Bone reaction to orthodontic forces on

vitreous carbon dental implants

Alan J. Sherman, D.D.S., A.M.Ed
Fullr~rton, Caljf.

I
mplants are becoming an important addition to the armamentarium of the
modem dentist. The subperiosteal implant can stabilize the “floating dentition,” and the
endosseous implant can replace an individual tooth or become an abutment root for a fixed
bridge.
Although the Council on Dental Materials of the American Dental Association3 has
stated that dental implant procedures are to be considered to constitute a new technique
that has not been adequately investigated, academies, congresses, study clubs, and uni-
versity postgraduate courses devoted to implants are being organized across the United
States and, indeed, around the world to disseminate the knowledge of dental implantol-
ogy. As the use of implants becomes more prevalent in the offices of general practitioners
and specialists, it is inevitable that some of these implants will be placed in the mouths of
patients who will subsequently require orthodontic treatment.
This investigation involved a limited series of vitreous carbon implants in dogs, using
a standard orthodontic technique with a force of 175 Gm. Tetracycline was used to label
new bone formation. Milch and associates” discovered that tetracycline antibiotics are
deposited in vivo in sites of bone formation and subsequently can be studied in undecal-
cified sections by fluorescence microscopy.
The purpose of this investigation was to study the movement of a vitreous carbon
dental implant under the stress of a classic orthodontic force.

Methods and materials

Dogs were used for this experiment, since Tayer and colleagues” reported that tooth
movement in dogs closely resembled tooth movement in human beings and since Greno-
ble and Kim8 reported successful implantation of vitreous carbon implants in dogs.
Pretreatment records included study models and periapical x-ray pictures of the dogs’
mandibular teeth. The implants (Fig. I) were inserted into the extraction sites of the
mandibular third premolars immediately after their removal and after the sites were
prepared to receive the implants.
The orthodontic appliances (Fig. 2) consisted of 0.040 inch (1.016 mm.) stainless
steel wire soldered to cast-gold crowns on the dogs’ mandibular fourth premolars and to
either cast-gold crowns or to stainless steel orthodontic bands on the dogs’ mandibular
canines. The fourth premolars and canines provided the anchorage to resist the orthodontic
force. The 0.040 inch (1.016 mm.) wire passed through 0.040 inch (I ,016 mm.) tubes
which were soldered to the superstructures of the implants. On the 0.040 inch (1.016
mm.) wire a measured length of open-coil spring, 0.010 by 0.040 inch (0.254 by 1.016
0002-Y416/78/0174-0079$00.90/0 0 1978 The C. V. Mosb) Co 79
 Am. J. Orrhod.
July 1978

Fig. 1. A vitreous carbon dental implant. The occlusal surface has a receptacle for a preformed dowel
post. The implant is designed with undercut areas to aid its retention in bone.

mm.), was compressed between the tube (on the implant) and a soldered stop mesial to the
implant, so that a force of 175 Gm. would push the implant in a distal direction.
For 70 days after the last surgical procedure, the appliances were used only as splints
to stabilize the implants and to permit bone healing in the surgical sites. The springs were
inactivated by tying them back to the soldered stops.
The animals were injected with 250 mg. of oxytetracycline 10 days prior to the
activation of the appliances, on the day of the activation, and weekly for the next 7 weeks
until the dogs were killed.
At all subsequent appointments after the metal tie-back ligatures were cut to activate
the springs, the arch wires and springs were cleaned and checked for easy movement of
the springs. At each appointment, the dogs were given a general anesthetic and periapical
x-ray films were taken of the experimentally involved teeth and the implants. Gross
measurements were made before the appliances were activated and again each time the
dogs were anesthetized. A pair of dividers was used to measure the distances between the
occlusal edge of the vitreous carbon implant and the most concave portion of the adjacent
teeth (mesial and distal) at the gingival crest. The dividiers were then placed on a metal
millimeter ruler for measurement of the distance.
Histological procedures
Sections of the dogs’ mandibles were dissected to include the implants and abutment
teeth. These sections were progressively dehydrated in 70 per cent, 95 per cent, and
absolute ethyl alcohol and desiccated under 15 inches of mercury vacuum. The sections
were embedded under vacuum in blocks of methyl methacrylate, polymerized with 0.5
Gm. benzovl net-oxide nw INl mm of methvl methnrrylnte
Volume 14
Number I Bone reaction to orthodontic forces on implants 81

Fig. 2. The orthodontic appliance with the coil spring tied back during the stabilization period. The 0.040
inch (1 .016 mm.) arch wire is passed through an 0.040 inch (1 .016 mm.) tube which is soldered to the
implant’s dowel post.

Sagittal and cross sections 100 to 150 pm. thick were cut with a diamond cutting
wheel on a Bronwill thin sectioning machine. The undecalcified sections were mounted on
glass slides and examined microscopically.

Color photography for recording ultraviolet fluorescence

The procedure for recording ultraviolet fluorescence of the samples involved the use of
a 200 watt-second electronic strobe fitted with a Kodak No. 47 Wratten filter as the
ultraviolet exciter source. The 35 mm. single lens reflex camera was fitted with a reversed
28 mm. lens which yielded a magnification at the film plane of x 2.25. A Kodak No. 12
Wratten filter was used as the barrier filter in the lens system, but because the No. 12
Wratten filter will fluoresce by itself, a Kodak No. 2B Wratten filter was placed in front of
the No. 12 filter.
The strobe-to-object distance was 8 cm., at a 30 degree angle. Exposure was deter-
mined empirically to be f8, using high-speed Ektachrome daylight film, rated at ASA 160.
(See Fig. 3 for physical appearance of photographic setup.)

Results
Of the original six implant sites, two of the implants were firm. functional. and
considered to be successful. A third implant had some mobility; it functioned, but the
degree of success was questionable. Other implants could not be used because the im-
plants either became excessively mobile or were fractured. The excessive mobility was
probably due to poor surgical technique, since there was an inadequate coolant spray
attachment for the laboratory air turbine drill which may have permitted the drill to
overheat the bone. The force needed to fracture an implant may have been caused by the
dogs biting on their wire cages or water pipes.
Although only two implants were suitable for orthodontic experiment, the results were
unambiguous. The implants did not move. The gross measurements of the interdental
 Am. J. Orthod.
Julv 1978

Fig. 3. Physical appearance of photographic set-up showing the single lens reflex camera aimed at a
prepared slide with the electronic strobe light set at a 30 degree angle toward the slide.

space mesial and distal to the implants never varied more than -t-OS mm. from the original
measurements.
The ultraviolet photographs of the histologic specimens showed a generalized fluores-
cence of the bone, indicating some new bone, but there was no concentric pattern of
fluorescence which would have indicated movement of the implant (Figs. 4 and 5).
Periapical radiographs of the implant areas showed the bone to have good trabecula-
tion and to be without any radiolucent areas which might have indicated an area of
pathosis (Fig. 6). Histologic evaluation by means of a light microscope showed bone
healing in close apposition to the vitreous carbon implant and closely adapted in the
grooves of the implant (Figs. 7 and 8).
Barbara Mills, M.D.,” of the University of Southern California School of Dentistry,
examined the histologic specimens and stated that in some areas the bone was separated
from the implant by connective tissue and in other areas it was separated only by what
appeared to be a dental cuticle, as described by Schroeder and Listgarten. I3 It definitely is
not a periodontal ligament. Mills based her opinion on a comparison with her work with
vitreous carbon implants in rabbits. Listgartenr3 examined electron microscopic photos
(X 100,000) of Mills’ work and stated that the layer of tissue separating the bone from the
implant was similar to or the same as the dental cuticle as described in his monograph.

Discussion
It has been traditional in dental schools to teach the “pressure-tension” theory of
orthodontic tooth movement and that the osteoclastic and osteoblastic activity was a result
Volume 74
Number 1 Bone reaction to orthodontic forces on implants 83

Fig. 4. Ultravioletphotugrsph &owing bone growth in close proximity to the implant (sagittal section).
Fig. 5. Ultraviolet photograph showing bone growth in close proximity to the implant (horizontal section).

of cells in the periodontal membrane. The “pressure-tension” theory has been supported
by the research of many investigators.14* I6 Other investigators,2, l2 however, have inter-
preted their work to support the elasticity theory or bending of the alveolar bone to explain
tooth movement. Another group of researchers, ‘, I5 have interpreted their findings to
explain different responses of the teeth to different forces.
Dental educators have taught that a blood supply is needed to support these bone
changes and that this blood supply must come from the periodontal membrane. If this
were all there was to orthodontic tooth movement, then the question “will an orthodontic
force move an implant?” should be easy to answer. Since the implant does not have a
peridontal membrane with all its organs similar to a tooth, then the answer must be,
“No.” However, the medullary space of bone has a rich blood supply, and capillaries do
 Am. J. Orrhod.
84 Shrrrnan Ju/y 1978

Fig. 6. Radiograph of dog’s mandible, showing the implant and the activated appliance. The bone
trabeculations closely follow the contours of the implant.

course through the Haversian canals of the compact bone. In addition, Friedenstein’
showed that “determined osteogenic precursor cells” exist in bone marrow. Furthermore,
perhaps the “cuticle” that Schroeder and Listgarten referred to that separated the bone
from the implant is the same cellular membrane that Owen” has said has a considerable
degree of functional integrity. Thus, since the elements to support osteoclastic and osteo-
blastic activity seem to be present, perhaps it would be possible to move an implant
orthodontically.
In the last decade, a number of researchers have investigated the biophysical prop-
erties of connective tissue, such as bone, cartilage, and tendon. Bassett’ reported on
electrical polarization, resulting from the application of orthodontic forces to a tooth and
correlated polarity to cell behavior. He found that, as in long bones, osteoblastic activity,
concavity, net compression, and electronegativity are associated with one another. Con-
versely, osteoclastic activity, convexity, net tension, and relative positivity are closely
associated.
The main unanswered question is: “What elements in the periodontal membrane are
responsible for tooth movement ?” DeAngelis4 stated that it was an oversimplification to
say that the differentiation of osteoclasts and resorption were induced by pressure or that
tension induces osteoblastic deposition of new bone simply because of distension of the
collagenous periodontal fibers, as this would not explain the changes which he observed
on the alveolar surfaces not directly contacting the periodontal membrane. Zengo and
colleagues1s concluded that tooth and bone function as transducers, converting mechanical
to electrical energy.
Thus, in orthodontics, we have an unusual condition wherein a physical force results
in a biochemical reaction. The periodontal membrane acts as a translator of these energies
into appropriate responses. Picton ** and Baumrind* have shown that the alveolus could be
Volume 74
Number I Bone reaction to orthodontic forces on implants 85

Fig. 7. Sagittal section of a mandible with an implant. The bone trabeculations are visible in close
proximity to the contours of the implant.
Fig. 8. Horizontal section of a mandible with an implant showing the bone regenerated in the surgical
site around the implant.

distorted by forces lower than those required to produce gross reduction in the periodontal
ligament.
The lack of movement by the vitreous carbon implant was probably a direct function
of the excellent bone healing around the implant and the rigidity of the implant material
which did not permit distortion of the alveolus. The previous sentence would be consistent
with the views of Epker and Frost,” who stated that some minimum amount of deforma-
tion would be required to generate enough “signal” for the cells to detect. Any less
deformation than the hypothetical minimum would not cause the mesenchymal cells to
differentiate into the appropriate cells to cause osteogenesis and osteoclasia. Thus, force
 Am. J. Orthod
July 1978

alone was not enough to move the implant (or an ankylosed tooth), even though force was
conducted through the implant to the bone.
if the bioelectric hypothesis of tooth movement and the above rationale were correct,
the carbon implant might prevent the differentiation of mesenchymal cells. Vitreous
carbon is an excellent conductor of electricity. If the alveolus were distorted during
application of the orthodontic forces, it might be possible that the electrically conductive
implants nullified the electrical potentials which formed on the socket walls where bend-
ing occurred.
The effect of electrically conductive implant materials on the bioelectric processes in
bone deserves investigation.

Conclusions
On the basis of a very small sample in dogs, it appears that orthodontic techniques
cannot be used to move a vitreous carbon implant. Therefore, one should not use implants
before the completion of orthodontic treatment in persons who may require orthodontic
service unless the implants are to be used for anchorage.
Alveolar bone heals in very close apposition to vitreous carbon implants in dogs. Prior
experiments with vitreous carbon implants have been conducted with free-standing im-
plants; in this study a substantial number of implants became excessively mobile and
exfoliated. Therefore, it is recommended that implants be stabilized through the bone-
healing period.
Because of the small sample, this study should be considered as only a pilot study and
observations made should be considered solely as guidelines.
I would like to acknowledge the support and guidance of Dale Grenoble, Ph.D., Harry L.
Dougherty, D.D.S., Keith Tanaka, D.D.S., and Mr. Michael Abbey of the University of Southern
California School of Dentistry.

REFERENCES
I. Bassett, C. A. L.: Biophysical principles affecting bone structure. In Bourne, G. H.: The biochemistry and
physiology of bone, New York, 1971, Academic Press, Inc., Vol. III, pp. l-76.
2. Baumrind, S.: A reconsideration of the propriety of the “pressure-tension” hypothesis, AM. J. ORTHOD.
55: 12-22, 1969.
3. Council on Dental Materials and Devices, and Council on Dental Research: Council reaffirms position on
dental endosseous implants, J. Am. Dent. Assoc. 90: 670, 1975.
4. DeAngehs, V.: Observations on the response of alveolar bone to orthodontic force, AM. J. ORTHOD. 58:
284-294, 1970.
5. Epker, B. N., and Frost, H. M.: Correlation of bone resorption and formation with the physical behavior of
loaded bone, J. Dent. Res. 44: 33-41, 1965.
6. Friedenstein, A. J.: Induction of bone tissue by transitional epithelium, Clin. Orthop. 59: 21-37, 1968.
7. Furstman, L., Bernick, S., and Aldrich, D.: Differential response incident to tooth movement, AM. J.
ORTHOD. 59: 600608, 1971.
8. Grenoble, D. E., and Kim, R. L.: Progress in the evaluation of a vitreous carbon endosteal implant, Oral
Implantol. 4: 216-235, 1973.
9. Milch, R. A., Rail, D. P., and Tobie, J. E.: Bone localization of the tetracyclines, J. Natl. Cancer Inst. 19:
87-93, 1957.
10. Mills, Barbara, University of Southern California School of Dentistry: Personal communication, May,
1974.
I I. Owen, M.: Cellular dynamics of bone. In Bourne, G. H.: The biochemistry and physiology of bone, New
York, 1971, Academic Press, Inc., Vol. III, pp. 271.298.
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Number I Bone reaction to orthodontic forces on implants 87

12. Picton, D. C. A.: On the part played by the socket in tooth support, Arch Oral Biol. 10: 945-955, 1965.
13. Shroeder, H. E., and Listgarten, M. A.: Monographs in developmental biology, Basel, 1971, S. Krager.
14. Skillen, William G., and Reitan, Kaare: Tissue changes following rotation of teeth in the dog, Angle
Orthod. 10: 140-147, 1940.
15. Storey, E., and Smith, R.: Force in orthodontics and its relation to tooth movement, Amt. J. Dent. 56:
I I-18, 291-304, 1952.
16. Stuteville, 0. H.: lnjuries to the teeth and supporting structures caused by various orthodontic appliances,
and methods of preventing these injuries, J. Am. Dent. Assoc. 24: 1494 1507, 1937.
17. Tayer, B. H., Gianelly, A. A., and Ruben, M. P.: Visualization of cellular dynamics associated with
orthodontic tooth movement, AM. J. ORTHOD. 54: 515-520, 1968.
18. Zengo, A. N., Bassett, C. A. L., Pawluk, R. J.. and Prountzos, G.: In viva bioelectric potentials in the
dentoalveolar complex, AM. J. ORTHOD. 66: 130-139, 1974.

1031 Rosecrans Ave. (92633)

THE JOURNAL 60 YEARS AGO

July, 1918
In estimating which of the three teeth (first or second bicuspid, or first molar) should be
extracted in any given case, many points arise which should be carefully balanced in the
mind of the operator before he makes his selection. The respective value of the teeth must
be considered as features, as organs of mastication, and in relation in their prospective
durability and their soundness at the time. These are all important points for consideration,
irrespective of the cardinal question as to which tooth would, by its removal, best effect the
required object, furnish the needed room, and allow the misplaced anterior tooth or teeth to
range in proper order with the others. Unquestionably the bicuspid teeth are superior as
features to the molars; indeed, the farther forward in the mouth a tooth is situated, the more
does it modify the form of the lips, the more is it seen in expression, and consequently the
more would its absence be remarked. It must be recollected, however, that there are two
bicuspids’ so much alike that when one is lost the other takes its place as far as appearance
goes. As an organ of mastication a molar is of greater value than a bicuspid. The present
soundness or otherwise of the bicuspids and molar is a question of the greatest importance,
and must often decide finally and peremptorily the question under consideration. Provided
the loss of either a bicuspid or a first molar would give the necessary space with equal ease
and certainty, or nearly so-one being carious and the other sound-there can be no
hesitation as to which should be extracted. The decayed tooth should be taken out, and a
double good will thus be effected, the regulation will be achieved, and a source of future or
perhaps present pain will be removed. (S. James A. Salter: Irregularities in the Position of
Teeth, Causes, etc. [I 8751 Quoted in Bernhard Wolf Weinberger: The History of Orthodon-
tia, International Journal of Orthodontia, predecessor of the American Journal of Orthodon-
tics, 4: 376, 1918.)