Relationships among maxillofacial morphologies, bone properties, and bone metabolic markers in patients with jaw deformities

Abstract

The aim of this study was to determine the relationships among bone properties, bone metabolic markers, and types of jaw deformity. The subjects were 55 female patients with jaw deformities. Skeletal morphology was examined using lateral cephalograms, and the patients were divided into three groups according to the type of anteroposterior skeletal pattern. Serum osteocalcin, bone alkaline phosphatase, and tartrate-resistant acid phosphatase isoform 5b, as well as deoxypyridinoline in urine, were measured as bone metabolic markers. Quantitative ultrasound (QUS) measurements were used to assess bone properties at the calcaneal bone. The bone volume and bone density of the condylar process were measured in 43 patients by computed tomography. There were no significant differences in bone metabolic markers and QUS parameters between the groups, although bone formation and resorption markers tended to be higher in patients with a protrusive mandible. On the other hand, patients with mandibular retrusion had a higher tendency to have small and dense condylar processes. In conclusion, the results suggest that growth depression or a degenerative change in the mandibular condyle is involved in the pathogenesis of mandibular retrusion, although risk factors for progressive condylar resorption were not determined.

A jaw deformity is an imbalance of the position, size, shape, or orientation of the upper and lower jaws. The pathogenesis of jaw deformities has not been elucidated, but genetic and environmental factors are thought to be involved. Trauma to the facial skeleton and habits such as digit sucking and mouth breathing can be attributed to jaw deformities. Some jaw deformities, such as mandibular prognathism, may be inherited. Internal derangement of the temporomandibular joint (TMJ) may lead to mandibular retrusion, open bite, and/or mandibular asymmetry.

The mandibular condyle undergoes a remodelling process as it responds to continuous stimuli from childhood to adulthood, and it is the primary centre of growth in the mandible. Therefore, the shape and volume of the mandibular condyle could be linked to the maxillofacial morphology. Progressive condylar resorption (PCR) is characterized by severe morphological changes to the condylar configuration, with a reduction in volume and decrease in ramus height. This can lead to occlusal and musculoskeletal instability, resulting in the development of jaw deformities such as mandibular retrusion and open bite. PCR is also known as idiopathic condylar resorption, idiopathic condylysis, and condylar atrophy. PCR leads to the development of late skeletal relapse after orthognathic surgery. Its aetiology, however, is not fully understood. This condition can be generated by excessive mechanical loading applied to or sustained by the joint structures to the extent that the pressure exceeds the adaptive capacity of the condyle. Therefore, poor bone properties of the mandibular condyle are likely to cause condylar resorption.

It has been reported that the bone mineral density (BMD) of the mandibular bone is significantly correlated with the BMD of skeletal bone. Poor bone properties are caused by an imbalance in skeletal turnover, which is maintained by the processes of bone formation and resorption. Bone metabolic markers are useful for the evaluation of bone metabolism.

The possibility that a bone metabolism disorder is one of the causes of PCR has been considered. However, there has been no study on bone properties and bone metabolic markers in patients with jaw deformities. The aim of this study was to determine the relationships among bone properties, bone metabolic markers, and types of jaw deformity.

Materials and methods

Subjects

This prospective study included 55 female patients whose jaw deformities had been corrected surgically at the university hospital in Niigata, Japan, between July 2012 and September 2014. Agreement to participate in this clinical study was obtained. Only female patients were included because the normal levels of bone metabolic markers and cephalometric items differ between males and females. No cases of cleft palate or craniofacial syndrome were included. The mean age of the subjects at surgery was 23 years (range 15–39 years). The study protocol was approved by the ethics committee of the study institution in Niigata, Japan, and informed consent was obtained from the subjects.

Cephalometric analyses

Skeletal morphology was examined using a lateral cephalogram (CX-150W; Asahi Roentgen Industrial Co., Ltd, Kyoto, Japan) that was taken with the teeth in centric occlusion immediately before surgery. The lateral cephalogram was traced and digitized by translating the landmark points. Nine measurements were made using cephalometric analysis software (CephaloMetrics AtoZ; Yasunaga Computer System Co., Ltd, Fukui, Japan): facial angle, A–B plane angle, mandibular plane angle, y -axis, gonial angle, ramus inclination, sella–nasion–A-point (SNA), sella–nasion–B-point (SNB), and A-point–nasion–B-point (ANB) ( Fig. 1 ).

Fig. 1
Measurements made on a lateral cephalogram. (1) Facial angle: angle between the FH plane and facial plane. (2) A–B plane angle: angle between line A–B and line N–Pog. (3) Mandibular plane angle: angle between the FH plane and mandibular plane. (4) Y -axis: angle between the FH plane and line S–Gn. (5) Gonial angle: angle between the ramus plane and mandibular plane. (6) Ramus inclination: angle between the ramus plane and FH plane. (7) SNA: angle between line S–N and line N–A. (8) SNB: angle between line S–N and line N–B. (9) ANB: difference between SNA and SNB. (FH, Frankfort horizontal; A, A-point; B, B-point; N, nasion; Pog, pogonion; S, sella; Gn, gnathion.).

The patients were divided into three groups according to the type of anteroposterior skeletal pattern: a group of 39 patients with skeletal class III malocclusions with or without open bite (class III group), a group of nine patients with skeletal class II malocclusions with or without open bite (class II group), and a group of seven patients with skeletal class I malocclusions who had facial asymmetry and/or open bite (class I group). The mean ± standard deviation (SD) age at surgery was 22 ± 6 years (range 15–39 years) in the class III group, 27 ± 9 years (range 17–38 years) in the class II group, and 22 ± 5 years (range 16–28 years) in the class I group.

Measurements of bone metabolic markers

As bone formation markers, the serum levels of osteocalcin (OC) and bone alkaline phosphatase (BAP) were measured by immunoradiometric assay (IRMA) and chemiluminescent enzyme immunoassay (CLEIA), respectively. As bone resorption markers, tartrate-resistant acid phosphatase isoform 5b (TRACP-5b) in serum and deoxypyridinoline (DPD) in urine were measured by enzyme immunoassay (EIA). Blood and urine samples were collected between 9:00 a.m. and 11:00 a.m. because bone metabolic markers are subject to circadian influence. Reference values used were the normal ranges established in healthy Japanese subjects.

Measurement of bone properties at the calcaneal bone

Quantitative ultrasound (QUS) is a portable and accurate technology for measuring bone properties without radiation exposure. QUS measurements at the calcaneal bone were made using an ultrasonometer device (Achilles A-1000 EXP II; GE Healthcare Japan Corporation, Tokyo, Japan). The patient’s right foot was placed on the foot positioner of the device, because it is considered that there is no significant difference in healthy human calcaneal bone density between the left and right foot. A transducer on one side of the heel converted an electrical signal into a sound wave, which passed through the patient’s heel. A transducer at a fixed distance on the opposite side of the heel received the sound wave and converted it into an electrical signal. This device measured the speed of sound (SOS; metres per second (m/s)) passing through the heel and the broadband ultrasound attenuation (BUA; decibels per megahertz (dB/MHz)) as a measure of frequency-dependent attenuation of the ultrasound wave passing through the heel. The stiffness index, which is a variable derived from the combination of SOS and BUA and accurately reflects BMD, was calculated using the following equation: stiffness index = [(0.67 × BUA) + (0.28 × SOS)] − 420.

Measurements of bone volume and bone properties at the mandibular condylar process

Bone volume and bone density of the mandibular condylar process were measured in 43 patients for whom helical computed tomography (CT) of the maxillofacial region was performed around the same time as the other examinations. Helical CT data were obtained in DICOM (digital imaging and communication in medicine) format. A multi-detector CT scanner was used (Aquilion ONE Global Edition; Toshiba Medical Systems Co. Ltd, Ohtawara city, Japan), with a tube voltage of 120 kVp, average tube current of 125 mA, 500 ms scan time, and thickness of 1 mm.

Three-dimensional images of the maxillofacial region were reconstructed and re-aligned to extract images of the mandibular condylar process using image processing software (ZioTerm 2009; Ziosoft, Inc., Tokyo, Japan). The Frankfort horizontal (FH) plane was used as a reference plane; this was formed by the bilateral uppermost points on the bony external auditory meatus (porion) and lowest point on the right inferior borders of the bony orbit (orbitale). The three points were determined manually using the sagittal plane, coronal plane, and axial plane of a multiplanar reconstruction (MPR) image ( Fig. 2 ). As the target region, the mandibular condylar process was defined as the area above the base plane that was parallel to the FH plane and passing through the most inferior point of the mandibular notch ( Fig. 3 ).

Fig. 2
Setting of the Frankfort horizontal plane on the reconstructed three-dimensional CT images. (A) Axial view. (B) Coronal view. (C) Midsagittal view. The bilateral uppermost points on the bony external auditory meatus (porion) and lowest point on the right inferior borders of the bony orbit (orbitale) were identified three-dimensionally and the Frankfort horizontal plane was defined as the plane passing through the bilateral porions and right orbitale.

Fig. 3
Definition of the mandibular condylar process. The mandibular condylar process was defined as the area between the Frankfort horizontal plane (A) and the plane parallel to the Frankfort horizontal plane and passing through the mandibular notch (B).

Measurements of the mandibular condylar process were performed using image analysis software (ImageJ; National Institutes of Health, Bethesda, MD, USA). Voxel data from above the base plane were used ( Fig. 4 ). The outer shape of the condylar process was clearly extracted with a threshold of over 350 Hounsfield units (HU), classified as D3 according to the Misch classification. The bone region in the extracted outer shape was then identified if voxel data were over 150 HU, classified as D4 according to the Misch classification. The size of voxel data was 0.43 × 0.43 × 0.50 mm, and the total volume (TV), bone volume (BV), and bone density (BV/TV) of the condylar process were calculated from the voxel data. The average value of measurements obtained on both sides was taken as the representative value for the subject.

Fig. 4
Measurements of bone volume and bone properties at the mandibular condylar process. The A plane is the base plane and the dotted line B is one of the cross lines between CT slices and the base plane. Voxel data from above the base plane were used. The outer shape of the condylar process was clearly extracted with a threshold of over 350 Hounsfield units (HU). The bone region in the extracted outer shape was identified if voxel data were over 150 HU. The size of voxel data was 0.43 × 0.43 × 0.50 mm, and the total volume (TV), bone volume (BV), and bone density (BV/TV) of the condylar process were calculated from the voxel data.

Statistical analysis

Mean and SD values of all measured parameters were calculated. Since it could not be assumed that some parameters had a normal distribution, Kruskal–Wallis one-way analysis of variance and pairwise comparisons were used to assess the significance of differences among the groups; Spearman’s correlation analysis was performed to assess the correlations between parameters. Probabilities of less than 0.05 were accepted as significant. Data were analyzed using IBM SPSS Statistics 21 for Windows (IBM Japan Ltd, Tokyo, Japan).

Results

All mean bone metabolic marker values were within the reference ranges, and there was no significant difference between the groups for any of the markers ( Table 1 ). On the other hand, BAP was significantly correlated with the facial angle, A–B plane angle, SNB, ANB, and ramus inclination, and TRACP-5b was significantly correlated with the facial angle, A–B plane angle, y -axis, ANB, and ramus inclination ( Table 2 ). These results indicated that bone metabolic turnover was enhanced in patients showing a tendency to mandibular protrusion.

Table 1
Results of measurements of bone metabolic markers ( N = 55); mean ± standard deviation values.
OC (μg/ml) BAP (μg/l) TRACP-5b (mU/dl) DPD (nmol/mmol Cr)
Skeletal class I ( n = 7) 5.8 ± 2.6 14.2 ± 6.5 288 ± 73 7.2 ± 1.5
Skeletal class II ( n = 9) 5.1 ± 2.2 10.1 ± 2.3 266 ± 94 6.1 ± 1.6
Skeletal class III ( n = 39) 6.4 ± 2.2 13.3 ± 4.0 332 ± 107 6.6 ± 1.6
Reference values a 3.1–12.7 2.9–14.5 120–420 2.8–7.6
OC, osteocalcin; BAP, bone alkaline phosphatase; TRACP-5b, tartrate-resistant acid phosphatase isoform 5b; DPD, deoxypyridinoline.

a Reference values are the normal ranges established in healthy Japanese subjects.

Table 2
Correlations between bone metabolic markers and cephalometric analysis items: Spearman’s correlation coefficients ( N = 55).
OC BAP TRACP-5b DPD
Facial angle 0.11 0.32 * 0.27 * 0.16
A–B plane angle 0.07 0.35 ** 0.36 ** 0.18
Mandibular plane angle −0.05 −0.21 −0.20 −0.15
y -axis −0.08 −0.27 −0.29 * −0.16
SNA 0.09 0.04 −0.12 −0.03
SNB 0.14 0.31 * 0.23 0.16
ANB −0.08 −0.35 ** −0.39 ** −0.19
Gonial angle 0.02 0.18 0.11 0.02
Ramus inclination −0.13 −0.35 ** −0.29 * −0.20
OC, osteocalcin; BAP, bone alkaline phosphatase; TRACP-5b, tartrate-resistant acid phosphatase isoform 5b; DPD, deoxypyridinoline; SNA, sella–nasion–A-point; SNB, sella–nasion–B-point; ANB, A-point–nasion–B-point.

* P < 0.05.

** P < 0.01.

There were no significant differences in QUS parameters at the calcaneal bone between the groups ( Table 3 ), and none of the QUS parameters showed an association with the characteristics of maxillofacial morphology ( Table 4 ). However, TRACP-5b showed positive correlations with SOS and the stiffness index ( Table 4 ).

Table 3
Results of measurements of QUS parameters at the calcaneal bone ( N = 55); mean ± standard deviation values.
SOS (m/s) BUA (dB/MHz) Stiffness index
Skeletal class I ( n = 7) 1571 ± 41 111.7 ± 6.2 94 ± 14
Skeletal class II ( n = 9) 1578 ± 43 115.7 ± 6.1 99 ± 15
Skeletal class III ( n = 39) 1571 ± 37 114.3 ± 11.5 96 ± 15
QUS, quantitative ultrasound; SOS, speed of sound; BUA, broadband ultrasound attenuation.

Table 4
Correlations between QUS parameters at the calcaneal bone and cephalometric analysis items and bone metabolic markers: Spearman’s correlation coefficients ( N = 55).
SOS BUA Stiffness index
Cephalometric analysis items
Facial angle 0.01 −0.06 −0.02
A–B plane angle 0.03 0.07 0.05
Mandibular plane angle 0.07 0.09 0.08
y -axis −0.001 0.09 0.05
SNA −0.001 −0.07 −0.02
SNB 0.04 0.04 0.06
ANB −0.07 −0.10 −0.09
Gonial angle −0.13 0.09 −0.05
Ramus inclination 0.06 0.02 0.03
Bone metabolic markers
OC 0.19 0.05 0.19
BAP 0.07 0.03 0.12
TRACP-5b 0.37 ** 0.24 0.38 **
DPD 0.26 0.04 0.25
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Jan 16, 2018 | Posted by in Oral and Maxillofacial Surgery | Comments Off on Relationships among maxillofacial morphologies, bone properties, and bone metabolic markers in patients with jaw deformities
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