Archs oral Bid. Vol. 38, No. 3, pp. 21g219, 1993 Printed in Great Britain. All rights reserved

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0003-9969/93 $6.00 + 0.00 1993 Pergamon Press Ltd

OF MANDIBULAR BONE DENSITY MEASUREMENT EX VW0 AND IN VW0 BY DUAL-ENERGY X-RAY ABSORPTIOMETRY VAN ‘T HoF,Z W. C. A. M. BUIJS,~P. HOPPENBROUWERS,’ W. KALK’ and F. H. M. CORSTENS’ ‘Department of Oral Function and Prosthetic Dentistry, *Department of Medical Statistics and ‘Department of Nuclear Medicine, Faculty of Medicine, Dental School, University of Nijmegen and University Hospital Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands

F. G. A.

CORTEN,’

M. A.

(Accepted 3 November 1992) Summary-Severe bone resorption is a vexing clinical problem, especially in patients without teeth. To study resorption in vivo, measurements of bone mineral density (BMD) of the mandible of both patients with and without teeth are needed. Using a Hologic QDR-1000 bone densitometer designed to measure lumbar spine and hips, ex vivo and in vim measurements were made in selected areas of the mandible. The mandible was positioned such that the X-ray beam was perpendicular to its sagittal plane. In this way the beam hits first one half of the mandible and then the other. The reproducibility+xpressed as coefficient of variation-of the ex viva measurements was 0.5%. For in vivo measurements this coefficient was 3%. The method used for mandibular BMD would make it possible to define an average BMD in several categories of the normal population and of patients, and to compare bone density in the mandible with that in the axial and perpendicular skeleton, Improvement may be obtained by repeating the measurement. The entrance dose per scan is low, equalling that of one bitewing/radiograph. Key words: bone density, mandible, dual-energy X-ray absorptiometry.

INTRODLJCI’ION

For many years it was assumed that local factors, such as the continuous wearing of ill-fitting dentures, were the sole cause of alveolar bone resorption. However, there is great variation in the reduction of the alveolar ridge among long-term denture wearers (Bergman and Carlsson 1985). The degree of alveolar bone resorption and the duration of edentulousness do correlate. Whether denture wearing has serious impact on alveolar bone loss remains controversial (Kalk and De Baat, 1989). Nowadays it is well accepted that there is a relation between alveolar bone loss in edentulous patients and metabolic bone disease (Bras, Van Ooij and Van den Akker, 1985; Habets, Bras and Borgmeyer-Hoelen, 1988). Bone mass itself is a principal determinant of bone strength and fracture risk (Johnston, Slemenda and Melton, 1991). Therefore, it is highly relevant to measure bone mineral content and mineral density. By this method it is possible to identify patients with a high risk of osteoporosis-related problems. There is little information about the bone mineral density of the mandible, especially in Coo. Neither is it known whether mandibular bone loss can be reduced or prevented by treatments similar to those used for osteoporosis of the axial and perpendicular skeleton. To answer these questions a method for accurately measuring the bone mineral density of the mandible in viva is required. Such methods are available for several other bony structures, for example lumbar vertebrae and hips (Rosenquist, Baylink and Berger, 1978; Von Wowern, Storm and Olgaard,

1988; Kribbs, Smith and Chesnut, 1983a, b). These studies indicate that in the normal individual, variations in the mandibular bone mass can be explained to some extent by variations in the cortical bone mass in other skeletal sites. Only weak correlations were found with skeletal sites consisting mainly of trabecular bone (Von Wowern, 1986; Kribbs et al., 1989, 1990). Elders et al. (1992) did not find a significant correlation between the height of the alveolar crest and bone mass measurements. The bone mineral content has been measured in vivo with high precision (2.1%) by a specially constructed dual-photon scanner. Dual-photon absorptiometry indicates that measurements of the mandibular bone mineral content can be used to predict the rate of residual ridge reduction (Von Wowem and Hjsrting-Hansen, 1991). Furthermore, the bone mineral content in the mandible as well as in the forearm was significantly lower in a group of patients with osteoporosis than in a control group (Von Wowern and Kollerup, 1992). A method for direct measurement of the bone mineral density of the mandible is therefore needed. Our purpose now was to develop such a method, reproducible both ex uivo and in viva, using dualenergy X-ray absorptiometry. MATERIALS

AND METHODS

Dual-energy X-ray absorptiometric measurements were made with a Hologic QDR-1000 bone densitometer (Hologic Inc., Waltham, MA, U.S.A.). This system uses an X-ray tube with 75 and 150 kV pulses 215

216

F. G. A. COKTENet al.

alternately applied across it as its source instead of a radioactive source (Hanzen et al., 1990). The source collimator is 2.3 mm, mounted beneath the table. X-rays cross the area of interest in the body and then hit the detector mounted above. Scan speed is 45 mm/s and step size is 1 mm. We used scan lengths of 15.250 cm and scan widths of 18 cm. One scan of the mandibular body took about 4.5 min. The apparatus has an internal calibration wheel composed of materials equivalent to bone and soft tissue as well as an empty ‘air’ segment. These materials rotate 60 times/s through the X-ray beam between the tube and patient, thus providing continuous calibration on a pixel (step)-by-pixel basis. Measurements in each pixel are made for both energies with all three calibration materials (bone, soft tissue and air) interposed. The bone mineral content in grams is calculated through an iterative procedure. The bone mineral ‘density’, in grams per area, is then calculated as bone mineral content per area (cm2). The values obtained by dual-energy X-ray absorptiometry are not volumetric, as the measurements are not made per unit volume but rather per cross-section of bone. We used the bone mineral density, defined as g/cm2. According to the information supplied by the manufacturer the entrance dose for the patient under all operating conditions is 0.02-0.05 mSv per scan (Operators Manual, 10 May, 1989) which is equal to about the exposure of one or two bitewing radiographs. One pair of bitewings gives an entrance dose of 0.021 mSv (Antoku et al., 1976). Ex vivo measurements For ex uivo measurements we used three mandibles (M) with their skulls (S), Ml + Sl and M2 + S2 being edentulous, and M3 + S3 with teeth. Looking forward to the in vivo measurements we had to face the fact that in vivo there are only two positions in which the X-ray beam does not hit other bone structures, meaning that the beam has to go in on one side of the mandible and out at the other. For both the ex vivo and the in vivo experiments, two different positions of the mandible were used. Position one: scan directions from caudal to cranial. The mandibles Ml, M2 and M3 were positioned with the left condyle to the table. The left condyle was fixed to a framework with a tissue-equivalent material, polymethyl methacrylate [see Fig. l(a)]. The intercondular line was perpendicular to the table. The mandible body was perpendicular to the long axis of the table and the direction of scanning was from caudal to cranial. The X-ray beam was perpendicular to the sagittal plane of the mandible. For the delineation of the region of interest, the deepest point of the alveolar processes was taken as a starting point for mandible Ml and M2 [Fig. l(b)]. For M3 the most caudal root apex was used for that purpose. In this way the region of interest is limited to the area free of tooth elements and their roots [Fig. l(c)]. Position two: scan direction from ventral to dorsal. The mandibles (Ml and M2) were fixed to their respective skulls (Sl and S2). The jaws of Ml were separated by a denture with porcelain teeth. A biteblock of polymethyl methacrylate was placed between the denture halves. Mandible M2 had no denture, only a polymethyl methacrylate bite-block.

Fig. 1. (a) Position one: the mandible alone; scan direction from caudal to dorsal. (b) The region of interest (ROI) of the edentate mandible. (c) The ROI of the dentate mandible.

The mandible, skull and bite-block were fixed together with sticking plaster. In the most ventral part of the bite-block a rectangular metal bar was fixed horizontally, which in its turn was held by a vertical bar. A tripod was used for fixation and reposition (see Fig. 2). The right-hand side of the mandible and skull were toward the table top. The sagittal plane of the mandible was parallel to the table top. The X-ray beam was perpendicular to the sagittal plane and the scan direction was from ventral to dorsal. For delineation of the region of interest, the standard software was used for the lumbar spine, as supplied by the manufacturer. The total mandible body was within this region. Subsequently, the total region of interest was arbitrarily divided into four parts, Ll, L2, L3 and L4 [see Fig. 2(a)]. With the use of the standard ‘compare program’, regions of interest could be delineated repeatedly. In vivo measurements The in vivo measurements were made in the same two positions of the mandible as the ex vivo measurements. Position one: mandibular scanning direction from caudal to cranial. The in vivo measurements in this position were made with one edentulous and one

Measurement of mandibular bone density

217

Standard deviations and coefficients of variations in comparable situations may be pooled by taking the squared mean. RESULTS

Ex vivo measurements Position one. Results on reproducibility for bone mineral density in position one are presented in Table 1. After repeated repositioning on a polymethyl methacrylate block and three measurements per mandible the pooled coefficient of variation was 0.4%. Position two. Results on reproducibility for bone mineral density in position two are presented in Table 2, demonstrating a pooled coefficient of variation of 0.5%. In vivo measurements Position one. The corresponding coefficients of variation in bone mineral density measurements of the edentate and dentate subjects, with the scan direction from caudal to cranial, were 2.5 and 1.7%, respectively (see Table 3).

Fig. 2. (a) Position two: fixation of the mandible to the skull with the help of the bite-block. The tripod was used for fixation and reposition. The scan direction was from ventral to dorsal. (b) Subdivision of the region of interest in four parts Ll-L4.

dentate patient. The subjects were lying on the table with their left ear toward the table top. The mandible and the skull of the two subjects were positioned with a ‘bite-block’ similar to that used ex vivo [Fig. 3(a)]. For the delineation of the region of interest for the edentulous subject, see Fig. 3(b), and for the dentate subject patient, see Fig. 3(c). Position two: mandibular scanning direction from ventral to dorsal. The in viva measurements in position two were made with two denture wearers. The methods of fixation and evaluation were practically identical to those in the ex vivo experiments. The position of the patient was rotated by 90” from position one. In position two the patient was lying with the right ear toward the table top [see Fig. 4(a)]. The long axis of the patient was perpendicular to the long axis of the Hologic table. Therefore an additional table was needed to carry the lower part of the body. For the delineation of the region of interest the same procedure was used as in the ex vivo experiment [see Fig. 4(b)]. Statistical analysis Standard deviations were calculated as those of a series of measurements of the same object under the same conditions. The coefficient of variation is the standard deviation divided by the mean x 100%.

Fig. 3. (a) The patient in position one, lying with the left ear toward the table top. The arrow indicates the scan direction, from caudal to cranial. The fixation and reposition of mandible was identical to the one used in the ex uiuo experiments. (b) The region of interest of an edentulous patient. (c) The region of interest in a dentate patient.

218

F. G. A. CORTENet al. Table 2. Standard deviation (SD) and coefficients of variation (CV%) of bone mineral density (BMD) measured ex viva on two edentulous mandibles, fixed to their resoective skull for different regions of interest (ROI) LlLL4

SD g/cm’

CV%

ROI Quantity

Fig. 2(a)

Range

Pooled

Range

Pooled

Ll L2 L3 L4 Total

0.006-0.008 0.008~.010 0.00~.040 O.Ol(M.030 0.00~.009

0.007 0.009 0.028 0.024 0.007

O.&o.7 0.5-0.6 0.3-2.0 0.6-1.7 0.34.7

0.7 0.6 1.2 1.2 0.5

rigidity of the equipment. The dentate investigated with good reproducibility

patient

can be

BMD

n = 6 per mandible.

Fig. 4. (a) The patient in position two, lying with the right ear toward the table top. The scan direction was from ventral to caudal, as the arrow indicates. (b) Subdivision of the region of interest into four parts Ll-L4. Position two. The corresponding coefficient of variation of the two denture wearers, with the scan direction from ventral to caudal, was 4.1% (see Table 4). DISCUSSION

The reproducibility of the ex vivo measurements of the mandibles alone and of those fixed to their skulls were both satisfactory. However, in vivo the reproducibility of the measurements was poorer for the dentate patient and for the three denture wearers. The difference of reproducibility between ex vivo and in viuo measurements can partly be explained by the

rigidity of the fixation equipment, the movement of the patient, and the mobility between the denture base and the underlying soft alveolar tissue. The three patients were wearing ill-fitting dentures. A wellfitting denture contributes to better fixation and consequently to a higher reproducibility. The reproducibility of bone mineral density in the dentate patient was much better, probably because of the

when the region of interest is limited to the area free of teeth and their roots. The data suggest that the reproducibility per area in the in oivo measurements was correlated with the distance of that area from the point of fixation: the shorter the distance, the better the reproducibility. In addition, it might be possible to improve the rigidity of our equipment. Elders et al. (1992) measured the alveolar bone height from bitewing radiographs and found a coefficient of variation of 4.4%. Kribbs et al. (1990), measured the bone mass of the mandible by radiographs-scanned by a microdensitometer-in osteoporotic and normal subjects. The precision with this technique was 1.5%. Von Wowem et al. (1999), measured the bone mineral content of the mandible and also of the forearm and lumbar spine by dualphoton absorptiometry. The coefficient of variation of the measurements was 0.8% ex vivo and 2.1% in vivo.

Our main finding is that using the Hologic QDR1000 one obtains in vivo a standard deviation of about 3%, taking into account the quadratic mean of the coefficients of variation. The Hologic, however, has been designed especially for studies on the lumbar spine and therefore a standard deviation of 1% is Table 3. Standard deviations (SD) and coefficients of variation (CV%) of the bone mineral density (BMD) in one edentate patient (n = 9) and one dentate patient (n = 6)

BMD

Edentate Dentate

ROI

SD g/cm2

CV%

Fig. 3(b) Fig. 3(c)

0.05 0.03

2.5 1.7

For the region of interest (ROI) see Figs 3(b) and (c). Table 4. Standard deviations (SD) and coefficients of variation (CV%) of the bone mineral density (BMD) as measured in vivo on the mandibles of two denture wearers SD g/cm2

Table 1. Standard deviation (SD) and coefficient of variation (CV%) of bone mineral density (BMD) of three mandibles ex vivo, after repeated repositioning on a polymethyl methacrylate block

BMD

BMD

CV%

SD g/cm* Range

Pooled

Range

Pooled

0.002~.010

0.006

0.14.8

0.4

n = 3 per mandible.

Quantity

CV%

ROI Fig. 4(b)

Range

Pooled

Range

Pooled

Ll L2 L3 L4 Total

0.044X06 0.03-0.05 0.04O.05 0.034.05 0.05~.05

0.05 0.04 0.05 0.04 0.05

8.C-11.0 3.0-4.4 3.0-4.0 2.1-3.0 3.84.4

10.0 3.7 3.5 2.6 4.1

Patient 1 had six measurements, patient 2 five measurements after full repositioning. For the region of interest (ROI) see Fig. 4(b).

Measurement of mandibular bone density obtained for the bone mineral density. In consequence, the discriminative power for measurements of bone mineral density in spines is about three times that for mandibles. For use in longitudinal studies it is important to know how great are the changes in bone mineral density with time in certain populations. The change of the bone mineral density in the postmenopausal period is about -2.4% per yr (Elders et al., 1989; Christiansen and Riis, 1989). The minimal detectable significant (95% confidence limit) difference between two measurements in a single subject is 8.4% for a coefficient of variation of 3%. Improvement may be obtained by repeating the measurement. Four measurements give a standard deviation of 8.4%: ,/4 = 4.2%. Thus to detect bone loss at 2.4% per yr would take about 2 yr. This method enables us to measure bone mineral density of the mandible with the same technique and to compare this with zones in the axial and perpendicular skeleton. Improvement of the reproducibility could be obtained by:

(4 Evaluation of the performance of the software and subsequent adaptation and improvement of the program. (b) Standardization of the angle between the two sides of the mandible using a synthetic mandible support in order to make sure that the base of the mandible (the part where the mandible is seated) is perpendicular to the surface and parallel to the length of the Hologic table. An artificial plate will be secured to the left and right of the base of the ‘mandibular fixation cap’, thus laterally supporting the lower and upper jaw. (4 The introduction of a lateral X-ray bone densitometer with a movable arm. Acknowledgements-We thank Mrs M. v.d. Ven and Mr M. Engels for technical assistance. REFERENCES

Antoku S., Kihara T., Russell W. J. and Beach D. R. (1976) Doses to critical organs from dental radiography. Oral Surg. 41, 251-260. Bergman B. and Carlsson G. E. (1985) Clinical long-term study of complete denture wearers. J. prosthet. Dent. 53, 5&61. Bras J., Van Ooij C. P. and Van den Akker H. P. (1985) Mandibular atrophy and metabolic bone loss. Mandibular ridge augmentation by combined sandwich-visor osteotomy and resorption related to metabolic state. Int. J. oral Surg. 14, 1621.

08

3813-B

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Christiansen C. and Riis B. J. (1989) Is it possible to predict the fast bone loser just after the menopause? Bone Miner. Res. 6, 317-332. Elders P. J. M., Netelenbos J. C., Lips P., Khoe E., Van Ginkel F. C., Hulshof K. F. M. A. and van der Stelt P. F. (1989) Perimenopausal bone mass and risk factors. Bone Miner. 7, 289-299. Elders P. J. M., Habets L. L. M. H., Netelenbos J. C., Van der Linden L. W. J. and Van der Stelt P. F. (1992) The relation between periodontitis and systemic bone mass in women between 46 and 55 years of age. J. clin. Periodont. 19, 492496. Habets L. L. M. H., Bras J. and Borgmeyer-Hoelen A. M. M. J. (1988) Mandibular atrophy and metabolic bone loss. Endocrinology, radiology and histomorphometry. Int. J. oral Maxillofac. Surg. 17, 208-211. Hanzen M. A., Hansager C., Overgaard K., Mauslew U., Riis B. J. and Christiansen C. (1990) Dual-energy X-ray absorptiometry: a precise method of measuring bone mineral density in the lumbar spine. J. Nucl. Med. 31, 11561162. Johnston C. C. Jr, Slemenda C. W. and Melton L. J. (1991) Clinical use of bone densitometry. New Engl. J. Med. 324, 1105-l 109. Kalk W. and De Baat C. (1989) Some factors connected with alveolar bone resorption. J. Dent. 17, 162-165. Kribbs P. J., Smith D. E. and Chesnut C. H. (1983a) Oral findings in osteoporosis: Part I. Measurement of mandibular bone density. J. prosthet. Dent. 50, 576-579. Kribbs P. J.. Smith D. E. and Chesnut C. H. (1983b) Oral findings in osteoporosis: Part II. Relationship be: tween residual ridge and alveolar bone resorption and generalized skeletal osteopenia. J. prosthet. Dent. 50, 719-724. Kribbs P. J., Chesnut C. H., Ott S. M. and Kilcoyne R. F. (1989) Relationships between mandibular and skeletal bone in an osteoporotic population. J. prosthet. Dent. 62, 703-707. Kribbs P. J., Chesnut C. H., Ott S. M. and Kilcoyne R. F. (1990) Relationships between mandibular and skeletal bone in a population of normal women. J. prosthet. Dent. 63, 86-89. Rosenquist J. B., Baylink D. J. and Berger J. S. (1978) Alveolar atrophy and decreased skeletal mass of the radius. ht. J. oral Surg. 7, 479481. Von Wowern N. (1986) Bone mass of mandibles. Dan. Med. Bull. 33, 2344. Von Wowern N. and Hjsrting-Hansen E. (1991) The mandibular bone mineral content in relation to vestibulolingual sulcoplasty. A 2-year follow-up. J. prosthet. Dent. 65, 804-808. Von Wowern N. and Kollerup G. (1992) Symptomatic osteoporosis: a risk factor for residual ridge reduction of the jaws. J. prosthet. Dent. 67, 656-660. Von Wowern N., Storm T. L. and Olgaard K. (1988) Bone mineral content by photon absorptiometry of the mandible compared with that of the forearm and the lumbar spine. Calc. 7%. Int. 42, 1577161.

measurement of mandibular bone density ex vw0 and ...

mandible support in order to make sure that the base of the mandible ... Engels for technical assistance. ... Bras J., Van Ooij C. P. and Van den Akker H. P. (1985).

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