Ovid: Cao: Clin Oral Implants Res, Volume 12(6).December 2001.604-608

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Volume 12(6), December 2001, pp 604-608

Bone mineral density in mandibles of ovariectomized rabbits [Original Articles] Cao, Tong; Shirota, Tatsuo; Yamazaki, Masataka; Ohno, Kohsuke; Michi, Ken-ichi Authors' affiliations: Tong Cao, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, National University of Singapore, Singapore Tong Cao, Tatsuo Shirota, Masataka Yamazaki, Kohsuke Ohno, Kenichi Michi, First Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, Tokyo, Japan Correspondence to: Tatsuo Shirota, DDS, PhD; First Department of Oral and Maxillofacial; Surgery; School of Dentistry, Showa University; 21-1 Kitasenzoku, Ohta-ku; Tokyo 145-8515; Japan; Tel: +81 3 3787 1151; Fax: +81 3 3787 7104; e-mail: [email protected] Date: Accepted 23 November 2000 To cite this article: Cao T, Shirota T, Yamazaki M, Ohno K, Michi K. Bone mineral density in mandibles of ovariectomized rabbits

Abstract: The purpose of this study was to evaluate the association between loss of ovarian function and bone mineral density changes in the mandibles of ovariectomized rabbits using peripheral quantitative computed tomography. Twenty-four adult female Japanese white rabbits were used in this experiment. The mandibular incisors were initially extracted to create implant bone. Twelve animals were bilaterally ovariectomized and the other twelve sham-ovariectomized 12 weeks after tooth extraction. All rabbits were sacrificed at 4 and 12 weeks after ovariectomy and shamovariectomy, with 6 rabbits in each of the four resultant groups. The edentulous parts of distal mandibular bodies were measured by peripheral quantitative computed tomography. There were significant decreases in total bone mineral density and trabecular bone mineral density in the mandibles of rabbits at 12 weeks post-ovariectomy. The results demonstrate the mineralized bone loss in the mandibles of ovariectomized rabbits.

Résumé Cette étude a été effectuée pour évaluer l'association entre la perte de la fonction ovarienne et les variations de densité minérale osseuse dans les mandibules de lapines ovariectomisées, à l'aide d' une tomographie par ordinateur permettant la quantification périphérique. Vingt-quatre lapines blanches japonaises ont été utilisées dans cette étude. Les incisives mandibulaires ont été enlevées pour créér de l'os implantaire. Douze animaux ont été ovariectomisées bilatéralement et les douze autres ont subi une ovariectomie simulée douze semaines après l'avulsion dentaire. Toutes les lapines ont été tuées quatre et douze semaines après l'ovariectomie ou l'ovariectomie simulée, répartissant quatre lapines dans chaque groupe. Les parties édentées distales ont été mesurées par tomographie par ordinateur permettant la quantification périphérique. Des diminutions significatives ont été enregistrées dans la densité minérale osseuse totale et dans la densité minérale osseuse trabéculaire au niveau des mandibules des lapines douze semaines après l'ovarieoctomie. Ces résultats démontrent une perte osseuse minérale dans les mandibules des lapines ovarieoctomisées.

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Zusammenfassung Es war das Ziel dieser Studie, den Zusammenhang zwischen dem Verlust der Funktion der Ovarien und den Veränderungen in der Dichte des Knochenminerals in den Unterkiefern von ovariektomierten Kaninchen durch periphere quantitative Computertomographie zu untersuchen. Vierundzwanzig ausgewachsene japanische weibliche weisse Kaninchen wurden für das Experiment verwendet. Die Unterkieferinzisiven wurden zu Beginn extrahiert, um Implantatknochen zu generieren. Zwölf Wochen nach den Zahnextraktionen wurden bei zwölf Tieren bilateral Ovariektomien durchgeführt und die anderen zwölf Tiere erhielten ScheinOvariektomien. Alle Kaninchen wurden 4 bzw. 12 Wochen nach Ovariektomie oder ScheinOvariektomie geopfert. Es resultierten 4 Gruppen mit je sechs Tieren. Der zahnlose Anteil der distalen Mandibularkörper wurde mittels peripherer quantitativer Computertomographie ausgemessen. Bei den Unterkiefern der Kaninchen 12 Wochen nach Ovariektomie bestand eine signifikante Abnahme in der totalen Dichte des Knochenminerals und in der Dichte des trabekulären Knochenminerals. Die Resultate demonstrieren den Verlust an mineralisiertem Knochen in den Unterkiefern von ovariektomierten Ratten.

Resumen Este estudio se realizo para evaluar la asociación entre la perdida de la función ovárica y los cambios en la densidad mineral del hueso en las mandibulas de conejas ovarectomizadas por tomografía computarizada periférica cuantitativa. Se usaron 24 conejas blancas adultas japonesas en este experimento. Los incisivos mandibulares se extrajeron inicialmente para crear hueso de implante. Se ovarectomizó bilateralmente a 12 animales y se simuló una ovarectomización en los otros 12 después de 12 semanas tras la extracción. Se sacrificó a todas las conejas a las 4 y 12 semanas tras la ovarectomización y la falsa ovarectimización con 6 conejas en cada uno de los cuatro grupos resultantes. Las partes edéntulas de los cuerpos mandibulares distales se midieron por medio de tomografía computarizada periférica cuantitativa. Existieron disminuciones significativas en la densidad mineral de hueso total y en la densidad mineral de hueso trabecular en las mandíbulas de las conejas a las 12 semanas tras la ovarectomización. Los resultados demuestran la perdida de hueso mineralizado en las mandíbulas de conejas ovarectomizadas.

Abstract FIGURE

Figure. No caption available.

Clinical studies have suggested that the greater risk for oral bone loss in females may be correlated with osteoporosis after menopause (Hildebolt 1997; Jeffcoat 1998). Experiments of titanium and hydroxyapatite-coated implantation on rats' tibiae revealed less bone-implant contact in the ovariectomized rats (Motohashi et al. 1999; Yamazaki et al. 1999). However, it is necessary to obtain the information in experimental studies to determine the relationship between oral bone loss and osteoporosis with loss of ovarian function. The ovariectomized animal has been widely used as a

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model of postmenopausal osteoporosis because the osteopenia that develops after ovariectomy has many qualitative similarities to the human disease (Wronski et al. 1988; Chow et al. 1992). It has been recognized as the preferred animal model for examining the clinical outcome of postmenopausal bone loss (Food and Drug Administration of United States of America, 1994) and rats have been the most widely used lower animal species (Wronski & Yen 1991). A former experimental study showed that periosteal bone formation was increased in cross-sections of mandibular cortices in adult ovariectomized rats (Miller et al. 1991). Another study demonstrated no significant differences in bone formation at the periosteal, endocortical and cancellous surfaces in dentulous mandibular cross-sections between sham-ovariectomized and ovariectomized groups of aged rats (Miller et al. 1997). In this study, bone mineral density (BMD) analysis has been performed using peripheral quantitative computed tomography (pQCT) on the mandibular edentulous trabeculae of ovariectomized rabbits. Various x-ray techniques have been employed to measure bone mineral content (Hassager & Christiansen 1995).

Early approaches, such as single-photon absorptiometry and single-energy x-ray

absorptiometry, were prone to systematic error, and have now been largely superseded by dualenergy techniques, principally dual-energy x-ray absorptiometry (DXA), or by tomography. DXA has been applied to the analysis of rat bone and this technique has been found to be both accurate and precise in vivo (Ammam et al. 1992; Griffin et al. 1993; Mitlak et al. 1994; Rozenberg et al. 1995) and ex vivo (Lu et al. 1994). Regional DXA analysis of the rat femur has demonstrated the ability to detect early loss of bone mineral density in a trabecular-rich region of bone, post-ovariectomy (Pastoureau et al. 1995; Rosen et al. 1995).

pQCT has been used for the clinical measurement of (BMD)

(Ruegsegger et al. 1991; Lehmann et al. 1992; Hangartner 1993; Butz et al. 1994; Wapniarz et al. 1994),

and has

also been applied to the study in vivo of models of osteoporosis in the rat (Sato et al. 1995). High sensitivity of BMD to ovariectomy in the trabecular locations of tibiae, femora, ilia and vertebrae was observed by pQCT (Breen et al. 1996; Augat et al. 1997; Ebbesen et al. 1997; Helterbrand et al. 1997). Regional analysis of BMD, coupled with the ability to differentiate cortical and trabecular bone, may prove valuable in the analysis of bone changes of mandible in ovariectomized animals. The purpose of this study was to evaluate the association between loss of ovarian function and the BMD changes in the mandibules of ovariectomized rabbits.

Material and methods Experimental animals Twenty-four adult female Japanese white rabbits (Japan Clea Co. Ltd., Tokyo, Japan) were obtained at 12 weeks of age, at an average weight of 3 kg, and allowed to acclimate for 1 week. The rabbits were housed in individual cages and maintained in a controlled environment at 24±1° C, humidity 55±5% with a circadian light rhythm of 12 hours. Standard laboratory chow (RC4, Oriental Yeast Co., Chiba, Japan) and water ad libitum were available to the rabbits. This study was approved by the Institutional Animal Use and Care Committee, Showa University.

Experimental design The bilateral mandibular incisors of each animal were initially extracted and the maxillary incisors were cut at the gingival edge under anesthesia with an intraperitoneal injection of pentobarbital sodium solution (Nembutal, Abbott Laboratories, North Chicago, IL, USA) at a dose of 25 mg/kg body weight. Twelve weeks after tooth extraction, bilateral ovariectomies were performed on twelve of the rabbits (Ovx group) under the same anesthesia as for the tooth

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extraction. Sham-ovariectomy was performed on the remaining 12 rabbits as a control (Sham group). For the sham-ovariectomy, the ovaries were lifted up and then returned to the original position. All rabbits were sacrificed at 4 and 12 weeks after ovariectomy or sham-ovariectomy with the formation of 4 groups of 6 rabbits, respectively. The success of the ovariectomy was confirmed at necropsy by marked atrophy of the uterine horns and no histological evidence of ovarian tissue at the surgical site. The substantial atrophy of the uterus horns confirmed the reduction of serum estrogen levels in the ovariectomized animals (Ismail et al. 1988). The left mandibles were collected, and then fixed in 10% formalin for 24 hours.

Peripheral quantitative computed tomography Measurement was carried out with a specially modified XCT Research SA+ pQCT device (Stratec, Pforzheim, Germany) using a third generation rotatetranslate computed tomographic technique with a fan beam. Measurements were acquired while the specimen was immersed in saline, in a tube with an internal diameter of 28 mm, and held in place by a gum plug. A lowresolution scout scan of the mandible was obtained. This contained very little anatomic detail but was sufficient to allow identification of the positions of the teeth. The front line of the first molar was then used as a reference line to allow positioning of further slices. Image sets of double slices perpendicular to the occlusal plane were obtained at 4.5 and 6.0 mm mesial to the reference line for measuring the edentulous bone (Fig. 1). Voxel dimensions were 0.2 mm×0.2 mm×0.5 mm. Voxels were therefore anisotropic, and because of the poor resolution perpendicular to the slice plane, coronal slices were acquired. Special Analysis Software version 5.40 supplied by the device manufacturer was used to draw in each slice.

Fig. 1. Radiograph of rabbit mandible. This illustrates the sites observed by pQCT in the mandible. [circled digit one] Reference line. [circled digit two] The site sampled at 4.5 mm distal from the reference line. [circled digit three] The site sampled at 6.0 mm distal from the reference line.

The total voxels of the mandibular edentulous bone in the slices were segmented into cortical and trabecular voxels. The cortical voxels were defined by the Separation mode 1 as exceeding the cortical threshold and the trabecular voxels by the Separation mode C3/P20 as not exceeding the trabecular threshold but exceeding the soft tissue threshold.

Statistical analysis Results were expressed as the mean ± the standard error of the mean (SE). The indices of

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pQCT measurements were compared by Fisher's PLSD analysis of variance between the Sham and Ovx groups. P values less than 0.05 were considered significant.

Results The coronal pQCT images of the mandibles are shown in Fig. 2 A-D.

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Fig. 2. The transverse pQCT images of the mandibles of ovariectomized rabbits obtained 6.0 mm distal from the reference line. A. The images at 4 weeks after sham surgery. B. The images at 4 weeks after ovariectomy. C. The images at 12 weeks after sham surgery. D. The images at 12 weeks after ovariectomy.

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Total BMD The pQCT measurements of total BMD are presented in Table 1. At 4 weeks after ovariectomy or sham-ovariectomy, there were no significant differences between the Sham and Ovx groups in the coronal image indices of 4.5 mm and 6.0 mm mesial to the front line of first molar. At 12 weeks after ovariectomy or sham-ovariectomy, there were significant decreases in total BMD in the Ovx group compared with those in the Sham group in both coronal image indices of 4.5 mm and 6.0 mm mesial to the front line of first molar.

Table 1. Total bone mineral density (BMD) (mg/cm3) of mandibles in rabbits

Trabecular BMD The pQCT measurements of trabecular BMD are presented in Table 2. There were no significant differences between the Sham and Ovx groups at 4 weeks after ovariectomy or shamovariectomy. In the Ovx group at 12 weeks after ovariectomy, trabecular BMD significantly decreased compared with those of the Sham group in both coronal image indices of 4.5 mm and 6.0 mm mesial to the front line of first molar.

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Table 2. Trabecular bone mineral density (BMD) (mg/cm3) of mandibles in rabbits

Cortical BMD The pQCT measurements of cortical BMD are presented in Table 3. At neither 4 nor 12 weeks after ovariectomy and sham-ovariectomy were there significant differences between the Sham and Ovx groups.

Table 3. Cortical bone mineral density (BMD) (mg/cm3) of mandibles in rabbits

Discussion DXA has previously been used to measure bone loss in ovariectomized rats (Griffin et al. 1993; Pastoureau et al. 1995) and it demonstrates sufficient precision to detect BMD changes. Both DXA and pQCT can be used to detect BMD changes in small animals. Although DXA can assess total BMD, pQCT is likely to be particularly valuable for the detection of the progression of diseases that may

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have differential effects in cortical and trabecular bone since trabecular bone is more metabolically active and cortical bone less so. A loss in BMD post-ovariectomy was found in the distal femur of rats by DXA measurement (Griffin et al. 1993). Either a reduction of total BMD in the proximal tibia (Sato et al. 1995) or decreases both in total BMD and trabecular BMD of the rat tibia and femur (Breen et al. 1996) were found in ovariectomized rats by using pQCT. In this study, pQCT has been performed on the mandibular edentulous bone of ovariectomized rabbits, demonstrating both total and trabecular bone loss. This study examined the effect of ovariectomy on bone loss in the mandibles of ovariectomized rabbits using pQCT. Significant decreases in total BMD and trabecular BMD but not cortical BMD were found in the mandibles of rabbits 12 weeks after ovariectomy. But the differences of all total, trabecular and cortical BMD between Ovx and Sham groups were not significant in the mandibles of rabbits 4 weeks after ovariectomy or sham-ovariectomy. The results of this study indicate that the loss of mineralized bone occurred after 4 weeks following ovariectomy and was significant at 12 weeks following ovariectomy in the mandibles of rabbits. Rabbits achieve skeletal maturity shortly after reaching complete sexual development, unlike other mammals such as the rat, mouse and guinea pig (Gilsanz et al. 1988). Other cited advantages of rabbits for studies such as ours include a shorter developmental period and faster bone turnover than bigger mammals such as primates (Gilsanz et al. 1988). The availability, ease and adaptability to experimental manipulation of the rabbit also make this animal a potentially appropriate animal model for the studies of osteoporosis and jaw bone loss. However, obtaining data on the mandibular trabecular bone is problematic because of the presence of teeth. In this study, extraction of the mandibular incisors and cutting of the maxillary incisors were employed to obtain a greater mandibular trabecular bone area for pQCT measurement and to limit dental influences. The results of this study suggest that the mandible with incisors extracted of ovariectomized rabbit is suitable for the study of oral and maxillofacial bone loss in association with ovarian function loss, especially for the study of oral trabecular bone loss. Data obtained from the mandible may directly represent more authentic information of jaw bone than those obtained outside jaw bone. The findings of this study indicate an association between ovarian function loss and mandibular bone loss especially in trabecular bone. This information would be of clinical value not only in the diagnosis and treatment of postmenopausal jaw bone loss, but also in the analysis of novel therapeutic agents for the treatment of postmenopausal jaw bone loss and in the planning and evaluation of dental implantation in postmenopausal patients. In summary, this study documents the total, trabecular and cortical BMD in mandibles of ovariectomized rabbits. The results of this study demonstrate the mineralized bone loss in the mandibles of ovariectomized rabbits, especially in the trabecular bone region. Acknowledgements: This study was supported in part by the Ministry of Education, Science, and Culture of Japan (Grant-in-Aid for Science Research, 11672006).

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Key words: mandible; bone density; osteopenia; ovariectomy; pQCT

Accession Number: 00001698-200112000-00008 Copyright (c) 2000-2006 Ovid Technologies, Inc. Version: rel10.2.2, SourceID 1.11354.1.251

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