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Effect of surgical sympathectomy on bone remodeling at rat incisor and molar root sockets.

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THE ANATOMICAL RECORD 219:32-38 (1987)
Effect of Surgical Sympathectomy on Bone
Remodeling at Rat Incisor and Molar Root Sockets
H.S. SANDHU, M.S. HERSKOVITS, AND I.J. SINGH
Division of Oral Biology, Faculty o f Dentistry, The University of Western Ontario, London,
Canada N6A 5 C l (H.S.S.); Department ofdnatomy, New York College of Osteopathic
Medicine, Old Westbury, Ny 11568 (M.S.
H.); Department of Anatomy, New York University
Dental Center, New York,NY 10010 (I.J.S.)
ABSTRACT
Sympathectomy was carried out in 4-week-old Sprague-Dawley rats
by unilateral surgical removal of the superior cervical ganglion. Sham-treated rats
served as controls. All rats were injected with tetracycline hydrochloride a t surgery
a s well as 36 h r prior to sacrifice. Rats were killed at 7, 14, or 21 days following
sympathectomy. Mandibular periosteal and endosteal surfaces were analyzed by
fluorochrome morphometry. Osteoclasts were identified by acid phosphatase staining, and incisor and molar root sockets were analyzed morphometrically. Following
sympathectomy, periosteal and endosteal apposition as well as the rate of mineralization were significantly lower. At the same time, a significant increase in the
number of osteoclasts per socket as well as in active and inactive bone resorption
surfaces was also seen. All parameters, however, returned to normal values 2-3
weeks after sympathectomy. The data provide the first direct quantitative evidence
that sympathetic neurons modulate bone resorption and bone remodeling in vivo.
The presence of adrenergic nerves in bone is well documented (Duncan and Shim, 1977), and several recent
studies have reported the effects of sympathetic denervation on skeletal tissues. Osteoblastic activity was decreased following sympathetic denervation (Singh et al.,
1981,1982; Herskovits and Singh, 1984).The changes in
osteogenesis following sympathectomy could possibly be
attributed to vascular changes andlor to the loss of direct
neurotrophic influences of adrenergic neurons on the
osteoblasts. However, there is little information on the
effects of denervation on the activity of osteoclasts during bone remodeling. The vascular abnormalities resulting from the reflex sympathetic dystrophy syndrome are
known to cause irregular bone remodeling (Basle et al.,
1983). Fell (1949) also noted a n increase in resorption
spaces in long bones of cats following lumbar sympathectomy. More recently, vasoactive peptides that stimulate osteoclastic activity in vitro (Hohmann et al., 1983)
have been shown to be sympathetic in origin (Hohmann
et al., 1986). Similar vasoactive peptides have also been
identified in human osteosarcoma cells (Hohmann and
Tashjian, 1984).These studies suggest that sympathetic
denervation may also influence the resorption component of bone remodeling. In the present investigation,
the rat mandible model described by Liu and Baylink
(1984) was used to study the effects of surgical sympathectomy on bone remodeling at the incisor socket and
the molar root socket.
MATERIALS AND METHODS
Four-week-old male Sprague-Dawley rats were used.
The left superior cervical ganglion was surgically removed under sodium pentobarbital anesthesia (5 mgl
100 gm b.wt.) in 15 rats. Another 15 rats served as sham0 1987 ALAN R. LISS. INC
treated controls in which all surgicai procedures were
accomplished, i.e. the superior cervical ganglion and the
sympathetic trunk were visualized but not cut. All rats
were injected with tetracycline hydrochloride (15 mg/kg
b.wt.) immediately following surgery and again 36 hr
prior to sacrifice. The presence of ptosis was considered
indicative of a successful sympathectomy. Five experimental and five control rats were killed at 7,14, and 21
days following surgery. At autopsy, left mandibles were
freed of soft tissue and fixed in 10%phosphate-buffered
formalin (pH 7.4). The mandibles were divided into a
medial block and a lateral block between the second and
third molars (Fig. 1).
Fluorescence Microscope Morphometry
The medial blocks were embedded in Spurr medium,
and 60-pm-thick sections were cut on a n Isornet@slowcutting machine and lapped down to sections 25 f 5 pm
thick on a Moruto lapping machine. These sections were
used to analyze the periosteal a s well as the endosteal
deposition of bone. Linear periosteal deposition, linear
endosteal deposition, and width of the second periosteal
and endosteal tetracycline labels were measured on a
semiautomatic lBM computer-based image analyzer. The
rates of periosteal and endosteal apposition (pmlday)
were derived by dividing the average distance between
the two tetracycline labels by the number of days between injections (Sandhu and Jande, 1982; Frost, 1983).
Baylink et al. (1970) have shown that tetracycline diffuses into bone that has attained up to 20% of its maximum mineral concentration. The time required to reach
Received July 10, 1986; accepted March 6, 1987.
33
BONE REMODELING FOLLOWING SYMPATHECTOMY
MEOIAL BLOCK
7 '
Y'Y
-Embedded in Spurr
-60pm section lapped down
to 2 5 p m
-Fluorochrome Morphometry
PERIOSTEAL APPOSITION
LATERAL 6?LOCK
-Decalcified in 5% Formic Acid
-Embedded according to Westen et 01. (1981)
-4pm sections lncuboted for Acid Phos.
histochemistry (Evans et al., 1979)
MOLAR SOCKET
INCISOR SOCKET
ENDOSTEAL APPOSITION
Rate of Initial
Mineralization
-Active Resorbing Surface
-Inactive Resorbing Surface
-Number of Osteoclasts/mm
-Number of Nuclei/Osteoclast
-Area of Osteoclast
Fig. 1 . Schematic of a rat mandible showing landmarks and measurements.
20% of maximum mineralization is determined by converting, by means of the apposition rate, the width of
the final tetracycline label to units of time. The maximum concentration divided by the time yields the initial
mineralization rate (% maximum/hr).
Histochemical Morphometry
The lateral blocks of mandibles were decalcified in 5%
formic acid containing 5% formalin. The bones were
embedded in a mixture of 2-hydroxyethyl methacrylate
(54.5%); methyl methacrylate (27.25%); 2-hydroxyethyl
acrylate (9.10%); propanol (9.10%); and BPO (1%). The
whole procedure was done at 0-4°C. This method is very
well suited for enzyme histochemistry of bone (Westen
et al., 1981). Sections 4 pm thick were stained for acid
phosphatase activity according to a method described by
Evans et al. (1979). Napthol AS-TFt phosphate was used
as substrate and hexazotized pararosaniline as a coupler
in 0.1 M acetate buffer (pH 5.5) at 37"C, with or without
10 mM tartrate, and counterstained with methyl green.
Osteoclasts were identified by the presence of tartrateresistant acid phosphatase. Since multinucleated cells
can appear mononuclear depending upon the plane of
the section (Thompson et al., 1975), number of nuclei
was not used as a criterion for osteoclastic identification.
All sections were cut perpendicularly to the long axis of
the incisor (Fig. 4a). The number of osteoclasts and osteoclast nuclei were counted separately in the incisor
socket and the third molar root socket. The inner perimeters of incisor socket and molar root were measured as
total length of these respective sockets (excluding the
marrow spaces). Morphometry was performed with a
semiautomatic image analysis system (Southern Micro
Instruments, Atlanta, Georgia): The images of bone sections were projected to a video screen and measurements
were made on a digitizing pad. The length of the incisor
socket did not differ significantly from animal to animal;
therefore, data were expressed as the number of osteoclasts per socket, whereas the osteoclast-lined bone surfaces and acid phosphatase-positive bone surfaces were
expressed in absolute millimeters. The length of the
molar root showed considerable variability. Therefore,
the distribution of osteoclasts was expressed as the num-
ber of cells per 1 mm of bone surface. The length of
osteoclast-lined bone surfaces was calculated as a percentage of the total bone length of the socket. A 2 0 ~
objective was used and the final magnification at the
video screen was 81x . The bone surfaces lined by osteoclasts were measured as active resorbing surfaces,
whereas acid phosphatase-positive bone surfaces devoid
of osteoclasts were termed inactive bone surfaces. The
area of osteoclasts was estimated from cell perimeter.
Data Analyses
Several sections per bone specimen were examined
and Student t tests were applied to means & standard
errors of the mean.
RESULTS
All sympathectomized animals but none of the sham
controls showed ptosis on the operated side. The average
body weight was not significantly different between control and sympathectomized rats a t any time during the
experiment.
Measures of Bone Formation
Figures 2 and 3 show the typical appearance of the
double-tetracycline labels in periosteal and endosteal
bone, respectively. Linear periosteal apposition, endosteal apposition, and the rate of initial mineralization of
periosteum and endosteum were significantly lower in
sympathectomized rats than in the controls 1week after
denervation (Table 1). However, 21 days after sympathectomy, periosteal and endosteal apposition as well a s
the rate of mineralization were not significantly different between the sympathectomized rats and the controls.
Measures of Bone Resorption
The typical appearance of the molar and incisor root
sockets is shown in Figures 4a and 4b, respectively. Acid
phosphatase-positive osteoclasts are seen in Figure 4c.
Following sympathectomy, the length of the bone surface of the incisor socket is not significantly altered a t
either 1 or 2 weeks following surgery (Table 2). The
osteoclastic parameters at days 7 and 14 after sympathectomy are presented in Tables 2 and 3 for the incisor
34
H.S. SANDHU, M.S. HERSKOVITS, AND I.J. SINGH
Fig. 4. a: A composite of the buccolingual section of rat mandible
showing the molar root socket (partly indicated by arrows) and the
incisor socket (indicated by triangles). The sections were stained for
acid phosphatase. x7. b: A part of the incisor socket showing enamel
Fig. 3.Endosteal surface of a mandible from a rat killed 1week after (E);periodontal ligament (PDL); osteoclasts (arrows); and bone (B). The
surgery. Tetracycline was administered at surgery and at 36 hr before section was stained for acid phosphatase and counterstained with
sacrifice. UV light, ~ 5 3 .
methyl green. ~ 5 3 c:. Higher magnification of areas in b, showing
acid phosphatase-positive osteoclasts (arrows) and bone (J3). x 340.
Fig. 2. Periosteal surface of a mandible from a rat killed 1week after
surgery. Tetracycline was administered at surgery and at 36 hr before
sacrifice. UV light, ~ 5 3 .
and molar socket, respectively. One week after sympathectomy, all measures of bone resorption-length of
bone occupied by osteoclasts (active resorbing surface);
inactive resorbing surface; number of osteoclasts per
incisor socket-were significantly higher in mandibles
of sympathectomized rats than in the controls (Table 2).
However, the number of nuclei per osteoclast as well as
the area of osteoclasts were significantly lower in sympathectomized rats (Table 2). Two weeks after sympathectomy, no differences in bone resorption in the incisor
socket were apparent between control and experimental
mandibles (Table 2).
At the molar root socket, the length of bone surface
was quite variable; therefore, the percentage of total
bone surface lined by osteoclasts was obtained. This
percentage of bone was not statistically different between the controls and the sympathectomized rats (Table 3). In sympathectomized rats, the number of
osteoclasts per 1 mm of bone surface was significantly
higher; however, the number of nuclei per osteoclast was
35
BONE REMODELING FOLLOWING SYMPATHECTOMY
TABLE 1. Bone formation in control and sympathectomized rats 1 week following
sympathectomy
Controls
Measurement
Linear periosteal
apposition (pdday)
Linear endosteal
apposition (pdday)
Rate of periosteal
mineralization
(% of maximumlhr)
Rate of endosteal
mineralization
(% of maximumihr)
Mean
Percentage
SEM
Sympathectomized
of
controls'
6.315 & 0.58
5.117 _+ 0.41
81.02
3.267 f 0.45
2.753 f 0.17
84.26
2.54 f 0.22
1.85 f 0.16
72.80
1.94 5 0.05
1.39 & 0.08
70.10
'Control and experimental values are significantly different (P
measurements on several tissue sections of five rats.
< 0.05). Each value is derived from
TABLE 2. Bone resorption parameters at the incisor socket following sympathectomy
1 Week after sympathectomy,
mean f SEM
Measurement
Bone length of incisor
socket (mdsection)
Length of bone occupied
by osteoclasts (mm)or active
resorbing surface
Length of inactive resorbing
surface reversal
lacunae (mm)
Number of osteoclasts/
incisor socket
Number of nuclei/osteoclast
Area of osteoclasts (mm2)
2 Weeks after sympathectomy,
Controls
Sympathectomized
3.48 f 2.08
3.58 f 0.17
NS
3.41
11.0 k 0.873
14.3 f 1.23
0.01
0.56 f 0.143
5.95 k 3.12
34.1 f 2.34
2.75 f 0.059
0.017 f 0.001
P1
Controls
mean SEM
Sympathectomized
P'
3.79 k 0.321
NS
13.0 f 4.45
14.5 f 2.95
NS
0.05
2.34
2.28 f 0.665
NS
45.4 f 4.74
0.01
38.0 f 12.0
46.0 f 8.16
NS
2.06 & 0.079
0.014 5 0.001
0.01
NS
2.52 f 0.11
0.017 5 0.001
2.95 f 0.14
0.014 & 0.001
0.01
NS
0.74
0.47
Each mean and its SEM is estimated from measurements on several tissue sections from five rats,
'Differences between experimental and control values were tested by Student's t statistic; NS = not significant.
significantly lower (Table 3). At 2 weeks after sympathectomy, the molar socket bone of control and experimental animals showed no differences (Table 3).
DISCUSSION
The present study clearly demonstrated a reduction in
periosteal bone apposition at the end of the first week
following sympathectomy. Three weeks after sympathectomy, these differences in bone apposition between
experimental and control animals were not apparent;
these findings support our earlier suggestions of a possible time-dependent compensatory mechanism (Singh
et al., 1982). The reversible nature of these effects after
only 21 days, however, is different from our earlier results of autoradiographic studies of osteoblastic activity
(Singh et al., 1981, 1982; Herskovits and Singh, 1984).
In those autoradiographic studies, osteoblastic activity
and bone formation did not reach normal levels until
about 90 days after sympathectomy. Possibly the tetracycline labeling technique used in the present study is
not sensitive to the small differences in cell activity that
can be assessed by autoradiography.
Bone apposition is a direct function of osteoblasts and
is dependent on a) the number of differentiated osteo-
blasts and b) the activity of osteoblasts. The possibility
remains that the number of differentiated osteoblasts
may also be affected by sympathectomy. The concomitant decrease in the rate of mineralization along with
the reduction in the rate of bone apposition is in accord
with the view that rate of mineralization may be controlled by osteoblasts (Baylink et al., 1970). Although it
was not clear whether the deficit was only sensory, or
both autonomic and sensory, denervation reportedly resulted in lower glycosaminoglycan (GAG) synthesis in
newts (Mescher and Munaim, 1986). It has also been
shown that the glycoproteins and GAGS are involved in
mineralization (Arsenault and Ottensmeyer, 1983). It is
possible, therefore, that the greater reduction in mineralization compared to that in bone apposition (71% of
controls vs. 81% of controls) noted in our data may be
due to denervation-related reduction in GAG levels.
It is also clear that, during the first week following
sympathectomy, there was an increase in bone resorption with a concomitant decrease in endosteal bone a p
position as well as periosteal and endosteal rates of
initial mineralization. These findings suggest the presence of sympathetic innervation of both periosteal and
endosteal bone surfaces. It is interesting that the nerve
36
H.S. SANDHU, M.S. HERSKOVITS, AND I.J. SINGH
TABLE 3. Bone resorption parameters at the molar root following sympathectomy
2 Weeks after sympathectomy,
mean f SEM
1Week after sympathectomy,
Measurement
% Bone length occupied
by osteoclasts
(active bone resorbing
surface)
Length of inactive resorbing
surface reversal
lacunae (mm)
Number of osteoclasts/mm
bone surface of molar
root socket
Number of nuclei/osteoclast
Area of osteoclasts (mm2)
Controls
19.38
2.7
0.11 k 0.042
9.10 k 1.06
3.13 k 0.110
0.018 k 0.001
mean f SEM
Sympathectomized
20.32
+_
1.10
0.519 k 0.494
11.6
* 2.14
2.53 f 0.159
0.019 k 0.002
P1
Controls
Sympathectomized
NS
12.0 f 3.78
11.8 5 2.47
NS
NS
1.04
1.14 f 0.425
NS
P1
* 0.51
0.05
19.65 f 6.32
22.71
0.01
2.97 k 0.134
0.017 k 0.001
2.95 & 0.118
0.019 k 0.001
NS
6.72
NS
NS
NS
Each mean and its SEM is estimated from measurements on several tissue sections from five rats.
'Differences between experimental and control values tested by Student's t statistic; NS = not significant.
processes in Haversian canals have been shown to terminate in the endosteum of the cranial marrow spaces
(Retzlaff et al., 1981). Some role of sympathetic neurons
in bone marrow cell dynamics and hemopoiesis has also
been shown (Webber et al., 1970; Miller and McCuskey,
1973).
Although Fell (1949) observed increased resorption
spaces in bones following sympathectomy, the present
investigation presents the first direct in vivo quantitative evidence that bone resorption was increased after
sympathetic denervation. The number of osteoclasts as
well as the total resorption surface was significantly
greater in the incisor socket of sympathectomized rats
than in the controls. The number of osteoclasts and their
activity are influenced by systemic factors such as parathyroid hormone, calcitonin, and vitamin D3 metabolite
1,25-(OH)2D3(Roberts, 1975; Thompson et al., 1975; Luben et al., 1976; Holtrop et al., 1979; Warshawsky et
a1.,1980; Liu et al., 1982; Chambers et al., 1985) Prostaglandins, Osteoclast Activating factor and Interleukin-I
are believed to be local regulators of the number and
activity of osteoclasts (Klein and Raisz, 1970; Tashjian
et al., 1973; Horton et al., 1974; Luben et al., 1977;
Holtrop and Raisz, 1979). Recently, some vasoactive peptides of sympathetic origin have been shown to modulate osteoclastic function (Hohmann et al., 1983, 1986).
It is possible that the sympathetic innervation acts
through modulation of parathyroid activity, thus accounting for a time-dependent compensatory mechanism in the bone changes.
Osteoclasts are not known to divide; however, it is
believed that new nuclei from monocytic fusion can be
added to osteoclasts under systemic stimuli (Jaworski et
al., 1981; Scheven et al., 1986). Our investigation showed
a significant decrease in the number of nuclei per osteoclast following sympathectomy, possibly reflecting a reduced systemic need for bone resorption.
Increased pO2, resulting from sympathectomy, is
known to cause inhibition of osteoblastic activity, of
growth of epiphyseal plate, and of cartilage calcification
(Brighton et al., 1969; Brighton and Heppenstall, 1971;
Brooks, 1972). The effects of increased pO2 on bone resorption, however, are controversial. A decrease in bone
resorption under hyperoxic tissue culture conditions has
been reported (Gray and Hamblen, 1976); other investi-
gators believe that pO2 has no effect on bone resorption
(Asher and Sledge, 1968; Melcher and Hodge, 1968).An
increase in bone resorption following sympathectomy in
cats (Fell, 1949) and following a n increase in pO2 has
also been reported (Goldhaber, 1966; Gray et al., 1978,
1980).
The reversible nature of the effects of sympathectomy
points towards transient vascular changes as the cause.
However, no changes in blood flow could be detected
following lumbar sympathectomy (Hohmann et al.,
1986). Furthermore, one cannot overlook the possibility
of indirect sympathetic influences on bone cell compartments as the surgical removal of a single superior cervical ganglion unilaterally certainly does not destroy
the whole adrenergic system, which may compensate for
the local deficit caused by the ganglionectomy. Pharmaceutical sympathectomy, which would destroy all of the
sympathetic system, has been shown to result in a n
inhibition of osteogenesis (Singh et al., 1981, 1982; Herskovits and Singh, 1984); however, the effects on bone
resorption parameters were not investigated in those
studies. It has also been reported that the periodontal
fibroblasts and the odontoblasts of the rat incisor do not
respond to a pharmaceutical sympathectomy (Klein et
al., 1981; Herskovits and Singh, 19861, whereas surgical
sympathectomy resulted in a delay in the proliferative
response of dental pulpal cells to trauma (Chiego et al.,
1986). It is not at all clear whether the sympathetic
modulation of bone remodeling is directly locally mediated or if it is the result of systemic effects.
A differential, function-dependent response to systemic perturbations has been shown in trabecular bone
in a series of excellent reports (Frost, 1973a,b, 1983) as
well as in alveolar bone (Saffar and Baron, 1977; Vignery and Baron, 1978, 1980; Liu and Baylink, 1984).
Our study showed that even sites with similar functions
(incisor socket and molar socket) may respond differently to systemic or local stimuli. The higher response
of osteoclasts at the incisor socket compared to the molar
socket could be attributed to a more rapid remodeling of
bone at the continually erupting incisor.
It appears reasonable to assume that the osteoclasts
were present on the acid phosphatase-positive bone surfaces sometime prior to the sacrifice of the rats. An
experiment with several shorter observation periods
BONE REMODELING FOLLOWING SYMPATHECTOMY
(hours rather than days) would be needed to further
elucidate the role of adrenergic neurons in the spatial
dynamics of osteoclasts, as well as the sequence of events
following surgical sympathectomy that lead to increased
bone resorption. Of particular interest would be the regulation of osteoclastic movement and the role of vasoactive peptides in the modulation of osteoclastic function.
ACKNOWLEDGMENTS
This research was supported by a grant from Ontario
Ministry of Health (H.S.) and grant RR 05332 to New
York University (I.J.S.).We thank Mrs. Linda Monteith
and Mr. Stephen Waldrup for skillful secretarial assistance and Mr. Lynden Keeping for his technical help.
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effect, socket, molar, surgical, remodeling, rat, incisors, sympathectomy, roots, bones
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