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Taken from the Journal of Periodontology 1976 May (256-260): On the Repair Potential

of Periodontal Tissues A. H. Melcher


-------------------------------On the Repair Potential of Periodontal Tissues
A. H. Melcher
THE TEETH ARE supported by the periodontium. The periodontium is a connective
tissue organ, protected by epithelium, that attaches the teeth to the bone of the jaws and
provides a continually adapting apparatus for their support during function. The four
connective tissues of the periodontium are the lamina propria of the gingiva, the
periodontal ligament, the cementum and the alveolar bone. For the purposes of this
discussion, the whole of the alveolar process, that is alveolar and supporting bone, will
be considered rather than just the alveolar bone, which in this author's view is a term
that should be restricted to the thimble of bone lining the socket of the tooth. The lamina
propria of the gingiva is protected by keratinized stratified squamous epithelium on its
masticatory surfaces, and by nonkeratinized epithelium on its crevicular and junctional
surfaces. A discussion of the healing potential of periodontal tissues should include all
of the above connective tissues and epithelium. For reasons that will be made clear later,
it is advisable to examine the alveolar part of the periodontium, that is the periodontal
ligament, alveolar bone and cementum as a unit.
The literature concerning healing of periodontal tissues will not be reviewed
exhaustively, inasmuch as this was done relatively few years ago.1 Most of the
published papers report histological evaluation of experiments, and there appears to be
little data available concerning either the biological processes underlying the response
of periodontal tissues to wounding or the interaction between the cells of the different
tissues of the periodontium when more than one periodontal tissue is involved in the
wound. In vivo experiments generally do not provide conditions in which questions of
this nature can be answered, and few attempts have been made to examine the tissues or
cells of the periodontium in vitro. This meeting could provide an ideal opportunity to
speculate about some of the gaps in our understanding against a background of what is
known. Consequently, this paper will discuss aspects of the potential for healing of, on
the one hand, gingival epithelium and connective tissue and, on the other, alveolar bone,
periodontal ligament and cementum. Some principles associated with the response of
bone to wounding will also be covered, as well as speculation on the interrelationship
between cells of the four connective tissues in healing of wounds that involve them all.
GINGIVA
It is well known that the gingival connective tissue and epithelium have a marked
capacity for regeneration. There is also evidence that crevicular and junctional
epithelium, together with the internal and external basal laminae, are regenerated
readily; that the junctional epithelium will reattach to enamel, cementum, dentine and
even, under some conditions, calculus; and, furthermore, it is claimed that regenerating
crevicular and junctional epithelium can differentiate from cells taking origin from the
germinative layers of keratinized masticatory epithelium.2-7
The lamina propria of the gingiva regenerates readily after wounding, and this is
accompanied by differentiation of gingival fibres.8 A fascinating question that may be
raised is why gingiva is able to regenerate after wounding and the architecture of its
fibres frequently to be restored, when most other connective tissues, for example that of
skin, tend to scar after wounding and to exhibit disorientation of the newly-formed
fibres. It may be conjectured that forces transmitted from the teeth to the regenerating
connective tissue regulate differentiation and orientation of gingival fibres, or that the
attachment of gingival connective tissue to bone or cementum prevents contraction, and

therefore distortion, during healing, but it is not known whether or not this is in fact the
case. It is perhaps pertinent at this juncture to distinguish between the terms
regeneration and repair: regeneration refers to restoration of architecture and function in
a healing wound, whereas repair refers to healing of a wound by tissue that does not
fully restore the architecture or the function of the part.9
RESPONSE OF BONE TO WOUNDING
As regeneration of bone is a matter of some considerable concern in the treatment of
periodontal disease, devoting a little attention to some of the principles associated with
bone repair in general, before looking at alveolar process in particular, could be of
interest. Regeneration of bone after wounding is achieved by cells, and bone cells are
found to occupy different compartments which, for the purpose of this discussion, could
be considered to number four, namely: osteocytes, bone cells in marrow, cells of
endosteum and the osteogenic cells of periosteum. It is worthwhile examining briefly
the contribution of each of these to wound healing.
Although the osteocytes in the vicinity of a wound may be active,10 it is unlikely that
they make any real contribution to restoring a bone defect. Similarly, although it is
claimed that bone marrow contains a highly potent population of osteoprogenitor cells
that may be distinct from the hemopoietic and endosteal populations,11 there is no
information concerning their contribution to healing of wounds in bone. Conceivably, it
is this population of osteoprogenitor cells, termed by Friedenstein11 Determined
Osteogenic Precursor Cells (DOP cells), that is responsible for the osteogenic response
that is obtained from transplants of bone marrow.12,13
Cells of endosteum cover all internal surfaces of bone including the walls of canals, the
wall of the medullary cavity, and the surfaces of trabeculae of cancellous bone, and are
believed by some authors to be active metabolically.14 They may play an important role
in wound repair in some sites,15 including the mandible.16 It is interesting to note that
cartilage is rarely deposited by these cells and is not frequently seen in endosteal callus,
whereas cartilage is commonly deposited by cells of periosteal callus.
It is widely accepted that the cells of periosteum make a major contribution to healing
of bone wounds, especially to fractures of long bones. Periosteum exhibits two features
that are important in any consideration of its role in healing: (1) It consists of at least
two layers, an outer fibrous layer that does not appear to possess osteogenic potential
and an inner cambium or osteogenic layer that does.17 The osteogenic layer appears to
be continuous with endosteum where canals open onto the surface of the bone. (2)
Depending on the state of its activity, the osteogenic layer may contain varying numbers
of cell strata, and the cells may exhibit different degrees of maturation.
The osteogenic layer of the periosteum of a young growing bone may be multilayered.
The outer layers of cells adjacent to the fibrous periosteum usually contain dividing
cells and thereby provide the font for a continuous supply of new osteoblasts. As the
bone surface is approached, the cells can be seen progressively to exhibit morphological
characteristics consistent with active synthesis, whereas the cells on the bone surface
can be recognized as active osteoblasts. The osteogenic layer of a periosteum in such a
state of activity may be in equilibrium, the rate of production of new cells capable of
differentiating into osteoblasts equalling the loss of cells from the compartment to the
osteocyte population.17 Alternatively, a unilateral increase in production of new cells,
or a decrease in the rate of transformation from osteoblasts to osteocytes, will lead to
increase in the thickness of the osteogenic layer or, if the reverse occurs, to a thinning of
the osteogenic layer.
As a given part of a bone approaches the end of its growth, division of progenitor cells
in the osteogenic layer of the periosteum ceases while differentiation and osteogenesis

continues, until all but the progenitor cells have become osteocytes. The periosteum
then exhibits a morphological structure consistent with that of mature bone, and
comprises a fibrous layer covering a single layer of attenuated progenitor cells
constituting the osteogenic layer. These apparently uncommitted progenitor cells retain
their capacity for division, and may be reactivated by trauma or by the stimuli which are
responsible for remodelling of bone. It is of interest that following injury, these
progenitor cells may differentiate into either chondroblasts or osteoblasts. The
periosteum in the vicinity of an actively-repairing wound of an adult animal may
resemble that of a young growing animal.
These two stages in the life cycle of periosteum have important clinical implications.
Tonna18 has shown that, shortly after fracture of a long bone in a young animal, some
of the cells in the periosteum divide while others simultaneously are synthesizing
extracellular protein. By contrast, in an older animal, division of progenitor cells occurs
first, and this is followed later by synthesis of extracellular protein by their
differentiating progeny. Such a finding is not surprising, as it is evident that the
multilayered osteogenic component of the periosteum of a young animal is a "goingconcern" in which progenitor cells are dividing and differentiated cells are engaged
actively in osteogenesis. Trauma in such a situation will be followed by continuation of
this activity, perhaps at an increased rate. On the other hand, if the relatively few cells of
the cambium layer of the periosteum of an adult were immediately to differentiate into
osteoblasts, and to secrete and surround themselves with extracellular substance of bone
without first dividing, there would be no cells left to divide and provide successors, and
the cambium layer of that area of the periosteum would soon be lost. Consequently,
trauma must be followed first by division of the progenitor cells of the periosteum. Only
then can some of the daughter cells differentiate into osteoblasts, backed by a
population of other daughter cells that have remained as progenitors and which
eventually will divide again. In this way, a continual source of cells that can
differentiate into osteoblasts and finally can be entombed as osteocytes, is assured.
Thus, though osteogenesis is initiated shortly after wounding of a young animal, it is
delayed in an adult.
The response of periosteum to surgical treatment is consistent with what has been
described above. The cells of a flap of periosteum that has been elevated from adult
bone and replaced do not give rise to new bone; the new bone that is deposited in the
site takes origin from cells of undisturbed periosteum surrounding the flap.16,19
However, if an osteoperiosteal flap is raised, new bone is deposited by the cells of the
flap.20 These observations suggest that the surgical maneuvers involved in elevating a
periosteal flap destroy most of the thin layer of cells that comprises the osteogenic layer
of the adult periosteum, and in consequence the capacity of the replaced periosteum to
produce new bone is lost. On the other hand, elevation of an osteoperiosteal flap does
not destroy these cells and they can engage in proliferation, differentiation, maturation
and osteogenesis after the flap is replaced.
ALVEOLAR PROCESS, PERIODONTAL LIGAMENT AND CEMENTUM
As far as is known, the fate of the cells of the osteogenic layer of the mucoperiosteum of
gingiva after elevation and replacement of a full-thickness flap such as is used in
periodontal surgery has not been investigated, but it would be surprising if the results
differed from that which occur elsewhere. However, it has been shown that osteogenesis
following elevation and replacement of a gingival flap may be preceded by necrosis and
resorption of bone,21 that excision of the mucoperiosteum hinders the repair process,22
and that resorption of alveolar process is less active, osteogenesis more active, and

restoration of alveolar process lost following surgery more complete under a splitthickness flap than under a full-thickness flap.23
The response of the cells of alveolar bone to trauma is vigorous, and is exemplified by
the extensive osteogenesis that is stimulated by tooth extraction (see 1 for review). This
is in contrast to the cells of some bones such as, for example, the flat bones of the skull
that do not exhibit a strong osteogenic response following wounding.19,24 Indeed, were
it not for the response of the endosteal and periosteal cells of the alveolar process, and
the cells on the periodontal surface of the alveolar bone, orthodontic movement of teeth
would be difficult if not impossible.
It is inadvisable to consider healing of alveolar bone separately from periodontal
ligament because, although the cells of the mucoperiosteum and endosteum of the
alveolar process make an important contribution to healing, deposition and resorption of
bone from the periodontal surface of the alveolar bone is accomplished by cells that
appear to arise in the periodontal ligament. In this context, it is important to note that the
periodontal surface of the alveolar bone is not covered by periosteum, but rather by
endosteum, and that therefore it must be regarded as an internal surface of bone.
Furthermore, cells of the periodontal ligament are responsible not only for osteogenesis
and osteoclasis, but also for fibrogenesis and fibroclasis in the ligament itself, and
cementogenesis and cementoclasis. Consequently, cells of periodontal ligament must
play an important role in healing of alveolar bone in a wound that involves both alveolar
process and periodontal ligament, and most wounds inflicted on periodontium during
periodontal therapy do involve both of these two tissues.
Regeneration of periodontal ligament does not appear to be as aggressive as that of
alveolar bone. Regeneration of periodontal ligament occurs in wounds involving the
periodontal space; however, if the wound is large, it may be colonized to a varying
degree by bone cells, and this can lead to ankylosis and obliteration of that part of the
periodontal space.25-28 It may seem strange that a connective tissue which, in normal
function, exhibits a high rate of turnover of extracellular protein,29,30 and that
possesses cells whose rate of deoxyribonucleic acid synthesis and mitosis has been
shown to respond to stimulus31,32 should not heal more readily relative to bone. This
question will be discussed further below. It is also of interest in relation to what appears
below, that regeneration of periodontal ligament in a wound involving the ligament and
alveolar bone is accompanied by regeneration of alveolar bone and reestablishment of
the periodontal space.26
Regeneration of cementum in the alveolar part of the periodontium is achieved by cells
that appear to take origin from periodontal ligament, and seems to occur quite readily
after wounding and tooth movement.1,3,28 Resorption of cementum may also occur
after wounding.26,28 There does not appear to be any information on the origin of the
cells that differentiate into functioning cementoblasts and deposit cementum on the root
surface adjacent to lamina propria of gingiva in healing of wounds in that area. It is
reasonable to suppose that they are derived from progenitors in the lamina propria of
gingiva, but the possibility that cells from periodontal ligament may have to migrate
into this area of the root to give rise to cementoblasts cannot be dismissed. Levine and
Stahl,33 Stahl et al.34 and Listgarten3 have found that after detachment of gingival
fibres and removal of cementum in a flap procedure, much of the root becomes covered
by epithelium, and not by cementum. This could mean either that epithelial cells
migrate onto the root surface faster than do cells of gingival connective tissue or
periodontal ligament, or that gingival connective tissue cells that have migrated into the
area do not attach to the root surface and do not secrete cementum. It is of interest that
in Listgarten's3 experiment cementogenesis occurred regularly, but was most advanced

in the most apical part of the wound adjacent to periodontal ligament; and furthermore,
that it has been shown that cells in the coronal part of periodontal ligament respond to
surgical treatment of gingiva by increased synthesis of deoxyribonucleic acid and that
they may migrate coronally.21,35,30 This question remains to be elucidated.
INTERACTION BETWEEN CELLS OF PERIODONTAL TISSUES
Periodontal therapy is concerned intimately with regeneration of alveolar process. It is
evident from the above that the cells of alveolar process have the capacity to effect
regeneration after wounding and moreover, it is claimed that osteogenesis can be
enhanced by the use of bone marrow grafts.37,38 This notwithstanding, restoration of
alveolar process lost in periodontal disease still cannot be achieved predictably, a
deficiency that may rest partially in the sequestered and inimicable environment of the
periodontium. However, there may be other reasons for the difficulty, and these could
originate in the behavioral characteristics of the cells of the part. Before discussing this
question there is an important point to be made. The tissue lost consequent to
periodontal disease is not only bone, but includes lamina propria of gingiva, periodontal
ligament and cementum. Should we not then, in therapy, be attempting to reconstruct
the entire organ that supports the tooth, that is periodontium, rather than only one of its
constituent tissues, namely bone? If one accepts this thesis, then it becomes evident that
regeneration of periodontal ligament is of prime importance as it provides continuity
between alveolar bone and cementum and also because it apparently contains cells that
can synthesize and remodel the three connective tissues of the alveolar part of the
periodontium.
Returning to the question raised earlier, it seems on the limited experimental evidence
available that periodontal ligament may not regenerate as readily as bone, and that this
could discourage hopes that regeneration of periodontium can be achieved. However, in
the types of experiments reported, the occupation of periodontal space by bone may
have been due to the fact that bone cells had a shorter distance to migrate to the center
of the wound, or indeed to most of the wound when much of the periodontal ligament
was destroyed, than the cells of the surrounding viable periodontal ligament, and that
they could enter the wound ahead of the periodontal ligament cells despite the fact that
bone had to be resorbed before bone cells could reach the periodontal space. In general
terms it would seem that like cells can aggregate and occupy a particular territory,
possibly excluding unlike cells; embryonic cells maintained in vitro have been shown to
exhibit this characteristic.39 Melcher26 has suggested that periodontal ligament cells
and their progeny have the capacity to inhibit osteogenesis, and that it is through this
homeostatic mechanism that the periodontal space is maintained throughout life.
However, this belief now seems to be too restrictive, and it is possibly closer to the truth
to postulate that bone and soft connective tissue cells of periodontal ligament exert
stimuli upon one another, and are acted upon by external stimuli that permit them
reciprocally to maintain or alter the balance of their territorial boundaries. If this
hypothesis can be shown to be credible, and there is some evidence that may support
it,28 and if the nature of the regulating stimuli could be determined, then it would be
possible to understand how the integrity of the periodontal space is normally maintained
throughout life. It would also be possible to explain why, after wounding, the
periodontal space can be occupied by bone cells, and why, provided the domain of the
bone cells and their mineralized extracellular substance is sufficiently large to resist
resorption stimulated by the movement of the functioning tooth, the newly deposited
bone will persist and will not be replaced by periodontal ligament. Thus, although it
may appear to be the case, it is by no means certain that periodontal ligament has a
diminished capacity for regeneration relative to bone.

As far as is known, no experimental data is available concerning the interaction between


cells of gingival connective tissue on the one hand and cells of alveolar process and
periodontal ligament, on the other, in healing of a wound that involves all three tissues.
It has been shown in other situations that osteogenesis in repair of a bone wound can be
inhibited by invasion of the site by nonosteogenic cells that presumably exclude the
migrating osteogenic cells,40 and it does not seem unreasonable to suppose that this
could be the case in wounds of periodontium. For example, if cells derived from
gingival connective tissue occupy the area of the wound adjacent to the alveolar process
and periodontal ligament, it is likely that no increase in the height of bone or periodontal
ligament will occur. This is because there is no evidence that the cells of gingiva exhibit
osteogenic potential. The replacement of gingival flaps raised in periodontal surgery in
direct contact with the crest of the alveolar process could theoretically favor such a
sequence of events, but such a hypothesis needs to be tested experimentally. Placing
bone, or particularly marrow grafts possibly assists cells of osteogenic potential to
colonize the grafted area by displacing lamina propria of gingiva and increasing the
distance that the gingival cells must migrate before they can colonize the wound. If
osteogenic cells are present in the grafted site, or are able to reach it before the cells of
gingival connective tissue, then it is possible that the height of the alveolar process will
be increased during healing. Unfortunately, such therapy does not take into account the
need for regeneration of periodontal ligament, and so does not necessarily lead to the
desirable outcome of a regenerated periodontium. If both periodontal ligament and bone
could be regenerated in a coronal direction, then cells apparently having the capacity to
regenerate and maintain the alveolar part of the periodontium, namely cementum,
periodontal ligament and alveolar bone, will colonize the wound. Then it should not be
overoptimistic to hope that the four connective tissues of the newly regenerated
periodontium could be maintained in proper relationship to one another. The foregoing
concept is based on theoretical beliefs about the phenotypic and social behavior of cells
of the tissues of the periodontium, and remains to be tested experimentally. However,
the successful isolation and culture of periodontal ligament cells,41 and the finding that
periodontal ligament cells exhibit some characteristics different from skin cells in
vitro,42 has made possible the design of in vitro experiments to explore some of these
phenomena. From the clinical standpoint, the design of surgical procedures that will
allow colonization of wounds coronal to the alveolar crest by cells derived from
periodontal ligament and bone rather than by cells derived from lamina propria of
gingiva or bone alone could provide a fruitful field for investigation.
Taken from the Journal of Periodontology 1976 May (256-260): On the Repair Potential
of Periodontal Tissues A. H. Melcher
-------------------------------Melcher, A. H.: Healing of wounds in the periodontium. A. H. Melcher and W. H.
Bowen (eds). Biology of the Periodontium, pp 497-529. London, Academic Press, 1969.
2. Listgarten, M. A.: Electron microscopic features of the newly formed epithelial
attachment after gingival surgery. J Periodont Res 2: 46, 1967.
3. Listgarten, M. A.: Electron microscopic study of the junction between surgically
denuded root surfaces and regenerated periodontal tissues. J Periodont Res 7: 68, 1972.
4. Listgarten, M.: Ultrastructure of the dento-gingival junction after gingivectomy.
J Periodont Res 7: 151, 1972.
5. Taylor, C. A., and Campbell, Marion M.: Reattachment of gingival epithelium to
the tooth. J Periodontol 43: 281, 1972.

6. Frank, R., Fiore-Donno, G., Cimasoni, G., and Ogilvie, A.: Gingival
reattachment after surgery in man: An electron microscopic study. J Periodontol 43:
597, 1972.
7. Listgarten, M. A., and Ellegaard, B.: Electron microscopic evidence of a cellular
attachment between junctional epithelium and dental calculus. J Periodont Res 8: 143,
1973.
8. Tonna, E. A., and Stahl, S. S.: A polarized light microscopic study of rat
periodontal ligament following surgical and chemical gingival trauma. Acta Odontol
Helv 11: 90, 1967.
9. Gillman, T.: Tissue regeneration. G. H. Bourne (ed), Structural Aspects of
Ageing, pp 143-176. London, Pitman, 1961.
10. Melcher, A. H., and Accursi, G. E.: Transmission of an "Osteogenic Message"
through intact bone after wounding. Anat Rec 173: 265, 1972.
11. Friedenstein, A. J.: Determined and inducible osteogenic precursor cells. Hard
Tissue Growth, Repair and Remineralization. Ciba Foundation Symposium 11 (New
Series), pp 169-182. Amsterdam, London, New York, Elsevier, Excerpta Medica, North
Holland, 1973.
12. Burwell, R. G.: Osteogenesis in cancellous bone grafts considered in terms of
cellular changes, basic mechanisms and the perspective of growth-control and its
possible aberrations. Clin Orthop 40: 35, 1965.
13. Turnbull, R. S., and Freeman, E.: Use of wounds in the parietal bone of the rat
for evaluating bone marrow for grafting into periodontal defects. J Periodont Res 9: 39,
1974.
14. Rasmussen, H., and Bordier, P.: The Physiological and Cellular Basis Or
Metabolic Bone Disease, p 33. Baltimore, Williams & Wilkins Company, 1974.
15. Melcher, A. H., and Irving, J. T.: The healing mechanism in artificially created
circumscribed defects in the femora of albino rats. J Bone Joint Surg 44B: 928, 1962.
16. Melcher, A. H.: Wound healing in monkey (Macaca irus) mandible: Effect of
elevating periosteum on formation of subperiosteal callus. Arch Oral Biol 16: 461,
1971.
17. Owen, Maureen: Cellular dynamics of bone. G. H. Bourne (ed), The
Biochemistry and Physiology Or Bone, vol. III, pp 271-298. New York and London.
Academic Press, 1971.
18. Tonna, E. A.: Protein synthesis and cells of the skeletal system. C. P. Leblond
and K. B. Warren (eds), Radioautography in Investigating Protein Synthesis. pp 215245. New York, Academic Press, 1965.
19. Melcher, A. H.: Role of the periosteum in repair of wounds of the parietal bone
of the rat. Arch Oral Biol 14: 1101, 1969.
20. Melcher, A. H., and Accursi, G. E.: Osteogenic capacity of periosteal and
osteoperiosteal flaps elevated from the parietal bone of the rat. Arch Oral Biol 16: 573,
1971.
21. Caffesse, R. G., Ramfjord, S. P., and Nasjleti, C. E.: Reverse bevel periodontal
flaps in monkeys. J Periodontol 39: 219, 1968.
22. Pfeifer, J. S.: The growth of gingival tissue over denuded bone. J Periodontol 34:
10, 1963.
23. Staffileno, H.: Significant differences and advantages between the full thickness
and split thickness flaps. J Periodontol 6: 421, 1974.
24. Prichard, J. J.: Repair of fractures of the parietal bone in rats. J Anat 80: 55,
1946.

25. Sherman, P. Jr.: Intentional replantation of teeth in dogs and monkeys. J Dent
Res 47: 1066, 1968.
26. Melcher, A. H.: Repair of wounds in the periodontium of the rat. Influence of
periodontal ligament on osteogenesis. Arch Oral Biol 15: 1183, 1970.
27. Atrizadeh, F., Kennedy, J., and Zander, H.: Ankylosis of teeth following thermal
injury. J Periodont Res 6: 159, 1971.
28. Line, S. E., Polson, A. M., and Zander, H. A.: Relationship between periodontal
injury, selective cell repopulation and ankylosis. J Periodontol 45: 725, 1974.
29. Stallard, R. E.: The utilization of H3-proline by connective tissue elements of the
periodontium. Periodontics 1: 185, 1963.
30. Carneiro, J., and Fava de Moraes, F.: Radioautographic visualization of collagen
metabolism in the periodontal tissues of the mouse. Arch Oral Biol 10: 833, 1965.
31. Weiss, R., Stahl, S. S., and Tonna, E. A.: Functional demands on the cell
proliferative activity of the rat periodontium studied autoradiographically. J Dent Res
47: 1153, 1968.
32. Roberts, W. E., and Jee, W. S. S.: Cell kinetics of orthodontically-stimulated and
non-stimulated periodontal ligament in the rat. Arch Oral Biol 19: 17, 1974.
33. Levine, H. L., and Stahl, S. S.: Repair following periodontal flap surgery with
the retention of gingival fibres. J Periodontol 43: 99, 1972.
34. Stahl, S. S., Slavkin, H. C., Yamada, L., and Levine, S.: Speculations about
gingival repair. J Periodontol 43: 395, 1972.
35. Ramfjord, S. P., Engler, W. O., and Hiniker, J. J.: A radioautographic study of
healing following simple gingivectomy II. The connective tissue. J Periodontol 37: 179,
1966.
36. Stahl, S. S., Tonna, E. A., and Weiss, R.: Autoradiographic evaluation of gingival
response to injury. III. Surgical trauma in mature rats. Arch Oral Biol 15: 537, 1970.
37. Hiatt, W. H., and Schallhorn, R. G.: Human allografts of iliac cancellous bone
and marrow in periodontal osseous defects. I. Rationale and methodology. J Periodontol
42: 642, 1971.
38. Hiatt, W. H., and Schallhorn, R. G.: Intraoral transplants of cancellous bone and
marrow in periodontal lesions. J Periodontol 44: 194, 1973.
39. Moscona, A. A.: Recombination of dissociated cells and the development of cell
aggregates. E. N. Wilmer (ed), Cells and Tissues in Culture Methods Biology and
Physiology, vol. I, pp 489-529. London and New York, Academic Press, 1965.
40. Melcher, A. H., and Dreyer, C. J.: Protection of the blood clot in healing
circumscribed bone defects. J Bone Joint Surg 44B: 424, 1962.
41. Brunette, D. M., Melcher, A. H., and Moe, H. K.: Culture and origin of
epithelial-like and fibroblast-like cells from porcine periodontal ligament explants and
cell suspensions. Arch Oral Biol (in press).
42. Marmary, Y.: Differences between cells derived from periodontal ligament and
skin in vitro. M.Sc.D. Thesis, University of Toronto, 1975.

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