0099-2399/92/1806-0275/$03.00/0 JOURNAL OF ENDODONTICS Copyright © 1992 by The American Association of Endodontists
Printed in U.S.A. VOL. 18, NO. 6, JUNE1992
Assessment of External Root Resorption Using Digital Subtraction Radiography Les H. Kravitz, DDS, MS, Donald A. Tyndall, DDS, MSPH, PhD, Charles P. Bagnell, PhD, and S. Brent Dove, DDS, MS
Digital subtraction radiography was investigated for its capability to detect and quantify experimentally produced external root resorptive defects in teeth. Using a long source to object X-ray technique and E-speed film, serial radiographs of teeth with artificial lesions in a dry human skull (soft tissue simulated) were obtained. Receiver operating characteristic analysis was used to evaluate the diagnostic performance for each imaging system (conventional versus subtraction). To explore the quantitative assessment potential of digital subtraction radiography, images were produced after sequential demineralization by HCI. The acid solution was analyzed for calcium concentration by atomic absorption spectrophotometry. Three-dimensional histogram quantification for each subtracted image was performed. In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography. In addition, digital subtraction radiography can provide quantification of experimentally produced external root resorptive defects.
form of root resorption on 98% of the posterior teeth and on 62% of the anterior teeth. These results were in agreement with an earlier study by Henry and Weinmann (4). While most cases of external resorption are repaired by cementum, when the resorption continues without early diagnosis and when the etiology is unknown, the prognosis is poor. Diagnosis of external root resorption is usually based on radiographic evaluation. However, operator bias is a factor when interpreting conventional radiographs. It has been reported that lack of agreement in radiographic interpretation exists between evaluators (5). There are even large discrepancies in the analysis of a single evaluator with himself at different time periods (6). Another factor complicating radiographic interpretation relates to the amount of mineral loss necessary for a change in the radiographic image. In two classic studies by Bender and Seltzer (7, 8), it was demonstrated that large amounts of cancellous bone of human jaws could be removed without creating changes detectable by conventional radiographic techniques. These authors concluded that bone lesions within the jaws could only be radiographically visualized when they also involved the cortical bone. Biological changes that occur due to disease are of diagnostic interest. These changes often occur against a background of unchanged anatomical structures. This stationary background can represent a complex radiographic pattern that conceals pathosis. "Noise" created by a stationary background pattern has been called both structured noise and anatomical noise (9), which distinguishes it from random noise. Structured noise creates a principal limitation on the visual detection capability of an observer interpreting radiographs produced by conventional techniques (10). Revesz et al. (9) found that detection of a radiological feature depends on both the feature itself and on the surrounding structures. These investigators also observed that lesion conspicuity depends directly on its contrast and inversely on the background complexity. This indicates that a reduction in background complexity increases lesion detectability. Digital subtraction radiology is a method for reducing structured noise by eliminating identical image features in serially obtained radiographs. This technique may be able to solve some of the problems associated with the radiographic diagnosis of external root resorption in patients being examined over a period of time.
External root resorption refers to the loss of cementum and/ or dentin from the roots of teeth and originates in the periodontal ligament. Exteraal resorption can be associated with periapical inflammation, luxation injuries, intentional replantation, nonvital bleaching, periodontal lesions, excessive mechanical or occlusal forces, impaction, tumors, cysts, corrosion of nonprecious posts, and bacterial invasion (1). External resorption may also be associated with systemic disturbances such as hyperparathyroidism, hypoparathyroidism, calcinosis, Gaucher's disease, Paget's disease, and Turner's syndrome (1). The phenomenon of multiple idiopathic root resorption has been described as well (2). A review of the literature reveals external root resorption is a commonly encountered phenomenon by dentists. Minor resorptions of the roots of teeth are universal. Seltzer et al. (3) examined several hundred teeth and observed some
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FIG 1. Laboratory set-up showing radiographic viewbox with a CCD camera overhead on the right, which displayed images on the RGB monitor on the left.
I=tG 2. Digital images were produced by superimposing two radiographs on the RGB monitor, subtracting the images, enhancing them by linear stretch across 256 gray levels, and then photographing them. A gamma correction program corrected for contrast differences between films. A real-time subtraction program was used so that when superimposition occurred, both images canceUed each other, leaving no discernible anatomical structures.
Success of the subtraction method is linked to imaging reproducibility. Reproducibility is dependent on projection, radiographic density, and contrast. It has been shown that differences in film density and contrast, within certain limits, can be corrected (11). Lack of reproducibility in positioning the patient has been reported to be the greatest obstacle in the application of the subtraction technique (12). Mechanical devices that secure a stable relationship between radiation source, object, and film provide a high degree of reproducibility. The proper use of occlusal stents (13) as well as cephalometric head stabilization methods (14) have been shown to considerably reduce sources of error attributable to variations in radiographic projection geometry. The extent to
which imaging geometry needs to be reproduced depends on the size of the changes studied, with smaller changes requiring higher reproducibility (12). Early diagnosis of external root resorption requires the identification of subtle dentin changes from longitudinally obtained radiographs. Digital subtraction radiography has been demonstrated to be a valuable tool for detecting small osseous changes between two radiographs (15). Unfortunately, 30 to 50% mineral loss must occur before such changes are evident in conventional radiographs. Ortman et al. (16) have demonstrated that digital subtraction radiography is capable of localizing a lesion with only 1 to 5 % of the bone mineral loss. This feature has allowed digital subtraction radiology to significantly improve one's diagnostic performance in the detection of small periodontal lesions (15). Kullendorff et al. (17) compared the diagnostic performance of conventional radiography with subtraction radiography in assessing periapical bone lesions. The periapical areas of dry human mandibles were radiographed and evaluated before and after the simulation of bone defects. The radioactive isotope J25I was used as a photon source for estimating alveolar bone loss. They found that subtraction radiography significantly increased the detectability of periapical osseous lesions compared with conventional radiography. Of particular interest was the finding that the subtraction technique was significantly superior in detecting lesions confined to cancellous bone. In a similar study, Tyndall et al. (18) compared the sensitivity of digital subtraction radiography with conventional radiography for detecting periapical defects in cortical and cancellous bone. Simulated bone lesions were created with various size round burs in a dry human mandible. A board of reviewers consistently demonstrated greater sensitivity in detecting cortical and cancellous bone changes for the digitally subtracted images. Of the two imaging systems tested, the digital subtraction system was capable of lowering the limit of detection for both cortical and cancellous bone defects. These results are in accordance with the findings of Kullendorffet al. (17).
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FiG 3. The top left image depicts a digitized conventional radiograph containing a #2 round bur defect. The bottom left image depicts a digital subtraction image containing the #2 round bur defect (arrow) that was produced from the digitized conventional radiograph above. The top right image depicts a digitized conventional radiograph containing a #8 round bur defect. The bottom right image depicts a digital subtraction image containing the #8 round bur defect (arrow) that was produced from the digitized conventional radiograph above.
1
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FiG 4. ROC curves from digital subtraction (DS) and conventional radiographic (CR) images for all defect sizes in facial and proximal locations. This represents the overall performance of each radiographic modality. The ROC curve is a graph of sensitivity, or the true-positive (TP) rate, against the complement of specificity, the false-positive (FP) rate, for all possible interpretations of a diagnostic test. The diagonal (arrow) represents a diagnostic performance at the pure chance level.
In addition to rendering important early diagnostic information, digital subtraction radiology has the potential to provide quantitative assessments of small bone density changes. Ruttimann and Webber (19) favor the use of bone wedges for quantitation. In their work, bone wedges, with known dimensions, were made from cortical bone and provided a means for calibrating lesion volumes in the subtrac-
tion images subsequently produced. In these investigations, the amount of bone removed was determined by weighing specimens on an analytic balance before and after defects were induced. The supplemental wedge of bone was placed in direct contact with the film packet and provided a means for calibrating lesion volumes in the subtraction images produced. Lesions were detected by observers viewing the radio-
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FIG 5. ROC curves from digital subtraction (DS) and conventional radiographic (CR) images for all defect sizes in the facial location. (TP) and P(FP) refer to true-positive percentage and false-positive percentage, respectively.
graphic subtraction image on a video monitor and then circling the lesion on a graphic overlay. Relative lesion volume was estimated as the product of the polygon area and the average gray level difference. Conversion to lesion volume in cubic millimeters was achieved using the bone wedge projection of the subtraction image. Projection of the bone wedge in each subtraction image allowed the calibration of gray levels into equivalent bone thickness. As these studies indicate, digital subtraction radiology may have the potential to be a sensitive technique for qualitatively and quantitatively evaluating external root resorption defects. To date, no literature on the application of digital subtraction radiography to external root resorption has been uncovered. MATERIALS AND M E T H O D S Detection of Artificially Induced Lesions of Varying Size and Position A long source to object distance (84 inches) technique was utilized to reduce the penumbra and increase the image sharpness (14, 18). The photon source was a Denar-Quint Sectograph with a rotating anode X-ray tube (Denar Corp., Anaheim, CA). Laser alignment beams (Gammex Lasers Inc., Milwaukee, WI) allowed for precise repositioning of the human skull. A dry human skull with removable teeth was used as the object to be imaged. Soft tissue was simulated by dental wax in one rope layer thickness. Artificial lesions were simulated by #V.-, 1, 2, 4, 6, and 8 round dental burs at two separate sites. Each lesion was created by drilling to the entire depth of the bur head. Lesions of each size were placed on two separate teeth. One was placed on a distal root surface and the other one was placed on a facial root surface. Lesion sites were constant since each bur removed tooth structure from the same two locations. Radiographs were obtained before lesion simulation and after each lesion was created by progressively larger dental burs. E-speed film (Eastman Kodak,
Inc., Rochester, NY) was used and processed according to the manufacturer's recommendations. The imaging parameters for each technique were the following: 75 kVp at 40 mA with 2.0 mm of aluminum equivalent filtration using a rotating anode X-ray source. A CCD Camera (Panasonic WV-C050; Panasonic Industrial Co., Secaucus, N J) was used to introduce the images into the digital subtraction system. Each film was placed on a masked viewbox of uniform intensity. The image processing was done on a Digital Equipment Corporation Computer (DEC LSI 11/73, RT 11; Digital Equipment Corp., Maynard, MA) with an Imaging Technology (512 System, ITEX/Q Software; Imaging Technology Inc., Woburn, MA) digital processing system. Digital images of each radiograph were produced by averaging 128 video frames (512 by 512 pixel matrix) and processing through two frame grabbers of 8 and 16 bits depth to produce a final image of 256 gray levels. A gamma correction program was used to correct for contrast differences between films (11). The digital subtraction image was generated in the following manner. Unaltered radiographs were stored in the computer's memory and displayed on the RGB monitor. The radiograph to be subtracted was imaged on the same monitor by placing it on the viewbox and under the CCD camera (Fig. 1). The real-time image was superimposed on the stored image of the original radiograph. A real-time subtraction program was used so that when superimposition occurred, the images canceled each other, leaving no discernible anatomical structures (Fig. 2). The second image (postlesion simulation) was then captured, gamma corrected, and subtracted from the first image (Fig. 3). After the images were subtracted, they were enhanced by a linear stretch algorithm which served to spread the narrow peak of gray levels (centered around 128) across all 256 gray levels. Both conventional images and subtracted images were photographed and then stored on hard disc memory. Four observers (one endodontist, two endodontic residents, and one general practitioner) independently evaluated each
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1 0.9. 0.8. 0.7" OoO-
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photographed image for simulated pathosis. Film readings were accomplished using previously reported methods (16). The observers were given a brief orientation session to become accustomed to reading photographed images of both conventional and subtracted films. Each photographed image was randomly displayed while the observers answered a questionnaire regarding the presence or absence of each simulated lesion. A confidence scale of 1 to 5 (1 = lesion definitely present, 2 = lesion probably present, 3 = uncertain, 4 = lesion probably not present, 5 = lesion definitely not present) was used for purposes of receiver operating characteristic (ROC) analysis. Since there was one simulated lesion on each film, 36 total films (three films of each of six bur hole sizes at two different locations), four observers, and one observer response per image, there was a
total of 144 possible responses per observer. This yielded a total of 576 observer responses for the four observers. Following the initial review by the observers, a second viewing of the films took place. In the second review, at least three days later, two observers viewed all of the subtracted images and the two other observers viewed all of the conventional images. This latter phase was used to determine interobserver and intraobserver reliability. ROC analysis was used to evaluate the diagnostic performance for each imaging system (conventional versus subtraction). ROC analysis provides the most meaningful approach to assess diagnostic performance since only ROC methodology distinguishes between the inherent diagnostic capacity of the observer's image interpretations, and any tendencies the observers may have to "underread" or "overread." The ROC
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FIG 8. ROC curves from digital subtraction (DS) and conventional radiographic (CR) images for #4, 6, and 8 defect sizes in facial and proximal locations. P(TP) and P(FP) refer to true-positive and false-positive percentage, respectively.
Quantitative Assessment
FIG 9. Teeth were sequentially demineralized, placed back into the skull, and radiogrephed. With an image grid superimposed within the RGB monitor, the exact location of the simulated lesion appeared on the grid such that three-dimensional gray level histograms of each lesion site were generated. The volume under the three-dimensional histogram was computed, which gave a weighted density of each lesion.
curve is a graph of sensitivity, or the true-positive rate, against the complement of specificity, the false-positive rate, for all possible interpretations of a diagnostic test (Figs. 4 to 8). Within the ROC illustrations, the diagonal represents a diagnostic performance at the pure chance level (arrow, Fig. 4). A higher ROC indicates greater discrimination capacity, while a lower ROC indicates less discrimination capacity. ROC analysis, positive predictive values, negative predictive values, sensitivity, and specificity were evaluated for conventional and subtraction images for both the distal aspect (separate values) and the facial aspect (separate values) of the teeth. All of the ROC analyses including the accompanying analytical statistics were performed at the University of Texas Health Science Center at San Antonio in the Department of Dental Diagnostic Sciences.
The preceding methodology with some modifications was applied to two new teeth in the same human skull to explore the quantitative assessment potential of digital subtraction radiography. The teeth were coated three times at 1-h intervals with a thin acid resistant layer (nail polish), except for the one area (2 x 2 mm) to be decalcified. Prealteration radiographs were obtained followed by demineralization of the teeth in a sequential fashion. Images were produced after each of 10 6 N hydrochloric acid baths. A pilot study determined the rate of decalcification so that meaningful images were generated over specified time intervals. Two teeth (one with a facial window and one with a proximal window) were placed in O-ring tubes containing 1 ml of 6 N HCI for 10-min intervals. At the end of each interval, the following occurred: The teeth were removed from the tubes, the tubes were placed on a vortex at setting 5 for 5 s, a 10-#1 sample was taken from each tube and placed in 16x 125-mm glass tubes containing 2 ml of 5% lanthanum oxide, and l0 ~zl of 6 N HC1 were added back to each of the original O-ring tubes. After the teeth were positioned back into the skull and a radiograph obtained, they were returned into their respective O-ring tubes for the next 10-min acid bath and the procedure was repeated. The acid solution was analyzed for calcium concentration using atomic absorption spectrophotometry (Perkin-Elmer 5100PC spectrometer with AS-51 auto sampler). This procedure was performed 10 times. The teeth were sequentially demineralized, placed back into the jaw, and radiographed. Subtractions (with enhancement) were performed for each film. The images were then registered on the RGB monitor with the registration grid. Each image was registered as an image grid superimposed within the RGB monitor. The exact location of the simulated lesion appeared on the grid such that three-dimensional gray level histograms of each lesion site were generated (Fig. 9). The volume under the threedimensional histogram was computed, which gave a weighted
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TABLE 1. Mean areas, P(A), under the ROC curves, SD, critical ratios (CR), and significance levels for comparisons between techniques ROC Curve
Technique
P(A)
SD
Fig. 4
Conventional Subtraction Conventional Subtraction Conventional Subtraction Conventional Subtraction Conventional Subtraction
0.73 0.87 0.84 0.87 0.68 0.87 0.61 0.77 0.84 0.97
0.06 0.05 0.06 0.06 0.09 0.06 0.08 0.08 0.06 0.03
Fig. 5 Fig. 6 Fig. 7 Fig. 8
CR
Significance Level
-1.64
p -- 0.05
-0.24
NS*
-1.60
p -< 0.05
-1.52
NS (p = 0.06)
-2.19
p < 0.01
* NS, not stgnificant.
TABLE 2. For each acid bath, the mean and total calcium removed, density values, and change in density values for facial and proximal lesion sites Ca2+ (mg/ml)*
No. of Acid Baths 0 1 2 3 4 5 6 7 8 9 10
X Total Caz+ (mg/ml)*
Density Values
ADensity Values
F'I"
P
F
P
F
P
F
P
0 0.25 0.36 0.61 1.53 2.48 2.40 2.66 3.03 3.45 3.96
0 0.69 1.03 1.94 3.01 3.52 4.00 2.79 4.66 4.57 5.24
0 0.25 0.61 1.22 2.75 5.23 7.63 10.29 13.32 16.77 20.73
0 0.69 1.72 3.66 6.67 10.19 14.19 16.98 21.64 26.21 31.45
126.98 126.62 126.43 125.64 125.15 124.52 124.01 123.84 123.06 121.35 119.57
126.53 126,21 125.98 125.06 123.19 121.03 118.34 116.58 112.74 109.65 105.46
0 0.36 0.19 0.79 0.49 0.63 0.51 0.17 0.78 1.71 1.78
0 0,32 0.23 0.92 1.87 2.16 2.69 1.76 3.84 3.09 4.19
* SD, < 0 . 0 1 .
1" F, facial; P, proximal.
density of each lesion in terms of density units. Three-dimensional histogram quantification for each subtracted image was then achieved. Best-fit regression lines were used to determine the relationship between subtracted image density units and the amount of calcium loss for each lesion. RESULTS The mean areas under each ROC curve, associated standard deviations, critical ratios, and significance levels for each technique are presented in Table 1. The overall performance of each radiographic modality for all lesion sizes in both locations is presented as mean ROC curves in Fig. 4. In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography (p _< 0.05). There was no statistically significant difference between the two techniques in detecting facial external root resorptive defects (Fig. 5); however, digital subtraction radiography was significantly superior to conventional radiography in detecting proximal external root resorptive defects (p _< 0.05) (Fig. 6). There was no statistically significant difference between the two techniques in detecting external root resorprive defects created by round bur #V2, 1, and 2 (p = 0.06), although digital subtraction performed better (Fig. 7). Digital
subtraction radiography was significantly superior to conventional radiography in detecting external root resorptive defects created by round bur #4, 6, and 8 as depicted in Fig. 8 (p _< O.Ol).
For each acid bath, the mean and total calcium removed, density values, and change in density values are reported for facial and proximal lesion sites (Table 2). Density values as a function of total calcium removed for facial and proximal lesions are plotted in Figs. 10 and 11, respectively. The slope and visual representation indicate a strong relationship exists between subtraction density units and calcium loss values, providing a possible method of quantifying digital subtraction radiography. DISCUSSION In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography. One factor contributing to digital subtraction's superiority is its ability to reduce structured noise, allowing detection to subtle changes that might otherwise be blended into the complex anatomical background of a conventional radiograph. Clinically, this may mean that dentin changes associated with external root resorption may be detected
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Density Units 128
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Fl,~ 10. Plot of density values as a function of total calcium removed for the facial lesion. Y = 126.51 - 0.31 x.
Density Units 130
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FIG 11. Plot of density values as a function of total calcium removed for the proximal lesion. Y = 127.28 - 0.67x.
earlier, allowing quicker intervention and thus improving the prognosis. For proximal external root resorptive lesions, digital subtraction radiography was significantly superior to conventional radiography; however, there was no difference between the two techniques in detecting facial external root resorptive defects. One of the hopes of this study was to show that digital subtraction radiography could in fact detect facial differences. In this study, digital subtraction radiography was not superior in the detection of single surface facial root defects. This may not be surprising when one considers the location of the lesion relative to the position of the root canal system. Superimposition of the radiolucent facial lesion over the radiolucent canal system reduced the observer's detection ability no matter which radiographic system was used. This was probably due to the reduction in contrast between the pathological lesion and normal canal anatomy, which made the defects considerably more difficult to identify. In reality, external root resorption usually involves more than one root surface, the extent depending on the degree of injury to the periodontal ligament. Although digital subtraction radiography was significantly superior to conventional radiography in detecting external root resorptive defects created by round bur sizes 4, 6, and 8, no statistically significant difference was found with the group of round burs #V2, 1, and 2. There are several possible explanations for this finding. First, while the defects created
by the 4, 6, and 8 burs were relatively larger than those created by the #V2, 1, and 2 burs, even the larger bur sizes created quite small defects. The smaller size burs may have produced defects too small to be reliably detected with either radiographic modality. Second, the most stringent criteria available were applied to the ROC curve area calculations and the subsequent statistical comparisons, namely, m a x i m u m likelihood and critical ratio. Digital subtraction performed better in the detection of round bur #l/z, 1, and 2 at the p = 0.06 level; however, this fell just short of the p _< 0.05 level used in this study. Possibly, if the #V2 round bur had been eliminated from this group, then round bur #1 and 2 might have been detected at a level considered significantly better using the subtraction technique. However, in this study, there were not enough replications of each bur size to do an individual analysis, which may have concealed the lower limit of detection that digital subtraction is capable of discerning (18). Future studies should include an individual analysis of each bur size so that the lower limits of detection can be determined. The ability to accurately quantify the changes associated with external root resorption is valuable. However, depending on the goal of the clinician, the question of whether to use a qualitative or quantitative assessment would have to be addressed on the basis of the individual case. From a clinical standpoint, a method of providing a more accurate quantitative measure of whether a pathological process is progressing
Vol. 18, No. 6, June 1992
or regressing should be a valuable tool. The strong relationship between subtracted image density units and calcium loss values as demonstrated in this study provides a possible method of quantifying external root resorption through the use of digital subtraction radiography. This approach to quantification has several limitations. First, this was a laboratory study and this method of quantification may not be clinically applicable. Second, the computer system used in this study may not have produced a universal calibration curve, as different systems may differ in the way density is measured. However, with further research, standard values could possibly be determined. Other investigators have projected bone wedges into subtraction images, allowing calibration of gray levels into equivalent bone thickness (19). While this provides a volume estimate of focal bone lesions, it does not provide information about the amount of bone demineralized. Another technique utilizes the radioactive isotope J2sI as a photon source for estimating alveolar bone loss (17). This technique also requires laboratory-controlled conditions and may not be clinically applicable. One obstacle in the use of digital subtraction is geometric reproducibility. The proper use of occlusal stents (13) as well as cephalometric head stabilization methods (14) has been shown to considerably reduce sources of error attributable to variations in radiographic projection geometry. The stent method requires stent fabrication from a customized impression of the occlusal surfaces of the teeth of interest. The stent is then coupled to a rigid device which is connected to the Xray source and film packet. While producing excellent results, this technique is costly, time consuming, and cumbersome. The advantage of cephalometric methods is that they eliminate the occlusal stent by the use of extraoral fixation. Another method, tomosynthetic reconstruction, is also a promising means of controlling geometry (20). With this technique, films are taken from eight different angles allowing three-dimensional reconstruction. Rigid geometry is not needed since radiographic angles can be calculated from any of the eight different films and the computer can match the geometry. This makes the imaging system clinically applicable to digital subtraction. In the near future, tomosynthetic imaging should be affordable for use in private practice. In this study, laser alignment beams allowed for precise repositioning. Laser alignment is a quick, reproducible, and very accurate technique, although its cost may be prohibitive in smaller private practices. The results of this study are based on artificial lesions created by a dental bur. Undoubtedly, changes within dentin that occur under biological conditions will differ from the type of defects produced in this study. The borders of artificially produced defects are relatively sharp compared with those of biological origin, which tend to be more diffuse. A more diffuse border could decrease radiographic detectability regardless of whether conventional radiographs or subtraction images are being interpreted. However, it is possible that the reduced ability to detect lesions would be even greater with conventional radiographs due to the extensive background noise present. Each of the observers in this study interpreted subtraction images for the first time. Despite this, overall observer performance was significantly better when subtraction images were interpreted compared with when conventional radio-
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graphs were interpreted. With even more experience, observer's diagnostic performance with subtracted images could conceivably improve. The subtraction technique does not change the radiation dose to the patient, as the technique is applied to serially obtained conventional radiographs. A personal computer with appropriate software and an adapted video camera can be used for image processing, thereby reducing the cost further and increasing its feasibility in private practice. Application of subtraction radiography to other clinical situations will make it useful in the endodontic practice. Other uses might include internal resorption, evaluation of periapical scars, and the monitoring of periapical bone healing following both conventional and surgical endodontic therapy. This study suggests that the application of digital subtraction radiography to radiographs of experimentally produced external root resorptive defects can render a superior diagnostic performance to that obtained with conventional radiography, although lesion location and size does influence system performance. Additionally, in a laboratory-controlled setting, digital subtraction radiography can provide quantification of experimentally produced external root resorption defects. Because many pathological changes of dental interest involve the root, subtraction radiography may be of value whenever it is desirable to evaluate these changes longitudinally. Digital subtraction radiography is a promising technique that is well suited to clinical situations to improve visual detectability of subtle changes without exposing the patient to additional radiation or discomfort. Future studies should explore other endodontic applications as well as the corroboration of laboratory findings to the clinical setting. This research was supported in part by the Research and Education Foundation of the American Association of Endodontists. The opinions, assertions, materials, and methodologies herein are private ones of the authors and are not to be construed as official or reflecting the views of the American Association of Endodontists or the Research and Education Foundation. The secretarial assistance of Ms. D. Lloyd in the preparation of this manuscript is gratefully acknowledged. The authors wish to thank Drs. S. Madison, J. Maroney, R. Stancill, and A. Sigurdsson for their participation. Dr. Kravitz is a former endodontic postgraduate student, School of Dentistry, University of North Carolina, Chapel Hill, NC, and is in private practice limited to endodontics in Atlanta, GA. Dr. Tyndall is a member of the Department of Diagnostic Sciences, School of Dentistry, University of North Carolina. Dr. Bagnell is a member of the Department of Pathology, School of Medicine, University of North Carolina. Dr. Dove is a member of the Department of Diagnostic Sciences, School of Dentistry, University of Texas Health Science Center at San Antonio, San Antonio, TX. Address requests for reprints to Dr. Donald Tyndall, Department of Diagnostic Sciences, School of Dentistry, University of North Carolina, Chapel Hill, NC 27514.
References 1. Cohen S, Burns RC (eds). Pathways of the pulp. 4th ed. St. Louis: CV Mosby, 1987:526. 2. Kerr DA, Courtney RM, Burkes EJ. Multiple idiopathic root resorption. Oral Surg 1970;29:552-65. 3. Seltzer S, Soltanoff W, Bender IB, Ziontz M. Biologic aspects of endodontics. I. Histologic observations of the anatomy and morphology of root apices and surrounding structures. Oral Surg 1966;22:375-85. 4. Henry JL, Weinmann JP. Pattern of resorption and repair of human cementum. J Am Dent Assoc 1951;42:270-90. 5. Goldman M, Pearson AH, Darzenta N. Endodontic success--who's reading the radiograph? Oral Surg 1972;33:432-7. 6. Goldman M, Pearson AH, Darzenta N. Reliability of radiographic interpretations. Oral Surg 1974;38:287-93.
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7. Bender IB, Seltzer S. Roentgenographic and direct observation of experimental lesions in bone.: I. J Am Dent Assoc 1961 ;62:152-60. 8. Bender IB, Seltzer S. Roentgenographic and direct observation of experimental lesions in bone: I1. J Am Dent Assoc 1961 ;62:708-16. 9. Revesz G, Dundel HL, Graber HA. The influence of structured noise on the detection of radiologic abnormalities. Invest Radio11974;9:479-86. 10. Kundel HL, Revesz G. Lesion conspicuity, structured noise and film reader error. Am J Roentgenol 1976;126:1233-8. 11. Ruttimann UE, Webber RL, Schmidt E. A robust digital method for film contrast correction in subtraction radiography. J Periodont Res 1986;21:48695. 12. Kinsey JH, Vanneli BD, Fontana RS, Miller WE, Johnson SA, Gilbert BK. Application of digital image change detection to diagnosis and follow-up of cancer involving the lungs. Proceedings of the Meeting on Application of Optical Instruments in Medicine 1975;70:99-112. 13. McHenry K, Hausmann E, Wikesjo U, Lyon-Bottenfield E, Chdstersson L. Methodological aspects and quantitative adjuncts to computerized subtraction radiography. J Periodont Res 1987;22:125-32. 14. Jeffcoat MK, Reddy MS, Webber RL, Williams RC, Ruttimann UE.
Journal of Endodontics Extraoral control of geometry for digital subtraction radiography. J Periodont Res 1987;22:396-402. 15. Grondahl HG, Grondahl K. Subtraction radiology for the diagnosis of periodontal bone lesions. Oral Surg 1983;55:208-13. 16. Ortman LF, Dunford R, McHenry K, Hausmann E. Subtraction radiography and computer assisted densitometric analyses of standardized radiographs. A comparison study with 12~1 absorptiometry. J Periodont Res 1985;20:644-51. 17. Kullendorff B, Grondahl K, Rohlin M, Henrikson CO. Subtraction radiography for the diagnosis of periapical bone lesions. Endod Dent Traumatol 1988;4:253-9. 18. Tyndall DA, Kapa SF, Bagnell CP. Digital subtraction radiography for detecting cortical and cancellous bone changes in the periapical region. J Endodon 1990;4:173-8. 19. Ruttimann UE, Webber RL. Volumetry of localized bone lesions by subtraction radiology. J Periodont Res 1987;22:215-6. 20. Van der Stelt PF, Webber RL, Ruttimann UE, Groenhuis RA. A procedure for reconstruction and enhancement of tomosynthetic images. Dentomaxillofac Radiol 1986; 15:11-8.
T h e W a y It W a s The pellagra "epidemic" involved over three million cases and 100,000 deaths between 1906 and 1940 in just the nine U.S. states which reported it. It totally disappeared when it was finally identified as a nutritional deficiency disease due to a lack of the B vitamin, nicotinic acid, and diet supplementation was adopted. Most text books attribute pellagra to a diet of the three m's: maize, meat, and molasses. But these were the primary food sources for many for decades before 1900--why did the epidemic first occur in 1906? Only recently (1987) has a theory been proposed. Nicotinic acid occurs naturally in the germ or embryo of corn kernels. But other enzymes in the germ cause enzymatic decay and spoilage. In 1901, a new method of milling corn by the Beall degerminator was introduced. The germ was removed in the milling process. Spoilage stopped, but pellagra began. Pellagra is associated with poverty and restricted diet; yet very rural populations too poor to afford "store bought" meal were spared. They still ground their corn in water-driven stone mills and thus ate undegerminated meal. And thus the notion of healthier "stone ground" flour was born.
Cosby Newell
Printed in U.S.A. VOL. 18, NO. 6, JUNE1992
Assessment of External Root Resorption Using Digital Subtraction Radiography Les H. Kravitz, DDS, MS, Donald A. Tyndall, DDS, MSPH, PhD, Charles P. Bagnell, PhD, and S. Brent Dove, DDS, MS
Digital subtraction radiography was investigated for its capability to detect and quantify experimentally produced external root resorptive defects in teeth. Using a long source to object X-ray technique and E-speed film, serial radiographs of teeth with artificial lesions in a dry human skull (soft tissue simulated) were obtained. Receiver operating characteristic analysis was used to evaluate the diagnostic performance for each imaging system (conventional versus subtraction). To explore the quantitative assessment potential of digital subtraction radiography, images were produced after sequential demineralization by HCI. The acid solution was analyzed for calcium concentration by atomic absorption spectrophotometry. Three-dimensional histogram quantification for each subtracted image was performed. In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography. In addition, digital subtraction radiography can provide quantification of experimentally produced external root resorptive defects.
form of root resorption on 98% of the posterior teeth and on 62% of the anterior teeth. These results were in agreement with an earlier study by Henry and Weinmann (4). While most cases of external resorption are repaired by cementum, when the resorption continues without early diagnosis and when the etiology is unknown, the prognosis is poor. Diagnosis of external root resorption is usually based on radiographic evaluation. However, operator bias is a factor when interpreting conventional radiographs. It has been reported that lack of agreement in radiographic interpretation exists between evaluators (5). There are even large discrepancies in the analysis of a single evaluator with himself at different time periods (6). Another factor complicating radiographic interpretation relates to the amount of mineral loss necessary for a change in the radiographic image. In two classic studies by Bender and Seltzer (7, 8), it was demonstrated that large amounts of cancellous bone of human jaws could be removed without creating changes detectable by conventional radiographic techniques. These authors concluded that bone lesions within the jaws could only be radiographically visualized when they also involved the cortical bone. Biological changes that occur due to disease are of diagnostic interest. These changes often occur against a background of unchanged anatomical structures. This stationary background can represent a complex radiographic pattern that conceals pathosis. "Noise" created by a stationary background pattern has been called both structured noise and anatomical noise (9), which distinguishes it from random noise. Structured noise creates a principal limitation on the visual detection capability of an observer interpreting radiographs produced by conventional techniques (10). Revesz et al. (9) found that detection of a radiological feature depends on both the feature itself and on the surrounding structures. These investigators also observed that lesion conspicuity depends directly on its contrast and inversely on the background complexity. This indicates that a reduction in background complexity increases lesion detectability. Digital subtraction radiology is a method for reducing structured noise by eliminating identical image features in serially obtained radiographs. This technique may be able to solve some of the problems associated with the radiographic diagnosis of external root resorption in patients being examined over a period of time.
External root resorption refers to the loss of cementum and/ or dentin from the roots of teeth and originates in the periodontal ligament. Exteraal resorption can be associated with periapical inflammation, luxation injuries, intentional replantation, nonvital bleaching, periodontal lesions, excessive mechanical or occlusal forces, impaction, tumors, cysts, corrosion of nonprecious posts, and bacterial invasion (1). External resorption may also be associated with systemic disturbances such as hyperparathyroidism, hypoparathyroidism, calcinosis, Gaucher's disease, Paget's disease, and Turner's syndrome (1). The phenomenon of multiple idiopathic root resorption has been described as well (2). A review of the literature reveals external root resorption is a commonly encountered phenomenon by dentists. Minor resorptions of the roots of teeth are universal. Seltzer et al. (3) examined several hundred teeth and observed some
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FIG 1. Laboratory set-up showing radiographic viewbox with a CCD camera overhead on the right, which displayed images on the RGB monitor on the left.
I=tG 2. Digital images were produced by superimposing two radiographs on the RGB monitor, subtracting the images, enhancing them by linear stretch across 256 gray levels, and then photographing them. A gamma correction program corrected for contrast differences between films. A real-time subtraction program was used so that when superimposition occurred, both images canceUed each other, leaving no discernible anatomical structures.
Success of the subtraction method is linked to imaging reproducibility. Reproducibility is dependent on projection, radiographic density, and contrast. It has been shown that differences in film density and contrast, within certain limits, can be corrected (11). Lack of reproducibility in positioning the patient has been reported to be the greatest obstacle in the application of the subtraction technique (12). Mechanical devices that secure a stable relationship between radiation source, object, and film provide a high degree of reproducibility. The proper use of occlusal stents (13) as well as cephalometric head stabilization methods (14) have been shown to considerably reduce sources of error attributable to variations in radiographic projection geometry. The extent to
which imaging geometry needs to be reproduced depends on the size of the changes studied, with smaller changes requiring higher reproducibility (12). Early diagnosis of external root resorption requires the identification of subtle dentin changes from longitudinally obtained radiographs. Digital subtraction radiography has been demonstrated to be a valuable tool for detecting small osseous changes between two radiographs (15). Unfortunately, 30 to 50% mineral loss must occur before such changes are evident in conventional radiographs. Ortman et al. (16) have demonstrated that digital subtraction radiography is capable of localizing a lesion with only 1 to 5 % of the bone mineral loss. This feature has allowed digital subtraction radiology to significantly improve one's diagnostic performance in the detection of small periodontal lesions (15). Kullendorff et al. (17) compared the diagnostic performance of conventional radiography with subtraction radiography in assessing periapical bone lesions. The periapical areas of dry human mandibles were radiographed and evaluated before and after the simulation of bone defects. The radioactive isotope J25I was used as a photon source for estimating alveolar bone loss. They found that subtraction radiography significantly increased the detectability of periapical osseous lesions compared with conventional radiography. Of particular interest was the finding that the subtraction technique was significantly superior in detecting lesions confined to cancellous bone. In a similar study, Tyndall et al. (18) compared the sensitivity of digital subtraction radiography with conventional radiography for detecting periapical defects in cortical and cancellous bone. Simulated bone lesions were created with various size round burs in a dry human mandible. A board of reviewers consistently demonstrated greater sensitivity in detecting cortical and cancellous bone changes for the digitally subtracted images. Of the two imaging systems tested, the digital subtraction system was capable of lowering the limit of detection for both cortical and cancellous bone defects. These results are in accordance with the findings of Kullendorffet al. (17).
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FiG 3. The top left image depicts a digitized conventional radiograph containing a #2 round bur defect. The bottom left image depicts a digital subtraction image containing the #2 round bur defect (arrow) that was produced from the digitized conventional radiograph above. The top right image depicts a digitized conventional radiograph containing a #8 round bur defect. The bottom right image depicts a digital subtraction image containing the #8 round bur defect (arrow) that was produced from the digitized conventional radiograph above.
1
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FiG 4. ROC curves from digital subtraction (DS) and conventional radiographic (CR) images for all defect sizes in facial and proximal locations. This represents the overall performance of each radiographic modality. The ROC curve is a graph of sensitivity, or the true-positive (TP) rate, against the complement of specificity, the false-positive (FP) rate, for all possible interpretations of a diagnostic test. The diagonal (arrow) represents a diagnostic performance at the pure chance level.
In addition to rendering important early diagnostic information, digital subtraction radiology has the potential to provide quantitative assessments of small bone density changes. Ruttimann and Webber (19) favor the use of bone wedges for quantitation. In their work, bone wedges, with known dimensions, were made from cortical bone and provided a means for calibrating lesion volumes in the subtrac-
tion images subsequently produced. In these investigations, the amount of bone removed was determined by weighing specimens on an analytic balance before and after defects were induced. The supplemental wedge of bone was placed in direct contact with the film packet and provided a means for calibrating lesion volumes in the subtraction images produced. Lesions were detected by observers viewing the radio-
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Journal of Endodontics
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FIG 5. ROC curves from digital subtraction (DS) and conventional radiographic (CR) images for all defect sizes in the facial location. (TP) and P(FP) refer to true-positive percentage and false-positive percentage, respectively.
graphic subtraction image on a video monitor and then circling the lesion on a graphic overlay. Relative lesion volume was estimated as the product of the polygon area and the average gray level difference. Conversion to lesion volume in cubic millimeters was achieved using the bone wedge projection of the subtraction image. Projection of the bone wedge in each subtraction image allowed the calibration of gray levels into equivalent bone thickness. As these studies indicate, digital subtraction radiology may have the potential to be a sensitive technique for qualitatively and quantitatively evaluating external root resorption defects. To date, no literature on the application of digital subtraction radiography to external root resorption has been uncovered. MATERIALS AND M E T H O D S Detection of Artificially Induced Lesions of Varying Size and Position A long source to object distance (84 inches) technique was utilized to reduce the penumbra and increase the image sharpness (14, 18). The photon source was a Denar-Quint Sectograph with a rotating anode X-ray tube (Denar Corp., Anaheim, CA). Laser alignment beams (Gammex Lasers Inc., Milwaukee, WI) allowed for precise repositioning of the human skull. A dry human skull with removable teeth was used as the object to be imaged. Soft tissue was simulated by dental wax in one rope layer thickness. Artificial lesions were simulated by #V.-, 1, 2, 4, 6, and 8 round dental burs at two separate sites. Each lesion was created by drilling to the entire depth of the bur head. Lesions of each size were placed on two separate teeth. One was placed on a distal root surface and the other one was placed on a facial root surface. Lesion sites were constant since each bur removed tooth structure from the same two locations. Radiographs were obtained before lesion simulation and after each lesion was created by progressively larger dental burs. E-speed film (Eastman Kodak,
Inc., Rochester, NY) was used and processed according to the manufacturer's recommendations. The imaging parameters for each technique were the following: 75 kVp at 40 mA with 2.0 mm of aluminum equivalent filtration using a rotating anode X-ray source. A CCD Camera (Panasonic WV-C050; Panasonic Industrial Co., Secaucus, N J) was used to introduce the images into the digital subtraction system. Each film was placed on a masked viewbox of uniform intensity. The image processing was done on a Digital Equipment Corporation Computer (DEC LSI 11/73, RT 11; Digital Equipment Corp., Maynard, MA) with an Imaging Technology (512 System, ITEX/Q Software; Imaging Technology Inc., Woburn, MA) digital processing system. Digital images of each radiograph were produced by averaging 128 video frames (512 by 512 pixel matrix) and processing through two frame grabbers of 8 and 16 bits depth to produce a final image of 256 gray levels. A gamma correction program was used to correct for contrast differences between films (11). The digital subtraction image was generated in the following manner. Unaltered radiographs were stored in the computer's memory and displayed on the RGB monitor. The radiograph to be subtracted was imaged on the same monitor by placing it on the viewbox and under the CCD camera (Fig. 1). The real-time image was superimposed on the stored image of the original radiograph. A real-time subtraction program was used so that when superimposition occurred, the images canceled each other, leaving no discernible anatomical structures (Fig. 2). The second image (postlesion simulation) was then captured, gamma corrected, and subtracted from the first image (Fig. 3). After the images were subtracted, they were enhanced by a linear stretch algorithm which served to spread the narrow peak of gray levels (centered around 128) across all 256 gray levels. Both conventional images and subtracted images were photographed and then stored on hard disc memory. Four observers (one endodontist, two endodontic residents, and one general practitioner) independently evaluated each
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1 0.9. 0.8. 0.7" OoO-
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photographed image for simulated pathosis. Film readings were accomplished using previously reported methods (16). The observers were given a brief orientation session to become accustomed to reading photographed images of both conventional and subtracted films. Each photographed image was randomly displayed while the observers answered a questionnaire regarding the presence or absence of each simulated lesion. A confidence scale of 1 to 5 (1 = lesion definitely present, 2 = lesion probably present, 3 = uncertain, 4 = lesion probably not present, 5 = lesion definitely not present) was used for purposes of receiver operating characteristic (ROC) analysis. Since there was one simulated lesion on each film, 36 total films (three films of each of six bur hole sizes at two different locations), four observers, and one observer response per image, there was a
total of 144 possible responses per observer. This yielded a total of 576 observer responses for the four observers. Following the initial review by the observers, a second viewing of the films took place. In the second review, at least three days later, two observers viewed all of the subtracted images and the two other observers viewed all of the conventional images. This latter phase was used to determine interobserver and intraobserver reliability. ROC analysis was used to evaluate the diagnostic performance for each imaging system (conventional versus subtraction). ROC analysis provides the most meaningful approach to assess diagnostic performance since only ROC methodology distinguishes between the inherent diagnostic capacity of the observer's image interpretations, and any tendencies the observers may have to "underread" or "overread." The ROC
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Kravitz et al. 1!
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Quantitative Assessment
FIG 9. Teeth were sequentially demineralized, placed back into the skull, and radiogrephed. With an image grid superimposed within the RGB monitor, the exact location of the simulated lesion appeared on the grid such that three-dimensional gray level histograms of each lesion site were generated. The volume under the three-dimensional histogram was computed, which gave a weighted density of each lesion.
curve is a graph of sensitivity, or the true-positive rate, against the complement of specificity, the false-positive rate, for all possible interpretations of a diagnostic test (Figs. 4 to 8). Within the ROC illustrations, the diagonal represents a diagnostic performance at the pure chance level (arrow, Fig. 4). A higher ROC indicates greater discrimination capacity, while a lower ROC indicates less discrimination capacity. ROC analysis, positive predictive values, negative predictive values, sensitivity, and specificity were evaluated for conventional and subtraction images for both the distal aspect (separate values) and the facial aspect (separate values) of the teeth. All of the ROC analyses including the accompanying analytical statistics were performed at the University of Texas Health Science Center at San Antonio in the Department of Dental Diagnostic Sciences.
The preceding methodology with some modifications was applied to two new teeth in the same human skull to explore the quantitative assessment potential of digital subtraction radiography. The teeth were coated three times at 1-h intervals with a thin acid resistant layer (nail polish), except for the one area (2 x 2 mm) to be decalcified. Prealteration radiographs were obtained followed by demineralization of the teeth in a sequential fashion. Images were produced after each of 10 6 N hydrochloric acid baths. A pilot study determined the rate of decalcification so that meaningful images were generated over specified time intervals. Two teeth (one with a facial window and one with a proximal window) were placed in O-ring tubes containing 1 ml of 6 N HCI for 10-min intervals. At the end of each interval, the following occurred: The teeth were removed from the tubes, the tubes were placed on a vortex at setting 5 for 5 s, a 10-#1 sample was taken from each tube and placed in 16x 125-mm glass tubes containing 2 ml of 5% lanthanum oxide, and l0 ~zl of 6 N HC1 were added back to each of the original O-ring tubes. After the teeth were positioned back into the skull and a radiograph obtained, they were returned into their respective O-ring tubes for the next 10-min acid bath and the procedure was repeated. The acid solution was analyzed for calcium concentration using atomic absorption spectrophotometry (Perkin-Elmer 5100PC spectrometer with AS-51 auto sampler). This procedure was performed 10 times. The teeth were sequentially demineralized, placed back into the jaw, and radiographed. Subtractions (with enhancement) were performed for each film. The images were then registered on the RGB monitor with the registration grid. Each image was registered as an image grid superimposed within the RGB monitor. The exact location of the simulated lesion appeared on the grid such that three-dimensional gray level histograms of each lesion site were generated (Fig. 9). The volume under the threedimensional histogram was computed, which gave a weighted
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TABLE 1. Mean areas, P(A), under the ROC curves, SD, critical ratios (CR), and significance levels for comparisons between techniques ROC Curve
Technique
P(A)
SD
Fig. 4
Conventional Subtraction Conventional Subtraction Conventional Subtraction Conventional Subtraction Conventional Subtraction
0.73 0.87 0.84 0.87 0.68 0.87 0.61 0.77 0.84 0.97
0.06 0.05 0.06 0.06 0.09 0.06 0.08 0.08 0.06 0.03
Fig. 5 Fig. 6 Fig. 7 Fig. 8
CR
Significance Level
-1.64
p -- 0.05
-0.24
NS*
-1.60
p -< 0.05
-1.52
NS (p = 0.06)
-2.19
p < 0.01
* NS, not stgnificant.
TABLE 2. For each acid bath, the mean and total calcium removed, density values, and change in density values for facial and proximal lesion sites Ca2+ (mg/ml)*
No. of Acid Baths 0 1 2 3 4 5 6 7 8 9 10
X Total Caz+ (mg/ml)*
Density Values
ADensity Values
F'I"
P
F
P
F
P
F
P
0 0.25 0.36 0.61 1.53 2.48 2.40 2.66 3.03 3.45 3.96
0 0.69 1.03 1.94 3.01 3.52 4.00 2.79 4.66 4.57 5.24
0 0.25 0.61 1.22 2.75 5.23 7.63 10.29 13.32 16.77 20.73
0 0.69 1.72 3.66 6.67 10.19 14.19 16.98 21.64 26.21 31.45
126.98 126.62 126.43 125.64 125.15 124.52 124.01 123.84 123.06 121.35 119.57
126.53 126,21 125.98 125.06 123.19 121.03 118.34 116.58 112.74 109.65 105.46
0 0.36 0.19 0.79 0.49 0.63 0.51 0.17 0.78 1.71 1.78
0 0,32 0.23 0.92 1.87 2.16 2.69 1.76 3.84 3.09 4.19
* SD, < 0 . 0 1 .
1" F, facial; P, proximal.
density of each lesion in terms of density units. Three-dimensional histogram quantification for each subtracted image was then achieved. Best-fit regression lines were used to determine the relationship between subtracted image density units and the amount of calcium loss for each lesion. RESULTS The mean areas under each ROC curve, associated standard deviations, critical ratios, and significance levels for each technique are presented in Table 1. The overall performance of each radiographic modality for all lesion sizes in both locations is presented as mean ROC curves in Fig. 4. In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography (p _< 0.05). There was no statistically significant difference between the two techniques in detecting facial external root resorptive defects (Fig. 5); however, digital subtraction radiography was significantly superior to conventional radiography in detecting proximal external root resorptive defects (p _< 0.05) (Fig. 6). There was no statistically significant difference between the two techniques in detecting external root resorprive defects created by round bur #V2, 1, and 2 (p = 0.06), although digital subtraction performed better (Fig. 7). Digital
subtraction radiography was significantly superior to conventional radiography in detecting external root resorptive defects created by round bur #4, 6, and 8 as depicted in Fig. 8 (p _< O.Ol).
For each acid bath, the mean and total calcium removed, density values, and change in density values are reported for facial and proximal lesion sites (Table 2). Density values as a function of total calcium removed for facial and proximal lesions are plotted in Figs. 10 and 11, respectively. The slope and visual representation indicate a strong relationship exists between subtraction density units and calcium loss values, providing a possible method of quantifying digital subtraction radiography. DISCUSSION In overall performance for detecting experimentally produced external root resorption, digital subtraction radiography was found to be significantly superior to conventional radiography. One factor contributing to digital subtraction's superiority is its ability to reduce structured noise, allowing detection to subtle changes that might otherwise be blended into the complex anatomical background of a conventional radiograph. Clinically, this may mean that dentin changes associated with external root resorption may be detected
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FIG 11. Plot of density values as a function of total calcium removed for the proximal lesion. Y = 127.28 - 0.67x.
earlier, allowing quicker intervention and thus improving the prognosis. For proximal external root resorptive lesions, digital subtraction radiography was significantly superior to conventional radiography; however, there was no difference between the two techniques in detecting facial external root resorptive defects. One of the hopes of this study was to show that digital subtraction radiography could in fact detect facial differences. In this study, digital subtraction radiography was not superior in the detection of single surface facial root defects. This may not be surprising when one considers the location of the lesion relative to the position of the root canal system. Superimposition of the radiolucent facial lesion over the radiolucent canal system reduced the observer's detection ability no matter which radiographic system was used. This was probably due to the reduction in contrast between the pathological lesion and normal canal anatomy, which made the defects considerably more difficult to identify. In reality, external root resorption usually involves more than one root surface, the extent depending on the degree of injury to the periodontal ligament. Although digital subtraction radiography was significantly superior to conventional radiography in detecting external root resorptive defects created by round bur sizes 4, 6, and 8, no statistically significant difference was found with the group of round burs #V2, 1, and 2. There are several possible explanations for this finding. First, while the defects created
by the 4, 6, and 8 burs were relatively larger than those created by the #V2, 1, and 2 burs, even the larger bur sizes created quite small defects. The smaller size burs may have produced defects too small to be reliably detected with either radiographic modality. Second, the most stringent criteria available were applied to the ROC curve area calculations and the subsequent statistical comparisons, namely, m a x i m u m likelihood and critical ratio. Digital subtraction performed better in the detection of round bur #l/z, 1, and 2 at the p = 0.06 level; however, this fell just short of the p _< 0.05 level used in this study. Possibly, if the #V2 round bur had been eliminated from this group, then round bur #1 and 2 might have been detected at a level considered significantly better using the subtraction technique. However, in this study, there were not enough replications of each bur size to do an individual analysis, which may have concealed the lower limit of detection that digital subtraction is capable of discerning (18). Future studies should include an individual analysis of each bur size so that the lower limits of detection can be determined. The ability to accurately quantify the changes associated with external root resorption is valuable. However, depending on the goal of the clinician, the question of whether to use a qualitative or quantitative assessment would have to be addressed on the basis of the individual case. From a clinical standpoint, a method of providing a more accurate quantitative measure of whether a pathological process is progressing
Vol. 18, No. 6, June 1992
or regressing should be a valuable tool. The strong relationship between subtracted image density units and calcium loss values as demonstrated in this study provides a possible method of quantifying external root resorption through the use of digital subtraction radiography. This approach to quantification has several limitations. First, this was a laboratory study and this method of quantification may not be clinically applicable. Second, the computer system used in this study may not have produced a universal calibration curve, as different systems may differ in the way density is measured. However, with further research, standard values could possibly be determined. Other investigators have projected bone wedges into subtraction images, allowing calibration of gray levels into equivalent bone thickness (19). While this provides a volume estimate of focal bone lesions, it does not provide information about the amount of bone demineralized. Another technique utilizes the radioactive isotope J2sI as a photon source for estimating alveolar bone loss (17). This technique also requires laboratory-controlled conditions and may not be clinically applicable. One obstacle in the use of digital subtraction is geometric reproducibility. The proper use of occlusal stents (13) as well as cephalometric head stabilization methods (14) has been shown to considerably reduce sources of error attributable to variations in radiographic projection geometry. The stent method requires stent fabrication from a customized impression of the occlusal surfaces of the teeth of interest. The stent is then coupled to a rigid device which is connected to the Xray source and film packet. While producing excellent results, this technique is costly, time consuming, and cumbersome. The advantage of cephalometric methods is that they eliminate the occlusal stent by the use of extraoral fixation. Another method, tomosynthetic reconstruction, is also a promising means of controlling geometry (20). With this technique, films are taken from eight different angles allowing three-dimensional reconstruction. Rigid geometry is not needed since radiographic angles can be calculated from any of the eight different films and the computer can match the geometry. This makes the imaging system clinically applicable to digital subtraction. In the near future, tomosynthetic imaging should be affordable for use in private practice. In this study, laser alignment beams allowed for precise repositioning. Laser alignment is a quick, reproducible, and very accurate technique, although its cost may be prohibitive in smaller private practices. The results of this study are based on artificial lesions created by a dental bur. Undoubtedly, changes within dentin that occur under biological conditions will differ from the type of defects produced in this study. The borders of artificially produced defects are relatively sharp compared with those of biological origin, which tend to be more diffuse. A more diffuse border could decrease radiographic detectability regardless of whether conventional radiographs or subtraction images are being interpreted. However, it is possible that the reduced ability to detect lesions would be even greater with conventional radiographs due to the extensive background noise present. Each of the observers in this study interpreted subtraction images for the first time. Despite this, overall observer performance was significantly better when subtraction images were interpreted compared with when conventional radio-
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graphs were interpreted. With even more experience, observer's diagnostic performance with subtracted images could conceivably improve. The subtraction technique does not change the radiation dose to the patient, as the technique is applied to serially obtained conventional radiographs. A personal computer with appropriate software and an adapted video camera can be used for image processing, thereby reducing the cost further and increasing its feasibility in private practice. Application of subtraction radiography to other clinical situations will make it useful in the endodontic practice. Other uses might include internal resorption, evaluation of periapical scars, and the monitoring of periapical bone healing following both conventional and surgical endodontic therapy. This study suggests that the application of digital subtraction radiography to radiographs of experimentally produced external root resorptive defects can render a superior diagnostic performance to that obtained with conventional radiography, although lesion location and size does influence system performance. Additionally, in a laboratory-controlled setting, digital subtraction radiography can provide quantification of experimentally produced external root resorption defects. Because many pathological changes of dental interest involve the root, subtraction radiography may be of value whenever it is desirable to evaluate these changes longitudinally. Digital subtraction radiography is a promising technique that is well suited to clinical situations to improve visual detectability of subtle changes without exposing the patient to additional radiation or discomfort. Future studies should explore other endodontic applications as well as the corroboration of laboratory findings to the clinical setting. This research was supported in part by the Research and Education Foundation of the American Association of Endodontists. The opinions, assertions, materials, and methodologies herein are private ones of the authors and are not to be construed as official or reflecting the views of the American Association of Endodontists or the Research and Education Foundation. The secretarial assistance of Ms. D. Lloyd in the preparation of this manuscript is gratefully acknowledged. The authors wish to thank Drs. S. Madison, J. Maroney, R. Stancill, and A. Sigurdsson for their participation. Dr. Kravitz is a former endodontic postgraduate student, School of Dentistry, University of North Carolina, Chapel Hill, NC, and is in private practice limited to endodontics in Atlanta, GA. Dr. Tyndall is a member of the Department of Diagnostic Sciences, School of Dentistry, University of North Carolina. Dr. Bagnell is a member of the Department of Pathology, School of Medicine, University of North Carolina. Dr. Dove is a member of the Department of Diagnostic Sciences, School of Dentistry, University of Texas Health Science Center at San Antonio, San Antonio, TX. Address requests for reprints to Dr. Donald Tyndall, Department of Diagnostic Sciences, School of Dentistry, University of North Carolina, Chapel Hill, NC 27514.
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7. Bender IB, Seltzer S. Roentgenographic and direct observation of experimental lesions in bone.: I. J Am Dent Assoc 1961 ;62:152-60. 8. Bender IB, Seltzer S. Roentgenographic and direct observation of experimental lesions in bone: I1. J Am Dent Assoc 1961 ;62:708-16. 9. Revesz G, Dundel HL, Graber HA. The influence of structured noise on the detection of radiologic abnormalities. Invest Radio11974;9:479-86. 10. Kundel HL, Revesz G. Lesion conspicuity, structured noise and film reader error. Am J Roentgenol 1976;126:1233-8. 11. Ruttimann UE, Webber RL, Schmidt E. A robust digital method for film contrast correction in subtraction radiography. J Periodont Res 1986;21:48695. 12. Kinsey JH, Vanneli BD, Fontana RS, Miller WE, Johnson SA, Gilbert BK. Application of digital image change detection to diagnosis and follow-up of cancer involving the lungs. Proceedings of the Meeting on Application of Optical Instruments in Medicine 1975;70:99-112. 13. McHenry K, Hausmann E, Wikesjo U, Lyon-Bottenfield E, Chdstersson L. Methodological aspects and quantitative adjuncts to computerized subtraction radiography. J Periodont Res 1987;22:125-32. 14. Jeffcoat MK, Reddy MS, Webber RL, Williams RC, Ruttimann UE.
Journal of Endodontics Extraoral control of geometry for digital subtraction radiography. J Periodont Res 1987;22:396-402. 15. Grondahl HG, Grondahl K. Subtraction radiology for the diagnosis of periodontal bone lesions. Oral Surg 1983;55:208-13. 16. Ortman LF, Dunford R, McHenry K, Hausmann E. Subtraction radiography and computer assisted densitometric analyses of standardized radiographs. A comparison study with 12~1 absorptiometry. J Periodont Res 1985;20:644-51. 17. Kullendorff B, Grondahl K, Rohlin M, Henrikson CO. Subtraction radiography for the diagnosis of periapical bone lesions. Endod Dent Traumatol 1988;4:253-9. 18. Tyndall DA, Kapa SF, Bagnell CP. Digital subtraction radiography for detecting cortical and cancellous bone changes in the periapical region. J Endodon 1990;4:173-8. 19. Ruttimann UE, Webber RL. Volumetry of localized bone lesions by subtraction radiology. J Periodont Res 1987;22:215-6. 20. Van der Stelt PF, Webber RL, Ruttimann UE, Groenhuis RA. A procedure for reconstruction and enhancement of tomosynthetic images. Dentomaxillofac Radiol 1986; 15:11-8.
T h e W a y It W a s The pellagra "epidemic" involved over three million cases and 100,000 deaths between 1906 and 1940 in just the nine U.S. states which reported it. It totally disappeared when it was finally identified as a nutritional deficiency disease due to a lack of the B vitamin, nicotinic acid, and diet supplementation was adopted. Most text books attribute pellagra to a diet of the three m's: maize, meat, and molasses. But these were the primary food sources for many for decades before 1900--why did the epidemic first occur in 1906? Only recently (1987) has a theory been proposed. Nicotinic acid occurs naturally in the germ or embryo of corn kernels. But other enzymes in the germ cause enzymatic decay and spoilage. In 1901, a new method of milling corn by the Beall degerminator was introduced. The germ was removed in the milling process. Spoilage stopped, but pellagra began. Pellagra is associated with poverty and restricted diet; yet very rural populations too poor to afford "store bought" meal were spared. They still ground their corn in water-driven stone mills and thus ate undegerminated meal. And thus the notion of healthier "stone ground" flour was born.
Cosby Newell
