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POSTEXTRACTION CHANGES IN THE ADULT MANDIBLE AS

ILLUSTRATED BY MICRORADIOGRAPHS OF MIDSAGITTAL


SECTIONS AND SERIAL CEPHALOMETRIC ROENTGENOGRAMS

DOUCLASALLENATWOOD,A.B.,M.D.,D.M.D.
Harvard School of Dental Medicine, Boston, Mass.

OF TEETH is a surgical procedure equivalent to amputation in


T which
HE EXTRACTION
a diseased or injured part of the body is removed for cause, not as a
natural process of life. As with an amputation, the extraction of teeth may lead to
functional,’ psychologic, and posturaJ3v4 as well as local changes. This report deals
with the local postextraction changes. There have been many approaches to the
study of these changes :
1. Models and Cowzparators: Over the years, many clinicians have observed
serial plaster casts of residual ridges and marveled at the continuing gross changes
in the shape of the ridges. Improved techniques of comparing different casts have
added new dimensions to this method.5-12
2. Gross Anatomy: Puzzling over these changes, clinicians have often re-
turned to a study of the gross anatomy of dry specimens. Study of this sort has
revealed clearly that residual ridges may vary widely in form, with two dramatic
forms being the knife-edge ridge and the low flat ridge. One finding seems to be
that the crest of the residual ridge is almost always imperfectly sealed by cortical
bone. Roentgenograms of dry specimens have aided such studies, particularly in
depicting both the minute trabecular character of the bone and the trajectories or
lines of force through the bone.ls-lQ
3. Histology: Considerable information concerning both the hard and soft
tissues of the edentulous mandible has been derived from histologic examination
of human material (obtained by biopsy, by surgery, or by post-mortem examina-
tion) and animal material (especially studies of postextraction healing) .20-32
4. Radiology: Clinical roentgenographic studies suggest differences in density
of bone, both between different individuals, and within the same indivdua1.33-37
Unless such studes are carefully standardized, they are fraught with danger of mis-
interpretation.36-37 Serial cephalometric roentgenograms following the extraction of
remaining teeth can provide a dynamic picture of the amount and location of resorp-
tion of residual ridges 38-39(Fig. 1) . Roentgenograms of the resorption of bone under
some periosteal mandibular implants give dramatic evidence of the resorbability of
even cortical bone.ll
5. Microradiography: In the past decade, microradiography has become a
valuable research too1.40-46Sognnaes 41 has shown clearly that in resorption of
Read before the Academy of Denture Prosthetics, Miami Beach, Fla.
810
POSTEXTRACTION CHANGES IN ADULT MANS)IBLE 811

Fig. l.-Tracings of 3 lateral cephalographs with the maxillae and mandibles carefully
superimposed. Note the changes in the shape of the residual ridges following the extration Of
the remaining teeth. (For other examples, see Atwood.9

teeth and bone, there is a complete removal of the organic and inorganic elements
simultaneously, regardless of the degree of calcification. Manson and Lucas42 have
shown that in the mandible (as others have shown in other bones43z45) there are
definite variations in the structure and activity of cortical bone at different ages.
There is much deposition and resorption in the early years, relative stability dur-
in.g the adult years, and increased activity favoring resorption in later years.
6. Other Techniques: Other techniques are available which include the
use of radioactive materials and tetracycline, as illustrated by McLean and Urist.4”
The most efficient use of all of the tools of modern research, however, depends on
the development of a good, working hypothesis which must be scientifically tested.
Such a hypothesis often comes from good clinical observation. The hypothesis of
L.ammie47 (tt la t in many patients, resorption of residual ridges may be due to an
a-trophying mucosa which seeks a reduced area) is an instance of this and is
worthy of further study by many research approaches.

MATERIAL AND METHODS

While a study of the patterns of bone resorption in lateral cephalometric roent-


genograms was under way, an opportunity arose to study microradiographically
some edentulous jaws from cadavers at the Harvard Medical School. It was
exciting to contemplate the investigation of roentgenograms of essentially two-
dimensional microscopic sections of the same structures which were being studied
with some difficulty because of the three-dimensional overlapping in the cephalo-
graphs. In the cephalograph, there is a clear image of the midsagittal projection of
the maxilla and mandible.38-3g Accordingly, the cadaver material was sectioned in
a midsagittal plane. Despite the fact that the cephalometric material and the micro-
radiographic material come from completely different and unrelated patients, the
similarities are quite dramatic. This report concerns primarily the microradiographic
study of edentulous ridges. The cephalometric study has been reported previ-
ou~ly,~~*~” but it provides an illustrative background for this study.
The cadaver material consisted of 15 males, age 54 through 86, and averaging
71 years, and 6 females, age 67 through 79, and averaging 74 years. Causes of
death were listed as either pneumonia, cardiac failure, or arteriosclerosis. ~\io past
dental history or other medical history is available.
ATWOOD J. Pros. Den.
812 Sept..Oct., 1963

Fig. Z.-A contact roentgenogram of midsagittal sections of 22 mandibles (of approximately


1 mm. thickness) shows a wide variation in the external size and form, and in the internal
density. The roentgenogram shows the outer compact cortex and inner less dense trabecular
medulla. All specimens are oriented as in a lateral cephalograph with inferior mandibular
border below and the labial surface toward the right (except D-Z which is reversed labio-
lingually).

In successive steps, the gross specimens were reduced in thickness by means


of an electric jig saw, wet grinding, an electric jeweler’s slotting saw, and, after
imbedding in methyl methacrylate to keep the large specimens together, dry grind-
ing, as reported in more detail by Sognnaes. 48 Contact roentgenograms of the
specimens were made when they were 5 mm. thick, and again when they were
1 mm. thick (55 kv., 10 Ma., l$$ seconds.) (Fig. 2). Contact microradiographs
were made when the specimens were about 100 p thick, with a Kodak Spectroscopic
Plate, Type 649-GH, and specially built microradiographic equipment41 (20 kv.,
15 Ma., for 5 to 10 minutes.) (Fig. 3).
The microradiographs were studied with care microscopically under low and
high power. Polaroid microphotographs were made of selected areas for detailed
study and for illustration.

SOFT X-RAYS

Gloss Slide
cooled with
photographic
emulsion.
Specimen of Bone
in cantoct with emulsion

Fig. 3.-A diagrammatic representation of the method of making microradiographs of thin


sections of bone (approximately 100~ in thickness).
Volume 13 POSTEXTRACTION CHANGES IN ADULT MANDIBLE 813
Number 5

FINDINGS

Microradiography of the mandible reveals certain things about bone in gen-


eral and about the mandible in particular.
Bone21-46 consists of an outer compact cortex and an inner less dense trabec-
ular medulla (Fig. 2). The cortex usually consists of outer periosteal lamellae, a
middle portion consisting of Haversian systems (osteons) and interstitial lamellae,
and an inner endosteal, more porous, portion which merges into the medulla

Fig. 4.-A microradiograph of cortical bone from the inferior border of the mandible (Fig.
2,B-3) showing the outer periosteal lamellae, a middle portion consisting of osteons and inter-
stitial lamellae, and an inner endosteal more porous portion. (x15.)

(Fig. 4). The cortex will vary in thickness from bone to bone, from person to
person, and from time to time, as a result of heredity, function, nutrition, hormone
metabolism, and many other factors.

HAVKRSIAN SYSTEM OR OSTEON

One of the structural units of bone is the Haversian system or osteon. It


consists of a central vascular channel surrounded by concentric layers of bone
(Fig. 5). Because osteons divide, bend, and twist, their appearance in a micro-
scopic section varies markedly, depending on the angle of section: true cross-
sectional, diagonal, or longitudinal (Figs. 5 and 6). Three-dimensional models
(Figs. 7 and 8) of osteons 4g have been constructed from serial sections in the
same way that Posseltso made his three-dimensional models of mandibular move-
ment space from serial “Gothic arch” tracings at different vertical openings.
Because of the remodeling of bone throughout life, an osteon has a life his-
tory much shorter than the life of the individual. Frost and his associates,51 using
a tetracycline in a 57-year-old man, estimate the biologic half life of an osteon
as 2.7 years in the femur and 8.6 years in the tibia. The first step in the formation
814 ATWOOD J. Pros. Den.
Sept.-Oct., 1963

of an osteon is the absorption of already existing bone (which may be either


lamellar, Haversian, or trabecular) by osteoclastic activity which is r.z:vealed in
microradiographs by the sharply crenated borders of Howship’s lacunae (Fig. 9).

Fig. 5.-A microradiograph of a lingual cortex (Fig. 2,B-3) showing the periosk al lamellae,
a longitudinal section of an osteon, various cross-sections of osteons, and interstiti; 31 lamellae.
The osteons show different degrees of closure and of calcification, some showing an inner ring
of increased mineralization. (x60.)

Fig. 6.-A microradiograph of the two crosslsectioned osteons shown in the lower left
corner of Fig. 5. Note the different degrees and sites of mineralization. (x240.)
POSTEXTRACTION CHANGES IN ADCLT MANDIBLE 815

Fig. 7. Fig. 8.

Fig. ‘7.-A three-dimensional model of a simple osteon from the cortex of an adult dog
ft:mur. It shows a spiral contour (2 turns in 1.5 mm.). A blindly ending osteon is present in the
center. The cross-sectional areas of most of the osteon are nearly the same. (From Cohen, J., and
Harris, W. H.: The Three-dimensional Anatomy of Haversian Systems, Bone & Joint Surg. 40-A:
419-434, 1958, by permission.)
Fig. S.-A three-dimensional model of more complex osteons. The variation in cross-
sectional areas of different parts of the same osteon is evident. The enlargement occurs grad-
ually as one goes distally. The abrupt horizontal cuts indicate anastamoses with other km-
modeled) systems. A blind osteon is seen at the right. (From Cohen, J., and Harris, W. H.:
The Threedimensional Anatomy of Haversian Systems, Bone & Joint Surg. 40:A:419-434, 1958,
by permission.)

After the formation of the absorption cavity or tunnel, the osteoclasts disappear
and the osteoblasts lay down concentric layers of bone forming the tubular osteon
around the central blood vessel.
As has been pointed out, 40,42,45there are two phases of osteon formation: the
rapid formation to about 75 per cent or less mineralization, followed by the much
more gradual completion of the job over several months. Hence, in a microradio-
816 ATWOOD J. Pros. Den.
Sept.-Oct.. 1963

graph, an osteon of low radiodensity (that is a dark osteon) is interpreted by


some45 as a newly formed, incompletely mineralized osteon. If such a dark osteon
has an inner ring of increased density (Fig. 9)) this is interpreted as an indication
that the osteon is not newly formed.
Another indication of incomplet’e osteon formation is the formation of osteons
whose central canal is over 25 per cent the width of the osteon itself. Frequently,
the dense inner ring is associated with this incomplete closure of the osteon, indi-
cating inactive osteon formation. There is usually a definite increase in older age
in the number of incompletely mineralized and incompletely closed osteons, espe-
cially in osteoporosis.
Fig. 9.

Fig. 10.
Fig. 9.-A microradiograph of the inferior border of a mandible (Fig. Z,B-I) showing evi-
dence of moderate osteoporosis with increased variation in the density of osteons, increased
number of incompletely closed osteons, and increased endosteal porosity. (x15.1
Fig. 10.-A microradiograph of a portion of the crest of the ridge (Fig. 2, J-1) showing
external resorption of both the lingual cortex and the trabeculae on the crest of the ridge. Also
evident is an osteon within a single trabecula, and evidence of internal bone formation, and
resorption of the trabeculae.
Volume 13 I’OSTEXTRACTION CHANGES IN ADULT MANDIBLE 817
Number 5

I II III Ip Y PL

Fig. Il.--The 6 orders of adult human mandibles in midsagittal profile: Order I, pre-
extraction; Order II, postextraction; Order III, high, well-rounded residual ridge; Order IV,
knife-edge residual ridge; Order V, low, well-rounded residual ridge; and Order VI, depressed
residual ridge.

Occasionally, the central canal of an osteon is completely occluded with calci-


fied material which appears even more radiopaque (whiter) in a microradiograph
than the osteon itself. Similar to and concomitant with plugged canals are calcified
osteocyte lacunae. These changes occur more often in older age and in instances of
osteoporosis.
In the medulla, the trabeculae are subject to bone addition (that is, lamellar
growth makes them thicker), to bone resorption (as shown by Howship’s lacunae),
and, if thick enough, to osteon formation (Fig. 10).

CLASSIFICATION OF FORMS OF MANDIBLES

Study of the gross outline form of the specimens (Fig. 2) and study of the
serial cephalographs of the previous study suggest the need for classification of
the various forms the adult mandible can assume before and after extraction. There
seem to be at least 6 orders of form of the anterior part of the mandible (Fig. 11) :
Order I: Pre-extraction: The lower central incisor is in its socket with very
t’hin labial and lingual cortical plates merged with the lamina dura (Fig. 2, E-l ).
Order II: Postextraction: The healing period includes clot formation, clot
organization, filling of the socket to the height of the cortical plates with new
trabecular bone, and epithelization over the socket site. The edges of the residual
ridge are still sharp (Fig. 2, D-1, F-4, J-l ) .
Order 1II: High, Well-Rounded Residual Ridge: The cortical plates are
rounded off, narrowing of the crest of the ridge has begun, and remodeling of the
internal trabecular structure has taken place (Fig. 2, R-4, C-Z, C-4, E-Z, H-4, J-2,
J-4).
Order IV: Knife-Edge Residual Ridge: There is marked narrowing of the
labiolingual diameter of the crest of the ridge with a compensatory internal remod-
eling which sometimes leads to an incredibly sharp crest of the ridge (Fig. 2, B-3,
Lb3, E-3, E-4, G-3, H-5).
Order p.: Low Well-Rounded Residu,al Ridge: The end result of progressive
labiolingual narrowing of a knife-edge ridge is the disappearance of the knife-edge
portion. A more widely rounded, but considerably lower residual ridge remains
(Fig. 2, B-l, D-2, D-4, G-2, J-3).
Order VI: Depressed Residual Ridge: Resorption has continued below the
level of the genial tubercle.
J. Pros. Den.
818 ATWOOD
Sept..Oct., 1963

GROSS FINDINGS

Other gross findings can be summarized as follows :


1. The lingual cortical plate was generally about 2 to 3 times as thick as the
labial cortical plate which all but disappears in some specimens.
2. The average vertical height of specimens in Orders II, III, and IV were
roughly the same 27.8, 25.6, and 26.3 mm., respectively) but that of Order V was
approximately two-thirds that of the others (18.2 mm.), indicating a sharp drop
off between Orders IV and V. Meanwhile, there was no significant difference in
Fig. 12.

Fig. 13.
Fig. 12.-A microradiograph of the crest of the residual ridge (Fig. 2, J-3) shows the
abrupt ending of the periosteal lamellar bone below the crest on both the labial and lingual
surfaces. (X15.1
Fig. 13.-A microradiograph of a portion of the crest of the residual ridge (Fig. 2, B-1)
shows an abrupt ending of the lingual periosteal bone and a zone of external resorption over
the crest of the ridge. (x15.1
Volume 13 POSTEXTRACTION CHANGES IN ADULT MANDIBLE 819
Numhrr 5

Fig. 14.-A microradiograph of the crest of the residual ridge (Fig. 2, B-l) shows Howship’s
laruna involving bone regardless of the density of the bone. (X60.)

the averages of the maxinlum widths of the different orders ( 12.0, 12.1, 11.7, and
I 1.9 mm., respectively).
3. There was little or no cortical layer at the crest of the ridge in Orders II,
III and V, but in Order IV where the remodeled labial and lingual plates merged
to form a knife-edge ridge. The cortical plate at the crest of the ridge averaged
4.5 mm. in a vertical direction.

M ICRORADIOGRAPHIC STUDY

A careful study of the microradiographic slides reveals the following main


points :
1. Periosteal LavnelEur Bone: In general, periosteal lamellar bone is sparse in
these midsagittal specimens, occurring to a greater degree on the lingual and in-
ferior borders of the mandible with little or none on the labial surface. In not a
single specimen was there any evidence of periosteal lamellar bone over the crest
o:r’the ridge, even in those specimens where there was an attempt to form a cortical
layer with trabeculae, Haversian systems, and interstitial lamellae (Fig. 12).
2. External Resorption: In all midsagittal specimens, there was evidence of
external resorption of the residual mandibular ridge of one degree or another. In
Orders III and V, there were crenated borders typical of Howship’s lacunae on
all 3 sides of the ridge: on the lingual surface, across the top, and down the labial
surface (Figs. 13 and 14). In Order IV, the knife-edge ridge, there was usually
considerably more resorption on the sides than at the top (Fig. 1.5). In general,
there was more resorption over a wider area on the labial than on the lingual sur-
face, but this was not invariable (Fig. 2, G-2, J-l ). In general, one can see clearly
where the resorption begins and ends. Because osteoclasts can resorb bone of
different degrees of mineralization with equal ease, One can observe a single HOW-
ship’s lacuna resorbing adjoining osteons of different mineralization (Fig. 14).
ATWOOD J. Pros. Den.
820 Sept.-Oct., 1963

Resorption takes place in lamellar bone, Haversian bone, and trabecular bone. The
great majority of the resorption taking place in these specimens is on the external
surface of the residual ridge.
3. Internal Remodeling: While a long bone grows in circumference by means
of periosteal new bone, the entire internal structure, including the cortex and the
medulla, is reconstructed.52 The same process, but in a reverse direction, seems
to take place in the residual ridge. As external resorption occurs, both the cortex
and the medulla are remodeled. As the ridge gets narrower labiolingually, the cor-
tical plates do not necessarily disappear. The ridge gets narrower mostly at the
expense of the medulla. In Order IV, the knife-edge ridge and the labial and
lingual cortical plates merge into one (Figs. 15 and 16).
4. Evidence of Osteoporosis: Microradiographic criteria for osteoporosis (Fig.
9) include : (1) increased variation in the density of the osteons, (2) increased
number of incompletely closed osteons, (3) increased endosteal porosity, and (4)
increased number of plugged osteons. Unfortunately, these criteria are not reliably
quantitated from specimen to specimen. None of the specimens showed advanced
osteoporosis, but about one half showed some evidence of it, (Fig. 2, B-l, B-3, C-Z,
D-4, E-3, H-5, J-l, J-Z, J-4), while the rest showed little or no evidence of osteo-
porosis (Fig. 2, C-4, D-1, D-3, E-Z, E,-4, F-4, G-Z, G-3, H-4, J-3). The average age
for the group with evidence of osteoporosis is 76 years, while that of the other group
is 69 years. Males and females are evenly divided between the two groups.

Fig. 15.-A microradiograph of the crest of the knife-edge residual ridge (Fig. 2, B-3) shows
external resorption of both the lingual and labial cortical plates, merging of the lingual and
labial plates, “new” osteons in the remodeled inner portion, and endosteal bone formation.
(X15.)
Volume 13 POSTEXTRACTION CHANGES IN ADULT MANDIBLE 821
Number 5

Fig. 16.-A microradiograph of portion of the knife-edge residual ridge (Fig. 2, B-3) shows
that only a small amount of the labial and lingual resorption will result in a sudden loss of
vertical height of the residual ridge. (x60.)

D[SCCSSION

Bone is a living tissue which requires a vital blood supply. Whenever new
bone is laid down beyond a certain thickness, it is invaded by absorption cavities,
thereby providing a blood supply to the osteocytes in the interior part of the bone.
The absorption cavities are converted to osteons, but the blood vessels remain
within the central canals. As a result of these vascular channels, even the densest-
appearing cortex is actually porous. This is clearly seen in the microradiographs.
Bone is a valuable tissue not only for its structural strength, but also as a
reservoir for calcium and phosphorous. There is accumulating evidence that the
“,young” or “new” osteons provide a quickly available, nonosteoclastic source of
these ions to the bloodstream. The microradiographs clearly show the difference in
the degree of calcification between different osteons in the same area of bone.
The classification of the adult mandible into six orders of anatomic form is
helpful in research, teaching, and clinical practice. We need more information con-
cerning the range of variation of time period for each order. Cephalometric studies
should give this information if they are carried out over a long enough period of
time.
The complete absence of periosteal bone over the residual ridge in all of these
midsagittal specimens, and the presence of external resorption on some part of
the residual ridge in every specimen is discouraging from a clinical point of view,
because it suggests the inevitability of resorption of residual ridges. Yet, we must
remember that nothing is known of the medical and dental history of these indi-
viduals. An interesting study would be to have bone biopsies of residual ridges of
persons who seem clinically to be having no resorption. Would they show evidence
of periosteal bone formation over the crest of the ridge?
J. Pros. Den.
822 ATWOOD Sept.-Oct., 1963

The uniform and continuous nature of the zone of external resorption of the
residual ridge suggests the presence of an external stimulus to osteoclastic resorp-
tion from an undetermined origin. It might be a dental prosthesis, increased mu-
cosal vascularity, a constricting mucoperiosteum, muscle action, the trauma of
mastication, or some other factor yet unknown. The degree of osteoclastic activity
was different in the various specimens, suggesting that different factors were at
work.
The role of surgical technique in relation to postextraction resorption of
residual ridges deserves further study. Obviously, if much cortical bone is removed,
the amount of residual ridge will be considerably less. Simpson30-32 found that
the level of bone formation in the socket was limited by a line joining the crests
of the socket and that new bone does not build up on the crest of the ridge. Per-
haps also, if too much soft tissue is excised (for example, all of the interdental pap-
illae and most of the gingival mucosa), and if the reduced mucosa is closely ap-
proximated in an esthetically successful surgical closure, the subsequent healing
and late cicatricial shrinking may result in the continuing resorption of residual
ridges. Perhaps the surgery predetermines the amount of resorption the prostho-
dontist will observe. Perhaps the knobby unesthetic residual ridges resulting from
a minimum of removal of bone give patients a longer lasting residual ridge than
the esthetic but too extensively excised ridge resulting from a generous alveolec-
tomy. 30.32,63-E&i
The suggestion of mild to moderate degrees of osteoporosis in approximately
one half of the specimens is not surprising since the average age of that group was
76 years. We do not know that osteoporotic bone will resorb more rapidly. We do
know that there is less of it to be resorbed and that the rate of replacement and
reconstruction is usually slower.

SUMMARY

1. Bone is a living tissue of varying size, shape, and density and is subject
to constant remodeling throughout life.
2. It is helpful in research, teaching, and patient care to classify adult
mandibles into 6 orders of anatomic form: I, pre-extraction; II, postextraction;
III, high, well-rounded residual ridge ; IV, knife-edge residual ridge ; V, low, well-
rounded residual ridge ; VI, depressed residual ridge.
3. Microradiography of thin sections of bone shows clearly the variations in
form and degree of mineralization of the various elements of bone.
4. Microradiography of midsagittal sections of 21 edentulous mandibles re-
vealed external resorption and an absence of periosteal bone on the residual ridges
in all specimens.
5. Evidence of mild to moderate osteoporosis was seen in one half of the
specimens (average age of this group, 76 years).
6. There are many avenues for the study of resorption of residual ridges. The
possible roles of a constricting mucoperiosteum and of surgical technique are dis-
cussed.
This microradiographic study would never have been accomplished without the encourage-
ment and experience of Dr. Reidar F. Sognnaes, formerly Charles A. Brackett Professor of
Volume 13 POSTEXTRACTION CHANGES IN ADULT MANDIBLE 823
Nmher 5

Oral Pathology, Harvard School of Dental Medicine, now Dean, School of Dentistry, Univer-
sity of California at Los Angeles, who generously made available to a member of the Prosthetic
Dentistry staff the extensive facilities of the Histopathology Department of the Harvard School
of Dental Medicine. Also, it is a pleasure to acknowledge the technical assistance of Mr. George
Pettingill. The author also expresses appreciation to Dean Roy 0. Greep, Associate Professor
Paul Goldhaber, and Assistant Clinical Professor David J .Farrell.

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188 LONC,WOOD A+E.
BOSTON, MASS.

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