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Roentgenographic and Direct Observation of Experimental Lesions in Bone: I†
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 702
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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.
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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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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
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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.
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 702
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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.
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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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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.