Electric currents, bone remodeling, and

orthodontic tooth movement

II. Increase in rate of tooth movement and
periodontal cyclic nucleotide levels by combined
force and electric current

Zeev Davidovitch, DAD., Mathew D. Finkelson, B.S.,

Shulamit Steigman, D.M.D., Joseph L. Shanfeld, Ph.D.,
Paul C. Montgomery, Ph.D., and Edward Korostoff, Ph.D.
Philadelphia, Pa.

Piezoelectric currents in mechanically stressed bone were implicated in the activation

of bone cells. The objectives of this experiment were to determine the usefulness of
exogenous electric currents in accelerating orthodontic tooth movement and to study
the effect of electric-orthodontic treatment on periodontal cyclic nucleotides. Maxillary
canines were tipped in five cats by 80 g force. Two groups of five cats each were
treated by an electric-orthodontic procedure to one maxillary canine for 7 and 14
days, respectively. Teeth treated by force and electricity moved significantly faster than
those treated by force alone. Enhanced bone resorption was observed near the anode
(PDL compression site), while bone formation was pronounced near the cathode (PDL
tension site). Staining for cyclic nucleotides was increased when electric stimulation
was added to the mechanical force. These results suggest that orthodontic tooth
movement may be accelerated by the use of locally applied electric currents.

From the Departments of OrthodonticsIPedodontics, Restorative Dentistry, and Pharmacology and

Microbiology, University of Pennsylvania School of Dental Medicine
This study was supported by National Institute of Dental Research Grant DE-03619.

ooO2-9416/80/010033+15$01.50/0 0 1980 The C. V. Mosby CO 33

 Mechanical forces are used to move teeth to new posittons in the jaws bccau~ ot their
ability to evoke local cellular responses in the periodontal ligament (PDL,) and alveolai~
bone’-” and because of the directional guidance they provide the moving teeth. The
mechanism involved in the activation of bone and PDL cells by mechanical forces is not
well understood, but there is evidence to support the possibility that electric currents are
generated within the stressed tissues’ G and that these current:, may charge macromol-
ecules that interact with specific sites in cell membranes’ or mobilize ions across ceil
membranes.X This “piezoelectric” phenomenon was observed to occur in mechanically
stressed alveolar bone in vitro” and in viva. li’
Exogenous electric currents have been employed in the last two decades. both experi-
mentally and clinically, in successful attempts to initiate osteogenesis in intact bones”. !”
or to enhance bone apposition in healing of uncomplicated’:‘, !-I or nonunion’“, Ifi fractures.
In spite of this encouraging clinical evidence. little is known about the mechanism which
produces the tissue changes seen after the application of electricity. Lavine and associ-
ates” reported that cells in bone fracture sites treated by constant D.C. currents presented
an increased number of membrane-bound vesicles, morphologic transition of rough en-
doplasmic reticulum to ribosome-lined cisternae, and vacuolization of the mitochondria.
Rodan, Bourret, and Norton’X reported that the application of oscillating electric tields to
chick chondrocytes in vitro resulted in enhancement of the incorporation of :‘H-thymidine
into DNA. It was suggested that Na’ and Ca” fluxes were responsible for this effect.
Brighton and Friedenberg’” observed alterations in oxygen consumption and tissue pH
near the cathode. The role of cyclic nucleotides in the mechanism of cell activation by
external electric currents in vivo was investigated by us earlier.2”--2Z Cyclic nucleotides
were selected as the main target of that investigation because of their implication as
intracellular “second messengers” in the action of specific bone cell activators, such as
parathyroid hormone and calcitonin,“:’ yr, on their target cells. By using immu-
nohistochemical techniques, we discovered that external electric currents increased bone
and PDL cyclic nucleotide contents.“‘; a step leading toward heightened enzymatic phos-
phorylation reactions, synthetic and secretory activities, and an enhanced rate of tissue
remodeling. Earlier”, 2Xwe studied the involvement of adenosine 3’.5’-monophosphate
(cyclic AMP. CAMP) in the periodontal tissue response to orthodontic treatment and
concluded that mechanical forces might not be the most efficient means to activate PDL
and alveolar bone cells. That conclusion, coupled with the recent observation that electric
current can activate a large number of cells in a small, well-delineated area,‘)’ led us to
hypothesize that the application of electric currents to periodontal tissues during orth-
odontic treatment will potentiate the effect of the mechanical forces and lead to an
enhanced rate of cell activation, tissue remodeling, and tooth movement.
The objectives of this study were (1) to examine the usefulness of electric currents as a
means to accelerate orthodontic tooth movement in cats and (3) to study the effect of a
combined electric-orthodontic treatment on the cyclic nucleotide profile and tissue turn-
over pattern of cat alveolar bone and PDL.

Methods and materials

Fifteen female cats, 10 to 12 months old, were the experimental animals. At this age
the development of their permanent dentition is complete, a stage comparable to late
adolescence in human beings. In each cat both maxillary canines were tipped by a method
described in detail elsewhere. 27 One end of a coil spring was attached to the canine, and
Volume 77
Number 1
Effect of electric currettts 35

Fig. 1. Occlusal view of the palate of a cat from Group A with coil springs stretched between the canines
and the third premolars. The coil springs (Unitek, 0.008 by 0.036 inch closed-coil) are secured to each
tooth by steel ligatures tied around retentive grooves cut into each of the four teeth. The generated
forces (80 Gm. at time of insertion) tip the canines distally. Photograph taken at the time of insertion.
Fig. 2. Occlusal view of the palate of a cat from Group C, treated by a combined force-electric
approach. The coil springs are applied as in Group A (Fig. 1). In addition, an electric device is placed,
delivering a constant D.C. current of 15 microamperes. The active electrodes are positioned mesial
(cathode) and distal (anode) to the left canine. The right canine receives sham electrodes. A detailed
description of the electric device is found in the preceding article. 26 Photograph taken at the time of
insertion.

the other end to the third premolar on the same side of the dental arch. In this manner 80
Gm. of force was generated, tipping the canine distally (Fig. 1). This force magnitude
may be considered light to medium in view of the relatively large size of the cat canine. In
addition to these coil springs, ten of the cats received maxillary electric devices (Fig. 2),
which delivered a constant D.C. current, 15 microamperes, to the periodontal tissues of
one randomly selected canine. The other canine received sham electrodes. A detailed
description of the electric device is found in our previous article.z6
The animals of Group A (five cats, mechanical force only) were treated for 14 days
and were not killed. The objective in treating this group was to compare the rate of canine
tipping at the two sides of the dental arch. There was no need to examine the tissues of
these cats, (1) because we have already reported the effect of orthodontic forces on
Fig. 3. Labial view of the maxillary dentition of a Group A cat (treated by force only). The dimensions
measured in the mouth to detect canine tipping are canine to third incisors la) and canine to second
premolar (b). Both dimensions are measured at the crown-gingival junction.
Fig. 4. Occlusal view of the anterior segment of the palate of a Group C cat (same as in Fig. 2) after 14
days of combined force-electric treatment to the left canine. Note that this canine has been tipped
distally appreciably more than the contralateral tooth, which was treated by force only.

periodontal cyclic nucleotides and (2) because in each of the electrically treated cats one
canine was treated by force only and thus served as the control for the contralateral tooth,
which was treated by a combined electric-orthodontic procedure. The animals of Group B
(five cats, simultaneous electric and force treatment) were killed after 7 days of treatment.
The animals of Group C (five cats, simultaneous electric and force treatment) were killed
after 14 days of treatment.
Measurements of canine movement were recorded by the same investigator on days
0,7, and 14 with Vernier calipers, accurate to 0.02 mm. Two dimensions were measured
directly in the mouth: (1) the distance between the mesial-gingival aspect of the canine and
the distal-gingival aspect of the third incisor and (2) the distance between the distal-
gingival aspect of the canine and the mesial-gingival aspect of the second premolar (Fig.
3). To avoid influence of possible mesial movement of the maxillary premolars (anchor
units) on the incisors by the acrylic plate, the acrylic was trimmed away from the lingual
aspect of the incisors.
Volume 71
Number 1 Effect of electric currents 37

Table I. Effect of mechanical forces with or without electric currents

on the rate of cat canine tipping
Amount of tooth movement*
Duration
Type of treatment (days) Canine to third incisor Canine to second premolar

Force only 7 0.25 t 0.06 0.30 + 0.06

Force + electricity 7 0.62 k 0.05t 0.70 f 0.1ot
Force only 14 0.15 2 0.03 0.08 2 0.03
Force + electricity 14 0.32 ‘- 0.03t 0.30 k 0.06t

*In mm. 2 S.E.M.

tp < 0.01

After the animals were killed, the maxillas of Groups B and C cats were processed for
immunohistochemical examination as described in the preceding article.*‘j Horizontal
serial sections, 5 microns thick, were stained for CAMP and guanosine 3’,5’monophos-
phate (cyclic GMP, cGMP). Each tissue section included both canines: the one treated by
electricity and force and the other treated by force only (control). The areas examined and
reported in this study are confined to the incisal third of the canine root and its surrounding
tissues. During force-induced tipping of canines the PDL in this region is compressed at
the distal aspect of the tooth and stretched at the mesial side. These locations are also
closest to the electrodes; the anode is placed nearest to the distal side of the PDL (com-
pression) and the cathode nearest to the mesial aspect of the PDL (tension).
The production, purification, and application of the anti-CAMP and anti-cGMP an-
tibodies, as well as the succeeding steps in the staining procedure, are described in the
preceding article .26

Results
Rates of canine tipping. In animals treated for 14 days, the rate of canine tipping was
greater during the first week than during the second (probably because of initial compres-
sion of PDL tissues). Statistically, the weekly tooth movement increments in Group A cats
(force only) were not significantly different from one side of the dental arch to the other.
However, canines treated by a combination of electricity and force (Groups B and C) were
tipped distally in all cases at a rate significantly faster (p < 0.01) than that demonstrated
by the contralateral canines treated by force only (Table I and Fig. 4). Occlusal alterations
had apparently little or no effect on the rate of canine tipping, because as the tooth tipped
distally it lost contact with its mandibular opponent. Sufficient room for unimpeded distal
tipping of the maxillary canines was provided by placing the distal acrylic about 3 mm.
away from the crown (Fig. 2).
Histology. The histologic appearance in low magnification of the tension and com-
pression sites near the two maxillary canines of one cat treated for 14 days by the
combined electric-force approach is seen in Fig. 5. In the tension sites (mesial), fingerlike
projections of new bone can be seen growing in the PDL toward the root. These pro-
jections are shorter in the control side (Fig. 5, a), treated by force only, than near the
canine treated also by electricity (cathode, Fig. 5, b). These differences in the length of
the bony projections were not caused by sectioning of the tissues at different angles, as the
tissue block was adjusted in the microtome for horizontal sectioning of the maxilla in
Fig. 5, A-D. For legend. see opposite page
Volume 17
Number 1
Effect of electric currents 39

every case. An examination of the PDL compression sites (distal) reveals that near the
control tooth (Fig. 5, c) the alveolar bone was undergoing resorption along the surface
opposite the root, while active apposition was occurring on the other side of the bone. In
contrast, the alveolar bone in the compression site of the electrically treated canine was
completely resorbed and was replaced by many mononucleated cells (anode, Fig. 5, d).
Immunohistochemistry. A higher magnification of the tension and compression sites
(Figs. 6 to 9) allows for the study of the staining pattern of the PDL and bone cells for
CAMP and cGMP. In particular, the staining intensity and the intracellular distribution of
stain deposits can be assessed and compared. The immunohistochemical staining pattern
for CAMP of periodontal tissues at the tension sites is seen in Fig. 6. Near the control
canine, which was tipped distally by force only (Fig. 6, a) the osteoblasts lining new bony
trabeculae in the PDL were stained distinctly for CAMP. The stain deposits were distrib-
uted rather uniformly over each cell, and some cells stained more intensely than others. In
a corresponding site near the canine treated by force and electricity (Fig. 6, b), the
osteoblasts stained intensely for CAMP and the cells were all stained similar to each other.
In some osteoblasts, however, heavy concentrations of stain were located in parts of the
cell, while the rest of the cell was stained more lightly.
The staining for CAMP at compression sites is seen in Fig. 7. Bone distal to the canine
tipped by force alone (Fig. 7, a) was undergoing resorption, and the osteoclasts in the
Howship’s lucunae were stained intensely for CAMP. In the corresponding local area
distal to the electrically treated canine (Fig. 7, b) the alveolar bone was replaced by
numerous mononucleated cells, a mixture of fibroblasts and inflammatory cells, which
displayed various degrees of staining intensity and distribution for CAMP. More labial,
closer to the anode, some alveolar bone was seen undergoing resorption by cells penetrat-
ing it from both the PDL and periosteal directions (Fig. 7, c). Mononucleated as well as
multinucleated cells could be seen at this site, all intensely stained for CAMP.
The cellular staining pattern for cGMP is presented in Figs. 8 and 9. In the tension site
mesial to the canine treated by force only (Fig. 8, a), the young osteoblasts lining the new
bony trabeculae in the PDL were stained intensely for cGMP and the stain deposits were
uniformly distributed for each cell over its entire area. However, the corresponding zone
near the contralateral tooth, treated by force and electricity (Fig. 8, b) contained larger
numbers of stained cells, and the cellular staining intensity was stronger. The osteoclasts
in the compression site distal to the control canine exhibited intense staining for cGMP
(Fig. 9, u). Staining intensity of a lesser magnitude was visible in the cells populating the
corresponding area distal to the electrically treated tooth, where the alveolar bone has been

Fig. 5. Periodontal tissues of cat maxillary canines after 14 days of treatment by force (a and c) or force
and electricity (b and d). A horizontal section, 5 microns thick, stained immunohistochemically for
CAMP. G, Gingival tissues. 8, Alveolar bone. P, Periodontal ligament. R, Canine root. a, Tension site,
force only. Note short new bony trabeculae growing toward the root. (Magnification, x83.) b, Tension
site, force and electricity. Note large new bony trabeculae in PDL. (Magnification, x83.) c, Compres-
sion site, force only. Note presence of alveolar bone, undergoing resorption from the PDL side. The
darkly stained cells on the periosteal side of the bone are active osteoblasts. (Magnification, x200.) d,
Compression sites, force and electricity. All the bone has already been resorbed and the area is
populated by many mononucleated cells, a mixture of fibroblasts, and migratory cells. (Magnification,
x200.)
 Fig. 6. Higher magnification of section shown In Fig. 5 (staining for CAMP’). a, A bony trabecula In PDL
tension site near canine treated by force only. The staining for CAMP In the osteoblasts is distributed
over large parts of each cell. Only a few cells appear to be stained very Intensely. b, A bony trabecula In
PDL tension site near canine treated by force and electricity. Most of the osteoblasts are stained very
intensely for CAMP. (Magnification, x 1.160.)

replaced by many mononucleated cells (Fig. 9, h). Labial to rhis site, near the anode,
where alveolar bone was seen to undergo degradation (Fig. 9. c’). the resorbing cells
contained many granular-like particles of stain for cGMP.

Discussion
The results obtained in this study can be evaluated on a clinical level as well as on the
basis of cellular biology. From the clinical standpoint, we have observed that during the

Fig. 7. Higher magnification of section shown in Fig. 5 (staining for CAMP). a, PDL and alveolar bone
distal to canine treated by force alone (compression). Osteoblasts on the PDL side are intensely stained
for CAMP. b, Tissue in compression site distal to canine treated by force and electricity displays
numerous mononucleated ceils but no bone. Some of these ceils are stained intensely for CAMP. c, An
alveolar bone spicule at the edge of the compression site of the canine treated by force and electricity.
Mononucleated cells are seen penetrating the bone from the PDL side (right), where the mechanical
force has compressed the PDL, and from the gingival side (left), where the tissue is in close proximity to
the anode. The alveolar bone is being resorbed from both sides. The resorbing cells are intensely
stained for CAMP. (Magnification, x 1,160.)
Volume II
Effect of electric currents 41
Number 1

Fig. 7, A-C. For legend, see opposite page

 Fig. 8. Osteoblasts along new bony trabeculae in PDL tension sites, stained immunohistochemically for
cGMP. a, Osteoblasts from canine treated by force only, stained rather uniformly, but the adjacent PDL
cells (osteoprogenitors?) are stained more intensely (arrow). b, Osteoblasts from canine treated by
force and electricity are stained intensely. Cyclic GMP is particularly concentrated over the cellular
periphery. (Magnification, x 1,160.)

application of electric currents to tissues surrounding orthodontically treated teeth the rate
of tooth movement was enhanced. An immunohistochemical examination of the involved
tissues revealed that cyclic nucleotides may be associated with tissue-remodeling pro-
cesses that result from the application of forces to teeth. with or without electricity.
This study confirmed the histologic observation made by many investigators in the
past, namely, that force-induced tooth movement is accomplished by the removal of bone
and PDL in compression sites and by formation of new bone and PDL components in
tension sites. However, when electric current was applied locally to the tissues around
mechanically stressed teeth. the degree of tissue remodeling appeared to be heightened,
which seemed to result in a more rapid rate of tooth movement. This outcome was
achieved when the electrodes were placed judiciously (that is, the anode was placed as
close as possible to the compression site, while the cathode was placed in close proximity
to the tension site). As reported in the preceding article,2” where no force was applied,
alveolar bone adjacent to the electrodes of a removable electric device, such as the one
used in this experiment, would undergo resorption near the anode and apposition of new
bone near the cathode. In the present experiment. the alveolar bone distal to electrically
treated canines underwent resorption as a result of the activation of bone resorbing cells by
two stimuli: mechanical stress and electric current. It was obvious that the combined
Volume 11
Number 1
Effkt of electric currents 43

Fig. 9. Tissues distal to maxillary canines (compression sites) stained immunohistochemically for
cGMP. a, PDL and alveolar bone distal to canine treated by force alone. An osteoclast on the PDL side
is stained very intensely for cGMP. b, Tissue in compression site near canine treated by force and
electricity (same as in Fig. 7, b). The numerous mononucleated cells display typical staining for cGMP;
that is, cGMP stains over the nuclear region as well as the cytoplasm. Some of the cells appear to be
intensely stained. c, An alveolar bone spicule at the edge of the compression site (same as in Fig. 7, c).
The cells resorbing the spicule from the PDL side (right) and the gingival side (leffj are stained very
intensely for cGMP, particularly on the side near the anode (the gingival side). (Magnification, x 1,160.)

treatment markedly enhanced the rate of alveolar bone resorption. A number of reports
have suggested that the generation of electric potentials in mechanically stressed bone may
be the signal which activates the cells that participate in the remodeling processes.‘-” In
this study, the application of a current from an external source to a mechanically stressed
bone either activated the cells in the involved area to a higher degree, incorporated more
cells in the remodeling process, or caused both responses. The immunohistochemical
evidence provided in this study tends to support the latter possibility.
This study suggests that electricity may be a useful adjunct in clinical trials of orth-
odontic tooth movement. Attempts at combining orthodontic treatment with other biologic
agents were tried in the past. 29-31However, when hormonesz9. 3oand drugs3’ were used,
their effects were not limited to the alveolar bone region but became rather systemic in
nature, affecting target cells throughout the body. Locally applied electricity, as used in
the present experiment, exerted its utmost effects in the tissues adjacent to the surface
electrodes. Practically no histologic or immunohistochemical evidence of effects of elec-
tricity could be noticed at regions more than 2 or 3 mm. away from the electrodes.
 Fig. 9, cont’d. For legend, see p. 43

Moreover, while the use of D.C. currents in orthopedics is usually based upon the
placement of electrodes into tissues, thus introducing the need for surgical intrusion, in the
present experiment electricity was applied through surface electrodes, obviating the need
to injure the oral tissues.
The amount of electric current used in this study (15 microamperes) was an optimal
level arrived at by preliminary experiments which revealed that currents higher than 20
microamperes, when used in our device, were capable of causing tissue damage, espe-
cially near the anode. The current used in this experiment was applied constantly through-
out the treatment period, up to 14 days. It is not known at this time whether a constant
presence of electricity is indeed necessary to activate bone and connective tissue cells or
whether an interrupted application would be more desirable. Future experiments will have
to clarify this question. Another question regarding the possible use of electricity in
orthodontics that will have to be answered relates to the behavior of the affected tissues
after the cessation of active treatment, that is, during the recovery period. We have
observed extensive bone resorption near the anode, where the alveolar bone and adjacent
PDL were compressed by the moving tooth. It is not known at the present time whether
the bone in this area will regenerate or whether it will be replaced irreversibly by soft
connective tissue. Future experiments should clarify this issue. In this context, it may be
beneficial to place a cathode, during the recovery period, in the area previously occupied
by the anode in order to induce osteogenesis and shorten the retention period. This
possibility deserves further attention.
Volume 17
Effect of electric currents 45
Number 1

The intense staining of cells in PDL tension sites of canines treated by force only
supports our earlier observations3*l 33 which asserted the involvement of both CAMP and
cGMP in the cellular response to tension in vivo. However, the addition of a cathode to
tension sites apparently intensified the involvement of the cyclic nucleotides in the cellular
response; more periodontal cells were stained for CAMP and cGMP near the cathode than
in sites treated by force only, and the cells were stained more intensely in sites treated by
the combined force-electric approach. In addition, while some of the cells in the force-
treated sites were stained less intensely than some of their neighboring cells, most or all of
the cells in electrically treated sites stained very intensely for both cyclic nucleotides. This
observation strongly suggests that on the cellular level the combination of mechanical
force and electric current has a high potency in activating bone and PDL cells.
As discussed in the preceding article, 26the significance of both CAMP and cGMP rests
in their role as mediators of the effects of external stimuli on bone cells.34 As visualized by
the immunohistochemical method used in this study, the staining reactions are also indi-
cative of phosphorylation reactions which, according to a recent view,35 are perhaps the
most significant cellular events that occur following the activation stage. Some light is
shed on the location of these reactions by the present microscopic methods. Additional
information may be derived from studies employing transmission electron microscopy,
which are currently in progress at our laboratory.
The role of CAMP in the metabolism of mineralized tissues is well established, as a
result of numerous studies involving hormones, such as parathyroid hormone,36-38 cal-
citonin,24. 3gand vitamin D .40, 41However, little is known regarding the role of cGMP in
cells of bone or cartilage. Rodan and colleagues34 reported on fluctuations of both CAMP
and cGMP levels in isolated cartilage cells in vitro after the application of mechanical
forces. Evidence from other tissues42-44 suggests that cGMP may play a role in the
synthesis of nucleic acids and proteins, as well as the secretion of cellular products. It is
not yet clear which of these specific functions involves cGMP in PDL and alveolar bone
cells.

Summary
The rate of tooth movement was studied in cats treated by mechanical forces that
tipped their maxillary canines distally and in cats receiving electric stimulation to tissues
surrounding orthodontically treated canines. Teeth treated by force and electricity moved
significantly faster than those treated by force alone. Histologic examination of the in-
volved tissues revealed that the enhanced tooth movement resulted from resorption of
bone as a result of the compressive force and the presence of the anode near the PDL
compression site. The degree of new bone formation (as judged by the length of the newly
formed bony trabeculae in the PDL) at electrically treated tension sites was higher than at
the corresponding sites of teeth treated by force alone. Examination of the involved tissues
by an immunohistochemical technique designed to localize cyclic nucleotides in cells
revealed that the cellular response to the combined force-electric treatment was more
pronounced than the response to force alone. These results suggest that orthodontic tooth
movement may be accelerated by the use of force in conjunction with other biologically
potent means which can generate a local response. Specifically, this study has demon-
strated that electric currents, in the range of 10 to 20 microamperes, can be used success-
fully for this purpose.
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