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Journal of Oral Rehabilitation 2000 27; 587–594

The effect of oestrogen deficiency on the alveolar bone

resorption caused by traumatic occlusion
S. KAWAMOTO & E. NAGAOKA Second Department of Prosthetic Dentistry, Kagoshima University Dental School,
Kagoshima City, Japan

SUMMARY This study, using 132 female rats, was mandibles were processed without decalcification,
designed to investigate whether oestrogen loss fa- and histomorphometric measurements were per-
cilitates alveolar bone alterations induced by trau- formed in the alveolar bone adjacent to the peri-
matic occlusion. Rats were ovariectomized (OVX) odontal ligament of the first molar. The statistical
or underwent sham-operation (Sham). Seven days assessment of the time- and group-specific differ-
after surgery, half of the rats in each group were ences by analysis of variance revealed significant
subjected to experimental traumatic occlusion differences between the OVX +trauma and
(trauma), and the other half were left untreated. Sham+ trauma groups in the resorption parame-
Thus, there were four groups: OVX + trauma, ters, but not in the formation parameters. The re-
Sham+ trauma, OVX, and Sham. Rats in each sults show that the alveolar bone dynamics induced
group were killed 1, 3, 5, 7, or 10 days after the by traumatic occlusion are enhanced by oestrogen
introduction of occlusal trauma. The resected deficiency.

Introduction the dynamics of alveolar bone in response to various

The integrity of the tissues supporting the teeth is Much information is available concerning the effects
essential for proper mastication. Periodontal diseases, of systemic agents on skeletal bone metabolism, partic-
although initiated mainly by bacterial irritants, are also ularly with respect to the status of osteoporosis. In
fostered by other factors, including abnormal mechani- human post-menopausal subjects, ovarian hormone
cal stress. The first description of trauma from occlu- deficiency gives rise to an imbalance of calcium
sion, by Karolyi (1901), was followed by numerous homeostasis leading to osteopenia (Heaney, Recker &
investigations. In animal studies, the possible role of Saville, 1978), and the same is true in an ovariec-
excessive biting forces in the pathogenesis of periodon- tomized rat model of oestrogen deficiency (Kalu,
tal disease was clarified (Glickman & Smulow, 1965; Hardin & Cockerham, 1984). For further characteriza-
Kenney, 1971; Lindhe & Svanberg, 1974). Addition- tion of the aetiologic mechanism of oestrogen defi-
ally, it has been reported that the clinical signs of ciency-induced osteoporosis, quantitative analyses
occlusal trauma are related to the severity of periodon- using bone histomorphometry have been extensively
titis (Pihlstrom et al., 1986; Jin & Cao, 1992). The performed (Wronski et al., 1985; Turner, Evans & Wak-
impairment of osseous support by extended periodon- ley, 1993; Dempster et al., 1995; Yamaura et al., 1996).
tal diseases is not readily restored and complicates These studies established that oestrogen deprivation
efforts to preserve the natural tooth. With continued induces net loss of bone volume due to increased bone
advances in effective procedures for periodontal disease resorption and inadequate compensation by bone for-
prevention and treatment with preservation of the mation. The effects of generalized skeletal osteopenia
supporting bone, it is increasingly important to identify on the jaw bones have been the focus of increased

© 2000 Blackwell Science Ltd 587


interest in dentistry. Several studies suggested an effect sacrifice. Four to seven rodents in each group were
of oestrogen loss on oral bones in human subjects killed with an overdose of sodium pentobarbital at
(Wowern & Stoltze, 1979; Wowern, 1981; Kribbs, each of 1, 3, 5, 7, and 10 days after the introduction of
1983; Nishimura, Hosokawa & Atwood, 1992), but the traumatic occlusion. In addition to these rats, as
there have been only a few detailed analyses using baseline controls, five rats in each of groups 3 and 4
animal models (Miller et al., 1991; Elovic, Hipp & were killed on the day of introduction of occlusal
Hayes, 1995). trauma (on day 0). Blood samples were collected by
We hypothesized that the sensitivity of the alveolar cardiac puncture immediately after death.
bone tissue to local factors is modified by systemic For confirmation of successful ovariectomy, the
regulators of bone mineral metabolism. In the present serum level of estradiol (E2) was measured using a
study, our objective was to examine whether oestrogen radioimmunoassay.
loss enhances the alveolar bone changes generated by
abnormal occlusal force.

Materials and methods The mandible was removed and bisected at the midline
suture. The left half was processed without decalcifica-
Female Wistar rats, aged 43 weeks, were purchased tion for quantitative analysis of bone histomorphomet-
from Kyudo Inc.* for this study. The animal use proto- ric parameters. Samples were fixed with 10% formalin
col was reviewed and approved by the Animal Experi- in phosphate buffer, then dehydrated by immersion in
ment Committee, Kagoshima University Dental School. a graded series of ethanol solutions and defatted in
During the experimental period, the rats were kept at acetone for 3 days each. The specimens were infiltrated
22 °C with a 12 h/12 h light – dark cycle and received with the embedding medium¶. The embedded samples
20 g per day of a commercially available standard diet were sliced in the bucco-lingual direction at the first
containing 1·19% calcium, 1·13% phosphorus, and 40 molar and ground to 25-mm thickness with a cutting
IU of vitamin D3. They were given tap water ad libitum. and grinding system**. The prepared sections including
After acclimatization for 1 week, they were divided the apex of the mid-mesial root of the first molar were
randomly into four treatment groups with/without the first observed with fluorescence microscopy, and then
experimental traumatic occlusion introduced 7 days af- stained with methylene blue and basic fuchsin for light
ter ovariectomy (OVX) or sham surgery (Sham), as microscopy.
follows: group 1 (OVX +trauma), group 2 (Sham + Histomorphometric measurements were performed
trauma), group 3 (OVX) and group 4 (Sham). At the on the alveolar bone surface adjacent to the periodon-
surgery, each rat was anaesthetized with an i.p. injec- tal ligament (PDL). The microscopic images generated
tion of sodium pentobarbital at 62·5 mg/kg. The bilat- by Nikon OPTIPHOTO and BIOPHOTO were displayed
eral ovariectomy in groups 1 and 3, and the sham on a colour monitor through a TV camera, and all
surgery in the other two groups, were performed via parameters were quantified using semiautomatic image
the dorsal approach. Additionally, experimental trau- analysis software†† on an NEC personal computer (PC-
matic occlusion was applied in groups 1 and 2: metal 9801DX). The perimeter measurements were obtained
was bonded to the occlusal surface of the maxillary left in rectangular fields, at magnification of 340 ×, in
molars with dental adhesive material† to produce trau- sequence from the buccal crest to the lingual crest
matic occlusion at 7 days after surgery. To confine the along the alveolar wall, as illustrated in Fig. 1. Accord-
vertical dimensions, all metal was trimmed to 1-mm ing to the method standardized by Parfitt et al. (1987),
thickness before bonding. Groups 3 and 4 served as the mineralized surface (MS) and mineral apposition
non-trauma control groups. All rats were injected in- rate (MAR), derived from the fluorescence, were em-
traperitonially with Calcein‡ and tetracycline hy- ployed as kinetic parameters. The osteoclast surface
drochloride§ 3 days and 1 day, respectively, prior to (Oc.S), eroded surface (ES), and osteoid surface (OS),
* Kumamoto, Japan. ¶
Rigolac, Oken-shoji, Tokyo, Japan.

Super Bond C&B, Sun Medical Co., Japan.
** Exact BS3000 and MG4000, Exact, Germany.

Nacalai Tesque Inc., Kyoto, Japan. ††
COSMOZONE 1S, Nikon, Japan.
Achromycin; Lederle Ltd., Tokyo, Japan.

© 2000 Blackwell Science Ltd, Journal of Oral Rehabilitation 27; 587–594


as static parameters, were measured and expressed as The E2 levels remained lower in the OVX groups than
percentages of the measured bone surface (BS) on in the Sham groups throughout the experimental
stained sections. period.

Statistical analysis Histomorphometry

The values of serum E2 were evaluated by the Mann– Figure 2 shows the alterations in the static parameters
Whitney U-test. Data obtained from bone histo- of the histomorphometry after introduction of occlusal
morphometry are reported as the mean value and trauma, Table 1 the values of the histomorphometric
standard error of measurement for each group. For parameters at each time point, and Table 2 the results
assessment of the group-specific differences, all values of the tests of significance of differences at each time
obtained were evaluated statistically using analysis of point and of group-specific differences tested by ANOVA.
variance (ANOVA), followed by comparison of the val-
ues at each time point by the Mann – Whitney U-test. A
Static parameters
P value of less than 0·05 was considered to indicate a
significant difference. Analyses were performed with a In the non-trauma groups (groups 3 and 4), moderate
STATVIEW 4.02J program on a Macintosh computer. sequential changes in each parameter were seen during
the experimental period, although there were no sig-
nificant difference between these two groups.
Results In both the trauma groups (groups 1 and 2), in
contrast, time-dependent changes of each parameter
E2 assay were clearly demonstrated. ES/BS and Oc.S/BS, as re-
sorption parameters, showed transient increase and
No time-specific differences of the serum E2 level after
then gradual decrease to the baseline level. Oc.S/BS
surgery were detected in any of the four groups. The
reached a peak on day 1 of traumatic occlusion and
values obtained at each time point in the OVX groups
then decreased gradually. The values of Oc.S/BS on
(groups 1 and 3) were therefore summed and com-
day 1 in groups 1 and 2 were increased to 431 and
pared with those in the Sham groups (groups 2 and 4).
347% of those of the baseline controls, respectively.
In these two pairs of groups, the mean serum E2 levels
ES/BS increased and remained elevated until day 7,
were 1·418 and 6·987 pg/mL, respectively (PB0·05).
then declined to the baseline. The ES/BS values on
days 1–7 in groups 1 and 2 ranged from 189 to 244%
and from 121 to 164% of those of the baseline con-
trols, respectively. On the other hand, OS/BS, as a
formation parameter, decreased transiently during the
period. The minimum values of OS/BS relative to the
baseline controls were 60% in group 1 and 35% in
group 2. The changes of each parameter in group 1
were generally similar to those in group 2. Significant
differences between the two groups were detected for
Oc.S/BS, but not for other indices (ANOVA).
Statistical comparison of groups 2 and 4 revealed
significant differences between them for Oc.S/BS, ES/
BS and OS/BS.

Kinetic parameters
Fig. 1. Schematic drawing of measured areas on a bucco-lingual
section at the mid-mesial root of the first molar. Each rectangular The values of MS were depressed transiently in the
measured field is 0·45 mm2. trauma groups (groups 1 and 2), but not in the non-

© 2000 Blackwell Science Ltd, Journal of Oral Rehabilitation 27; 587 – 594

trauma groups (groups 3 and 4). ANOVA revealed a

significant difference between MS in the non-trauma
groups, but not in the trauma groups. No significant
changes of MAR were seen during the experimental
period in any group.

Oestrogen deficiency, manifested as a generalized
skeletal osteopenia, was noted in the OVX groups
(groups 1 and 3) within 7 days after surgery. This
finding is consistent with the data reported by Ismail et
al. (1988), and it provided confirmation that the circu-
lating levels of oestrogen were already reduced before
the introduction of experimental occlusal trauma in
the OVX group.
For the examination of the influence of occlusion
status on tooth-supporting tissue, experimental studies
in animals have been extensively performed. In some
studies, experimental traumatic occlusion was simu-
lated by raising the vertical dimension of occlusion
(Bhaskar & Orban, 1955; Wentz, Jarabak & Orban,
1957; Safavi et al., 1974; Jorgensen, 1980). The de-
struction of the alveolar bone proper by traumatic
occlusion was assessed by radiographic or histologic
methods. However, there have been no quantitative
analyses of occlusal trauma in bone tissues. King, Keel-
ing & Wronski (1991) employed histomorphometry to
demonstrate the time course of changes in alveolar
bone induced by orthodontic tooth movement. We also
designed the present study to quantify histomorpho-
metrically the bone changes caused by traumatic occlu-
sion. Moreover, we examined whether the alterations
were intensified by systemic and metabolic factors.
Previous studies have demonstrated that the alveolar
bone adjacent to the PDL undergoes a remodelling
sequence. In the rat, it was confirmed that the molar
teeth migrate spontaneously, corresponding to bone
modelling and remodelling in the tooth socket (Baron,
1973). Using dynamic histomorphometric methods, Vi-
gnery & Baron (1980) demonstrated coordinated activ-
ities of bone formation and resorption in the tooth
socket during molar drift. In our study, similarly, both
Fig. 2. Alterations of the static parameters. (A) Osteoclast surface bone formation and resorption activities were noted in
(Oc.S/BS). Significant differences were found between groups 1
the tooth sockets of untreated rats.
and 2, 1 and 3, and 2 and 4 (by ANOVA). (B) Eroded surface
(ES/BS). Significant differences were found between groups 1
In the present study, sequential changes of bone
and 3, and 2 and 4 (by ANOVA). (C) Osteoid surface (OS/BS). No resorption and formation were identified after the ap-
significant differences were detected. plication of experimental traumatic occlusion. It has

© 2000 Blackwell Science Ltd, Journal of Oral Rehabilitation 27; 587–594


Table 1. Histomorphometric parameters before and after introduction of traumatic occlusion

Day 1. OVX+trauma 2. Sham+trauma 3. OVX 4. Sham

Oc.S/BS (%) 0 – – 1·560 (1·127)† 1·260 (0·287)‡

1 6·124 (1·449) 4·374 (1·020) 1·685 (0·600) 1·054 (0·402)
3 5·354 (1·049) 2·900 (0·889) 1·668 (0·714) 1·412 (0·425)
5 4·441 (1·228) 1·947 (0·672) 1·596 (0·251) 0·853 (0·299)
7 3·571 (0·668) 1·583 (0·368) 1·996 (0·689) 0·664 (0·114)
10 1·116 (0·593) 2·120 (0·858) 1·120 (0·716) 0·580 (0·089)

ES/BS (%) 0 – – 12·132 (4·228)† 16·434 (3·556)‡

1 23·841 (3·849) 23·968 (4·799) 7·567 (2·625) 7·812 (0·844)
3 29·634 (2·311) 19·993 (1·602) 14·621 (3·789) 13·614 (2·633)
5 22·933 (0·463) 26·983 (5·088) 11·968 (2·174) 11·402 (1·147)
7 24·627 (2·569) 23·798 (4·583) 13·647 (2·581) 12·079 (1·964)
10 12·453 (2·825) 16·740 (2·617) 13·846 (4·751) 9·534 (2·977)
OS/BS(%) 0 – – 14·574 (7·495)† 16·801 (4·455)‡
1 12·552 (1·850) 6·025 (4·249) 17·895 (4·922) 13·692 (5·993)
3 8·783 (2·667) 6·522 (1·940) 10·622 (6·765) 16·318 (2·952)
5 17·673 (2·447) 11·587 (3·307) 15·811 (2·542) 17·861 (1·629)
7 12·400 (1·796) 11·105 (3·651) 17·139 (7·302) 17·885 (2·351
10 15·378 (4·267) 17·760 (4·223) 13·372 (6·263) 12·815 (2·545)
MS (%) 0 – – 5·128 (1·022)† 4·046 (0·441)‡
1 * * 5·389 (0·577) 3·640 (0·378)
3 5375 (1·230) 5·098 (1·232) 5·468 (0·519) 3·913 (1·435)
5 3·605 (0·939) 3·095 (1·133) 5·119 (0·729) 3·380 (0·635)
7 4·081 (1·139) 3·488 (0·631) 5·793 (1·106) 3·860 (0·777)
10 6·278 (1·774) 3·547 (1·152) 5·515 (0·491) 3·530 (0·060)
MAR (mm/day) 0 – – 8·021 (0·240)† 8·152 (0·474)‡
1 * * 8·467 (0·297) 8·094 (0·199)
3 8·776 (0·196) 8·034 (0·444) 8·249 (0·311) 8·210 (0·208)
5 8·709 (0·196) 8·648 (0·324) 8·324 (0·327) 8·181 (0·289)
7 8·533 (0·817) 8·458 (0·224) 8·884 (0·126) 8·147 (0·055)
10 8·026 (0·029) 8·158 (0·543) 8·247 (0·350) 8·320 (0·090)

The measured value of each parameter is expressed as the mean and standard error for the mean (in parentheses). Four to seven rats
were killed per timepoint in each group.
* Not determined; † baseline control of the OVX groups (groups 1 and 3); ‡ baseline control of the Sham groups (groups 2 and 4); –,
not applicable.

been reported that transient accelerated resorption and ported to be 26 mm/day for molars (Ohshima et al.,
suppressed formation parallel to the bone dynamics 1991), and 750 mm/day for incisors (McKee & War-
were found at pressure sites in orthodontically-treated shawsky, 1984).
rats (King et al., 1991). In that study, persistent force Regarding the formation activities, the transient re-
produced by an orthodontical appliance brought about duction of OS/BS reported here was similar to that in
a sequence of cellular activities resulting in enhanced orthodontically pressed sites. The values of OS/BS re-
resorption and suppressed formation at pressure sites, turned to the baseline on day 10 after the application
and the curves for both resorption and formation were of traumatic occlusion. Bridges, King & Mohammed
attenuated as a result of the tooth relocation. We (1988) reported that the bone density lost due to tooth
observed findings similar to these in our study, even movement was recovered within about 2 weeks in
though the mechanical stress was applied in a different adult rats. In our study, it remained unclear whether
manner. It is probable that the intermittent depressive bone formation was elevated in response to the bone
stress produced by traumatic occlusion is weakened by loss and whether the bone loss was restored.
intrusion of the tooth and/or elongation of the con- The kinetic indices, MS and MAR, did not show
tralateral molars. The degree of elongation was re- significant differences in the trauma groups. The values

© 2000 Blackwell Science Ltd, Journal of Oral Rehabilitation 27; 587 – 594

Table 2. Differences (P values) between the groups before and after introduction of traumatic occlusion (by the
Mann–Whitney U-test)

Day Groups 1–2 Groups 1–3 Groups 1–4 Groups 2–3 Groups 2–4 Groups 3–4

Oc.S/BS (%) 0 – – – – – NS
1 NS NS B0·05 NS B0·05 NS
3 NS B0·05 B0·05 NS NS NS
5 NS NS B0·05 NS NS NS
7 B0·05 NS B0·05 NS NS NS

ANOVA† B0·05 B0·05 * * B0·05 NS

ES/BS (%) 0 – – – – – NS
1 NS B0·05 B0·05 B0·05 B0·05 NS
3 B0·05 B0·05 B0·05 NS B0·05 NS
5 NS B0·05 B0·05 NS B0·05 NS
7 NS B0·05 B0·05 NS NS NS

ANOVA† NS B0·05 * * B0·05 NS

OS/BS (%) 0 – – – – – NS
3 NS NS NS NS B0·05 NS

ANOVA† NS NS * * B0·05 NS
MS (%) 0 – – – – – NS
1 * * * * B 0·05

ANOVA† NS NS * * NS B0·05
MAR (mm/day) 0 – – – – – NS
1 * * * * * NS
3 NS NS B0·05 NS NS NS
7 NS NS NS NS NS B0·05
10 NS NS B0·05 NS NS NS


* Not determined; NS, not significant; –, not applicable.

Group-specific differences tested by ANOVA.

of MS indicate the accumulation of surface mineralized In this study, we examined whether systemic agents
during the last 3 days prior to sacrifice. We speculate acted synergistically on the alterations of bone kinetics
that the measured sites were subjected to irregular produced by local factors. Several investigations have
pressure and tension induced by jiggling force, and that demonstrated, during molar tooth drifting, the effects
therefore the effect of oestrogen loss, observed in the on bone turnover of metabolic and hormonal factors,
non-trauma groups, was masked. No significant differ- such as bisphosphonate (Hardt, 1988), prostaglandins
ences of MAR were detected among the four groups. (Lasfargues & Saffer, 1992), 1,25(OH)2D3 (Takano-Ya-
This result is consistent with the observation made by mamoto, Kawakami & Yamashiro, 1992), and parathy-
Yamaura et al. (1996) that the mineralizing function of roid extracts (Roberts, 1975). However, in our study in
osteoblasts is not facilitated by OVX. bucco-lingual sections, OVX alone produced no signifi-

© 2000 Blackwell Science Ltd, Journal of Oral Rehabilitation 27; 587–594


cant alteration of bone kinetics compared with sham BRIDGES, T., KING, G. & MOHAMMED, A. (1988) The effect of age
operation. A possible reason for this discrepancy is the on tooth movement and mineral density in the alveolar tissues
of the rat. American Journal of Orthodontics, 93, 245.
difference in the measured surfaces of sections. The
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It is well known that surgical termination of the Journal of Periodontology, 36, 141.
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