Roentgenographic and Direct Observation of Experimental Lesions

JOURNAL OF ENDODONTICS
Copyright © 2003 by The American Association of Endodontists
Printed in U.S.A.
VOL. 29, NO. 11, NOVEMBER 2003
Roentgenographic and Direct Observation of
Experimental Lesions in Bone: I†
I. B. Bender,* D.D.S., and Samuel Seltzer,** D.D.S., Philadelphia
diolucency. The purpose of this study was to find out under what
specific conditions bone destruction in vitro was not detectable by
roentgenographic examination, and to correlate the known location
and extent of artificially produced bone lesions with the roentgenograms of those lesions. The general procedure was to create
lesions of various sizes, gradations and anatomic locations in
mandibles. The visible evidence of bone destruction was then
compared with the appearance of these lesions in the usual dental
roentgenograms.
Artificial lesions simulating pathological conditions
were made in mandibles from human cadavers.
Roentgenograms of the lesions were made and
compared with the specimens of bone. Lesions in
cortical bone can be detected roentgenographically only if there is perforation of the bone cortex,
erosion from the inner surface of the bone cortex,
or extensive erosion or destruction from the outer
surface. Lesions in cancellous bone cannot be detected roentgenographically. Extensive disease of
bone may be present even when there is no evidence of it on roentgenograms.
MATERIALS AND METHOD
Human mandibles obtained at necropsy were studied. Both wet
and dry specimens were used. Color photographs and roentgenograms of the specimens were taken prior to experimentation. The
mandibles were cut into block sections. Experimental lesions of
various types were then made with diamond stones, endodontic
reamers, files and dental burs. Roentgenograms were made of the
experimental lesions in the bone sections. All roentgenograms
were taken at the same target film distance and angulation (except
for the deliberate variation of angulation described in the first
experiment). All films were exposed for two seconds at 65 kvp, 10
ma. and were developed together for three minutes.
It is not uncommon to find clinical signs of bone disease in spite
of negative roentgenographic findings. For example, in many instances of acute alveolar abscess, even though pus is draining
through the root canal, no changes can be detected by roentgenographic examinations. In many of the acute total pulpitides the
initial roentgenograms fail to indicate pathological changes, yet
roentgenograms taken several days later may show changes in the
apical tissues.1 Periodontal lesions involving the bifurcation are
not always seen on roentgenographic examination. Roentgenograms taken after extraction of teeth often fail to show distinct
areas of rarefaction, in spite of the extensive cavitation. The
trabeculae over the sockets appear normal and if the lamina dura
could somehow be obliterated there would be no way of determining roentgenographically that a tooth had been removed recently.
Instrumentation of the root canal beyond the apex with reamen and
files usually does not produce roentgenographic changes in the
trabecular pattern of bone even though the instruments have displaced some of the cancellous bone. In acute mastoid, march
fracture, and osteomyelitis, roentgenograms also often appear negative.
Thus it seems that extensive bone destruction may occur under
some conditions without being detectable through changes in ra-
EXPERIMENTAL EVIDENCE
Effects of Depth of Lesions in Cortical Bone
Holes were drilled into a section of the mandible with round
burs of various sizes (no. 2 to no. 8). The buccal plates were drilled
(1) to a depth of 1 mm., (2) halfway into the buccal cortex, (3) all
the way through the buccal cortex (perforation) and (4) deep
enough to perforate both buccal and lingual bone plates. Roentgenograms of these artificial lesions were taken at various angulations.
Effect of Depth
From Albert Einstein Medical Center, Northern Division, department of dentistry.
* Associate professor in oral medicine.
** Associate professor in histopathology, School of Dentistry, University of
Pennsylvania.
† Bender IB, and Seltzer S. Roentgenographic and direct observation of experimental lesions in bone I. J Am Dent Assoc 62:152-60, 1961. Copyright (c) 1961
American Dental Association. All rights reserved. Reprinted by permission of ADA
Publishing, a Division of ADA Business Enterprises, Inc.
Lesions 1 mm. deep did not appear on the roentgenogram,
regardless of the size of bur used. As the depth of lesions increased
there was greater radiolucency and the shadows became more
pronounced, irrespective of bur size. Thus loss of a superficial
layer of the outer surface of bone is not ordinarily detectable. As
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FIG 1. A: Four holes of different depths were drilled in the mandible with a no. 8 round bur. Roentgenograms show only two or three holes,
depending on angulation. B: Roentgenogram showing three holes. The fourth is not perceptible. The radiolucency increases with depth of cut.
The shadow is darkest in area where cortex has been perforated. C: Note change in shape and size of holes and gradations in shadow as
angulation is changed. The hole made by cutting halfway through the cortex can hardly be seen. D: Note further change in shadow and shape
of hole as the angle is increased. Also, distal root is completely denuded of bone in B. A change in angulation produces an impression of bone
regeneration.
more and more bone is removed from a given region from the outer
cortex inward the shadow deepens and the area of rarefaction
becomes more pronounced, hence more readily observed.
The roentgenograms were similar, whether taken from the buccal or lingual side. From the roentgenographic evidence alone it
would not have been possible to determine on which side the
lesions had been made.
Effect of Angulation
As the roentgenographic angulation was increased, the rounded
shadows became elongated and their densities decreased. These
effects of angulation were especially pronounced for perforations.
The elongation of shadows increased with the depth of the cut as
well as with the degree of angulation, a fact to be taken into
consideration in evaluating roentgenograms. It was not so much
the diameter of the bur as it was the depth of the cut that produced
a recognizable lesion (Fig. 1).
The angulation effect provides an explanation of the roentgenographic images of the nasopalatine and the mental foramens. At
some angulations, particularly in roentgenograms of the nasopalatine area, the image produced is more cylindrical than circular. In
an occlusal film, made with the x-ray tube positioned on the
foramen, a more distinct circular shadow is obtained.
Artificial Lesions in Cancellous Bone
The cancellous bone of the mandible was drilled to various
depths and roentgenograms were made. No evidence of drilling
could be seen in the roentgenograms. More and more cancellous
structure was removed until there was a complete hollow within
the bone. All the bone marrow was removed up to the junction of
the innermost surface of the cortex and the cancellous portion of
the bone. Roentgenographic examination still failed to show
changes in the trabecular pattern of the bone or in its radiolucency.
When a bur eroded the innermost surface of the bone cortex a clear
and distinct radiolucent shadow appeared.
This evidence indicates that destruction of the cancellous portion of the bone does not produce changes discernible in roentgenograms taken under the conditions described. Changes become
manifest only if there is encroachment on the innermost surface of
the cortical bone or if there is frank perforation (Fig. 2 and 3).
Artificial Lesions in the Cortex and its Junction with
Cancellous Bone
A block section of the mandible was prepared in the manner
previously described. The cancellous bone up to the junction with
the cortex was removed and a roentgenogram was taken. Then the
bone was split in half mesiodistally, to yield separate lingual and
buccal plate sections, each consisting of cortex and trabeculae at
the junction. In the lingual section, the trabeculae at the junction
were scraped with a bone chisel. In the buccal section, the tissue at
the junction was left undisturbed. Roentgenograms of the section
with junction trabeculae reduced, showed loss of trabecular structure or pattern. The bone had a foamy appearance (Fig. 3,C).
Roentgenograms of the section with junction trabeculae intact
showed an intact trabecular pattern (Fig. 3,D).
A part of the separate buccal plate was sliced sagitally from the
outer surface with a diamond stone to remove the cortical bone
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FIG 2. A: After cancellous bone has been removed. There is no apparent evidence of any disturbance. B and C: Specimen of bone showing
amount of cancellous structure that was removed. Notched area is part of lingual canal. D: Side view shows absence of cancellous bone and
small amount of trabeculae present at the innermost surface of the bone cortex. Trabeculae are absent in notched area that forms lingual aspect
of mandibular canal. Roots of molar tooth articulate with the buccal cortex. Distal root appears to be within cancellous bone.
(Fig. 3,G,H,I). The other part was not cut so that comparative
effects could be observed on the same specimen. The cortex was
removed until the junction area of the cortical and cancellous bone
was exposed. The specimen thus produced was about 2 mm. thick.
Bur marks were then drilled in (1) the outer surface of the buccal
plate, (2) the inner surface of the junction area where the outer
buccal plate had not been removed and (3) the inner surface of the
junction area where the cortex had been removed.
Roentgenograms revealed definite and distinct areas of rarefaction where the bur had been drilled into the inner or outer surface
of the cortex. The bur mark was barely discernible in the junction
area although the bone was almost perforated. The trabecular
pattern was intact on both sides of the bone, but there was a
pronounced difference in the densities (Fig. 3,E and F).
From these experiments it may be inferred that areas of rarefaction manifest themselves only if there is erosion of the cortex from
the inner or outer surface or if there is frank perforation. The
trabeculae indicated on the roentgenograms are those which are
present at the junction of cortex and cancellous bone. If the
trabeculae in the interior of the cancellous bone or in the marrow
are destroyed, the difference of the trabecular pattern on the roentgenogram is not disturbed.
Trabecular Patterns in Roentgenograms of Intact and
Dissected Junction Areas
A mandible obtained from a 48 hour autopsy specimen was
sectioned and graded amounts of cortex were removed from a
portion of both lingual and buccal sides. Graded amounts of the
junction area also were removed so that a 3 mm. and a 2 mm.
thickness of cancellous bone remained.
In roentgenograms, the trabecular pattern and trabeculae could
be seen when the junction was not encroached upon. As more and
more of the junction area was removed, the bone became more
radiolucent and the trabeculae and the trabecular pattern became
FIG 3. The split halves of bone specimen in Figure 2 are shown
above. A: The lingual portion in which the trabeculae were scraped.
Foamy appearance can be seen in the roentgenogram, C; as a result
of reducing trabecular structure. Mandibular canal can also be seen.
B: Buccal portion in which the trabeculae were left intact. The
roentgenogram, D, was taken prior to drilling holes in trabecular
structure. E: Before removal of buccal plate up to the junction area.
Note that trabecular pattern can still be discerned. F: Showing
distinct areas of radiolucency as a result of drilling the cancellous
and cortical bone to the junction area from cancellous and cortical
sides. G, H and I: Specimens of bone illustrating side views, the
sagittal cut to the junction area and the bur mark drilled to junction
area. Note denuded areas of bone on root surface.
Vol. 29, No. 11, November 2003
FIG 4. Roentgenographic changes occurred as cortical bone was
removed mesial to first molar. When junction area of bone was
removed there was loss of trabecular pattern with hardly any visualization of cancellous structure. A: Before cortex was removed. B:
After removal of buccal plate to junction area. C: After removal of
lingual and buccal plate. Some junction area is present. D: Further
removal of junction area. E and F: Complete removal of junction
area. Views from lingual and buccal sides respectively. G: Specimen
before experiment. H and I: After experiment.
more difficult to discern (Fig. 4). The inference is that the trabecular pattern originates at the junction of the cortex and cancellous
bone.
Changes in trabecular pattern were the same whether bone was
removed from the junction area on the outer (cortical) side or
trabecular extensions were reduced in depth from the inner (cancellous) side at the junction area.
When the bone plate over dentigerous regions is removed completely, changes in pattern do not readily occur because the lamina
dura has junction areas of cancellous bone that affect the ultimate
trabecular appearance. This explanation is in accord with the
observations of Goldman, Millsap and Brenman.2
Cancellous bone is comparatively radiolucent and it is less
dense than cortex or alveolar bone proper. The alveolar bone
proper is dense because of its relatively smaller content of fibrillar
matter and large content of cementing substance. The cementing
substance is particularly dense because of its greater content of
calcium salt per unit volume.3 Superimposition of bone or a montage can increase the bone quantity to such an extent that the effect
of greater density is produced in the roentgenograms. This effect is
observed, for instance, in roentgenograms of the external and
internal oblique ridge region.
Other Observations
The nutrient canals could be seen roentgenographically only
when they were present in the bone cortex. For direct examination,
the foramens were located with endodontic reamers or files and
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705
FIG. 5. Numerous nutrient foramens are present in anterior portion of
mandible. On lingual surface foramens run in horizontal direction,
whereas on labial aspect they run in vertical direction. Reamers
perforate cortex and enter cancellous portion of bone.
then dissected out by removing the buccal or lingual plate of bone
with diamond stones. The nutrient canals were observed as small
tubes that traverse the cortex vertically on the buccal side. They
also traverse the cortex in a general horizontal direction (penetrating the bone at a 45 degree angle) on the lingual side in the region
of the genio tubercles as shown in Figure 5.
The mental foramen was most radiolucent when the central
beam was parallel with the orifice. At 180 degree angulation the
foramen appeared darker and more distinct; at 90 degrees it appeared less dark and more diffuse. The roentgenographic image of
the foramen opening varied from circular to funnel shaped.
The mandibular canal appeared more distinct and rarefied when
the cortex was removed. Examination of the specimens in some
instances showed the canal notched throughout the body of the
mandible in the molar and bicuspid region on the lingual side. In
other instances the canal was surrounded by a distinct layer of bone
plate suspended in the cancellous structure.
The roots, in several instances, appeared to be denuded of
buccal bone near the apical third (Fig. 3,F). This condition could
not be detected by means of roentgenograms. In many instances,
the bone was extremely thin in the apical areas on the buccal side.
Such denuded areas were not observed on the lingual side.
The teeth were encased completely in lamina dura which joined
with the outer cortex. The alveolus and the lamina dura are cortical
bone; the lamina dura therefore has a junction area in contact with
trabeculae. The presence of lamina dura accounts for the greater
amount of trabeculae found in dentigerous regions, especially
between the teeth and towards the alveolar ridge (Fig. 3,D).
Where the alveolar process was thick in the molar region and
there was a layer of cancellous bone between the lamina dura and
the cortical plate, trabeculae could be seen across the roots of the
teeth on the alveolar process. The bone appeared normal when the
teeth were extracted. Where the cortex was thin, or thick but with
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no intervening cancellous bone, the bone specimen had a foamy
appearance and trabeculae could not be seen in the region where
the teeth were extracted.
DISCUSSION
The assumption that results obtained with cadaver material are
valid for bone under clinical conditions receives support from the
experimental work of Ardran.4 He removed about one half in or of
the inner cancellous structure of vertebrae obtained from human
cadavers and found that the artificial lesions could be seen in
roentgenograms taken laterally. When water was put into the bone
cavities, the lesions could not be seen from any angle. In such
experiments water is added to produce an environment more
closely approximating the radiolucency of the tissue fluid associated with bone in vivo. Ardran’s work seems to indicate that
roentgenographic examination of bone in vivo would be even less
discriminating than it would be for specimens obtained from cadavers.
There is much histologic evidence of apical or periodontal
disease without roentgenographic manifestation. A review of Burket’s5 protocols of human necropsy material shows that in many
instances roentgenographic examination yielded negative results
when cancellous bone was diseased, and sometimes even when
cortex was involved—probably because only superficial cortex
was removed.
Goldman, Millsap and Brenman2 observed that the removal of
the buccal and lingual alveolar plates had no effect on the trabecular pattern around the teeth. This observation is not contrary to our
finding that trabecular patterns change if the innermost surface of
the cortex is removed. They did not attach any significance to the
junction area; they were describing the region around the teeth in
a dry specimen, whereas we were observing the body of the
mandible in a wet specimen. In and around the teeth there is more
cortex, crestal bone or lamina dura, and therefore more junction
surface to exhibit trabeculae. Where junction surface is present the
trabecular pattern does not change.
In view of the experimental evidence presented, early stages of
bone disease cannot be detected by means of roentgenograms. Also
the size of a rarefied area on the roentgenogram is not correlated
with the amount of tissue destruction. A small area of rarefaction
can be indicative of as much or more bone destruction as a large
rarefied area on the roentgenogram.
The afore-mentioned experiments emphasize that routine roentgenograms may not detect the presence of secondary neoplasms or
inflammation causing bone destruction. Whereas this point has
been recognized for minute lesions, it has not been realized that
Journal of Endodontics
large lesions may go undetected with the usual roentgenographic
procedures. Early metastatic carcinoma in bones often cannot be
detected by means of a roentgenographic examination, even
though the patient has bone pain. As the disease progresses it
destroys more of the marrow spaces, invades the cortex and produces lesions which show up on roentgenograms. Shackman and
Harrison6 have demonstrated that a patient may have extensive
metastases without demonstrable roentgenographic abnormality.
However, with tomography large areas in cancellous bone may be
detected by tomograms made in the correct plane.
Although similar experiments have not been made on the maxilla, similar findings could reasonably be expected.
SUMMARY
Mandibles from human cadavers were dissected and artificial
lesions were made to simulate pathological conditions. A comparison was made of roentgenogram with the actual sections of bone,
as observed visually.
It is evident from these experiments that, by the methods ordinarily employed for taking roentgenograms, lesions in cortical
bone can be detected roentgenographically only if there is perforation on the bone cortex, erosion from the inner surface of the
bone cortex, or extensive erosion or destruction from the outer
surface. Lesions in cancellous bone cannot be detected roentgenographically.
The apparent cancellous destruction that is manifest on roentgenograms is really an erosion of the innermost surface of the bone
cortex at the junction are between cortex and cancellous bone.
No defect can be visualized beyond the junction area as it
encroaches on the marrow spaces.
Extensive disease of bone, therefore may be present even when
there is no evidence of it on roentgenograms.
References
1. Seltzer S. The role of endodontics in complete mouth reconstruction.
J.A.D.A. 1955;51:320.
2. Goldman HM, Millsap JS, Brenman HS. Origin of registration of the
architectural pattern the lamina dura and the alveolar crest in the dental
radiograph. Oral Surg., Oral Med. & Oral Path. 1957;10:741.
3. Sicher H. Some principles of bone pathologies. J. Oral Surg. 1949;7:
104.
4. Ardran GM. Bone destruction not demonstrated by radiography. Brit. J.
Radiol. 1951;24:107.
5. Burket LW. Human necropsy protocols. Unpublished data.
6. Shackman R, Harrison CV. Occult metastases. Brit. J. Sur. 1948;35:
385.