has also been postulated that in addition to condylar injury, damage of the meniscal disk as well as medial dislocation of the condylar neck predisposes towards the formation of TMJA [16]. This possibly would occur by osteogenesis caused due to traction of the lateral pterygoid muscle on the bone after sagittal fracture of the mandibular condyle [17]. However, in spite of the many theories trying to explain the etiopathogenesis of the disease, none of them completely explain the formation of TMJA. Recently, extra-articular factors have been suggested as possible important predisposing, initiating, and/or perpetuating
factors that could play a role in the pathogenesis of this condition [18]. One of the most important extra-articular factors is the activity of the masticatory muscles. It has been suggested that chronic arthralgia inhibits the normal use of the joint, inducing reflex muscle splinting to protect the joint [19]; thus, the patients themselves tend to immobilize the joint. The masticatory muscles in these conditions adapt to a restricted range of mouth opening by shortening [20]. Thus, these muscles could become an additional, extraarticular cause of mandibular movement restriction. These effects are generally more evident when joint pathology exists for a longer period. Based on this concept, it has been shown clinically that injection of Botulinum toxin, as an adjunct to surgical therapy, in the masseter muscles of patients operated for TMJA has improved outcomes [18]. Botulinum toxin works by blocking the presynaptic cholinergic nerve endings, thus causing relaxation of the voluntary muscle [21]. Hence, it is seen that there is clinical benefit in the treatment of TMJA by reducing the activity of elevator muscles of the mandible. Studies regarding the characteristics of masticatory muscles in TMJA patients have not been carried out so far. To understand muscular contributions to the etiopathogenesis of TMJA, it is important to know the muscular response of the elevator muscles of the mandible in this condition. Muscle thickness and cross-sectional areas have been used as indirect measures of muscle activity [22]. Muscle thickness is a linear measurement of the thickest region of the muscle, and crosssectional area is the measurement of the circumference of the muscle. The aim of this study was to investigate if there is a difference in the thickness of the elevator muscles of the mandible in patients suffering from bilateral TMJA as compared to an unaffected population. The objective of the study was to measure the thickness and cross-sectional areas of masseter and medial pterygoid muscles in young patients suffering from long-standing bilateral temporomandibular joint ankylosis (bTMJA) in comparison to sex- and agematched controls.
Materials and methods Patient selection Records of patient files from two, tertiary care, teaching university hospitals (Unit NAM, Nair Hospital Dental College, Mumbai, India; and Maharaja Agrasen Medical College, Agroha, India) were reviewed from the year 1995 to 2010 for cases of bTMJA. As the study consisted of evaluating retrospective patient records, no additional examinations were performed. Furthermore, the information was analyzed
Clin Oral Invest
anonymously, and considering these factors, a formal ethical committee clearance was not required. Inclusion criteria All patients diagnosed with bilateral temporomandibular joint ankylosis due to traumatic etiology, in the age range of 16– 20 years on presentation, with increased severity of the disease (defined by the authors as: having the disease for more than 6 years duration; and presenting with less than 8 mm of interincisal distance on maximal mouth opening) were included in the study. None of the chosen patients had documented evidence of any other temporomandibular joint disorders or bruxism. Such narrowly defined inclusion criteria were taken to have as homogenous a patient population as possible. All included cases had to be with adequate documentation, using computed tomography (CT) scans with axial section CT cuts of at least 3 mm thickness, and representation of the appropriate axial slice containing the lingula for measurement. The lingula is a bony prominence that is seen at the plane of mandibular foramen, the region where the inferior alveolar nerve runs into the ramus of the mandible [23]. As the control population, age- and sex-matched individuals were chosen, who were documented with adequate CT scans. The chosen control subject included patients in the age range of 16–19 years, with cystic/pathologic lesions of the maxilla that did not affect the musculoskeletal structures of the masticatory system. The diagnoses of the control group of patients were as follows: dentigerous cyst (four cases), ameloblastoma (three cases), keratinizing cystic odontogenic tumor (three cases), adenomatoid odontogenic tumor (two cases), and one case each of mucoepidermoid carcinoma, aneurysmal bone cyst, and juvenile ossifying fibroma. None of the control subjects had documented histories or findings of any form of temporomandibular joint disease/disorders or bruxism. The CT scans were obtained using Siemens Somatom Sensation 4-slice CT scanner (Siemens AG, Forchheim, Germany), with settings of 140 kVp, 300 mA, 3 mm slice thickness, and no gantry tilt. According to the imaging protocol, the patients were instructed to keep their mouth gently closed and relaxed during the scanning period.
Fig. 1 Representative examples of axial cross sections of CT scans of the patients included in this study. The masseter muscles are outlined in red, and the medial pterygoid muscles are outlined in blue. Axial sections showing the mandibular foramen at the lingula (green arrow) were chosen. The calibration scale can be seen at the right-hand side of the scan. a Example of a bTMJA patient. b Example of a control subject
The images of the chosen axial section were traced onto an acetate paper, and outlines of the masseter and medial pterygoid muscles were drawn (Fig. 1). From this, the thickness and the cross-sectional areas of the muscles were calculated using an image-analyzing software (Image J 1.4q, National Institute of Health, USA) and calibrated according to the scale provided in the CT scan slides. The measurements made were: masseter muscle thickness (M-Th) (in mm), masseter muscle cross-sectional area (M-CSA) (in mm2), medial pterygoid thickness (mP-Th) (in mm), and medial pterygoid crosssectional area (mP-CSA) (in mm2). Two rough working tables were made with the characteristics entered separately corresponding to two different groups of patients: bTMJA and control. The values of the muscle thickness and CSA were presented for the corresponding groups and entered as right and left sides. The tables also contained the following patient characteristics: age, sex, age at onset of TMJA, duration of the condition, and maximal mouth opening. To improve the accuracy of the measurements, the thickness and CSA measurements were performed by two examiners (VVK, KS) working together. They worked together on the tracings and came to an agreement on the outline of the muscles. The same two examiners also evaluated the TH and CSA values. Statistical analysis
Measurements Axial sections of the CT scans were assessed for masseter as well as the medial pterygoid muscles (Fig. 1). A standard reproducible plane was chosen for all the patients to avoid variations in the measurements of muscle thickness and cross sections, because the thickness and cross-sectional area of the muscles differ at different planes. The reproducible axial plane was chosen corresponding to the section containing the lingulae bilaterally.
For both the bTMJA and the control group, first a Wilcoxon test was done to evaluate if there is a difference in masseter and medial pterygoid muscle (thickness and cross-sectional area) between the right and left sides. It was seen that there were no differences in the left and right sides, so the mean of the left and right values for each patient was used to make subsequent analyses between the groups. To analyze the difference in the muscle thickness between the control group and the bTMJA patients (for the masseter
Clin Oral Invest
data as well as for the medial pterygoid data), Mann-Whitney U tests were used. To correct for multiple testing, the Holm’s Bonferroni procedure was used (Holland and Copenhaver, Psychol Bull 1988; 104: 145–149). p values less than or equal to 0.05 were considered statistically significant.
Bonferroni- Holm’s correction of p values yielded similar outcomes. A column to Table 2 presents the corrected p values.
Discussion
Results A total of 167 cases of TMJA (age range from 3 to 45 years) were identified, out of which 69 were cases of bTMJA and 98 cases of unilateral TMJA. Out of the 69 cases of bTMJA, 54 cases had to be excluded as they either did not have adequate documentation or did not fit the inclusion criteria. This resulted in only 15 cases chosen as the test group of study. Fifteen CT scans (sample size matched to the number of bTMJA patients) were chosen randomly from the pool of general patients that had the same age range, who were evaluated at the hospitals, served as the matched controls. Table 1 shows the mean age of the included patients, mean age of onset, the mean duration of complaint, and the mean maximal inter-incisal distance along with the standard deviation and range. In the evaluation of differences between the right and left sides of the masseter and medial pterygoid (thickness and cross-sectional areas) within the groups of bTMJA and controls (using Wilcoxon test), it was seen that there were no statistically significant differences (p>0.05) between the groups. Table 2 shows the mean thickness and cross-sectional areas of the masseter and medial pterygoid muscles in control as well as bilateral TMJA patient groups. When comparing the mean thickness and cross-sectional areas of the masseter muscles between the bTMJA and the control group, statistically significant differences were found. The masseter muscle thickness and its CSA were larger in the group of bTMJA as compared to controls (Table 2). The thickness of medial pterygoid muscles was larger in the group of bTMJA as compared to controls, but there were no statistically different values for the CSA of medial pterygoid muscle.
TMJA is an extensively described entity with many articles describing the bony maxillomandibular and cephalometric characteristics [24–27]. However, the thickness of elevator muscles in this patient population has not been reported so far. Ultrasound [24–27], CT scans, as well as MRI are methods that have been consistently documented to measure muscle thickness. Ultrasound is a cost effective and noninvasive method whereby one can measure the muscle thickness both in contraction as well as relaxation. However, it is technique sensitive, and reproducibility may often be an issue. Moreover, although it is useful to evaluate masseter muscle, it is not possible to evaluate medial pterygoid muscle using ultrasound. MRI is considered as the gold standard for measuring soft tissue thickness. Although superior, it is expensive and not routinely carried out for patients with TMJA. CT scans are routinely carried out for preoperative assessment of TMJA patients. Various studies have used CT scans for measurement of masseter and medial pterygoid muscle thickness, hence a reliable method [28, 29]. Since it was a retrospective study, and CT scan records were readily available, we chose this method of measurement. Slice thickness of 3 mm, although not as accurate as 1-mm slice thickness, has been reported to be sufficient for the evaluation of muscle properties as measured in this study [30]. TMJA is usually seen in young patients [11, 31–33]. The reason for choosing the age group of 16 to 19 years was to find a comparable group of sufficient numbers of patients with the condition. Including patients with a larger age group variation would mean that, due to the difference in the age, it would not have been possible to meaningfully compare muscle parameters of the patients (and controls). The stringent inclusion criteria in our study ensured that only small groups of patients with very similar characteristics were chosen. None of the patients included in the study were operated previously, which
Table 1 Characteristics of the study population
bTMJA (15 subjects) Control (15 patients)
Age of presentation (in years)
Age of onset (in years)
Duration of restricted mouth opening (in years)
Maximal inter incisal distance at presentation (in millimeters)
17.5 (SD: 1.1; range: 16–19) 17.8 (SD: 1.1; range: 16–19)
8.8 (SD: 1.9; range: 5–12) N.A.
8.8 (SD: 1.7; range: 6–12) N.A.
2.5 (SD: 2.0; range: 0–8) W.N.L.
The mean age of the included patients (in years), mean age of onset (in years), the mean duration of complaint (in years), and the mean maximal interincisal distance (in millimeters) are listed. The standard deviation and range of the values are presented in parenthesis bTMJA bilateral temporomandibular joint ankylosis, SD Standard deviation, N.A. not applicable, W.N.L. within normal limits (exact mouth opening was not measured in the control group)
Clin Oral Invest Table 2 Mean thickness and cross-sectional areas of the masseter and medial pterygoid muscles in control as well as bilateral TMJA patient groups Muscle parameter
Side
Number of observations
Mean
SD
p value
Corrected p valuea
M-Th (in mm)
CONTROL bTMJA CONTROL bTMJA CONTROL bTMJA CONTROL bTMJA
15 15 15 15 15 15 15 15
10.58 19.41 430.14 734.89 9.15 11.53 254.59 267.47
1.76 2.37 66.80 156.75 1.15 1.35 45.68 65.35
