Radiography of the mandible prior to endosseous implant treatment
Localization of the mandibular canal and
assessment of trabecular bone
AKADEMISK AVHANDLING
som for avlaggande av odontologie doktorsexamen vid Odontologiska Fakulteten, Lunds Universitet, offentligen kommer att forsvaras i aulan, Tandvardshogskolan, Malmo fredagen den 12 april, kl 09.15, 1996.
av
Christina Lindh
leg. tandlakare
VQL 2 6 NS 0 1 Organization Document name LUND UNIVERSITY DOCTORAL DISSERTATION Department of 0r41 Radiology Date of issue Faculty of Odontology 1996-04-12 S-214 21 Malmb, Sweden CODEN: SE-LU0DD5/0D0R-96/100+ 139 P Authors) Sponsoring organization Christina Lindh Title and subtitle Radiography of the mandible prior to endosseous implant treatment. Localization of the mandibular canal and assessment of trabecular bone.
Abstract Mandibular autopsy specimens were examined with different radiographic techniques in order to evaluate the visibility of the mandibular canal and the measurement accuracy of distances related to the mandibular canal. Hypocycloidal, spiral and computed tomography (CT) were superior to periapical and panoramic radiography in visualising the mandibular canal. The tomographic techniques were more accurate when measurements of distances related to the mandibular canal were performed. No difference in measurement accuracy was found between the tomographic techniques. Concerning visibility of the mandibular canal, interobserver agreement was lowest for periapical radiography and highest for CT. Intraobserver agreement was moderate or good for all techniques. A high interobserver variation was found for measurability of distances related to the mandibular canal. The trabecular bone tissue in mandibular autopsy specimens was studied concerning different characteristics. Quantitative measurements of bone mass were performed and expressed as bone mineral density and trabecular bone volume. There was a significant correlation between these two measures. Significant inter- and intra- mandibular variations were found for bone mineral density as well as for trabecular bone volume. A classification system to be used prior to implant treatment, based on the trabecular pattern in periapical radiographs, was proposed. The proposed classification system was compared with the 2 classification system proposed by Lekholm and Zarb (1985) and evaluated in terms of diagnostic accuracy and observer performance. The highest accuracy was found when the proposed classification system was Ss used together with reference images. The diagnostic accuracy of the classification system devised by Lekholm and Zarb (1985) was not possible to evaluate. Interobserver agreement was similar with and without reference images but higher than for the Lekholm and Zarb (1985) classification. Intraobserver HI agreement was comparable for the classification systems. Keywords mandible; endosseous implantation; radiography; panoramic radiography, tomography; bone mineral content; bone mineral density; trabecular pattern
Classification system and/or index terms (if any)
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ISSN and key tide ISBN 0348-6672 91-628-1954-2 Recipient's notes Number of pages 139 Price
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Signature . r ( Date Radiography of the mandible prior to endosseous implant treatment
Localization of the mandibular canal and
assessment of trabecular bone
Christina Lindh
From
the Department of
Oral Radiology
Faculty of Odontology
Lund University, Malmo, Sweden
1996 ISSN 0348 6672
ISBN 91-628-1954-2
Graphic Systems AB, MalmO, Sweden, 1996 CONTENTS
Page
PREFACE 5
DEFINITIONS AND ABBREVIATIONS 6
INTRODUCTION 7
AIMS 11
MATERIAL AND METHODS 12
RESULTS 24
DISCUSSION 29
CONCLUSIONS 36
ACKNOWLEDGEMENTS 38
REFERENCES 40
APPENDIX Paper 1 47 Paper II 53 Paper III 61 Paper IV 69 Paper V 89 Paper VI Ill
NEXT PAGE(S) left BLANK PREFACE
This thesis is based on the following papers, which will be referred to in the text by their Roman numerals:
I Lindh C, Petersson A. Radiologic examination for location of the mandibular canal: a comparison between panoramic radiography and conventional tomography. Int J Oral Maxillofac Implants 1989; 4: 249-53.
II Lindh C, Petersson A, Klinge B. Visualisation of the mandibular canal by different radiographic techniques. Clin Oral Impl Res 1992; 3: 90-7.
HI Lindh C, Petersson A, Klinge B. Measurements of distances related to the mandibular canal in radiographs. Clin Oral Impl Res 1995; 6: 96-103.
IV Lindh C, Nilsson M, Klinge B, Petersson A. Quantitative computed tomography of trabecular bone in the mandible. Dentomaxillofac Radiol 1996; 25. In press.
V Lindh C, Petersson A, Klinge B, Nilsson M. Trabecular bone volume and bone mineral density in the mandible. Dentomaxillofac Radiol Submitted.
VI Lindh C, Petersson A, Rohlin M. Assessment of the trabecular pattern prior to endosseous implant treatment. Diagnostic outcome of periapical radiography in the mandible. Accepted for publication in Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996. DEFINITIONS
Bone mass = quantitative description of the bone tissue that can be measured as bone mineral density and trabecular bone volume
Bone mineral density = the average amount of mineral expressed as 3 Ca10(PO4)6(OH)2 per unit volume of bone tissue (mg/cm )
Trabecular bone volume = the fractional area of trabeculae expressed as the percentage of trabeculae within a given volume of bone tissue
Trabecular bone pattern = qualitative description of the bone tissue representing the spatial distribution of trabeculae within the bone tissue
ABBREVIATIONS
CT = computed tomography
QCT = quantitative computed tomography
ROI = region of interest
BMD = bone mineral density
TBV = trabecular bone volume
TTBV = total trabecular bone volume INTRODUCTION
Edentulousness may not only imply impaired oral function and loss of alveolar bone but is often also accompanied by reduced self-confidence (Blomberg and Lindquist
1983). The standard of living has increased over the last decades and many people are no longer willing to accept removable partial or full dentures (Chen and Scharer
1993). Efforts have been made to provide edentulous patients with fixed bridges, attached to dental implants (Izikowitz 1968, Adell et al. 1970, Natiella et al. 1972).
Dental implants may be classified according to their position and are defined as endosseous when they are inserted into the bone tissue in the jaws and as subperiostal when inserted with immediate penetration of the oral soft tissues and placed under the periosteum overlying the cortical bone. Endosseous implants are the most common form of implants in use (Worthington 1988). The term osseointegration was coined by
Branemark and is defined as a direct structural and functional connection between ordered, living bone and the surface of a load-carrying implant (Branemark 1985).
The simultaneous publication of a 15-year follow-up report of patients who had been treated with osseointegrated implants (Adell et al. 1981) together with the Toronto conference in 1982 (Zarb 1983) led to rapid and widespread acceptance of the osseointegration concept (Albrektsson 1988).
In the treatment of the completely edentulous patient, implants are most commonly placed in the anterior section of the maxilla or mandible. In partially edentulous patients, however, implants are commonly needed in the posterior section of each arch, reflecting the pattern of tooth loss. Placement is more complex in the posterior parts of the jaws. In the mandible, fixture placement posterior to the mental foramina is associated with a certain risk of trauma to the inferior alveolar nerve. Criteria for success proposed by Schnitman and Shulman (1979), Me Kinney et al. (1984), Albrektsson et al. (1986) and Smith and Zarb (1989), include absence of paresthesia or violation of the mandibular canal. Few patients with partially edentulous jaws were treated during the early period (1961-1981) of clinical research and application of osseointegrated implants (Jemt et al. 1989). The placement of osseointegrated implants posterior to the mental foramen was regarded as experimental, since no five- year results had been published for such implants (Albrektsson et al. 1986). However, in some follow-up reports dealing with completely edentulous patients, paresthesia or pain associated with injuries to the mental nerve were reported (Henry et al. 1986,
Albrektsson 1988).
Implant treatment planning requires teamwork and the radiologist is expected to provide information about the amount of bone available for implant placement. In mandibular posterior sections, the location of the mandibular canal is of utmost importance as measurements of the height of the alveolar crest, superior to the canal, must be made prior to implant placement. If this height is not sufficient, implants can be placed buccally or lingually to the canal, but location of the mandibular canal in a bucco-lingual view is then a prerequisite. Periapical and panoramic radiographs show the mandibular canal in a two-dimensional direction, but tomography is needed to obtain a three-dimensional representation. The inferior neuro-vascular bundle is, however, not always surrounded by a defined cortical wall (Olivier 1927, Carter and
Keen 1971) and, according to Worth (1975), there are wide variations in the radiographic appearance of the mandibular canal. Total absence of demonstrable canals in radiographed mandibles has also been reported (Littner et al. 1986, Heasman
1988). No studies have been performed comparing the ability of different radiographic techniques to visualise the mandibular canal and the possibility of measuring distances related to the canal and what results various observers may arrive at. Failure of osseointegration should be regarded as the ultimate complication of implant treatment (Worthington et al. 1987) and bone quality is often mentioned as a factor of great importance to the treatment outcome after dental implant treatment (Albrektsson et al. 1988, Engquist et al. 1988, Berman 1989). However, bone quality is a comprehensive term and there is no clear definition to be found in the literature.
Adequate implant treatment is considered to be dependent on the fixture's being primarily stable at installation (Lekholm et al. 1985). Stability is possible to achieve if the fixture reaches a cortical layer of bone. This is, however, only possible to a limited extent in the jaws and consequently the trabecular bone tissue must be of great importance. Several trabecular bone tissue characteristics probably influence osseointegration.
The mandible seems to be the bone within the human skeleton that is most exposed to a severe decrease in the amount of mineralised bone tissue throughout life (von
Wowern 1986) and mineral measurements of the mandibular bone tissue have been performed (von Wowern 1985 a,b). Several methods are available for bone mineral measurements (Tothill 1989). The use of CT has developed rapidly during recent years and it is the only method, besides photon scattering methods, that offers the possibility of measuring the mineral content of the trabecular bone independently of surrounding cortical bone. The principle of bone mineral determination by CT is that a thin transverse slice through the body is analysed and the bone mineral content is calculated using the linear attenuation coefficient (Hounsfield unit) in different parts of the object (Jonson 1988). The use of Hounsfield units measured at CT has been discussed as an indicator of bone density in selecting patients for implant therapy
(Laney 1986, Me Givney et al. 1986, Berman 1989). None of the above authors has, however, defined the term bone quality or described a method for mineral measurements with the aidofCT. The trabecular part of the bone is named after the thin bony trabeculae that form it and their particular arrangement may be one characteristic influencing the bone quality.
Wide normal variations of the trabecular pattern of the jaws have been found (Parfitt
1962). The classification of jaw bone quality proposed by Lekholm and Zarb (1985) is the most widely used in connection with implant treatment. This classification is based
on a description of "the thickness of the layer of cortical bone and the density of the trabecular bone" (Lekholm and Zarb, 1985). Illustrations of cross-sections of bone
show the different bone quality classes, where high density trabecular bone shows a dense trabecular pattern and low density trabecular bone a sparse trabecular pattern.
Visualisation of a cross-section of the jaws can only be achieved by tomography. The low resolution of tomography makes the trabecular pattern hard to detect. Periapical
radiography is a widely used technique and suggested as part of the routine
radiographic examination prior to implant treatment and the trabecular pattern can be visualised with this technique. No investigation has been performed to evaluate the possibility of using periapical radiographs in the preoperative radiographic evaluation of bone quality.
10 AIMS
The studies on mandibles presented in the separate papers (I-VI) of this thesis were carried out with the following specific aims:
1. To investigate the visibility of the mandibular canal using different radiographic
techniques (1,11).
2. To determine the accuracy of measurement of the distance between the superior
border of the mandibular canal and the alveolar crest and the distance between
the mandibular base and the inferior border of the mandibular canal for different
radiographic techniques (III).
3. To evaluate the observer performance of the detectability of the mandibular canal
and of the measurability of distances related to the canal (1,11,111).
4. To measure the mineral content of the trabecular bone using QCT (IV).
5. To investigate the correlation between the bone mineral density and the
trabecular bone volume (V).
6. To construct a classification system for the assessment of the trabecular pattern
with the aid of periapical radiography and to compare the diagnostic outcome of
this classification system and that proposed by Lekholm and Zarb (1985) (VI).
11 MATERIAL AND METHODS
Patients (I)
The patients were selected from the file of patients that were examined at the
Department of Oral Radiology, Lund University, Malmo, Sweden. They were referred to the department by oral surgeons and prosthodontists for the purpose of examining the posterior part(s) of the mandible prior to endosseous implant treatment. Fifteen consecutive patients, aged 41-72 years, were examined by panoramic radiography.
In addition, the posterior edentulous mandibular regions (n=23) of these patients were examined by hypocycloidal tomography.
Autopsy specimens (II-VI)
From individuals aged 62 - 94 years (mean 79 years) who before death had donated their bodies to research, 15 mandibular autopsy specimens were taken. There was no history of disease or treatment that may have altered bone metabolism. The whole body was fixed using a mortal perfusion technique and thereafter the mandibles were removed, degloved and post-fixed in neutralised buffered formalin solution. This method preserves the structure and tissues, including fat. The number and regions of mandibular sections examined in the different studies are shown in Table I.
After the radiographic examination, the mandibles were mounted in a precision saw
(Exakt Apparatebau, Nordstedt, Germany) and the anterior and posterior sections were cut into thin bone slices. The sections from six mandibles were cut alternately into 2 mm and 5 mm thick slices and those from nine mandibles into 2 mm thick slices.
12 Table I. Radiographic technique used for examination of anterior and posterior sections from 15 mandibular autopsy specimens, performed assessments and number of observers in Papers II-VI.
Paper No and region Radiographic Performed No of ofmandibular technique assessment observers sections
II 12 posterior Periapical Visualisation of 2 radiography mandibular canal Panoramic radiography, OP5/Scanora Tomography, hypocycloidal/spiral Computed tomography Contact radiography
ni 12 posterior Panoramic Measurements of 4 radiography, distances related OP5/Scanora to the mandibular Tomography, canal hypocycloidal/spiral Computed tomography Contact radiography
IV 6 anterior Computed Bone mineral 1 27 posterior tomography density
V 6 anterior Contact Trabecular 1 16 posterior radiography bone volume
VI 6 anterior Periapical Classification of 7 17 posterior radiography trabecular pattern
13 Radiographic techniques (I-VI)
Altogether five imaging techniques were used (Table I). An additional filter of 3 mm aluminium was attached to the X-ray tube to compensate for the lack of soft tissue at all examinations except CT and periapical radiography in Paper VI. In the latter study, an 0.5 cm thick acrylic plate was placed buccally of the mandibular section in order to compensate for the missing soft tissue. In order to obtain reference points, tantalum pins (length 1.5 mm, 0 0.5 mm) were inserted at the buccal side of each edentulous section (Figure 1). In the posterior sections, a tantalum pin was inserted just beneath the mental foramen and two other pins 1 and 2 cm distally to the foramen. In the anterior sections, one tantalum pin was inserted 1 cm on each side of the midline.
Periapical radiography
In Paper II two periapical radiographs and in Paper VI one periapical radiograph were taken of a mandibular section. A dental X-ray machine (Siemens Heliodent, Erlangen,
Germany) operating at 70 kVp (Paper II) or at 60 kVp (Paper VI) was used together with films of speed group E (Ektaspeed, Eastman Kodak Co, Rochester, N.Y., USA).
All films were placed parallel to the alveolar crest and the mandibular body.
Panoramic radiography
Two different panoramic machines were used, Orthopantomograph Model OP5
(Siemens, Bensheim, Germany) with Titan 2 HS screens (Siemens) and Scanora
(Soredex, Helsinki, Finland) with Trimax T6 screens (3M, X-ray Products/3M, St
14 •. ,._>-"• • ••*
D c )3 B A
tantalum pin
Figure 1. Schematic drawing of a mandible illustrating the sites (A - F) where observations of the mandibular canal (Paper II) and measurements of distances (Dl - D3) were performed (Paper III). The regions outlined in the middle and on the right side mark the regions where measurements of BMD, TBV and TTBV were performed (Papers IV and V) and where assessments of the trabecular pattern were made (Paper VI).
Paul, MN, USA). The voltage setting was 55-60 kV and 63 kV for the
Orthopantomograph and the Scanora, respectively.
Hypocycloidal tomography
The apparatus used was a Polytome U (Massiot/Philips, Paris, France) with a Siemens
Bi 125/30/50R tube, nominal focus size 0.6 mm x 0.6 mm and focus-film distance 1.50 m. A hypocycloidal motion was used with a tomographic angle of 48 and without a grid. The circular collimator had a diameter of 1.5 cm, resulting in a field size with a
15 diameter of 6.5 cm. Exposure data for the patient examinations (Paper I) were 60 kV and 500-600 mAs and for the autopsy specimens (Papers II and III) 55-67 kV and 80-
120 mAs. A multi-film cassette with four pairs of rare-earth screens and four films was used, and the distance between the depicted layers was 3.3 mm (Petersson and
Gratt 1985). Cross-sections, about 1.3 mm thick, perpendicular to the buccal and lingual bone plates of the posterior sections of the mandibles, were obtained at 3.3 mm intervals from the mental foramen to about 2.5 cm posterior to the foramen. The patients (Paper I) were seated with the head immobilised in a cephalostat. The
cephalostat was rotated and the patient positioned so that the tomographic plane gave perpendicular cross-sectional cuts of the posterior mandibular section.
Spiral tomography
Spiral tomography was performed with the Scanora X-ray machine. Cross-sections
(4 mm thick) perpendicular to the buccal and lingual bone plates were obtained of the posterior sections of the mandibles at intervals of 4 mm from the mental foramen to
about 2.5 cm posterior to the foramen. Four exposures per film were obtained with a field size of 7 cm x 10.2 cm.
Computed tomography (CT)
CT images were obtained with a Somatom DRG scanner (Siemens, Erlangen,
Germany) at 125 kV and 230 mAs using a standard convolution kernel. Contiguous
2 mm thick slices were taken in the coronal plane perpendicular to the buccal and lingual bone plates. Images were obtained from the mental foramen, where a tantalum pin was inserted, to about 0.5 cm posterior to the most distally inserted tantalum pin.
In addition to this, 2 mm thick axial slices were taken and reformatted CT images were
16 made from the axial scans. The reformatted CT images were made at the sites of the reference points perpendicular to the buccal and lingual bone plates. The reformatted images were used only for investigation of the visibility of the mandibular canal (Paper n).
Contact radiography
The thin bone slices, cut from the anterior and posterior mandibular sections, were radiographed with a Siemens PH 125/100 R tube, focus-film distance 0.7 m, or with a
Siemens Bi 150/30/52 R 100 tube, focus-film distance 0.75 m. During exposure, the sections were placed in direct contact with the film packet (Strukturix D7, Agfa
Gevaert, Belgium). The films were developed manually and a contact radiograph of every thin bone slice was obtained.
Localization of the mandibular canal (I-HI)
Visibility of the mandibular canal
The visibility of the mandibular canal in the panoramic radiographs and tomograms of patients (Paper I) was interpreted at the mental foramen as well as 1 and 2 cm distally to the foramen. The radiographs of the autopsy specimens (Paper II) were interpreted according to the visibility of the mandibular canal at the sites of the tantalum pins, between the pins and 0.5 cm distally to the most posteriorly inserted pin. In both investigations, the visibility of the canal was assessed according to a three-point scale as definitely not visible, of questionable visibility and clearly visible.
17 The radiographs in Paper I were interpreted independently by two oral radiologists. In
cases of disagreement the radiographs were reexamined and the two observers made a joint decision. The same two observers as above and one periodontologist assessed
the visibility of the mandibular canal in Paper II. Two of the three observers made the
observations twice. The visibility of the mandibular canal was judged by majority
decision. In cases where none of the observers had awarded the same score, a new
interpretation and a joint decision was made. The contact radiographs that served as
gold standard in Paper II were assessed by the three observers at the same time and a
unanimous decision about the visibility of the canal was taken.
Measurements of distances related to the mandibular canal
The same sites as in Paper II were used for measurements of distances related to the
mandibular canal in Paper III. Four observers performed measurements of the
distances related to the mandibular canal in Paper III. Two oral radiologists, one
periodontologist and one general practitioner who had experience of implant treatment
and/or treatment planning served as observers. One of the oral radiologists
participated in both Papers II and III. Prior to all observations, guidelines were
discussed and in addition written instructions were given. The following distances
were measured: between the superior border of the mandibular canal and the alveolar
crest (Dl), the height of the mandibular canal (D2) and between the mandibular base
and the inferior border of the mandibular canal (D3) (Figure 1, page 15).
Measurements on the CT images were, however, performed only by three observers,
all oral radiologists. Measurements on contact radiographs performed by one observer
served as the gold standard. In the contact radiographs where the mandibular canal
was not surrounded by a cortical border, histological sections, obtained from the thin
18 bone slices, were examined by light microscopy in order to localize the neuro-vascular bundle.
Bone mass measurements (IV,V)
Bone mineral density
A ROI was defined when moving a cursor on a tablet enclosing the trabecular bone, 1-
2 mm from the inner margin of the cortex, in the CT images obtained perpendicular to the buccal and lingual bone plates. The CT scanner was calibrated according to the method described by Nilsson et al. (1988) for determination of bone mineral density
(BMD) using a) BMD simulating substances samples placed in a phantom simulating the skull and b) the same samples placed in free air. The calibration equation could be described by the equation
3 4 2 BMD (mg/cm ) = 0.960 (Humean + 14) - 2.3 x 10" (Humean + 14)
where Humean is the mean Hounsfield value in the trabecular part of the mandible. Air calibration, with no object in the gantry, was always performed immediately before scanning. BMD was expressed as the amount of calcium hydroxyapatite in mg/cm3 within the trabecular bone tissue. Measurements were performed of both anterior and posterior sections in six of the 15 mandibles.
Trabecular bone volume
A contact radiograph was placed on a viewing box with fixed light intensity in front of a Hamamatsu CCD video camera C 4742, 1018 x 1000 pixels, with a Canon TV
19 Zoom lens V6 x 16, 16 -100 mm, 1:1.9. The image was digitised in a frame grabber hardware card (Synoptics Sprynt using intel i860 RISC chip at 25 MHz offering a
50 MFlops processing rate) installed in a Dell 433/T microcomputer. Two Mitsubishi
Diamond Pro 17 screens (1280 x 1024 pixels) showing 255 greylevels were connected to the computer. Two ROIs were defined; one automatically transferred from the CT image of the same bone slice and one outlined when moving a cursor on a tablet enclosing the trabecular part of the bone as close as possible to the inner margin of the cortex (Figure 2). An image processing programme (Semper 6 Plus, Synoptics Ltd,
Cambridge, UK) was used for measurements of the trabecular bone volume. A coarse threshold was set manually so that all features were registered to define the trabeculae within the ROI. The image analyser then automatically applied local thresholding to the source image, whereby the threshold was set to half the height value at all transition points between background and foreground. The TBV within the ROI was given as the fractional area percentage of trabeculae. It was described as the TBV in the ROI transferred from the CT image and as the TTBV in the other ROI (Figure 2).
Measurements were performed on both anterior and posterior sections in six of the nine mandibles
Figure 2. The sizes of the two ROIs outlined on the contact radiographs. The ROI to the left is transferred from the CT image enclosing the TBV and the ROI to the right from that enclosing the TTBV.
20 Assessment of the trabecular pattern in periapical radiographs (VI)
Twenty-six periapical radiographs from 23 edentulous mandibular sections were assessed according to the trabecular pattern (three radiographs were excluded from assessment as they served as reference images and six radiographs were duplicated in order to increase the material). Three classifications were used and seven observers, four oral radiologists, two periodontologists and one oral surgeon, assessed the radiographs. Three observers assessed all radiographs a second time after three weeks. The three classifications were:
A. A written classification describing the trabecular pattern as
* dense trabeculation
* alternating dense and sparse trabeculation
* sparse trabeculation.
B. The written classification described above together with reference radiographs presenting each of the three classes.
C. The classification proposed by Lekholm and Zarb (1985), consisting of four classes. The observers had the schematic drawings and the written description of this classification at hand.
The reference images were validated on the basis of the measurements of the TTBV as described in Paper V. The gold standard was based on the mean TTBV value of each of the 23 mandibular sections.
21 Statistical methods and data analysis (I-VI)
The statistical significance of differences between ratings given for the two radiographic methods, panoramic radiography and hypocycloidal tomography, in
Paper I was tested with the Wilcoxon signed rank test.
Differences between the measurements on the radiographs and on the contact radiographs for the distances Dl and D3 were calculated in Paper III.
In Papers IV and V, differences in BMD, TBV and TTBV between mandibles and between sections within mandibles were investigated using analysis of variance with repeated measurements. Differences between TTBV and TBV were calculated for all mandibles using the same type of analysis. In Paper V, the correlation between TBV and BMD as well as between TTBV and BMD within mandibles and for the total material was calculated.
Measurement precision
The measurements of BMD were performed twice on 20 CT images (Paper IV) and the measurements of TBV and TTBV were performed twice on 20 contact radiographs (Paper V), by the same observer. The measurement precision (s) was calculated as s = Vzd2/2n, where d was the difference between duplicate measurement and n was the number of duplicate measurements.
22 Diagnostic outcome
The analysis of diagnostic accuracy in Paper VI was based on a gold standard, which in turn was based on the mean TTBV of each of 23 mandibular sections. The accuracy of the classification with reference images was compared with that of the classification without reference images. For each of the ten observations and each of the 26 images, it was checked whether the assessments according to the classification with or without reference images were closest to the gold standard as defined by the mean TTBV values.
Interobserver agreement in Paper I and inter- and intraobserver agreement in Paper II were calculated with two different measures: the overall agreement, which concerns the total number of sites where the observers agree, and using the Kappa index as described by Cohen (1960). With respect to both inter- and intraobserver agreement in Paper VI, two different measures were calculated. Interobserver agreement was described by the estimated probability that two observers agreed when assessing the same image and intraobserver agreement as the estimated probability that the same observer agreed with himself/herself when assessing the same radiograph twice.
Interobserver agreement was also calculated as Kappa index for several observers
(Fleiss 1971) and intraobserver agreement as Kappa index according to Cohen (1960).
Kappa index was interpreted according to Landis and Koch (1977).
23 RESULTS
Localization of the mandibular canal (MI)
Visibility of the mandibular canal
The results concerning the frequency of clearly visible canals at the observation sites in
Papers I and II and the sites where measurements of the distance between the superior border of the canal and the alveolar crest were possible to perform in Paper III are shown in Table II. Direct CT showed the highest number of clearly visible canals apart from contact radiography, but this technique is not clinically applicable and served as a gold standard. Periapical radiography showed a low number of clearly visible canals, while the lowest number was found in reformatted CT images.
Hypocycloidal and spiral tomography were superior to panoramic radiography in visualising the mandibular canal. In 7% of the sites it was not possible to identify a cortical outline of the mandibular canal on the contact radiographs.
Measurements of distances related to the mandibular canal
The observers had difficulties in identifying the superior border of the mandibular canal and reported unmeasurable distances to a high degree (Table II). The number of sites where all observers performed measurements of the distance between the superior border of the mandibular canal and the alveolar crest was at most 44 out of 71 possible sites for direct CT. Spiral and hypocycloidal tomography showed a higher number of sites (18 and 12, respectively) where all observers performed measurements of the above distance, than the two panoramic techniques with OP5 and Scanora (6 and 4, respectively).
24 Table n. Percentage of clearly visible mandibular canals (Papers I and II) and of sites where it was possible to measure the distance between the superior border of the mandibular canal and the alveolar crest (Paper III). The figures in Papers I and II are based on a joint decision by two observers (Paper I) or a majority decision by three observers (Paper II). In Paper III the figures are based on the mean numbers of measurements performed by four observers.
Radiographic technique Visibility (%) Possible to measure (%)
Patients Autopsy Autopsy specimens specimens
Periapical radiography - 25
Panoramic radiography, 25 24 44 OP5
Panoramic radiography, - 25 32 Scanora
Hypocycloidal tomography, 52 47 47 Polytome
Spiral tomography, - 53 53 Scanora
Computed tomography - 75 77 coronal plane
Computed tomography - 18 reformatted images
Contact radiography - 93 93
25 The distance between the mandibular base and the inferior border of the mandibular canal was easier to measure.
The mean values of the differences between the observers' measurements and the measurements on the contact radiographs exceeded 1 mm in a clear majority of the panoramic radiographs while it was below 1 mm in a clear majority with the tomographic techniques, both concerning the distance between the alveolar crest and the superior border of the mandibular canal and the distance between the mandibular base and the inferior border of the canal. The accuracy of measurements with the tomographic techniques appeared to be similar.
Observer agreement
Interobserver agreement was similar for panoramic OP5 and hypocycloidal tomography in Papers I and II. In the latter investigation interobserver agreement, calculated as the Kappa index, varied between 0.31 and 0.53 (mean 0.42) for panoramic techniques and between 0.19 and 0.57 (mean 0.35) for the three tomographic techniques (reformatted CT images excluded), indicating moderate and fair agreement for the two techniques. The highest agreement rates were found for the
Scanora panoramic technique and the CT-techniques. For reformatted CT images agreement meant that the observers could not identify the mandibular canal. The intraobserver agreement rates indicated moderate or good agreement for all techniques.
26 Bone mass measurements (IV,V)
Bone mineral density
Significant differences in BMD, measured by QCT, were found between the fifteen
mandibles (p = 0.0001). With one exception, the BMD values were significantly higher
in anterior sections than in posterior sections of the same mandible (p <, 0.05). The
mean BMD values of the five mesial slices within a posterior section were higher than
the mean BMD values of the five distal slices in 16 of 24 examined sections.
Significant differences between the mesial and distal five slices were found in nine of
these sections.
Trabecular bone volume
Analysis of values of TBV showed a significant mandibular variation (p < 0.001). The
mean TBV values were significantly higher (p = 0.0001) in the anterior than in the
posterior sections and the same results were found concerning values of the TTBV.
The values of TTBV were significantly higher than the TBV values for individual
slices and mean values from sections of mandibles as well as mean values from
mandibles.
The correlation between BMD values and TBV and TTBV values, respectively, was
r = 0.69 for BMD/TBV and r = 0.70 for BMD/TTBV (p = 0.0001) for the whole material. Considering individual mandibles, the correlation was significant in seven of the nine mandibles for BMD/TBV and six for BMD/TTBV.
27 Assessment of the trabecular pattern in periapical radiographs (VI)
The accuracy could not be estimated for the classification presented by Lekholm and
Zarb (1985). Overall, 58% of the ratings were concordant with the gold standard with the proposed classification system with reference images and 50% without reference images. The highest accuracy was obtained for the images with dense trabeculation
(78%) and the lowest for the images with sparse trabeculation (28%).
The highest interobserver agreement rate, expressed as the estimated probability of agreement, was found for the classification without reference images, 64%. The corresponding figure for the classification with reference images was 60% and for the
Lekholm and Zarb (1985) classification 49%. The Kappa index was 0.32, 0.35 and
0.33, respectively, for the three classifications.
Intraobserver agreement was 75% for the method with reference images, 86% without reference images and 76% for the classification by Lekholm and Zarb (1985). The highest Kappa indices, were found for the classification without reference images
(0.61, 0.65 and 0.75 for three observers).
28 DISCUSSION
Paresthesia and sensory disturbance cause, without doubt, serious problems for the
individual patient. In a multicenter study involving nine centres, a 4% incidence of
residual inferior alveolar nerve paresthesia was reported in connection with dental
implant treatment after three years (Higuchi et al. 1995). Thus, the distance between
the alveolar ridge and the mandibular canal is important to measure, not only to avoid
interference with the neuro-vascular bundle during surgery, but also to ensure
selection of accurate fixture length. A predominance of failure of osseointegration has namely been found among fixtures of the shortest length (Friberg et al. 1991, Quirynen
et al. 1991, Henry et al. 1993, Lekholm et al. 1994).
Panoramic and periapical radiographs are the first choice for the radiological appraisal before implant treatment. These techniques have, however, a number of disadvantages for the three-dimensional assessment of the jaw bone and related anatomical structures. Conventional tomography can give a cross-sectional view and locate the mandibular canal in a bucco-lingual direction. CT has also been applied for this type of examination (Schwartz et al. 1987, Casselman et al. 1988, Besimo et al. 1995).
Hypocycloidal tomography has commonly been used but is today often replaced by a spiral tomographic X-ray technique and CT. The Scanora X-ray machine, which is designed for dentomaxillofacial radiography, uses a spiral tomographic motion. In the present studies the Scanora machine was set to produce images with a section thickness of 4 mm, which is recommended by the manufacturer (Hallikainen et al.
1992), while the section thickness of hypocycloidal tomography was thinner, about 1.3 mm. A larger section thickness might simplify the depiction of thinner structures such as the borders of the mandibular canal (Ekestubbe and Grondahl 1993). However, other anatomical borders that may vary in shape or angulation within a 4 mm thick
29 section, such as the alveolar crest, might become more difficult to identify (Ekestubbe and Grondahl 1993). CT images do not suffer from the inherent lack of sharpness that is characteristic of film-based tomography. However, the application of CT will result in a radiation dose that is considerably higher for all organs exposed than those reported for panoramic radiography or conventional tomography (Clark et al. 1990,
Ekestubbe et al. 1993).
The observers could not detect the mandibular canal in the different radiographs to a rather high frequency. The visibility of the mandibular canal has been found to be higher in other investigations (Klinge et al. 1989, Stella and Tharanon 1990). This may be explained by the fact that several observers were engaged in the present investigations and only one observer performed the measurements in the previous studies. Besides, in 7% of the contact radiographs the cortical outline of the mandibular canal could not be seen, which is in agreement with Stella and Tharanon
(1990), who failed to identify the mandibular canal in about 17% of the sections from autopsy specimens. The visibility and measurability of the mandibular canal were studied with partly different observers in Papers II and III. Yet, the results were similar for most of the techniques confirming the validity of the results.
Tomography was superior to panoramic techniques in visualising the mandibular canal, a result in accordance with that of Klinge et al. (1989). In the latter study, direct CT was found to be the most accurate tomographic method for measurements, whereas in the present investigations CT and conventional tomographic techniques were found to be equal concerning measurement accuracy. However, in the study by Klinge et al.
(1989), different observers interpreted the conventional radiographs and the CT images and the discrepancy might be explained by observer variation. The reliability of hypocycloidal and spiral tomography has been investigated in two separate studies by
30 Grondahl et al. (1991) and Ekestubbe and Grondahl (1993). The results from those studies showed, like the present investigations, a relatively large variation between observers' ability to measure the distance between the alveolar crest and the superior border of the mandibular canal, a difference that might have clinical significance.
Direct CT images obtained in the coronal plane in partially dentate patients can show image degradation from dental restorations which can be avoided by obtaining reformatted images from axial scans. The mandibular canal was, however, often difficult to identify in the reformatted CT images, a result that was unexpected as other investigators have reported a high accuracy of measurements in such CT images
(Lamoral et al. 1990, Quirynen et al. 1990). It might be difficult to distinguish the mandibular canal from surrounding osteoporotic bone with reformatted techniques
(Quirynen et al. 1990). The results of CT techniques are highly dependent on the performance of the CT machine.
Based on these investigations, it is suggested that in cases where there is no doubt about the visibility of the superior border of the canal, with a wide residual ridge and clearly ample ridge height, panoramic radiography may suffice for the planning of implant treatment. In all other cases a tomographic technique is required.
Bone mineral content may be an essential factor in the prediction of osseointegration in connection with implant treatment. Friberg (1994) suggested bone quality should be rated according to the hardness during drilling, which in turn may depend on the amount of mineral. He found a high fixture loss in mandibles with "very hard bone".
Similar observations were reported by Truhlar et al. (1994). Mineral measurements of the bone tissue with QCT has been applied to several bones in the body (Ruegsegger et al. 1981, Hosie and Smith 1986, Cann and Genant 1980, Genant et al. 1985,
31 Sartoris et al. 1986). Klemetti (1993) used QCT to determine whether bone mineral density of the trabecular portion of the mandible was correlated to general osteoporosis status in postmenopausal women. The potential advantages of QCT over other quantitative techniques such as single- and dual-photon absorptiometry are its suitability for precise three-dimensional anatomical location, for direct mineral measurements and for spatial differentiation of trabecular bone from cortical bone.
The advantage of single-energy CT, giving a high precision in the measurements, was utilized in the present investigations. Single-energy CT assumes that bone tissue consists of water-equivalent soft tissue and bone mineral. However, the amount of fat will affect the accuracy of measurements. In another field of development for QCT, dual-energy CT, the CT number for bone tissue is measured at two different X-ray tube potentials. The accuracy will be improved compared to single-energy CT but the precision will be less (Cann 1988). In the BMD measurements in this thesis, a modified single-energy CT method was used, taking into account the influence of fat
(Nilsson et al. 1988).
In general, variations in bone mineral content, as measured with QCT, and bone mass will take a parallel course. However, during the first phase of the mineralisation, the bone tissue only contains 80% of the bone mineral (Mosekilde, 1989) and an increase in the remodelling will result in a decrease in bone density. If, on the other hand, a reduction of the remodelling space occurs and the trabecular bone osteons become older, this will lead to an increase in bone density. Changes in remodelling space will be responsible for bone mineral changes of 5% to 15% (Eriksen et al. 1994). These circumstances are important to consider when longitudinal changes of the bone mass are to be evaluated, but should not influence the measurements performed in the present study.
32 The BMD measurements with the aid of QCT presented significant inter- and intramandibular variations within small regions. Such variations of the trabecular bone mass between regions of one and the same mandible as well as between mandibles were also found by von Wowern (1977), with the aid of electronic point-counting.
This implies that when measuring BMD prior to implant treatment the precise implant host bed should be evaluated. The measurement of a whole mandible will not be useful for the prediction of bone mass. Klemetti et al. (1993) made QCT measurements of the trabecular bone mass of the mandible in patients. They obtained higher BMD values than in the present investigation. This can be due to that the patients in the study by Klemetti et al. (1993) were younger than the individuals in the present investigation, but also to different calibration procedures of the CT scanner.
The results presented a high correlation between BMD and TBV, indicating that the average amount of mineral per unit volume corresponds to a certain percentage of trabeculae occupying a given volume in the mandible. Thus, few trabeculae corresponded to a low mineral content and a large number of trabeculae corresponded to a higher mineral content. This was not evident before the results of our study were presented. However, no precise definition can be made concerning the shape, size and thickness of the trabeculae.
The TBV was measured from the ROI transferred from the CT images. An image artifact is always generated in CT images where there is a sharp gradient in density in the object as between cortical and trabecular bone tissue. Therefore, the transitional layer where the bone architecture changes from dense to more sparse is difficult to identify in the CT images. This so-called junction area was, however, clearly detectable in the contact radiographs and included in the measurements of the TTBV.
33 Thus the resulting measurements of the TTBV and TBV differed, with the values of
TTBV being significantly higher than the values of TBV.
Functional changes that influence the bone tissue are not only determined by mass, but are also related to structure, i.e. how mass is spatially distributed (Ruttimann et al.
1992). Analysis of vertebral trabecular bone has shown that the biomechanical competence was more closely correlated to age-related structural changes than to the mineral content (Mosekilde et al. 1987). The trabecular structure of the jaw bones is revealed indirectly by periapical radiographs which make up high-resolution images.
Although the complexity of the three-dimensional architecture but only a two- dimensional pattern can be recorded by this technique, it was considered worthwile to explore a classification system to be used prior to implant treatment based on the trabecular pattern in periapical radiographs. The different trabecular patterns were validated by means of morphometric measurements of the TTBV obtained from cross- sections of the mandibular sections.
Not only hard bone quality as suggested by Friberg et al. (1991) and Truhlar et al
(1994) but also poor bone quality has been considered to be a reason for implant failure. Poor bone quality has even been regarded to be a relative contraindication to implant treatment (Chen and Scharer 1993, Oikarinen et al. 1995). In the literature on implant treatment, poor bone quality has frequently been identified as bone quality of class 4 as proposed by Lekholm and Zarb (1985). Several studies have indicated the highest failure rates among fixtures inserted in bone of quality class 4 (Engquist et al.
1988, Jaffin and Berman 1991, Lekholm et al. 1994, Hutton et al. 1995). The classification system proposed by Lekholm and Zarb (1985) has not been evaluated in terms of diagnostic accuracy and observer performance. In the present investigation, the accuracy of this classification could not be estimated as the cross-sectional
34 illustrations of bone totally differed from the appearance actually found in cross-
sectional slices of mandibular bone. These findings might indicate that patient
selection according to bone quality and the grounds for follow-up studies on implant
success and failure are mainly based on personal experience and the opinion of the
surgeon, which may be subjective.
In this thesis, quantitative and qualitative bone tissue characteristics have been
investigated with the aid of QCT and periapical radiography, which can be applied in
further analysis of bone tissue in vivo in order to increase the reliability of patient
selection prior to endosseous implant treatment and the prediction of treatment
outcome. Furthermore, the results warrant that the QCT method and the classification
system based on periapical radiography enable us to retrospectively evaluate bone tissue characteristics and how these relate to implant success or implant failure.
35 CONCLUSIONS
1. Hypocycloidal, spiral and direct computed tomography of the posterior section of
the mandible were superior to periapical and panoramic radiography in visualising
the mandibular canal. Reformatted CT images visualised the mandibular canal to
the lowest extent.
2. Tomographic techniques were more accurate than panoramic techniques for
measurements of the distance between the superior border of the mandibular
canal and the alveolar crest and between the inferior border of the mandibular
canal and the mandibular base.
3. Concerning detectability of the mandibular canal, interobserver agreement was
lowest for periapical radiography and highest for CT, while intraobserver
agreement was moderate or good for all radiographic techniques. There was a
great variation between the observers as to whether or not they could identify the
borders of the mandibular canal and consequently the extent to which they could
perform measurements of distances related to the mandibular canal.
4. The mineral content of the trabecular bone, measured with QCT, varied between
mandibles and between and within sections of the same mandible.
5. The bone mineral density was highly correlated to the trabecular bone volume.
As these bone tissue properties varied within small areas, it may be important to
assess individual sites of the mandible prior to implant treatment.
36 6. The proposed classification system of the trabecular bone pattern consisted of
three classes: dense trabeculation, alternating dense and sparse trabeculation or
sparse trabeculation. The highest diagnostic accuracy was obtained when the
classification system was implemented with reference images. The accuracy was
highest for images with dense trabeculation (78%) and lowest for images with
sparse trabeculation (28%). The diagnostic accuracy of the classification system
devised by Lekholm and Zarb (1985) was not possible to evaluate. Interobserver
agreement for the proposed classification system was similar whether reference
images were used or not and higher than for the classification presented by
Lekholm and Zarb (1985). Intraobserver agreement was similar for the
classification systems.
37 ACKNOWLEDGEMENTS
I wish to express my sincere gratitude to all those who have supported me in various ways and contributed to the completion of this thesis.
Special thanks are due to: Arne Petersson, my supervisor, for never-failing support and patience throughout the study and for being a mos* valuable coworker and teacher.
Madeleine Rohlin, for devoting much time and interest to this work and for providing invaluable criticism and advice.
Bjorn Klinge, my other supervisor, for introducing me into this field of research and for always valuable comments and discussions.
Mats Nilsson for expert help and advice and for always showing kind interest and support.
Per-Erik Isberg and Jan Lanke for help with the statistical analysis.
The Institute for Postgraduate Dental Education in Jonkoping for making the Scanora X-ray machine accessible to me.
The Department of Anatomy, Lund University, for making autopsy specimens avalaible for this research.
The linguistic revision of the thesis was done by John Gulliver, Authorized Translator, Goteborg.
This work was supported by grants from the Faculty of Odontology, Lund University, the Swedish Dental Association and the South Swedish Dental Society.
38 The papers were reprinted from:
Paper I. The International Journal of Oral and Maxillofacial Implants, Volume 4, Lindh C and Petersson A. Radiologic examination for location of the mandibular canal: a comparison between panoramic radiography and conventional tomography, Pages 249-253, Copyright (1989), with kind permission from Quintessence publishing Co, Inc, 551 N. Kimberly Drive, Carol Stream, Illinois 601 88, USA.
Papers II and III. Clinical Oral Implant Research, Volume 3, Lindh C, Petersson A, Klinge B. Visualisation of the mandibular canal by different radiographic techniques, Pages 90-97, Copyright (1992) and Volume 6, Lindh C, Petersson A, Klinge B. Measurementsof distances related to the mandibular canal in radiographs, Pages 96- 103, Copyright (1995), with kind permission from Munksgaard International, Publishers Ltd, 35 Norre Sogade, P 0 Box 2148, DK-1016 Copenhagen K, Denmark.
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45 NEXT PAGE(S) left BLANK Radiologic Examination for Location of the Mandibular Canal: A Comparison Between Panoramic Radiography and Conventional Tomography
Christina Lindh, DDS*/Arne Petersson, DDS, PhD*
Panoramic radiography was compared with conventional tomography as techniques for visualizing the mandibular canal. Tomography gave a significantly clearer image of the canal at and 1 cm posterior to the mental foramen, while no differences were found between the methods 2 cm posterior to the mental foramen. Thus, tomography could be of great value in locating the mandibular canal before implant surgery in edentulous mandibular posterior segments. (INT J ORAL MAXILLOFAC IMPLANTS 1989;4:249-253.)
Key words: mandible, radiography; panoramic radiography; tomography
reoperative planning for implant surgery in the pos- Material and Methods Pterior segments of the mandible is more complicated than for other regions. Intraoral and panoramic radio- Fifteen consecutive patients (ten women, aged 41 to graphic examination combined with a clinical exami- 72 years, and five men, aged 57 to 63 years) referred nation provides information related to the skeletal to- to the Department of Oral Radiology by prosthodontists pography and dimensions of the mandible. However, and/or oral surgeons for radiologic examination of the in the premolar and molar regions of the mandible it edentulous posterior quadrants of the mandible were is also necessary to consider the level of the mandibular selected for the study. From these patients, 23 man- canal vertically as well as in the buccolingual di- dibular posterior segments were examined by pan- mension. To locate the mandibular canal, three- oramic radiography and frontal multisection tomog- dimensionally computed tomography has been sug- raphy. 1 gested. However, this technique is not always readily Panoramic radiographs were taken using an Or- available and it is an expensive procedure. In situations thopantomograph Model OP5 (Siemens, Bensheim, with slight or moderate rcsorption of the residual ridge, West Germany) and high-speed, rare-earth screens there may be enough bone superior to the mandibular (Siemens Titan 2 HS). The patients were positioned canal for implant placement, provided the canal can for normal exposure of teeth and jaws with bite blocks. be identified. Therefore, a need does exist for deter- Frontal tomography was performed with the patient mining which radiographic method is most suitable. in the seated position and the head immobilized in a The aim of this study was to compare panoramic cephalostat. The cephalostat was rotated and the patient radiography with conventional tomography for location positioned so that the tomographic plane gave perpen- of the mandibular canal. dicular cross-sectional cuts of the mandibular posterior segment. The apparatus used was a Polytome U (Massiot/Philips, Paris, France) with a Siemens Bi
'Department of Oral Radiology, School of Dentistry, Lund Univer- 125/3O/5OR tube, nominal focus size 0.6 x 0.6 mm sity, Carl Guslafs vag 34, S-2H 21 Malmb, Sweden. and focus-film distance 1.50 m. A hypocycloidal mo-
47 Lindh
Number • 33 30 - 25 mi 19 ^^ 20 ^H 1G
10 Fig 1 Overall distribution of the scores 0,1, and 2 (n = 63) NXVMppg for tomography (tomo) and 0 orthopantomography (opg), • • showing that the mandibular i 1 2 canal is better visualized with 0 tomography than orthopan- Score tomography.
„Number
: 16 15 - : io 1 10 iilii^
5 Fig 2 Distribution of the scores 0,1, and 2 (n = 22) for ESS opg tomography (tomo) and or- ^: i ^. IJJJJ^ • thopantomography (opg) at 0 •H iffissss tomo the mental foramen, showing 0 1 2 that the mandibular canal is better visualized with tomog- Score raphy than orthopantomog- raphy. tion was used with a tomographic angle of 48 degrees The panoramic radiographs and tomograms were and without a grid. The circular collimator had a di- each interpreted independently by two oral radiologists. ameter of 1.5 cm, resulting in a field size with a di- The judgments were then compared and, in cases of ameter of 6.5 cm at the film level. Exposure data for disagreement, the radiographs were re-examined and a frontal tomography were 60 kV and 500 to 600 mA. A joint decision made. The visibility of the mandibular multifilm cassette containing four pairs of rare-earth in- canal was interpreted at the mental foramen as well as tensifying screens (3M Trimax, X-ray Products/ 3M, 1 and 2 cm posterior to the foramen. The distinctness St Paul, Minnesota) and Wicor-X OG films (CEA, of the canal was rated from 0 to 2 (0 = the mandibular Strangnas, Sweden) was used, and the interspace be- canal could not be identified; 1 = the mandibular ca- tween the different tomographic sections was 3.3 mm.2 nal was visible, but had diffuse borders; and 2 = the The multifilm cassette covers a total thickness of ap- mandibular canal was clearly visible). proximately 1 cm of the examined object, and two to The overall interobserver agreement was calculated three exposures were made on each posterior segment by comparing the recordings for each observer. The to image the mental foramen and at least 2 cm posterior proportion of interobserver agreement was also calcu- to the foramen. lated using the Kappa index as described by Cohen.'
48 Lindh
Number 20
Fig 3 Distribution of the scores 0,1, and 2 (n = 23) for tomography (tomo) and or- thopantomography (opg) 1 cm posterior to the mental foramen, showing that the mandibular canal is better Score visualized with tomography than orthopantomography.
Fig 4 Distribution of the scores 0,1, and 2 (n = 18) for tomography (tomo) and or- thopantomography (opg) 2 cm posterior to the mental fo- ramen. No differences are found between tomography and orthopantomography in the visualization of the man- dibufar canal.
Statistical differences between the ratings given for incompletely blurred in the tomograms, producing par- the radiographic methods were tested with the Wilcox- asite streaks. The difficulties in judging the two ortho- on's signed-rank test. The following levels of signifi- pantomograms resulted from the fact that the mental cance were considered: P < 0.05, P < 0.01, and foramen was not visible. As the mental foramen was P < O.OOl. the starting point for interpretation of the mandibular canal, it was not possible to use these orthopantomo- Results grams. The overall distribution of the scores 0, I, and 2 for Six regions were impossible to diagnose in the tomo- tomography and orthopantomography is shown in Fig grams and two in the orthopantomograms. Therefore, 1. The mandibular canal could not be identified in the comparisons are based on 63 judgments. Difficulties 17% of the regions in the tomograms and in 35% in in judging the regions in the tomograms were mainly the orthopantomograms. The distribution of the scores caused by the fact that teeth were situated in or near 0, 1, and 2 in the three regions is shown in Figs 2, 3, the region. These teeth outside the focal plane were and 4. Figures 5a to 5d illustrate a mandibular canal
49 Lindh
Figs 5a to 5d Left side of the mandible of the same patient is examined by orthopantomography (A) and frontal tomography (B, C, D). The panoramic radiograph shows a mandibular canal with diffuse borders. The mandibular canal (arrows) is more visible in the frontal tomograms. The tomographic sections are placed near the mental foramen (B), and 1 cm (C) and 2 cm (D) posterior to the mental foramen.
that is more clearly visualized in the tomograms as The overall intcrobscrver agreement is shown in compared to the orthopaiitomogram. Altogether, to- Table 1. The Kappa index was 0.54 for tomography mography revealed significantly (P < 0.001) higher and 0.52 for orthopantomography. scores than orthopantomography. Significantly higher scores were given for tomography in the region of the Discussion mental foramen (P < 0.01) and 1 cm posterior to the mental foramen (P < 0.05), while no differences in Endosscous implant treatment is a practical procedure the scores were found 2 cm posterior of the foramen. in edentulous areas of the posterior mandibular seg-
50 Lindh
dibular canal three-dimensionally with a high degree Table 1 Interobserver Agreement Between of accuracy to be able to position the implants lingually Observers or buccally to the mandibular canal. In such situations, Radiographic method tomography is necessary to give a cross-sectional image of the mandible. Conventional multisection tomogra- Difference Tomography Orthopan tomography in score (n = 63) (n = 67) phy has the advantage of being faster and easier to perform than computed tomography, and it is also less affected by possible artifacts from tooth fillings or
Summary and Conclusions ments. A preoperative radiographic examination is per- This study showed a similar and moderate agreement formed to determine suitable sites and directions for between the readings of two observers for both radio- implant placement as well as length of the implants. graphic techniques. The interobserver agreement of In patients with slight resorption of the residual ridge, 65% to 67% is normal for this type of study. The true one limitation of placing endosseous implants may be diagnostic accuracy of the radiographic methods is not a high location of the mandibular canal. A radiographic known, since the real anatomic position of the mandib- examination is therefore necessary to identify the men- ular canal could not be determined in the patients. • tal foramen and mandibular canal to avoid the risk of damaging the inferior alveolar nerve. Panoramic ra- diography is the most common way to visualize the References canal, but, according to our results, the mandibular 1. Schwarz MS, Rothman SLG, Rhodes ML, Chafetz N: canal is often difficult to locate in the premolar and Computed tomography: Part I. Preoperative assessment of the molar regions with this technique. In these regions, mandible for endosseous implant surgery. Int } Oral Maxillofac conventional tomography could be used to better vi- Implants 1987;2:B7-141. sualize mandibular canals that cannot be clearly seen 2. Petersson AR, Gratt BM: A rare-earth screen multi-section . cassette for temporomandibular joint tomography: a technical in panoramic radiographs. A better choice might be report. Dentomaxillofac Radiol 1985;14:31-56. 1 2 computed tomography, ' but patients with such prob- 3. Cohen J: A coefficient of agreement for nominal scales. Educ lems receive low priority for examination with this tech- PsychoiMeas 1960;20:37-46. nique in Sweden. 4. Casselman JW, Quirynen M, Lemahieu SF, Baert AL, Bonte J: Computed tomography in the determination of anatomical In some patients, the residual ridge is markedly re- landmarks in the perspective of endosseous oral implant sorbed and it thus becomes necessary to locate the man- installation. / Head Neck Pathol 1988;7:25>-264.
Resume Zusammenfassung Resumen Examen radiologique pour la localisation du ftadiologische Untersuchung zum Examen radioldgico para la ubicacidn del canal mandibulaire: Une comparaison entre Lokalisieren des Unterkieferkanals: Ein canal mandibular: Una comparacidn entre la tomographie panoramique et la Vergleich zwischen Pantomographie und la tomograffa convencional y la panorimica tomographie conventionnelle konventioneller Tomographie Se compar6 la radiograna panor£mica con La radiographie panoramique fut compare Panorama-Rontgentechnik wurde mil la tomografia conventional como t£cnicas avec la tomographie conventionnelle, en konventioneller Tomographie als Techniken para la visualizaci6n del canal mandibular. tant que techniques permettant de vergfichen, den Unterkieferkanal sichtbar La tomografia suministr6 una imagen del visualiser fe canal mandibulaire. La zu machen. Tomographie gab ein canal significativamente mas clara a nivel tomographie a donn6 une image nettement signifikant klareres Bild des Kanals an und 1 del foramen mentoniano, lo mismo que 1 plus claire du canal au niveau du trou cm hinter dem Foramen mentale, wahrend cm posteriormente al foramen mentoniano. mentonnier et 1 cm en arriere de celui-ci, keine Unterschiede zwischen den No se encontraron diferencras entre los alors qu'aucune difference ne fut observed Methoden 2 cm hinter dem Foramen m^todos cuando los ex^menes se entre les m^thodes 2 cm en arriere du trou mentale gefunden wurden. realizaron, 2 cm posteriormente al foramen mentonnier. Par consequent, la Dementsprechend konnte Tomographie mentoniano. Por esto, la tomografia podrta tomographie pourrait etre tr6s utile pour von gropem Wert im Lokalisieren des tener gran valor en ta localizact6n del canal locaiiser le canal mandibufaire avant une Unterkieferkanals vor Implantatchirurgie in mandibular antes de la cirugfa para chirurgie d'implantation sur les segments zahnlosen hinteren Segmenten des implantes en segmentos mandibulares postGrieurs d'une mandibule 6dent6e. Unterkrefers sein. posteriores, ed^ntulos.
51 NEXT PAGE(S) left BLANK Visualisation of the mandibular canal by different radiographic techniques
Lindh C, Petersson A, Klinge B. Visualisation of the mandibular canal Christina Lindh1, by different radiographic techniques. Arne Petersson1, Clin Oral Impl Res 1992: 3: 90-97. Bjorn Klinge2 'Departments of Oral Radiology and 6 mandibles were radiographically examined bilaterally to visualise the 2Periodontology, Lund University, mandibular canal. 5 imaging techniques were used: periapical radi- Centre for Oral Health Sciences, ography, panoramic radiography, hypocycloidal tomography, spiral Malmo, Sweden tomography and computed tomography (CT). Panoramic radiographs were obtained with 2 different X-ray machines. The CT-examinations comprised direct images and standard reconstructions based on axial slices. The specimens were subsequently sectioned for contact radiography. The Key words: mandibular nerve - panor- D visibility of the mandibular canal was estimated by 3 observers at special amic radiography - tomography - en- reference points on all radiographs and classified as clearly visible, ques- dosseous implantation tionable visibility or not visible. The contact radiographs served as the Christina Lindh, Dept of Oral Radi- "gold standard". The inter-observer and the intra-observer agreement ology, Lund University, Centre for Oral were assessed by calculating the overall agreement and the x value. Health Sciences, Carl Gustafs vag 34, Direct coronal computed tomography, as well as spiral and hypocycloidal S-22114 Malmo, Sweden tomography, gave better visualisation of the mandibular canal than peri- Accepted for publication 16 January apical and panoramic radiography. 1992
Installation of oral implants has become a common der of the mandibular canal using hypocycloidal method of treatment for both completely and par- tomography. tially edentulous patients. The placement of im- The aim of this study was to investigate the plants requires careful preoperative radiographic visibility of the mandibular canal in autopsy speci- examination. In the posterior part of the mandible, mens as assessed with different radiographic tech- it is necessary to determine the amount of bone niques. The radiographic findings were compared superior to the mandibular canal. Interference with with contact radiography of sections of the pos- the inferior alveolar neurovascular bundle can cause serious problems for the patient, such as paraesthesiae and loss of osseointegration of the implant. The inferior alveolar neurovascular bundle is not always surrounded by compact bone, however. Total absence of demonstrable canals has been reported in 4 of 46 radiographed mandibles by Littner et al. (1986) and in 10 of 96 dry man- dibles by Heasman (1988). The results of treatment with intraosseous implants in partially edentulous patients were described in a prospective multicentre study. Depending on the position of the implants, 6-8% of the patients complained of remaining pa- raesthesiae in the lower lip (Van Steenberghe et al. 1990). We believe that one reason for this may be the difficulty in determining preoperatively the exact location of the mandibular canal from radio- graphs. Linear tomography has been described as a precise technique for locating the mandibular canal within the mandible (Stella & Tharanon ing. 1. Schematic drawing of a mandibular side segment with 1990), but Grondahl et al. (1991) found a relatively reference points A to F. The tantalum pins are inserted at A, C large variation between observers in measuring the and E. Observations are also made 0.5 cm posterior to each distance from the alveolar crest and the upper bor- pin at B, D and F.
53 Radiographic visualisation of the mandibuiar canal Table 1. Concordant and disconcordant scores on a 3-point scale, for 3 dibuiar side segment (i.e., right and left side of the observers concerning the visibility of the mandibuiar canal related to mandible). On each side, one pin was placed just radiographic technique beneath the mental foramen, one pin 1 cm pos- Each of 3 terior to the foramen and the 3rd pin 2 cm posterior 3 observers 2 observers observers to the foramen. All side segments of the mandibles awarded the awarded the awarded a were examined radiographically and thereafter sec- Radiographic same score same score different score technique (%) (%) (%) tioned for contact radiography. 3 observers, 2 oral radiologists and 1 periodontologist with experience periapical radiography of implant surgery, assessed the radiographs inde- (1=72) 38 44 18 panoramic radiography pendently. The observations were made with the 0P5 aid of a magnifying viewer (X-produkter, Malmo, (1=72) 47 43 10 Sweden) over a view-box with fixed-light intensity. panoramic radiography Prior to the assessments, the observers had a joint Scanora discussion about how to define the visibility of the (i=72) 61 29 10 hypocycloidal tomo- mandibuiar canal. The canal was assessed as visible graphy if the superior border was clearly seen and the (i-72) 41 41 18 following three-point scale was used: 1 = definitely spiral tomography not visible; 2 = questionable visibility; 3 = clearly 0=72) 46 40 14 computed tomography visible. Observations were made at the sites of the coronal plane tantalum pins between the pins and 0.5 cm pos- C=71) 62 34 4 terior to the most posteriorly inserted pin (Fig. 1). computed tomography 2 observers performed their observations 2x reconstruction with an interval of at least 1 week. The inter- and (n-71) 55 39 6 intra-observer agreements were calculated with 2 different measures; the overall agreement, which concerns the total number of sites where the ob- terior part of the mandible, the latter being re- servers agree, and the kappa value (x), which takes garded as the "gold standard". In addition, the into account the contribution of agreement by inter- and intra-observer agreements were calcu- chance (Cohen 1960). lated using the different radiographic techniques. When the observations were performed, the as- sessements from each observer and each radi- Material and methods ographic technique were compared and the visi- bility of the mandibuiar canal was judged by ma- 6 mandibles were removed from dead individuals jority decision. In cases where none of the who had donated their bodies to research. 1 speci- observers had awarded the same score (Table 1), a men was edentulous and 5 were partly edentulous. new interpretation and a joint decision was made. The mandibles were degloved and fixed in 10% The 3 observers assessed the contact radiographs neutralised buffered formalin solution. To obtain together and made a unanimous decision about the reference points, 3 tantalum pins (1.5 mm x 0.5 visibility of the mandibuiar canal according to the mm) were inserted at the buccal side of each man- 3-point scale. These observations served as the
Table 2. Interobserver agreement concerning visibility of the mandibuiar canal related to radiographic technique, expressed as overall agreement and kappa value (x)
Observers
MB B/C A/C
Overall Overall Overall agreement agreement agreement Radiographic method (%) X (%) X (%) X periapical radiography (fl=72) 52.8 0.20 58.3 0.19 50.0 0.17 panoramic radiography 0P5 (n-72) 55.5 0.31 65.3 0.36 63.9 0.37 panoramic radiography Scanora (n=72) 72.2 0.53 73.6 0.51 66.7 0.45 hypocycloidal tomography (n=71) 57.7 0.37 57.7 0.24 53.5 0.28 spiral tomography (1=72) 72.2 0.54 52.8 0.19 55.6 0.22 computed tomography coronal plane (n-71) 77.5 0.57 64.8 0.28 77.5 0.42 computed tomography reconstruction (n-71) 66.2 0.59 67.6 0.35 70.4 0.45
54 Lindh et al.
Table 3. The intra-observer overall agreement and kappa value (x) on scoring the visibility of the mandibular canal related to radiographic Periapical radiography technique 2 periapical radiographs were taken at each side Observer A Observer B segment of the mandible. These were obtained using a parallelling technique with a film holder Overall Overall (Eggen) attached to the tube of a dental X-ray Radiographic agreemenlt agreemenlt technique (%) V. (%) X machine using 70 kV (Siemens Heliodent, Erlang- en, Germany). Ektaspeed film was used (Eastman periapical radiography (n=72) 69.5 0.46 73.6 0.46 Kodak Company, Rochester, NY, USA). The ex- panoramic radiography OP5 posure time was 0.64-0.80 s.. (n=72) 68.1 0.44 73.6 0.54 panoramic radiography Scanora (n=72) 66.7 0.45 88.9 0.79 hypocycloidal tomography (i=71) 78.9 0.68 73.2 0.56 Panoramic radiography spiral tomography (n=72) 70.8 0.55 76.4 0.61 computed tomography Panoramic radiographs were obtained with an Or- (coronal plane) 0=71) 80.3 0.54 77.5 0.60 thopantomograph Model OP5 (Siemens, Bens- computed tomography heim, Germany) and a Scanora (Soredex, Helsinki, (reconstruction) (n=71) 87.4 0.75 76.1 0.47 Finland). With the Orthopantomograph, the volt- age setting was 55-60 kV and Siemens Titan 2 HS screens were used. With Scanora, the voltage setting was 63 kV and Trimax T6 (3M, X-ray "gold standard", with which each radiographic Products/3M, St Paul, MN, USA) screens were technique was compared. used. The mandibles were fixed in a position corre- sponding to that of a patient. Radiographic examination Hypocycloidal tomography 5 imaging techniques were used: periapical radi- ography, panoramic radiography, hypocycloidal Hypocycloidal tomography was performed with a tomography, spiral tomography and computed Universal Polytome (Massiot/Philips, Paris, tomography (CT). Panoramic radiographs were France) with a Siemens Bi 125/30/50R tube. The obtained with 2 different X-ray machines. The CT- focus-film distance was 1.50 m. A hypocycloidal examinations comprised direct images and stan- motion was used with a tomographic angle of 48 dard reconstructions based on axial slices (Figs. degrees and without a grid. The circular collimator 2A-G). At all examinations, except CT, an ad- had a diameter of 1.5 cm, resulting in a field size with ditional filter of 3 mm Al was attached to the X- a diameter of 6.5 cm. Exposure data were 55-67 kV ray tube. and 80-120 mAs. A multi-film cassette with 4 pairs
Table 4. Distribution of scores 1, 2 and 3 at the sites of the reference points A to F using different radiographic techniques and contact radiography: 1 =not visible; 2=questionable visibility; 3=clearly visible
Radiographic technique
Panoramic Panoramic Hypocyc- CT CT 13eriapical radiography radiography loidal Spiral coronal reconstruc- Contact radiography OP 5 Scanora tomography tomography plane tion radiography (1=72) 0=72) (1=72) 0=72) 0=72 ) (n=71I) 0=71 ) (n=72)
Ref. point 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
A 9 1 2 7 2 3 7 5 1 11 1 1 10 1 11 6 6 12 B 8 2 2 8 4 7 3 2 5 7 2 10 3 2 7 9 1 2 12 C 8 1 3 8 1 .3 7 3 2 5 2 5- 4 1" 7 2 2 8' 11 1 2 10 D 7 1 4 7 2 3 8 4 5 2 5 7 1 4 1 11 9 2 1 1 11 E 8 1 3 9 2 1 7 3 2 5 4 3 7 1 4 3. 1 8 10 1 1 1 11 F 7 1 4 7 2 3 7 2 3 5 3 3* 7 2 3 2 1 8 8 1 2 1 11 I 47 7 18 46 9 17 43 11 18 26 11 34 28 6 38 12 6 53 53 5 13 67
' One of the scores 3 corresponds to a score 1 for the contact radiograph. " This score 2 corresponds to a score 1 for the contact radiograph.
55 Radiographic visualisation of the mandibular canal
Fig. 2. Radiographs with all radiographic techniques from one left mandibular side segment.
of rare-earth screens containing 4 films was used obtained at 3.3 mm intervals from the mental for- (Petersson & Gratt, 1985). The distance between the amen to 2.5 cm posterior to the foramen. depicted layers was 3.3 mm. The specimens were oriented in a position such that tomographic cuts Spiral tomography were perpendicular to the lower border of the man- dible and to the buccal and lingual bone plates. Spiral tomography was performed with the Scano- Cross-sections (1.7 mm thick) of the mandibles were ra X-ray machine. The specimens were oriented in
56 Lindh et al.
Fig. 2 (cont'd). (A) Periapical radiograph. (B) Panoramic radio- graph (OP5). (C) Panoramic radiograph (Scanora). (D) Tomo- graphic section (Polytome). (E) Tomographic section (Scanora). (F) Computed tomography (coronal plane). (G) Computed tomography (reconstruction). (H) Contact radiograph. the same way as in the Polytome. Cross-sections scribed before. 4 exposures per film were obtained (4 mm thick) of the mandibles were obtained at with a field size of 7 x 10.2 cm. intervals of 4 mm along the same region as de- Computed tomography Computed tomography was performed with a So- matom DRG (Siemens, Erlangen, Germany). Con- tiguous 2-mm thick slices were taken in the coronal plane, angled perpendicularly to the inferior bor- der, and to the buccal and lingual bone plates of the mandibular side segment. In addition to this, 2 mm-thick axial slices were taken and CT standard reconstructions were made from these images. The reconstructions were made at the sites of the refer- ence points.
25 50 75 Sectioning and radiography of sections Number The mandibles were mounted in a precision saw. Fig. 3. Overall distribution of scores 1, 2 and 3 for different radiographic techniques and contact radiography concerning Slices 2 mm and 5 mm thick were cut using an visibility of the mandibular canal. Score l=not visible, score Exact cutting unit (Exakt Apparatebau, Nordstedt, 2 = questionable visibility, score 3 = clearly visible. Germany). The sections were then radiographed
57 Radiographic visualisation of the mandibular canal
Fig. 4. (A) A hypocycloidal tomographic section with the Polytome from a left mandibular side segment. The area registered as the mandibular canal is indicated with arrows. (B) Corresponding contact radiograph were the mandibular canal is not visualised. with a Siemens pH 125/100 R tube, focus film vations were made. The radiographic examinations distance 0.70 m (Fig. 2H). During exposure, the with the first-mentioned methods did not cover sections were placed in contact with the film packet the region behind the most posteriorly inserted (Strukturix D7, Agfa-Gevaert, Belgium). tantalum pin, which made it impossible to make the most posterior observation. Results The overall distribution of the scores 1, 2 and 3 for the different radiographic techniques and con- Observer performance tact radiography is shown in Fig. 3. Computed The number of sites with totally concordant results tomography in the coronal plane showed the among the 3 observers was highest for the Scanora highest number of clearly visible canals adding all panoramic technique and computed tomography reference points, and reconstructed images from in the coronal plane (Table 1). Direct computed computed tomography showed the highest number tomography also showed the least number of sites of canals definitely not visible. There was hardly where the observers totally disagreed in their scor- any difference between the other 2 tomographic ings: only 4% of the observations. techniques, hypocycloidal and spiral tomography, The inter-observer agreement rates are presented and they both gave better visualisation of the man- in Table 2. Higher agreement rates were found for dibular canal than the 2-dimensional radiographic all combinations of observers when CT-techniques techniques. Panoramic and periapical radiography and Scanora panoramic technique were employed. visualised the mandibular canal to the same extent. The intra-observer agreement rates were similar for The overall distribution of the scores 1, 2 and 3, all techniques, except for higher agreement rates related to both radiographic technique and refer- using CT for one observer and Scanora panoramic ence points compared to contact radiography, is radiography for the other observer (Table 3). How- shown in Table 4. The tomographic techniques, ever, the high inter- and intra-observer agreement except CT-reconstructions, showed fewer score 1 found on direct CT-images applies to clearly visible (definitely not visible) at the reference point A, due mandibular canals, but the consistency concerning to the fact that the mental foramen was often the reconstructed CT-images relates to the canals clearly visible at tomography. It was not possible definitely not visible. to identify the mandibular canal on the contact radiographs at the sites of 5 reference points from 2 different mandibular side segments. In spite of Visibility of the mandibular canal this, the canal was classified as visible at the same With hypocycloidal and computed tomography, 71 reference point with some of the radiographic tech- observations were made of the 12 mandibular side niques (see Table 4 and Fig. 4). Score 2 was segments; with the other techniques, 72 obser- awarded when the superior border of the mandibu-
58 Lindh et al. lar canal was impossible to interpret, but in some Two-dimensional radiographic techniques visu- tomographic sections, 2 "holes" were seen sur- alised the mandibular canal to a lesser extent than rounded by a sclerotic border, and it was imposs- the tomographic techniques. The superior border ible to decide which was the mandibular canal. of the mandibular canal was clearly visible in 48% of the examined sections using hypocycloidal tomography, which corresponds well to 52% found with hypocycloidal tomography of patients Discussion (Lindh & Petersson 1989). Comparing the tomo- Direct computed tomography visualised the man- graphic techniques with panoramic radiography, dibular canal best of the examined techniques, and CT-scans have been found to be more precise in it also gave a high inter- and intra-observer agree- measuring the distance between the bony crest and ment rate. The exact position of the canal in re- the mandibular canal compared to panoramic radi- lation to the alveolar crest was not examined in ography (Tal & Moses 1990), and the tomographic our study, but it has earlier been shown that more radiographs have an additional advantage in pre- exact measurements are obtained with direct com- surgical planning, since they reveal the horizontal puted tomography cDmpared with hypocycloidal dimension and shape of the mandible, and the tomography and panoramic radiography (Klinge topography and buccolingual location of the man- et al. 1989). This method might, however, be diffi- dibular canal. cult to use in patients, owing to difficulties in pa- In conclusion, we recommend a tomographic tient-positioning and the fact that metal fillings in method for revealing the location of the mandibu- the teeth may create artifacts in the image. Further- lar canal. Not only do these methods give a 3- more, the cost of a CT-examination is higher than dimensional image of the mandible and the loca- that of conventional tomography. tion of the mandibular canal, they also give better The reconstructed image from computed tomo- visualisation of the canal. Further studies are in graphy gave the poorest visualisation of the man- progress in our laboratories to investigate the visu- dibular canal of all examined methods. This alisation of the mandibular canal and to obtain method has been recommended as having several a better understanding of the influence of bone important advantages in the determination of ana- structure on the radiographic image. tomical landmarks prior to oral implant instal- lation, and of the maximal implant length, taking into account the location of the mandibular canal (Casselman et al. 1988). In the latter study, the Acknowledgements reconstruction technique gave almost perfect esti- We would like to express our sincere gratitude to the Deparment mates of the bone height and width. The authors of Anatomy, Lund University for making human specimens point out, however, that the mandibular canal is available for this project and to the Institute for Postgraduate more difficult to distinguish from the surrounding Dental Education Jonkoping, for making the Scanora X-ray bone on the reconstructed images than on the cor- machine accessible to us. onal sections. Furthermore, only one dissected hu- man mandible was examined and the results from our study show that variations exist in the presence Zusammenfassung of a cortical lining of the mandibular canal. The 6 Unterkiefer wurden bilateral rontgenologisch untersucht, um quality of the images from the CT-reconstruction den Mandibularkanal darzustellen. 5 verschiedene bildgebende method may, however, depend on the performance Techniken kamen zur Anwendung, namlich periapikale Ront- of the CT-machine, and it is possible that better genbilder, Panoramarontgen, hypocycloidale Tomographie, reconstructions can be obtained using other equip- Spiraltomographie und Computertomographie (CT). Die Pano- ramarontgen wurden mit 2 verschiedenen Geraten hergestellt. ment. Die CT-Untersuchungen beinhalteten direkte Bilder und Stan- No differences were found between periapical dartrekonstruktionen basierend auf axialen Schnitten. Die Pra- radiography and the panoramic techniques con- parate wurden anschliessend fiir Kontaktrontgenbilder ge- cerning visibility of the mandibular canal. How- schnitten. Die Sichtbarkeit des Mandibularkanals wurde von 3 Untersuchern an speziell definierten Referenzpunkten auf alien ever, the periapical radiographs gave the lowest Rontgenbildern beurteilt und als klar sichtbar, fraglich sichtbar inter-observer agreement rate of the examined tech- und nicht sichtbar eingestuft. Die Kontaktrontgenbilder dienten niques. Clinically, the panoramic techniques are als "Gold Standart". Die Uebereinstimmung zwischen den Un- advantageous, as periapical radiographs are techni- tersuchern und innerhalb jedes Untersuchers wurde durch Be- cally very difficult to obtain in edentulous man- rechnung der Gesamtiibereinstimmung und des x-Wertes ermit- telt. Sowohl direkte koronale Computertomographie als auch dibular side segments, depending on resorption of spirale und hypocycloidale Tomographie ergaben eine bessere the alveolar crest being positioned at the same level Darstellung des Mandibularkanales als periapikale und Panora- as the floor of the mouth. marontgen.
59 Radiographic visualisation of the mandibular canal References panoramic radiography and conventional tomography. Inl J Oral Maxillofac Implants 4: 249-253. Casselman J. W, Quirynen M., Lemahieu S. F., Baert A. L., Littner M. M., Kaffe I., Tamse A., Dicapua P. (1988) Re- Bonte J. (1988) Computed tomography in the determi- lationships between the apices of the lower molars and nation of anatomical landmarks in the perspective of en- mandibular canal - a radiographic study. Oral Surg 62: dosseous oral implant installation. J Head & Neck Patholog 595-602. 1: 255-264. Petersson A., Gratt B. M. (1985) A rare-earth screen multi- Cohen J. (1960) A coefficient of agreement for nominal section cassette for temporomandibular joint tomography: scales. Educ Psychol Meas 20: 37-46. a technical report. Dentomaxillofac Radiol 14: 31-36. Grondahl K., Ekestubbe A., Grondahl H.-G., Johnson T. Stella J. P., Tharanon W. (1990) A precise radiographic method (1991) Reliability of hypocycloidal tomography for the to determine the location of the inferior alveolar canal in evaluation of the distance from the alveolar crest to the the posterior edentulous mandible: implications for dental mandibular canal. Dentomaxillofac Radiol 19: 200-204. implants (I). Technique. Inl J Oral Maxillofac Implants 5: 15-22. Heasman P. A. (1988) Variation in the position of the inferior Tal H., Moses O. (1991) A comparison of panoramic radi- dental canal and in significance to restorative dentistry. J ography with computed tomography in the planning of im- Dent 16: 36-39. plant surgery. Dentomaxillofac Radiol 20: 40-42. Klinge B., Petersson A., Maly P. (1989) Location of the man- Van Steenberghe D., Lekholm U., Bolender C, Fohner C, dibular canal, comparing macroscopical findings, conven- Henry P., Herrmann I., Higuchi K., Laney W., Linden U., tional radiography and computed tomography. / Oral Astrand P. (1990) The applicability of osseointegrated oral Maxillofac Implants 4: 327-332. implants in the rehabilitation of partial edentulism: a pro- Lindh C, Petersson A. (1989) Radiological examination for spective multicenter study on 558 fixtures. Inl J Oral Maxillo- location of the mandibular canal. A comparison between fac Implants 5: 272-281.
60 Clin Oral lmpl Res 1995: 6: 96-103 Copyright © Munksgaard 199S Printed ill Denmark • All rights reserved CLINICAL ORAL IMPLANTS RESEARCH ISSN0905-7161
Measurements of distances related to the mandibular canal in radiographs
Lindh C, Petersson A, Klinge B. Measurements of distances related to the C. Lindh1, A. Petersson2, mandibular canal in radiographs. B. Klinge2 Clin Oral Impl Res 1995: 6: 96-103. © Munksgaard, 1995 Departments of 'Oral Radiology and 2Periodontology, Lund University, Centre for Oral Health Sciences, Malmo, Before implant surgery in the mandibular side segment, it is of utmost Sweden interest to locate the mandibular canal in radiographs to avoid inter- ference with the neurovascular bundle during surgery. Six mandibular specimens were radiographically examined with 2 panoramic and 3 tomo- graphic techniques. The distances between the superior border of the ca- Key words: mandibular nerve - nal and the alveolar crest and between the mandibular base and the inferior radiography - dental implantation - border of the canal were measured. In addition, the height of the canal endosseous was measured. The measurements were performed by 3 or 4 observers and Christina Lindh, Centre for Oral Health compared with measurements on contact radiographs of the same areas. Sciences, Lund University, Carl Gustavs Tomography gave more accurate values of the above distances than pan- vag 34, S-214 21 Malmo, Sweden oramic techniques. The variation between observers in detecting the man- Accepted for publication dibular canal was large. 17 October 1994
The use of endosseous dental implants has in- et al. 1990; Astrand et al. 1991; Henry et al. 1993). creased in recent years and is expected to expand Before implant surgery in a resorbed mandibular further in the future. As the use of osseointegrated side segment, it is of utmost importance to be able implants in the treatment of the edentulous jaw has to measure the height of the alveolar crest superior proved to be successful (Adell et al. 1990), even to the canal as accurately as possible. In situations partially edentulous patients can benefit from en- where the height of the alveolar crest superior to dosseous implants as an alternative to alveolar the canal is not sufficient for implant placement, tissue-borne prostheses. As for the completely implants can be placed buccally or lingually to the edentulous patient, treatment planning for par- canal provided sufficient space is found to ensure tially edentulous patients requires teamwork. The adequate implant length. The location of the canal radiologist is expected to provide information in the buccolingual direction must then be as- about bone quantity and quality and about ana- sessed. tomical landmarks essential for the placement of The radiographic examination for detecting the implants. The anatomical landmark of special in- mandibular canal is usually initiated with peri- terest in the side segment of the mandible is the apical and panoramic radiographs. Periapical mandibular canal, as it carries the neurovascular radiographs particularly demonstrate the trabecu- bundle. Surgery in this region can adversely affect lar pattern of the bone but visualize the mandibu- neurosensory function over the distribution of the lar canal to a lesser extent than panoramic radio- peripheral nerves of the mandible, resulting in par- graphs (Lindh et al. 1992). Furthermore, a perfect esthesia that may lead to permanent or long-last- isometric projection does not always give a com- ing neurosensory alteration or loss (Misch & plete view of the region between the alveolar crest Crawford 1990; Terry & Zarb 1991). Reports on and the superior border of the canal but is an ab- the use of implants in partially edentulous jaws solute condition for accurate depiction of the man- have been published, and when the posterior parts dibular canal. of the mandible are involved, complications with sensory disturbance are reported (van Steenberghe A rotational panoramic radiograph is valuable for estimating the vertical height of the mandible
61 Measurements of the mandibular canal in radiographs but has the same limitations as the periapical pin also served as reference points (Fig. 1). The radiograph in not visualizing the canal in a bucco- mandibles were radiographically examined and lingual direction. Panoramic radiography has, thereafter sectioned for contact radiography and however, in comparison with computed tomo- histology. graphy (CT), been found to be sufficiently accurate in measuring the vertical bone depth of the man- dible (Tal & Moses 1991). Earlier studies have Radiographic examinations shown that tomographic techniques visualize the At all examinations except CT an additional filter mandibular canal to a greater extent than two-di- of 3 mm Al was attached to the X-ray tube. The mensional radiographs (Klinge et al. 1989; mandibles were positioned, as accurately as poss- Lindh & Petersson 1989; Lindh et al. 1992). Tomo- ible, in a position similar to that of a patient. The graphy can consequently be used when panoramic radiographs were retaken until the image quality radiography fails to visualize the mandibular canal was considered optimal by the oral radiologist who and when a cross-sectional view is wanted. performed the examinations. Measurements for location of the mandibular Panoramic radiographs were obtained with an canal have been carried out using CT (Casselman Orthopantomograph Model OP5 (Siemens, Bens- et al. 1988; Quirynen et al. 1990), hypocycloidal heim, Germany) and a Scanora X-ray unit (Sored- tomography (Petrikowski et al. 1989; Stella & ex, Helsinki, Finland). With the Orthopantomo- Tharanon 1990; Grondahl et al. 1991) and spiral graph, the voltage setting was 55-60 kV and Sie- tomography (Ekestubbe & Grondahl 1993). Klinge mens Titan 2 HS (Siemens, Erlangen, Germany) et al. (1989) compared the accuracy of 4 radio- screens were used. With the Scanora, the voltage graphic techniques in measuring the distance be- setting was 63 kV and Trimax T6 (3M, X-ray tween the alveolar crest and the superior border Products/3M, St. Paul, MN, USA) screens were of the canal. With the exception of the studies by used. Grondahl et al. (1991) and Ekestubbe & Grondahl Three tomographic techniques were used: hypo- (1993), only one observer has made the measure- cycloidal tomography, spiral tomography and CT ments but, as also known from other studies, vari- with direct images. Hypocycloidal tomography ous observers may arrive at different results when was performed with a Universal Polytome (Massi- measuring in the same radiographs (Akesson et al. ot/Philips, Paris, France) with a Siemens Bi 125/ 1992). 3O/5OR tube. The focus-film distance was 1.5 m. A The primary aim of this study was to, in vitro, hypocycloidal motion was used with a tomo- compare the accuracy of measurements with dif- graphic angle of 48° and without a grid. The circu- ferent radiographic techniques using several ob- lar collimator had a diameter of 1.5 cm, resulting servers. The distances between the alveolar crest, in a field size with a diameter of 6.5 cm. Exposure the base of the mandible and the mandibular canal were measured and so was the height of the man- dibular canal. All measurements were compared with measurements on contact radiographs of the same areas. A second aim was to find out the rea- son why measurements could not be carried out as a number of invisible canals were found in a pre- vious study of the same material (Lindh et al. 1992).
Material and methods Six mandibles were removed from individuals aged 62-89 years (mean 76) who had donated their bodies to research before death. The specimens were degloved and fixed in 10% neutralized buf- fered formalin solution. Three tantalum pins were inserted at the buccal side of each mandibular side segment to serve as reference points when measur- ing the radiographs. The tantalum pins were in- Fig. 1. Schematic drawing of a mandibular side segment as de- serted just beneath the mental foramen, 1 and 2 picted in a panoramic view. The tantalum pins were inserted at A, C and E. B, D and F also served as reference points for cm posterior to the foramen. The areas between measuring the distances Dl, D2 and D3. The measurements the pins and 0.5 cm distal to the most posterior were made perpendicular to the tangent line X-Y.
62 Lindh et al.
data were 55-67 kV and 80-120 mA. A multi-film with experience of implant treatment and/or treat- cassette with 4 pairs of rare-earth screens and 4 ment planning. The CT images were assessed by 3 films was used, and the distance between the de- oral radiologists (including the two above), as the picted layers was 3.3 mm (Petersson & Gratt 1985). oral radiologists unlike the other observers were The specimens were oriented in a position such familiar with the CT equipment. Prior to the ob- that tomographic cuts were perpendicular to the servation period, the guidelines for measurements lower border of the mandible and to the buccal were discussed and, in addition to this discussion, and lingual bone plates. Cross-sections, about 1.3 written instructions were given. When assessing a mm thick (Curry et al. 1990), of the mandibles tomographic cut where the canal was difficult to were obtained at 3.3-mm intervals from the mental identify, the observers were told to look at the ad- foramen to 2.5 cm posterior to the foramen. Spiral jacent cuts as well to facilitate the interpretation. tomography was performed with the Scanora X- ray unit according to the technique described by Ekestubbe & Grondahl (1993). The specimens were oriented in the same way as in the Polytome. Measurements Cross-sections in 4-mm-thick contiguous layers In the panoramic radiographs, the outlines of the were obtained along the same region as described base of the mandible as well as the line tangent to before. Four exposures per film were obtained, the base and the lines perpendicular to this, with a field size of 7X 10.2 cm. CT was performed through the reference points, were traced on trans- with a Siemens Somatom DRG (Siemens, Erlang- parent paper. The following distances were meas- en, Germany). Contiguous 2-mm thick slices were ured: taken in the coronal plane, angled perpendicular to the inferior border, and to the buccal and lin- Dl=the distance between the superior border of gual bone plates of the mandibular side segment. the mandibular canal and the alveolar crest. D2=the height of the mandibular canal. D3=the distance between the mandibular base and Sectioning and radiography of sections the inferior border of the mandibular canal. The mandibles were mounted in a precision saw. The measurements were made at the sites of the Slices 2 mm and 5 mm thick were cut using an tantalum pins and 0.5 cm posterior to each pin Exact cutting unit (Exakt Apparatebau, Nord- (Fig. 1). stedt, Germany). The sections were then radio- In the hypocycloidal and spiral tomographic im- graphed with a Siemens PH 125/100 R tube, focus- ages, the same distances (Fig. 2) were measured at film distance 0.7 m. During exposure, the sections the same sites as for the panoramic radiographs were placed in contact with the film packet with the same digimatic caliper (Mitutoyo, Tokyo, (Strukturix D7, Agfa Gevaert, Belgium). Japan) to the nearest 0.1 mm. The CT images were measured directly on the screen using the computer program. If the observers had to exclude measure- Histology ments, they were asked to note the reason for the The 2-mm slices were further processed for embed- exclusion. ding in Kulzer light-curing resin (Technovit 7.200 VLC). Ground sections of about 230 um in thick- ness were made using the Exact equipment and the technique according to Donath (1988). The 5-mm blocks were decalcified in formic acid, trimmed and embedded in paraffin. Serial 7-um-thick sec- tions were cut through the entire extension of the block, and step serial sections at 98-|im intervals (every 14th section) were stained with hematoxylin and eosin and, when applicable, examined with the light microscope.
Observers With the exception of the CT images, 4 observers assessed the radiographs independently. Two of the observers were oral radiologists, one a peri- tance oeiween me superior ana mierior oo: odontologist and one a general practitioner, all ndible. The distances Dl, D2 and D3 were
63 Measurements of the mandibular canal in radiographs Finally, the measurements were performed with hypocycloidal and computed tomography because the same caliper, by one of the observers, on the the radiographic examination did not cover the re- contact radiographs. The histological slides were gion behind the most posteriorly inserted pin at used to identify the neurovascular bundle at 5 sites one site, which made one observation for each of where the bundle was neither wholly nor partially these two tomographic methods impossible and surrounded by a compact outlining and therefore decreased the possible maximum number of meas- undetectable on the contact radiographs (Fig 3A, urements to 71. As the neurovascular bundle was B). All measurements were compared with the cor- not possible to identify at one site on the histologi- responding measurements on the contact radio- cal section, the number of measurements for each graphs. The values from the Scanora panoramic distance that could be compared with the true radiographs and hypocycloidal tomography were value was 70 for hypocycloidal and computed corrected for the magnification factor 1.3, and the tomography and 71 for the other radiographic values from the Scanora tomographic radiographs methods. for the magnification factor 1.7, as referred to by The measured values from the tomographic im- the operating instructions for the X-ray equip- ages deviated less from the measurements on the ment. The values from the OP5 panoramic radio- contact radiographs than the measured values graphs were corrected for the magnification factor from the panoramic views, as shown in Tables 1 1.3 according to Tronje et al. (1985). The measure- and 2. The observers in general underestimated the ments of the height of the mandibular canal were distances related to the mandibular canal, except made twice at 30 sites on the contact radiographs, for hypocycloidal tomography. The mean height of by the same observer. The precision of a single the mandibular canal as measured on the contact measurement was expressed as the standard devi- radiographs (n = l\) was 3.0 mm, with a standard ation, SD=v'ld2/2n, where d is the difference be- deviation of 0.7 mm. The measurement precision tween two measurements of the height of the canal in the contact radiographs was 0.3 mm. and n is the number of duplicate measurements. The observers reported unmeasurable distances to a high degree, and the variation between the Results observers concerning identification of the borders of the mandibular canal was large. One of the ob- A maximum of 72 measurements were available for servers (D) had generally recorded few measure- each distance and radiographic method, except for ments and for none of the distances more than 39
Fig. 3. a. Contact radiograph of a sec- tion of a mandibular side segment where the mandibular canal cannot be de- tected, b. Corresponding histological section with the neurovascular bundle indicated with arrows. Note that there is no compact outlining around the neuro- vascular bundle.
64 Lindh et al.
Table 1. Differences in mm between the observers' measurements and Table 2. Differences in mm between the observers' measurements and the measurements in the contact radiographs for distance D1 (between the measurements in the contact radiographs for distance D3 (between the superior border of the mandibular canal and the alveolar crest), re- the mandibular base and the inferior border of the mandibular canal), ported as mean values and standard deviations (SD) for each radio- reported as mean values and standard deviations (SD) for each radio- graphic technique graphic technique Observer Observer Radiographic Radiographic technique A B C D E technique A B C D E OP5 mean -2.8 -2.2 -1.0 -1.8 OP5 mean -1.3 -1.6 -1.6 -1.4 panoramic SD 2.5 2.7 2.5 2.6 panoramic SD 1.0 1.0 1.3 0.7 n 19 32 62 12 n 30 49 64 27 Scanora mean -1.3 -2.4 -1.4 -2.6 Scanora mean -1.1 -1.2 -0.8 -0.9 panoramic SD 2.3 2.5 1.9 2.8 panoramic SD 0.7 0.8 0.7 0.8 n 30 15 38 9 n 48 51 40 39 Hypocycloidal mean 0.0 0.2 0.6 -0.2 Hypocycloidal mean 0.0 -0.5 0.7 1.1 tomography SD 2.1 1.7 3.1 2.7 tomography SD 1.4 1.9 2.6 3.1 n 28 37 36 30 n 33 48 46 35 Spiral mean -0.6 -0.3 -0.5 -0.7 Spiral mean 0.1 -0.3 0.5 -0.2 tomography SD 2.3 3.3 1.9 1.6 tomography SD 1.9 2.2 2.1 1.6 n 42 44 44 19 n 44 54 48 28 Computed mean -0.6 -1.0 -1.3 Computed mean -0.2 -0.1 -0.4 tomography SD 2.4 2.0 2.4 tomography SD 2.2 1.7 1.6 n 53 50 58 n 55 50 59
recordings with any radiographic method. Only study and this investigation was the relatively large one observer had made more than 60 measure- number of invisible canals, which resulted in diffi- ments at any distance. This observer (C) had in culties in measuring the position of the canal. In general performed most measurements and at no other studies where mandibular specimens have site with any radiographic method less than 36. been used for the same purpose, nothing or very Measurements of the distance D3 showed the least little has been mentioned about difficulties in de- number of missing data. Comparing the 3 tomo- tecting the mandibular canal (Petrikowski et al. graphic methods, computed tomography showed 1989; Quirynen et al. 1990; Tal & Moses 1991). the least number of missing measurements for Klinge et al. (1989), however, found invisible ca- every distance and observer. Comparing hypocyc- nals in 36% of the sites in panoramic radiographs loidal with spiral tomography, spiral tomography where the measurements were made by one ob- showed fewer missing data (Tables 1, 2). server. In our investigation, the percentage of un- The reasons reported why a recording could not measurable sites for measuring the distance be- be carried out are shown in Table 3 for the distance tween the alveolar crest and the mandibular canal Dl and D3. Most of the missing data of Dl were in panoramic radiographs varied between 14% and due to invisibility of the superior border of the 88% among the observers. Stella & Tharanon mandibular canal and to a lesser extent to diffi- (1990) reported invisible canals in 17.5% of hypo- culties in identifying the alveolar crest. Concerning cycloidal tomograms as well as on the correspond- D3, all measurements were due to invisibility of ing slices of the mandibular specimens, which is the inferior border of the mandibular canal. The considerably fewer compared with our results, number of sites where all observers measured the where the observers reported unmeasureable dis- distances, related to radiographic technique, are tances between the alveolar crest and the superior shown in Table 4. border of the canal in 48-60%. One explanation of the difference between the results could be that, in the investigation by Stella & Tharanon (1990), Discussion only one observer performed the measurements A primary aim of this study was to find out which and fewer measuring sites were used. A recent clin- radiographic method was most accurate in locat- ical study (Ekestubbe & Grondahl 1993) suggested ing the mandibular canal. In an earlier study, the that the larger thickness of the image layers with visibility of the mandibular canal assessed with the the Scanora technique simplifies the detection of same radiographic techniques was investigated thinner structures such as the border of the man- (Lindh et al. 1992). A result common to the latter dibular canal compared with hypocycloidal tomo-
65 Measurements of the mandibular canal in radiographs
Table 3. Reported reasons (all observers) for not measuring the distances in the different radiographic techniques. The figures are given in per cent of the total number of missing measurements
Invisible Invisible Invisible Invisible superior border alveolar alveolar crest inferior of mandibular crest and superior border of canal border of mandibular mandibular canal Radiographic canal technique % % % %
0P5 panoramic 52 3 40 Scanora panoramic 65 1 37 Hypocycloidal tomography 44 B 2 43 Spiral tomography 32 9 5 38 Computed tomography 24 23
graphy. This explains our finding that the borders et al. (1991), who found better agreement between of the mandibular canal were better identified with oral radiologists in evaluation of the distance from spiral tomography than with hypocycloidal tomo- the alveolar crest to the mandibular canal on hypo- graphy. Though in some rare cases, what is iden- cycloidal tomograms than between oral surgeons. tified in a tomographic cut as the mandibular canal This could be due to the fact that oral radiologists, could be an artifact or the bony trabeculae (Lindh especially from the same department, have the et al. 1992). We found at five sites that the neuro- same policy in radiographic interpretation of vascular bundle was not surrounded by a compact tomographs and are more aware of the errors of outlining, and we had to use the histological slide interpretation than other observers. to identify the neurovascular bundle. The histo- In the comparison of the measurements from logical slides were found to be unsuitable for meas- the different radiographic techniques, the same urements due to dimensional changes during prep- magnification factors were used as when measur- aration. ing in radiographs from patient examinations, as The observers in this study were presented with our aim was to simulate a clinical situation. The both verbal and written instructions, and the cri- greatest inaccuracy of measurements was found teria for the measurements were well defined. In when using panoramic images. This is consistent spite of this, the interobserver variation of per- with the recommendation by Tronje et al. (1981) formed measurements was large. Two observers (A that, when great accuracy is necessary, the use of and B) are oral radiologists at the same depart- panoramic films is inadvisable and that vertical ment, and though there was a variation in the measurements must be regarded with caution. number of measurements between these two ob- Measurements on tomographic images were more servers, they were more concordant than the other accurate than those on panoramic radiographs. observers in detecting the mandibular canal. This This strengthens the recommendation to use tomo- corresponds with the results reported by Grondahl graphy before implant surgery in the posterior part of the mandible, not only because these im- ages show the mandibular canal in a buccolingual direction but also because of the greater accuracy Table 4. Number of sites where all observers performed measurements of such measurements. CT examination visualized of the distances D1 (between the superior border of the mandibular canal and the alveolar crest), D2 (the height of the mandibular canal) and D3 the mandibular canal to a greater extent than the (between the mandibular base and the inferior border of the mandibular other two tomographic techniques but was not canal), related to radiographic technique more accurate when the distances were measured. In the study by Klinge et al. (1989), the results Number of sites showed that CT gave the most accurate position of Radiographic technique Dl D2 D3 the mandibular canal, but in that investigation only one observer assessed the radiographs, which 0P5 panoramic (u=72) 6 5 20 could be a source of error when comparing the Scanora panoramic (n=72) 4 4 28 Hypocycloidal tomography (n=71) 12 16 18 results with those of this study. Direct CT examin- Spiral tomography (n=72) 18 26 26 ation of the mandibular side segment is difficult to Computed tomography (n=71)" 44 44 44 perform, as the patient has to bend his or her neck in an extreme position. Furthermore, metallic den- * Computed tomography was measured by 3 observers and the other techniques by 4 observers. tal restorations in the opposite upper jaw create
66 Lindh et al. artifacts, making it difficult to see the canal. CT uncertainty about the visibility of the superior bor- is an expensive examination and delivers a greater der of the mandibular canal. radiation dose than panoramic and other tomo- We believe that, under special circumstances, graphic examinations (Clark et al. 1990; Ekestub- panoramic together with periapical radiographs be et al. 1993). One should require a substantial can form the radiographic basis for implant increase in the information provided by CT to jus- surgery in the posterior part of the mandible. This tify the risk associated with the radiation required. may be the case when radiographic and clinical Perhaps this increase in information could be examination leave no doubt about, either the loca- achieved with a CT examination performed with tion of the mandibular canal or whether the height axial slices and reconstructions of the side segment of the crest superior to the canal is sufficient for of the mandible. In an earlier study, we have shown implant placement. The same conditions are pres- that reconstructed images from a Somatom DRG ent when nerve transpositioning is to be done, showed extremely low visibility of the mandibular which can be performed with successful results in- canal (Lindh et al. 1992). Newer CT equipment dependent of the height of the alveolar crest (Ro- may give better information concerning the visi- senquist 1991). However, in all other cases we rec- bility of the mandibular canal, and in addition to ommend a tomographic method for detecting the this, increase the possibility of measurements. mandibular canal and for measuring vertical dis- Under- as well as overestimation of the distance tances within the alveolar bone of the posterior between the alveolar crest and the superior border part of the mandible. Direct CT examination is not of the mandibular canal could be devastating for the necessary for accurate measurements and still result of the implant operation. Overestimation of leaves many unsolved problems. We could not find the distance could result in insertion of an implant, any differences between hypocycloidal and spiral which may interfere with the neurovascular bundle tomography concerning accuracy, but spiral tomo- and cause paresthesia of the chin and lower lip. graphy visualizes the mandibular canal to a some- Underestimation might lead to a decision to use what greater extent and visualization is, without a shorter implant than necessary, which could be doubt, an absolute condition for measurements. one of the factors that affects the prognosis of the treatment (Henry et al. 1993). In this study there was a tendency to underestimate the distance from Resume the alveolar crest to the superior border of the Avant la chirurgie implantaire dans les zones mandibulaires, il mandibular canal. A detailed statistical analysis est extremement important de localiser le canal mandibulaire was not considered meaningful for two reasons. dans les radiographies afin d'eviter l'interference avec le fais- One was the small number of jaws, which in turn seau neurovasculaire durant la chirurgie. Six mandibules ont depends on the limited supply of autopsy speci- ete radiographiees avec deux panoramiques et trois tomo- mens, and the other reason was the great observer graphies. Les distances entre le bord superieur du canal et le rebord alveolaire, et entre la base mandibulaire et Ie bord infe- variation in detecting the mandibular canal. rieur du canal ont ete mesurees ainsi que la hauteur de canal. The distance between the inferior border of the Les mesures ont ete effectuees par trois ou quatre personnes et mandibular canal and the mandibular base was comparees avec les mesures de radiographie de contact des me- easier to measure than any other distance meas- mes zones. La tomographie donne des valeurs plus justes des distances mentionnees que les radiographies panoramiques. La ured in this study. This could be due to the fact variation interindividuelle etait importante. that the mandibular base is easier to identify than the alveolar crest and/or that the inferior border of the mandibular canal is better visualized than the Zusammenfassung superior border of the canal. In addition, the re- gion of the mandible that extends from the canal Vor Implantatchirurgie im Seitenzahnbereich des Unterkiefers ist es von allergrOsstem Interesse, den Mandibularkanal auf to the bottom of the mandible is not significantly ROntgenbildern zu lokalisieren, um eine Verletzung des neuro- affected by bone resorption and atrophy (Abrah- vaskula'ren Stranges wShrend des chirurgischen Eingriffes zu ams 1992). Heasman (1988) found that- the mean vermeiden. Sechs UnterkieferprSparate wurden mit zwei Pano- diameter of 190 canals at the vertical level of third rama- und drei Tomographietechniken r6ntgenologisch unter- molars was 3.25 mm±0.39 mm and our corre- sucht. Die Distanzen zwischen der oberen Begrenzung des Ka- nals und dem Kieferkamm und der unteren Begrenzung des sponding measurements on contact radiographs of Kanals und der Kieferbasis wurden ausgemessen. Zusatzlich the mandibular side segments gave a value of 3.0 wurde die Hohe des Kanals ermittelt. Die Messungen wurden mm with a standard deviation of 0.7 mm. Based von drei oder vier Untersuchern durchgefahrt und mit Messun- on these findings, it may be possible to recommend gen auf Kontaktrontgenbildern derselben Regionen verglichen. Die Tomographie ergab genauere Werte der obengenannten measurements between the mandibular base and AbstSnde als die Panoramatechniken. Die Unterschiede im the inferior border of the canal and of the height Auffinden des Mandibularkanals zwischen den Untersuchern of the alveolar bone before surgery when there is waren betrachtlich.
67 Measurements of the mandibular canal in radiographs
Heasman, P. A. (1988) Variation in the position of the inferior Resumen dental canal and its significance to restorative dentistry. Antes de la cirugía de implantes en el segmento lateral de la Journal of Dentistry 16: 36-39. mandíbula, es de sumo interés localizar el canal mandibular Henry, P. J., Tolman, D. E. & Bolender, C (1993) The applica- en radiografías para evitar interferencias con el paquete neuro- bility of osseointegrated implants in the treatment of par- vascular durante la cirugía. Seis especímenes mandibulares fue- tially edentulous patients: three-year results of a prospective ron examinados radiográficamente con dos técnicas panorámi- multicenter "study. Quintessence International 24: 123-129. cas y tres tomográficas. Se midieron las distancias entre el borde Klinge, B., Petersson, A. & Maly, P. (1989) Location of the superior del canal y la cresta alveolar y entre la base mandibu- mandibular canal: comparison of macroscopic findings, con- lar y el borde inferior del canal. Además, se midió la altura del ventional radiography and computed tomography. Interna- canal. Las medidas fueron realizadas por tres o cuatro observa- tional Journal of Oral & Maxillofacial Implants 4: 327-332. dores y comparadas con mediadas en radiografía de contacto Lindh, C. & Petersson, A. (1989) Radiologie examination for de las mismas áreas. La tomograña dio valores más exactos de location of the mandibular canal: a comparison between pan- las distancias que las técnicas panorámicas. Las variación entre oramic radiography and conventional tomography. Interna- observadores en descubrir el canal de mandibular fue grande. tional Journal of Oral & Maxillofacial Implants 4: 249-253. Lindh, C, Petersson, A. & Klinge, B. (1992) Visualisation of the mandibular canal by different radiographie techniques. References Clinical Oral Implants Research 3: 90-97. Misch, C. E. & Crawford, E. A. (1990) Predictable mandibular Abrahams, J. J. (1992) CT assessment of dental implant plan- nerve location - a clinical zone of safety. International ning. Oral and Maxillofacial Surgery Clinics of North Amer- Journal of Oral Implantology 7: 37-40. ica 4: 1-18. Petersson, A. R. & Gratt, B. M. (1985) A rare-earth screen Adell, R., Eriksson, B,, Lekholm, U., Brånemark, P.-I. & Jemt, multisection cassette for temporomandibular joint tomo- T. (1990) A long-term follow-up study of osseointegrated im- graphy: a technical report. Dentomaxillofacial Radiology 14: plants in the treatment of totally edentulous jaws. Interna- 31-36. tiona! Journal of Oral & Maxillofacial Implants 5: 347-358. Petrikowski, C. G., Pharoah, M. J. & Schmitt, A. (1989) Presur- Akesson, L., Håkansson, J. & Rohlin, M. (1992) Comparison gical radiographie assessment for implants. Journal of Pros- of panoramic and intraoral radiography and pocket probing thetic Dentistry 61: 59-64. for the measurement of the marginal bone level. Journal of Quirynen, M., Lamoral, Y., Dekeyser, C, Peene, P., van Steen- Clinical Periodontology 19: 326-332. berghe, D., Bonte, J. & Baert, A. L. (1990) The CT scan Åstrand, P., Borg, K., Gunne, J. & Olsson, M. (1991) Combi- standard reconstruction technique for reliable jaw bone vol- nation of natural teeth and osseointegrated implants as pros- ume determination. International Journal of Oral & Maxillo- thesis abutments; a 2-year longitudinal study. International facial Implants 5: 384-389. Journal of Oral & Maxillofacial Implants 6: 305-312. Rosenquist, B. (1991) Fixture placement posterior to the mental Casselman, J. W., Quirynen, M., Lemahieu, S. F., Baert, A. foramen with transpositioning of the inferior alveolar nerve. L. & Bonte, J. (1988) Computed tomography in the determi- International Journal of Oral & Maxillofacial Implants 7: 45- nation of anatomical landmarks in the perspective of endos- 50. seous oral implant installation. Journal of Head & Neck Path- Stella, J. P. & Tharanon, W. (1990) A precise radiographie ology 7: 255-264. method to determine the location of the inferior alveolar ca- Clark, D. E., Danforth, R. A., Barnes, R. W. & Burtch, M. L. nal in the posterior edentulous mandible: implications for (1990) Radiation absorbed from dental implant radiography: dental implants. 1. Technique. International Journal of Oral & a comparison of linear tomography, CT scan, and panoramic Maxillofacial Implants 5: 15-22. and intra oral techniques. Jorunal of Oral Implantology 16: Tal, H. & Moses, O. (1991) A comparison of panoramic radi- 156-164. ography with computed tomography in the planning of im- Curry,T. S., Dowdey, J. E. &Murry,R. C. (1990) Christensens plant surgery. Dentomaxillofacial Radiology 20: 40-42. introduction to the physics of radiology. 4th edn. Philadelphia: Terry, B. C. & Zarb, G. A. (1991) Report on the 4th Interna- Lea & Febiger, p. 246. tional Cohgress on Preprosthetic Surgery. Palm Springs, Donath, K. (1988) Die Trenn-Dünnschlifftechnik zur Herstel- USA, 18-20 April. International Journal of Oral and Maxillo- lung Histologischer Präparaten von nicht schneidbaren Ge- facial Surgery 20: 314-316. weben und Materialen. Der Präparator 34: 197-206. Tronje, G., Eliasson, S., Julin, P. & Welander, U. (1981) Image Ekestubbe, A. & Gröndahl, H.-G. (1993) Reliability of spiral distortion in rotational panoramic radiography. Vertical dis- tomography with the Scanora technique for dental implant tances. Acta Radiológica 22: 449-455. planning. Clinical Oral Implants Research 4: 195-202. Tronje, G., Welander, U, McDavid, W. D. & Morris, C. R. Ekestubbe, A., Thilander, A., Gröndahl, K. & Gröndahl, H.- (1985) Horizontal and vartical magnification. 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68 QUANTITATIVE COMPUTED TOMOGRAPHY OF TRABECULAR BONE IN THE MANDIBLE
C. Lindh*, M. Nilsson**, B. Klinge***, A. Petersson*
* Department of Oral Radiology, Centre for Oral Health Sciences, Lund University,
Malmo, Sweden
** Department of Radiation Physics, University Hospital, Malmo, Sweden
*** Department of Periodontology, Karolinska Institutet, Stockholm, Sweden
Running title: Quantitative computed tomography
Key Words: Mandible; x-ray tomography computed; osteoporosis; dental implantation
69 ABSTRACT
Objectives: To evaluate the potential use of quantitative computed tomography (QCT) for the assessment of bone mineral density of the edentulous mandible prior to implant placement.
Methods: Ten 2 mm thick CT slices of anterior and posterior edentulous sections from
15 mandibles were obtained perpendicular to the buccal and lingual plates. The bone mineral density, expressed as the amount of calcium hydroxyapatite in mg/cm , of the trabecular bone, was calculated using a method that takes into account the influence of fat.
Results: The variation of bone mineral density between mandibles was high. Anterior sections showed higher values than posterior sections and a variation was found within sections of the same mandible.
Conclusions: CT provides a site-related measure of the bone mineral density in the mandible and appears potentially useful as a non-invasive method to determine a parameter that may reflect bone quality prior to implant placement.
70 INTRODUCTION
Bone quality is referred in many follow-up studies of implant treatment as a factor of
great importance in the outcome1'5. However, it is obvious that the term 'bone
quality' is open to considerable interpretation and there is no real consensus in the
literature6. Bone quality probably reflects a number of aspects of bone morphology of
which the degree of mineralization may be one. The radiological methods that have
been developed for determining the bone mineral density (BMD) are mainly used to
study skeletal changes in osteoporosis and other metabolic bone diseases7.
Densitometric measurements have been made from intra-oral and panoramic
radiographs of the mandible to find signs of osteoporosis8'10. Dual photon
absorptiometry11''2 and dual energy X-ray absorptiometry13 have been used to measure
BMD of the mandible and to correlate it with that of other parts of the skeleton. Both
these methods measure an integrated sum of cortical and trabecular bone density.
However, the consistency of the trabecular bone is particularly significant in implant
treatment, especially when the cortex is thin and the implant is inserted mainly in trabecular bone. Computed tomography (CT) is the only non-invasive pre-operative
method where it is possible to obtain information on the degree of mineralization of trabecular bone as distract from the cortex. At present, it is mainly used pre- operatively to evaluate jaw bone volume and to make measurements of bone height
and width14*17. Although, it has been suggested by a number of workers in this field that CT scans could provide radiological densiometric readings of the bone tissue in
Hounsfield units I8"20, there are no previous reports on the measurement of BMD for the purpose of evaluation of bone quality in the jaws prior to implant treatment.
Quantitative computed tomography (QCT) has the major advantage of enabling trabecular and cortical bone density to be evaluated separately. Bone mineral content
71 has been assessed of the mandible11-12 but QCT of the trabecular bone density has been limited to correlating it with the degree of skeletal osteoporosis in postmenopausal women21. The aim of the present study was to evaluate the possible use of QCT for measuring the trabecular BMD in the edentulous mandible prior to implant placement.
72 MATERIAL AND METHOD
Material
The material consisted of 15 mandibles from individuals aged 62-94 years (mean 79 years) who before death had elected to donate their bodies to medical research. There was no history of disease or treatment that may have altered bone metabolism. The whole body was fixed in formalin using a mortal perfusion technique. The mandibles were later removed, degloved and post-fixed in 10% neutralized buffered formalin solution. This method preserves both the structure and tissues, including fat. The mandibles were wholly or partially edentulous and sections without teeth, six anterior and 27 posterior, were examined. To obtain reference points, two tantalum pins (1.5mm x 0.5mm) were inserted at the buccal side of each edentulous section. In the posterior sections, one pin was inserted just beneath the mental foramen and the other pin 2 cm distally. In the anterior sections the pins were inserted 1 cm from the midline on each side.
Production of CT images
CT images were obtained with a Somatom DRG scanner (Siemens, Erlangen, Germany) at 125 kV and 230 mAs with a slice thickness of 2 mm using a standard convolution kernel. The mandibles were carefully positioned with the scanning planes perpendicular to the buccal and lingual plates. Ten direct CT images were obtained of the section between the tantalum pins (Figure 1), except for one mandible (no. 6), where seven slices were taken. The accuracy of slice-thickness and table-feed was checked with a weekly quality assurance programme. The region of interest (ROI) was defined manually on each image as the trabecular bone, 1-2 mm from the inner
73 margin of the cortex (Figure 2 left). However, if there was a break in the inner cortex, the innermost part was included in the ROI (Figure 2 right). Every CT image was enlarged in order to increase the accuracy when the region of interest was superimposed on the image using a graphic tablet. The enlargement procedure did not affect the quantitative data obtained.
Figure 1. Schematic drawing of a mandible illustrating how the CT scans were obtained perpendicular to the mandible in the anterior and posterior sections as indicated by the tantalum pins.
74 Outline of Outline of ROI ROI
Figure 2. Schematic drawings of CT images illustrating how the region of interest (ROI) was allocated between the cortical (A) and the trabecular (B) bone. The margin between A and B is well defined on the left but difficult to identify on the right.
Calibration of the CT scanner for BMD determination
The calibration procedure is described in detail by Nilsson et aP2. The CT scanner was calibrated for BMD determination using a) BMD simulating substances samples placed in a phantom simulating the skull and b) the same samples placed in free air (simulating the mandibles in this study). Due to the very hard beam filtration of the Somatom DRG unit (added filtration 2.5 mm Al + 0.4 mm Cu), the beam hardening in
75 the lower part of the skull phantom is not very pronounced. The calibration equation did therefore not significantly differ for these two situations and could be described by the equation
3 4 2 BMD (mg/cm ) = 0.960 (Humem +14) - 2.3 x 10" (Hu^+14)
where HU,,,^,, is the mean Hounsfield value in the trabecular part of the mandible. It must be stressed that this calibration is valid only for this type of CT scanner, for a slice thickness of 2 mm and using a specific convolution kernel.
The Somatom DRG scanner uses Caesium iodide (Cs I) scintillation detectors which are very sensitive to variations in temperature. Effects of drifting on the sensitivity of the detector, both as a whole and for individual detector elements, have to be corrected at least every hour. This procedure, called air calibration is performed with no object in the gantry. In this study, 'air calibration' was always carried out immediately prior to scanning.
Statistical analysis
Differences in BMD between mandibles and different sections of the mandibles were investigated using analysis of variance with repeated measurements. A statistically significant difference was considered to be present when p ^ 0.05. The measurement of BMD was performed twice in 20 CT images. The second measurement was made at least one week after the first one and the entire procedure with window-setting and enlargement was repeated. The precision of single measurements was expressed as the standard deviation s = Vd2/2n , where d is the difference between two measurements
76 and n is the number of duplicate measurements. The measurement precision was estimated to be s=17 mg/cm3-
77 RESULTS
The results of the measurements of BMD are shown in Table I. Significant differences
(p=0.0001) in mean BMD were found between the fifteen mandibles. Measurements were performed in both anterior and posterior sections in six mandibles, and, with the exception of one (no.8), the differences were significant (p < 0.05): values were higher in anterior than in posterior sections, as shown in Figure 3. The variation between different slices within a section was also large, as can be seen from the maximum and minimum values in Table I. The mean BMD for the first five slices were compared with those of the last five in the 12 mandibles where measurements were made on both left and right posterior sections; those for the first five slices were higher in 16 of the 24 sections examined (Figures 4 and 5). However, significant differences were found in only nine of these sections. An example of a CT image with a high BMD is shown in Figure 6 (left) and one with low BMD in Figure 6 (right).
78 Table L Mean and standard deviation (SD) of BMD (amount of calcium hydroxyapatite in mg/cm3) in 33 sections of 15 mandibles. Minimum and maximum values are given for the different slices within the mandibular sections.
Mandible Section Side Mean SD Min Max value value value
1 posterior R 294 47 236 382 anterior 580 99 433 683 posterior L 348 53 281 425
2 posterior R 177 56 112 271 anterior 457 115 351 700 posterior L 341 161 72 543
3 posterior R 207 45 122 277 posterior L 238 51 149 310
4 posterior R 134 53 41 200 anterior 349 93 214 440 posterior L 207 170 -35 461
5 posterior R 479 58 379 541 posterior L 410 77 244 484
6 posterior R 169 35 101 210
7 posterior R 176 55 78 261 anterior 444 86 308 563 posterior L 107 151 -147 274
8 posterior R 194 46 139 260 anterior 233 77 113 394 posterior L 213 38 169 271
9 anterior 354 60 257 452 posterior L 224 92 -3 303
10 posterior R 205 45 152 309 posterior L 207 24 160 236
11 posterior R 11 35 -52 68
12 posterior R 162 78 64
posterior L 132 80 42 t o 0 O
13 posterior R 227 41 153 267 posterior L 209 70 100 304
14 posterior R 197 34 142 249 posterior L 181 19 154 216
15 posterior R 462 89 398 602 posterior L 487 84 359 613
79 Mean of BMD 600
500 -
400 -
1 Leftpost | | Anterior 1 Right post 4 7 Mandible no.
Figure 3. Histogram showing mean values for BMD in anterior and posterior sections of six mandibles
Mean of BMD 600
500 -
300 -
Flight first 4 5 7 8 10 12 13 14 15 Mandible no.
Figure 4. Histogram showing mean values for BMD of the first five and last five scans of the right posterior sections in twelve mandibles.
80 Mean of BMD 600
500 400 r 300
200
100 Left 0 |i last Left first -100 1 2 3 4 5 7 8 10 12 13 14 15 Mandible no.
Figure 5. Histogram showing mean values for BMD of the first five and last five slices of the left posterior mandibular sections in twelve mandibles.
Figure 6. CT images from a site in the mandible where BMD was high (left) and low (right)
81 DISCUSSION
We determined BMD by single-energy QCT. The precision is higher than that for
dual-energy QCT but the accuracy is lower due to the errors arising from the fat
content of the trabecular bone23'24. The method used in our study reduces its influence
on the derived values by taking into account the fact that, with few exceptions, the
trabecular bone is replaced by fatty bone marrow with increasing age22. This is
illustrated by the negative BMD value found at four sites, which indicates that there is no or very little mineral within these trabecular bone specimens. This affects both density and atomic composition of the region being investigated. The effective atomic
number of trabecular bone is reduced, mainly due to the higher proportion of carbon
in fat and bone marrow and the relatively lower calcium hydroxyapatite content. As a
consequence, the BMD is reduced. The change in density as recorded by CT will therefore be a function of the reduction in both density and mean atomic number in individuals with a lower BMD. This will lead to a non-linear calibration curve that can be described by a two-degree polynomial. Different workers calibrate their CT units with different concentrations of bone mineral-simulating substances (for example
KjHPC^ or CaHPO4). However, the liquid in the sample is commonly of the same atomic composition, regardless of the 'BMD' concentration. Therefore, the variation in effective atomic number in such samples does not reflect that of human trabecular bone, and this will lead to erroneous results, especially for low and high BMDs. For instance, using a calibration based on KJHPO,, solutions in water for the Somatom CT unit will yield a correct BMD result for a human trabecular bone specimen with a mean value of about 320 Hounsfield units, but will give results that are 6 % too low and too high at 40 and 580 Hounsfield units, respectively.
82 Taguchi et al.24 studied the effect of the size of the ROI in QCT and found that a
ROI < 1 cm2 with a 2 mm slice thickness gave unacceptable results, but the values for
ROI > 1 cm2 those more than 1 cm2 were consistent. If axial scans are used, the buccal and lingual plates at a specific site limit the area that is possible to measure. In contrast, none of our perpendicular slices was less than lcm2,which gave a larger area to measure. The precision of a single measurement was also found to be high.
However, direct CT scans perpendicular to the buccal and lingual bone plates are difficult to obtain clinically because of difficulties in patient positioning. We therefore intend to compare the results of BMD measurements in reformatted axial scans with those from the direct images in our study.
QCT has previously been used to measure mineral content in the trabecular bone of lumbar vertebrae22. However, results from measurements in other parts of the skeleton should not be compared with those in the mandible, as the latter seems to be subject to a more marked decrease in the amount of bone mineral through life25. This was confirmed by Klemetti et al.21, who found no correlation between BMD in the trabecular bone of the mandible, femoral neck or lumbar spine. Using mandibular autopsy specimens gave us an opportunity to compare BMD with other measurements such as of the trabecular bone volume at the same site which we will report subsequently.
We found higher values of BMD in the trabecular bone of anterior compared with posterior sections and also marked variations within the same section. This is in agreement with Klemetti et al.21. However, they found generally higher values of
BMD. This could be due to the fact that their patients were younger than the individuals we examined. There are also several other reports confirming that the bone in the anterior part of the mandible is denser than in the posterior and that
83 variations in bone density are found in the same region26"28. However, it is not clear whether dense bone means the high quality required for successful implant treatment.
In a clinical follow-up study, Friberg et al.3 found the highest fixture loss in mandibles with the densest bone and in maxillas with low density trabecular bone. They suggested that failure may be due to overheating during drilling at bone sites with high density.
The future demands for implant treatment are difficult to predict but will probably increase in the partially dentate population. This, together with the fact that the anterior teeth in the mandible are usually retained the longest, makes it important to be able to estimate bone quality in the posterior parts of the jaw. In our view, bone quality must be described in a more detailed way, which should include not only mineral content but also the volume and structure of both cortical and trabecular bone.
BMD measurements of the trabecular bone are needed because the skeleton undergoes age- related changes which affect trabecular bone, due to its higher turn-over rate, more than they affect cortical bone29. QCT gives a site-related measure of BMD which could be an advantage since, as shown in our study, the bone tissue varies within a small area.
84 REFERENCES
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87 I NEXT PAGE(S) I left BLANK TRABECULAR BONE VOLUME AND BONE MINERAL DENSITY IN THE MANDIBLE
C. Lindh*, A. Petersson*, B. Klinge**, M. Nilsson***
* Department of Oral Radiology, Centre for Oral Health Sciences, Lund University,
Malmo, Sweden
** Department of Periodontology, Karolinska Institutet, Stockholm, Sweden *** Department of Radiation Physics, University Hospital, Malmo, Sweden B Running title: Bone morphometry in the mandible
Key words: dental implantation; tomography, x-ray computed; bone density, bone mineral content
89 ABSTRACT
Objectives: To explore the correlation between trabecular bone volume and bone mineral density in mandibular autopsy specimens.
Methods: The bone mineral density of the trabecular bone was obtained from quantitative computed tomography. Two mm thick CT-slices of anterior and posterior edentulous sections from nine mandibles were evaluated. Thereafter the sections were cut into 2 mm thick bone slices and contact radiography was performed. A computer- based image analysis system was used for morphometric measurements of trabecular bone volume in the contact radiographs.
Results: A significant correlation was found between trabecular bone volume and bone mineral density. The trabecular bone volume varied significantly between and within mandibles.
Conclusion: The high correlation between trabecular bone volume and bone mineral density ascertains the possibility to use quantitative computed tomography prior to implant treatment.
90 INTRODUCTION
Osseointegration is defined as a direct structural and functional connection between ordered, living bone and the surface of a load-carrying implant1. When inserting endosseous implants in the jaws the main part of the fixture is anchored in the trabecular part of the bone. Therefore, it is extremely important to achieve knowledges of the properties of the trabecular bone and to evaluate different preoperative techniques for assessing the state of the bone tissue before implant treatment. Plain radiography2 as well as tomographic techniques3-4 are commonly used to assess the alveolar bone but these techniques leave difficulties in determining the structure of the trabecular bone.
Wide normal variations have been found in the structure of the trabecular bone of the human skeleton5, as well as of the mandible6"8. Several techniques have been used at bone morphometry and in the last decades computer-based systems have shown to be helpful tools in bone morphometric analysis9'10. Mostly stained sections and microradiographs from bone biopsies of the femur and spine have been analysed for estimates of percentage bone volume11 and for analysis of bone architecture12. Bone morphometry has a role to play in measuring the form and structure of the trabeculae, but there is also a need to study the relationship between morphometric data and other factors that contribute to the properties of the trabecular bone. The degree of mineralisation is a factor that may reflect bone quality13 and this parameter can be investigated by means of several methods14. Quantitative computed tomography is however the only non-invasive method that allows mineral measurements of the cortical and trabecular bone components separately. Bone mineral density measured with quantitative computed tomography has been related to histological findings in vertebrae15, but regarding the mandible only cortical bone mass has been object of
91 comparisons between morphometric data and measurements of mineral content16. The trabecular bone volume in the mandible has not previously been compared with measurements of bone mineral density obtained with quantitative computed tomography.
The aim of our study was to correlate, in mandibular autopsy specimens, the bone mineral density obtained from quantitative computed tomography, to the trabecular bone volume measured in contact radiographs with aid of computer-based image analysis. The trabecular bone volume was measured in two different ways; in the same region of interest as defined at computed tomography and further in a region of interest showing the maximum outline of the trabecular bone volume.
The following abbreviations are used:
CT = computed tomography
QCT = quantitative computed tomography
ROI[ = region of interest outlined on a CT-image and automatically transferred
to a corresponding contact radiograph
ROI2 = region of interest outlined on a contact radiograph
BMD = bone mineral density expressed as amount of calcium hydroxyapatite
in mg/cm3 in ROIj
TBV = trabecular bone volume calculated as the fractional area percentage of
trabeculae within ROI,
TTBV = total trabecular bone volume calculated as the fractional area
percentage of trabeculae within ROI2
92 MATERIAL AND METHODS
The material consisted of nine, wholly or partially edentulous, mandibular autopsy specimens from individuals aged 62 - 94 years (mean 81 years) who before death had donated their bodies to research. There was no history of any systemic, endocrine or skeletal bone disorders that may have affected bone metabolism. The full body was fixated using a mortal perfusion technique with formalin as fixation solution. The mandibles were later removed, degloved and post-fixed in 10% neutralised buffered formalin solution. To obtain reference points, two tantalum pins (length 1.5mm,
0 0.5mm) were inserted at the buccal side of each edentulous section of the mandibles.
In the posterior sections one pin was inserted just beneath the mental foramen and the other pin 2 cm distally. In the anterior sections the tantalum pins were inserted 1 cm from the midline on each side. Six anterior and 16 posterior edentulous sections were prepared for examinations.
Calculation of bone mineral density
The mandibles were examined with CT and direct images of 2 mm thick slices perpendicular to the buccal and lingual bone plates were obtained from each section, between the tantalum pins. The ROI[ was traced when moving a cursor on a tablet on each image, defining the trabecular bone 1-2 mm from the inner margin of the cortex.
The mineral content was calculated within ROI, from every CT-image as described previously by Lindh et alP. BMD was presented as the amount of calcium hydroxyapatite in mg/cm3 according to the method stated by Nilsson et al.18. The monitor screen of the CT-unit was photographed using a Polaroid camera, and a photo of every CT-image with the outlined RO^ was obtained (Figure 1).
93 Cutting procedure and radiography of mandibular bone slices
Each mandible was cut into one anterior and two posterior sections. Each section was mounted in a precision saw and the areas between the tantalum pins were cut into six to ten 2 mm thick slices using an Exact cutting unit (Exakt Apparatebau, Nordstedt,
Germany). The slices were radiographed with a Siemens Bi 150/30/52 R 100 tube, focus-film distance 0.75 m (35 kV, 100 mAs) and focus size 0.6 mm. During exposure the mar.dibular slices were placed in direct contact with the film packet
(Strukturix D7, Agfa Gevaert, Belgium). The films were developed manually and a contact radiograph of each 2 mm mandibular bone slice was obtained (Figure 1). To control the developing procedure films were exposed with the same exposure parameters with an aluminium step wedge serving as a density reference. These films were developed next to every fourth of the contact radiographs and densitometric measurements of the steps in the aluminium step wedge were performed.
94 Figure 1
Schematic drawing of a mandible illustrating how the CT scans and the thin bone slices were obtained perpendicular to the mandible in the anterior and posterior sections as indicated by the tantalum pins. A CT image is shown to the left and the corresponding contact radiograph of the same mandibular slice to the right.
95 Analysis of the trabecular bone volume (TBV) within ROI,
A contact radiograph was placed on a view box with fixed light intensity in front of a
Hamamatsu CCD video camera C 4742, 1018 x 1000 pixels, with a Canon TV Zoom lens V6xl6, 16 - 100 mm, 1:1.9. The images were digitized in a frame grabber hardware card (Synoptics Sprynt using intel i860 RISC chip at 25 MHz offering 50
MFlops processing rate) installed in a Dell 433/T microcomputer. Two Mitsubishi
Diamond Pro 17 screens (1280 x 1024 pixels) showing 255 greylevels were connected to the computer. A photo of the corresponding CT-image was scanned by the same video camera and shown, side by side together with the contact radiograph from the same mandibular slice, on one of the screens. The two images were zoomed to be of approximately the same size on the monitor screen. A Semper 6 Plus (Synoptics Ltd,
Cambridge,UK) image analysis program was used for image analysis and processing.
Prior to further analysis this program made a final correction for positioning and enlargement between the two images. The ROI, outlined on the CT-image was filled in moving a cursor on a tablet, whereafter the analysis program automatically transferred the ROIj to the contact radiograph. The contrast and brightness of the radiograph were set to give the best possible image of the trabeculae. The measurements were performed in a room with no daylight and care was taken to keep the CCD camera exposure parameters such as zoom-factor, diaphragm, gain and offset constant. A coarse threshold was set manually in a way that all features were registered to define the trabeculae within the ROIj. The image analyser then automatically applied local thresholding on the source image whereby the threshold was set to the half height value at all transition points between background and foreground. This ensured repeatability of the measurements and minimised operator errors and also preserved the morphology of the features independent of their size.
96 The TBV within the ROIj was calculated given as the fractional area percentage of
trabeculae.
Analysis of total trabecular bone volume (TTBV) within ROI2
A contact radiograph was placed on the view box, digitized and shown on one of the
screens. The image was enlarged as much as possible to increase the accuracy when
separating the trabecular and cortical bone components. The cursor was moved on a
tablet in a way that the trabecular part of the bone was enclosed as close as possible to
the inner margin of the cortex. The thresholding procedure was done as described
above and the TTBV was given as the fractional area percentage of trabeculae within
ROIj.
Statistics
The correlation between TBV and BMD as well as between TTBV and BMD within
mandibles and for the total material was calculated.
The mandibles where measurements were performed in both anterior and posterior
sections (n=6) were first analysed concerning differences in TBV between mandibles
and between anterior and posterior sections within mandibles. A second analysis was
performed in the same way concerning differences in TTBV. These differences were
investigated using analysis of variance with repeated measurements. Differences between TBV and TTBV was calculated for all mandibles (n=9) using the same type
of analysis. A difference was considered statistically significant when p < 0.05.
97 The measurement of TBV as well as of TTBV was performed twice in 20 radiographs, with at least one week in between. The precision of a single measurement was expressed as the standard deviation s = VEdV2n, where d is the difference between two measurements and n is the number of duplicate measurements. The TBV measurement precision was estimated to be s = 2.8% and TTBV measurement precision s= 1.7%.
98 RESULTS
The correlation between BMD values, TBV and TTBV values, respectively, are
shown in Table I and Figures 2 and 3. A significant correlation (p = 0.0001,
BMD/TBV; r = 0.69 and BMD/TTBV; r = 0.70) was found for the whole material
and considering individual mandibles the correlation was significant in seven for
BMD/TBV and six for BMD/TTBV of the nine mandibles (Table I).
The results of the measurements of TBV and TTBV are shown in Table II. The
analysis of TBV values showed a significant mandible variation (p < 0.001).
Measurements were performed in both anterior and posterior sections in six of the nine
mandibles. The mean TBV values were significantly higher (p = 0.0001) in anterior
than in posterior sections and concerning TTBV values the same results were found.
The values of TTBV were significantly higher (p < 0.0001) than the TBV values both
concerning individual slices, mean values from sections of mandibles and mean values from mandibles.
99 Table I. Correlation (r) between bone mineral density (BMD), trabecular bone volume
(TBV) and total trabecular bone volume (TTBV) respectively, measured in the slices
(n) of nine mandibles.
BMD/TBV BMD/TTBV
Mandible
1 25 0.85 *** 25 0.87 ***
2 26 0.77 *** 26 0.77 ***
3 20 0.46* 20 0.33
4 24 0.66 *** 23 0.43*
5 18 0.41 18 0.29
6 7 0.86* 7 0.87*
7 29 0.86 *** 29 0.80 ***
8 23 0.25 23 6.28
9 17 0.79 *** 17 0.65 **
Significant correlation, *p < 0.05 , **p <, 0.01, ***p < 0.001
100 mg/cm3 t 1 i i i r i i t r -200 -100 0 100 200 300 400 500 600 700 BMD
Figure 2 Correlation between trabecular bone volume (TBV) and bone mineral density (BMD).
TTBV
mg/cm3 20 -I i i i i i r -200 -100 0 100 200 300 400 500 600 700 BMD
Figure 3 Correlation between total trabecular bone volume (TTBV) and bone mineral density (BMD).
101 Table II. Mean and standard deviation (SD) of trabecular bone volume (TBV) and total trabecular bone volume (TTBV) in the slices (n) of 22 sections of nine mandibles
TBV % TTBV %
Mandible Section Side n mean SD n mean SD
1 posterior right 9 40 6.0 9 44 4.7 anterior 7 68 4.8 7 71 5.6 posterior left 9 46 7.0 9 51 6.4
2 posterior right 9 34 7.8 9 39 6.7 anterior 8 60 6.9 8 65 8.2 posterior left 9 45 18.8 9 47 15.1
3 posterior right 10 42 14.1 10 41 9.9 posterior left 10 36 8.9 10 41 8.0
4 posterior right 9 36 7.0 8 38 2.9 anterior 6 56 2.4 6 57 6.1 posterior left 9 45 7.0 9 52 5.5
5 posterior right 9 52 4.7 9 58 3.2 posterior left 9 45 5.1 9 53 7.4
6 posterior right 7 36 2.7 7 39 5.7 left 9 39 3.9
7 posterior right 10 45 5.8 10 47 6.5 anterior 9 54 7.4 9 54 5.6 posterior left 10 38 7.6 10 41 6.2
8 posterior right 8 38 2.7 8 41 1.4 anterior 6 47 5.5 6 50 6.1 posterior left 9 39 3.2 9 44 2.0
9 anterior 7 57 8.0 7 58 6.0 posterior left 10 27 5.1 10 34 6.0 DISCUSSION
The specimen preparation was critical in our study as the trabecular bone volume was correlated to bone mineral density in the same bone slices. Contact radiographs of 2 mm thick bone slices were used for measurements of the trabecular bone volume. A thickness of 2 mm was choosen, because the trabecular bone volume should be compared to bone mineral density by means of QCT in images of 2 mm thick slices. Furthermore, a thickness of 2 mm was necessary to preserve the trabecular structure at the preparation and no artifacts were found in the images. All trabeculae in the whole depth of the slice were imaged as the method was based on the attenuation of X-rays, which was an advantage, as we actually wanted to make estimates of a volume and not only of the trabeculae at the surface of a slice.
Computer-based image analysis has been found to be precise and time-saving in morphometric measurements of bone samples compared to manual methods9'19. The contact radiographs were analysed with aid of an image analysis program according to its shading of grey. Converting a grey-level image to a binary image, where the grey- level image contains a mix of small and large features and varying back-ground level, presents a problem for the image analyser. To overcome this a coarse threshhold was set manually in a way that all features were registered. Together with the fact that special care was taken to keep all exposure parameters constant gave a high precision in the measurements. For high contrast objects the spatial resolution of the video camera at the zoom factor used was 5 line pairs/mm which corresponds to a capacity to detect objects of the size of 100 u,m. This could be compared to the trabecular width of lll±26um found by Bergot et alP- in a study of vertebral trabeculae. According to this the video camera had a sufficient resolution capacity in detecting bone trabeculae.
103 There is a considerable variation in the literature with respect to the terms used for various values obtained in bone morphometry20. The most commonly used histomorphometric bone parameter has been the trabecular bone volume, which reflects the amount of bone within the spongy space21. However, the term trabecular bone volume can be questioned and is according to Parfitt et al.22 not correct as these authors mean that the term "bone' includes both mineralised bone and osteoid. The osteoid is not possible to detect in contact radiographs and /wsfo-morphometry was not performed. However, we found the term trabecular bone volume appropriate to apply as it is often used in the literature and describes our measurements in the best possible way.
We found an overall high correlation between bone mineral density and trabecular bone volume. This is certainly due to the fact that the measurements were performed in the same part of the skeleton and moreover at the same site. The correlation between similar variables, but from different parts of the skeleton, has been analysed23.
When the mandible is involved precautions must be taken in comparisons with other parts of the skeleton as there are studies that indicate that at least the mineral content in the mandible do not correlate to other parts of the skeleton2425. However, for some mandibles in our study the correlation between bone mineral density and trabecular bone volume was not significant. This was probably due to that difficulties arose when cutting the mandibular sections into 2 mm thick bone slices. This was particularly obvious for anterior sections, resulting in a variation of the number of bone slices that could be obtained. Accordingly there could have been some displacement in relation to the CT-slices.
104 The significant difference found in trabecular bone volume, between mandibles and
between sections of the same mandible, corresponds with results from other
investigations of human mandibles7-8'17. The trabecular bone occupies only 20% of the
fraction of the skeleton but has a relatively large surface involved in remodeling
activity, which explains the higher metabolic bone activity compared to cortical bone26.
The percentage of bone tissue within the trabecular bone gives a much better
indication of osteoporosis than the percentage of bone tissue between the periostal
surfaces21. This probably makes the trabecular bone interesting in implant treatment as
it is likely to be a major determinant of bone strength27.
When defining the region of interest in the CT images, one must be aware of the fact
that an image artifact always is generated in CT images where there is a sharp gradient
in density in the object. Due to the nature of the convolution cernels used in the
filtered back-projection algorithms, the area just adjacent to a high-density object (as
the cortical bone in the images in this study) is shown in the image with too low
Hounsfield number. This problem can partly be overcome if ultra high resolution
cernels are used when reconstructing the images, but this will in its turn give rise to an
extremely noisy image and will seriously impair quantification of the bone mineral
density in those trabecular parts that are not affected by this artifact. In this study we
have used standard konvolution cernels and have drawn the region of interest at a
"safe" distance from the cortical border. When transferring the RO^ from the CT
images to the contact radiographs we accordingly discovered that an additional
amount of trabecular bone was visible outside the region of interest. In a separate
study28 we wanted to relate measurements of trabecular bone volume to assessments
of the trabecular pattern in intra-oral radiographs. It has been found that the trabecular pattern seen in plain radiographs is formed in the junction area between trabecular and cortical bone29. Therefore, we measured the total trabecular bone
105 volume as well, which was found to give significantly higher values than values of trabecular bone volume, but also correlated significantly to values of bone mineral density.
In conclusion we have investigated two properties of the trabecular bone tissue that could be of importance for the outcome of implant treatment. We found a high correlation between bone mineral density measured by QCT and trabecular bone volume, which ascertains the usefulness of QCT prior to endosseous implant treatment, a method that will be further evaluated in a clinical study. Significant variations were found in trabecular bone volume between and within mandibles, which emphasize the importance of specific site classifications prior to implant treatment.
106 ACKNOWLEDGEMENT
We wish to express our gratitude to Per-Erik Isberg, Department of Statistics, Lund University, for statistical analysis.
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14. TothillP. Methods of bone mineral measurement. PhysMedBiol 1989; 34: 543-72.
15. Ito M, Hayashi K, Uetani M et al. Bone mineral and other bone components in vertebrae evaluated by QCT and MRI. Skeletal Radiol 1993; 22: 109-13.
16. von Wowern N. Dual-photon absorptiometry of mandibles: in vitro test of a new method. ScandJDent Res 1985; 93: 169-77.
17. Lindh C, Nilsson M, Klinge B, Petersson A. Quantitative computed tomography of trabecular bone in the mandible. Dentomaxillofac Radiol. 1996; 25. In press.
18. Nilsson M, Johnell O, Jonsson K, Redlund-Johnell I. Quantitative computed tomography in measurement of vertebral trabecular bone mass. A modified method. Acta Radiol 1988; 29: 719-25.
19. Rooryck V, Klinge B. Computer-assisted image processing for quantitative measurements of fractional bone area. Acta Odontol Scand 1995; 53: 115-22.
20. RevellPA. Histomorphometry of bone. JClinPathol 1983; 36: 1323-31
21. Boyce BF, Courpron P, Meunier PJ. Amount of bone in osteoporosis and physiological senile osteopenia. Comparison of two histomorphometric parameters. Metab Bone Dis RelatRes 1978; 1: 35-8.
22. Parfitt MA, Drezner MK, Glorieux FH et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR histomorphometry nomenclature committee. JBone and Miner Res 1987; 2: 595-610.
23. Geraets WGM, van der Stelt PF, Netelenbos CJ, Elders PJM. A new method for automatic recognition of the radiographic trabecular pattern. JBone and Miner Res 1990; 5 :227-33.
24. von Wowern N, Storm TL, Olgaard K. Bone mineral content by photon absorptiometry of the mandible compared with that of the forearm and lumbar spine. Calcif Tissue Int 1988; 42: 157-61.
25. Klemetti E, Vainio P, Lassila V, Alhava E. Trabecular bone mineral density of mandible and alveolar height in postmenopausal momen. Scand J Dent Res 1993; 101: 166-70.
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28. Lindh C, Petersson A, Rohlin M. Assessment of the trabecular pattern prior to endosseous implant treatment. Diagnostic outcome of periapical radiography in the mandible. Accepted for publication in Oral Surg Oral Med Oral Pathol Oral Radiol Endod
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110 ASSESSMENT OF THE TRABECULAR PATTERN PRIOR TO ENDOSSEOUS IMPLANT TREATMENT
Diagnostic outcome of periapical radiography in the mandible
Christina Lindh, Arne Petersson, Madeleine Rohlin
Department of Oral Radiology, Centre for Oral Health Sciences, Lund University,
Malmo, Sweden
Running title: Trabecular pattern in the mandible
111 ABSTRACT
Objectives: To study the diagnostic outcome of periapical radiography in the assessment of the bone trabecular pattern of the mandible.
Study design: Mandibular autopsy specimens were radiographed. Seven observers assessed the radiographs with the aid of a proposed classification with and without reference images and the classification presented by Lekholm and Zarb12. Accuracy was estimated on the basis of morphometric measurements of trabecular bone volume.
Observer agreement was calculated as the estimated probability of agreement between and within observers and as Kappa index.
Results: With the classification proposed by us, the overall accuracy was 58% with and 50% without reference images. The accuracy for assessing dense trabeculation was higher (78%) than that for sparse trabeculation (28%). The accuracy of the classification by Lekholm and Zarb12 was not possible to evaluate. The interobserver agreement varied between 49% and 64% and the intraobserver agreement between
75% and 86%.
Conclusion: The new classification with reference images is recommended to assess the trabecular pattern in periapical radiographs prior to implant treatment.
112 INTRODUCTION
High clinical success is described in many follow-up reports concerning implant treatment both for the totally1 and for the partially edentulous patient2'3. The successful outcome of implant surgery is said to be dependent on the status of the implant bed4. A well-founded preoperative evaluation of the bone characteristics will therefore facilitate the appraisement of components contributing to high clinical success. The preoperative evaluation of jaw bone characteristics is mostly done on the basis of radiographic examinations5-6. However, the concept bone quality is confusing as there is no clear definition of the term7.
Radiographic indices have been suggested for the description of bone quality in, for example, the hip joint to predict the outcome of surgical interventions8-9. Attempts have also been made to categorize the jaw bone quality 10'n. The classification by
Lekholm and Zarb12 is the most widely used in connection with assessment of bone tissue prior to and during endosseous implant surgery. It is not clear from the original publication whether the classification is intended to be applied to preoperative radiographs, during surgery or both. Furthermore, the classification by Lekholm and
Zarb12 has not been evaluated in terms of diagnostic accuracy and observer performance.
Plain radiography providing a two-dimensional image of the jaw bone is a cheap and widely used technique. It was therefore considered useful to explore the diagnostic value of periapical radiography for the assessment of bone characteristics. The aim of this study was to investigate the observer performance and the diagnostic outcome of periapical radiography in the assessment of the trabecular pattern of the mandible.
113 Three classification systems for the assessment of the trabecular pattern were evaluated.
114 MATERIAL AND METHODS
Material
The material consisted of nine mandibular autopsy specimens from individuals aged
62 to 94 years (mean 81 years) who before death had donated their bodies to research.
Six mandibles were edentulous and three were partially dentate. The specimens were degloved and fixed in 10% neutralized buffered formalin solution. Then, six anterior sections were taken from the edentulous specimens and 17 edentulous posterior sections from all specimens for examination.
Radiographic examination
Prior to the radiographic examination, tantalum pins (length 1.5mm, 0 0.5mm) were inserted at the buccal side of each edentulous section of the mandibles. In the posterior sections, a tantalum pin was inserted just beneath the mental foramen and another pin two centimeters distally to the foramen. In the anterior sections one tantalum pin was inserted one centimeter on each side from the midline.
The sections were examined using a Siemens Heliodent EC dental x-ray unit (Siemens,
Bensheim, Germany) operating at 60 kVp and Ektaspeed Plus film (Eastman-Kodak
Co, Rochester, N.Y., USA) with the film placed parallel to the mandibular body.
During exposure a 0.5 cm thick acrylic plate was placed buccally of the mandibular section in order to compensate for the lack of soft tissue. Twelve radiographs of randomly chosen mandibular sections were exposed using different exposure times.
The preferences of four oral radiologists were used to identify one radiograph imaging the anterior section and one imaging the posterior section to present images of optimal
115 density for the purpose of assessing the trabecular pattern. The density of these two radiographs served as a reference when exposure times were chosen for the examinations of all sections. Neither these two radiographs nor the other ten were further used in the study.
Number of radiographs and observers
Twenty-three radiographs were obtained from the mandibular sections. Three radiographs used as reference images were not included in the assessment. Of the remaining 20 radiographs, six were randomly chosen for duplication and added to the original radiographs. Thus, 26 radiographs in all were presented to seven observers, four oral radiologists, two periodontologists and one oral surgeon. All observers had experience of implant treatment and/or treatment planning. During assessment the use of a magnifying viewer (X-produkter, Malmo, Sweden) was recommended. The observers were asked to assess the region outlined by the images of the two tantalum pins and the region between the alveolar ridge and the cortical bone of the mandibular base (Figure 1). In the radiographs from the anterior sections the area of the mental spine was to be left out of consideration. After three weeks three observers were asked to assess all radiographs a second time.
116 Classifications for radiographic assessment of the trabecular pattern
Each observer assessed the radiographs using three classifications:
A. A written classification presented in the text of Figure 1 describing the trabecular pattern as
* dense trabeculation,
* alternating dense and sparse trabeculation or
* sparse trabeculation.
B. The written classification described above together with reference radiographs presenting each of the three classes as presented in Figure 1.
C. The classification proposed by Lekholm and Zarb12, consisting of four classes. The observers had the schematic drawings and the written description presented in Figure 2 at hand.
Measurement of the total trabecular bone volume
Following the radiographic examinations each mandibular autopsy specimen was cut into one anterior and two posterior sections. The sections were further cut into six to ten 2 mm thick bone slices perpendicular to the buccal and lingual bone plates, using an Exakt cutting unit (Exakt Apparatebau, Nordstedt, Germany). The slices were radiographed with a Siemens Bi 150/30/52 R 100 tube, focus-film distance 0.75 m
(35kV, 100 mAs) and focus size 0.6 mm. Contact radiographs were obtained by placing the mandibular slices in direct contact with the film packet (Strukturix D7,
Agfa Gevaert, Belgium).
117 Figure 1.
Reference images from mandibular sections presenting the trabecular pattern as (A) dense trabeculation (B) alternating dense and sparse trabeculation and (C) sparse trabeculation are shown to the left. The region between the tantalum pins from the alveolar crest to the mandibular base was assessed. Corresponding contact radiographs (D,E,F) of 2 mm thick cross-sectional slices of the mandibular sections are shown to the right.
118 Figure 2.
A proposed classification of jaw bone quality according to Lekholm and Zarb12: (1) almost the entire jaw is comprised of homogeneous compact bone; (2) a thick layer of compact bone surrounds a core of dense trabecular bone; (3) a thin layer of cortical bone surrounds a core of dense trabecular bone of favourable strength; (4) a thin layer of cortical bone surrounds a core of low density trabecualr bone. (From Lekholm U and Zarb GA. Patient selection and preparation. In: Branemark P-I, Zarb GA, Albrektsson T, eds. Tissue-Integrated Prostheses. Osseointegration in Clinical Dentistry. Chicago, Bl:Quintessence, 1985:202. With kind permission from Quintessence publishing CO.,inc.)
119 Thereafter, a contact radiograph was placed on a view box with fixed light intensity in front of a Hamamatsu CCD video camera C 4742, 1018 x 1000 pixels, with a Canon
TV Zoom lens V6xl6, 16 - 100 mm, 1:1.9. The images were digitized in a frame grabber hardware card (Synoptics Sprynt using intel i860 RISC chip at 25 MHz offering 50 MFlops processing rate) installed in a Dell 433/T microcomputer. Two
Mitsubishi Diamond Pro 17 screens (1280 xlO24 pixels) showing 255 graylevels were connected to the computer. The image was enlarged as much as possible to increase the accuracy when separating the trabecular and cortical bone components. The contrast and brightness of the radiograph were set to give the best possible image of the trabeculae. The procedure was performed in a room with no daylight and care was taken to keep the CCD camera exposure parameters such as zoom-factor, diaphragm, gain and offset constant. A Semper 6 Plus (Synoptics Ltd, Cambridge, UK) image analysis program was used for image analysis and processing. A region of interest
(ROI) was outlined by moving a cursor on a tablet in a way that the trabecular part of the bone was enclosed as close as possible to the inner margin of the cortex. A coarse threshold was set manually in a way that all features were registered to define the trabeculae within the ROI. The image analyzer then automatically applied local thresholding on the source image whereby the threshold was set to the half height value at all transition points between background and foreground. This ensured repeatability of the measurements and minimized operator errors and also preserved the morphology of the features independent of their size. The total trabecular bone volume (TTBV) within ROI was calculated given as the fractional area percentage of trabeculae.
The measurement was performed twice in 20 radiographs with at least one week in between. The precision of a single measurement was expressed as the standard
120 deviation s = VSd2/2n, where d is the difference between two measurements and n is the number of duplicate measurements. The TTBV measurement precision was s=1.7%.
Validation of reference images
The reference images of classification B were validated on the basis of the TTBV measurements. The mean values and standard deviations (SD) of the TTBV were calculated for each mandibular section (Table I). The radiograph of the posterior section presenting the highest mean TTBV in combination with the lowest SD was selected as the reference image showing dense trabeculation. The radiograph of the posterior section presenting the mean TTBV closest to the overall mean TTBV of all sections, together with the highest SD, was chosen as the reference image showing dense and sparse trabeculation. Finally, the radiograph of the posterior section presenting the lowest mean TTBV and a low SD, was selected as the reference image showing sparse bone trabeculation. Contact radiographs corresponding to the reference images showing dense trabeculation, alternating dense and sparse trabeculation and sparse trabeculation, respectively, are presented in Figure 1.
Analysis of observer agreement
With respect to both inter- and intraobserver agreement, two different measures were calculated. Interobserver agreement was described by the estimated probability that two observers agreed when assessing the same image. The estimate is computed using all pairs of judgements performed by two different observers assessing the same object. Six of the images occurred twice in the material, increasing the number of
121 pairs available for the interobserver study. The interobserver agreement was also calculated as Kappa index for several observers13.
The intraobserver agreement was expressed as the estimated probability that the same observer agreed with himself/herself when assessing the same radiograph twice. It was taken into account that six of the images occurred twice in the material and consequently were assessed twice by all observers and four times by the observers who performed all assessments twice. The intraobserver agreement was also calculated as
Kappa index14, based on three observers' assessments. The six-point scale as proposed by Landis and Koch15 was used to interpret the Kappa index.
Analysis of accuracy
The gold standard was based on the mean TTBV of each of the 23 mandibular sections. The mean TTBV was calculated from the TTBV of 6-10 slices of each section (Table I). The overall mean TTBV of the 23 sections, i.e. the whole material, was 48 % (SD 9.5 %). Seven sections with a mean TTBV ranging between 53% and
71% were subjectively chosen to represent sections with dense trabeculation. Eleven sections with a mean TTBV ranging between 41% and 52% represented sections with alternating dense and sparse trabeculation and five sections with a mean TTBV between 34% and 40 % represented sparse trabeculation.
The accuracy of the classification with reference images was compared with the classification without reference images. For each of the ten observations and each of the 26 images, it was checked whether the assessments according to the classification
122 with or without reference images were closest to the gold standard as defined by the mean TTBV values.
123 Table I. Mean and standard deviation (SD) of total trabecular bone volume (TTBV) in the slices (n=number of slices) of 23 mandibular sections of 9 mandibles. Radiographs of the sections in bold were used as reference images.
Mandible Section Side n TTBV Mean SD
1 posterior right 9 44 4.7 anterior 7 71 5.6 posterior left 9 51 6.4
2 posterior right 9 39 6.7 anterior 8 65 8.2 posterior left 9 47 15.1 alternating dense/sparse trabeculation 3 posterior right 10 41 10.0 posterior left 10 41 8.0
4 posterior right 8 38 2.7 anterior 6 57 6.1 posterior left 9 52 5.5
5 posterior right 9 58 3.2 dense posterior left 9 53 7.4 trabeculation
6 posterior right 7 39 5.7 posterior left 9 39 3.9
7 posterior right 10 47 6.5 anterior 9 54 5.6 posterior left 10 41 6.2
8 posterior right 8 41 1.4 anterior 6 50 6.1 posterior left 9 44 2.0
9 anterior 7 58 6.0 posterior left 10 34 6.0 dense trabeculation
124 RESULTS
Observer agreement
As shown in Tables II and III, the interobserver agreement expressed as the estimated probability of agreement was 60% with the classification with reference images, 64% without reference images and 49% with the method proposed by Lekholm and Zarb12.
The Kappa index was 0.32, 0.35 and 0.33, respectively, for the three classifications.
As can be seen in Table III, the observers mainly used only two classes, class 3 and 4, as presented in Figure 2, when the classification proposed by Lekholm and Zarb12 was applied.
The corresponding figures for the intraobserver agreement, which are presented in
Tables III and IV, were 75% for the method with reference images, 86% without reference images and 76% with Lekholm and Zarb's12 method. Kappa indices based on three observers' assessments were, for the classification with reference images
0.81, 0.67 and 0.36 (mean 0.61) and for the classification without reference images
0.61, 0.65 and 0.75 (mean 0.67). The corresponding figures for the Lekholm and
Zarb12 classification were 0.05,0.5 and 0.74 (mean 0.43).
125 Table II. Interobserver agreement of assessment of the trabecular pattern in periapical radiographs of the mandible. Figures in bold correspond to agreement within pairs of observers. The observers had a written classification with and without reference images as described in Figure 1 at hand, describing the trabecular pattern as: dense trabeculation, dense and sparse trabeculation (dense/sparse) and sparse trabeculation.
With reference images Without reference images
Trabecular Dense Dense/sparse Sparse Dense Dense/sparse Sparse pattern
Dense 404 260 173 657 429 59 Dense/sparse 461 210 316 80 Sparse 88 55
Total 1596 1 596 Table HI. Interobserver and intraobserver agreement of assessment of the trabecular pattern in periapical radiographs of the mandible. Figures in bold correspond to agreement within pairs of observers (upper part of the table) and within observers (lower part of the table). The observers had the classification proposed by Lekholm and Zarb12 consisting of four classes as described in Figure 2 at hand.
INTEROBSERVER AGREEMENT
Class 1 2 3 4
1 5 21 102 20
2 12 260 85
3 600 328
4 163
Total 1596
INTRAOBSERVER AGREEMENT
Class 12 3 4
1 2 2 0 0
2 6 13 3
3 101 23
4 24
Total 174
127 Table IV. Intraobserver agreement of assessment of the trabecular pattern in periapicai radiographs of the mandible. Figures in bold correspond to agreement when assessing the radiographs more than once. The observers had a written classification with and without reference images as described in Figure 1 at hand, describing the trabecular pattern as: dense trabeculation, dense and sparse trabeculation (dense/sparse) and sparse trabeculation.
With reference images Without reference images
!-• Trabecular Dense Dense/sparse Sparse Dense Dense/sparse Sparse oo pattern
Dense 62 15 6 101 19 2 Dense/Sparse 54 23 44 4 Sparse 14 4
Total 174 174 Accuracy
It was quite obvious that the trabecular pattern as observed by contact radiography of the mandibles was different from the schematic drawings of jaw bone quality classification presented by Lekholm and Zarb12 (compare Figure 1 with Figure 2). Therefore, we considered that it was not possible to estimate the accuracy of this classification.
Table V presents the accuracy of our classification with and without reference images. Overall, 58 % of the ratings were concordant with the gold standard with reference images and 50% without reference images. It was easier to assess the radiographs with alternating dense and sparse trabeculation with the aid of reference images than without reference images. The two classifications were comparable for dense or sparse trabeculation . The highest accuracy was obtained for the images with dense trabeculation, where 78% of the ratings with reference images and 75% of those without reference images were concordant with the gold standard (Table V). The accuracy for assessing radiographs with alternating dense and sparse trabeculation was 57% with reference images and 44% without reference images. Corresponding figures for assessing sparse trabeculation were only 28% and 26%, respectively. Two of the observers considered that the reference images did not facilitate the classification. Notwithstanding, both observers increased their accuracy with the aid of the reference images, 69% and 62% as compared to 46% and 46% without reference images.
129 Table V. Accuracy of radiographic assessment of the trabecular pattern in the mandible compared to a gold standard (coded TTBV mean values from morphometric measurements of contact radiographs). The upper part of the table presents observers' assessments comparing the classifications with and without reference images in radiographs validated as having dense trabeculation. The middle and lower parts of the table present the corresponding comparisons in radiographs validated as having alternating dense and sparse trabeculation (dense/sparse) and sparse trabeculation, respectively. Figures in bold refer to observers' assessments concordant with the gold standard.
Observers' assessments of mandibular sections with a mean TTBV £ 53%
Classification with reference images Classification without reference images Dense Dense/sparse Sparse Total
Dense 54 4 2 60 Dense/sparse 6 9 0 15 Sparse 2 2 1 5
Total 62 15 3 80~
Observers' assessments of mandibular sections with a mean TTBV = 41%-52%
Dense Dense/sparse Sparse Total
Dense 21 24 19 64 Dense/sparse 7 44 6 57 Sparse 1 6 2 9
Total 29 74 27 130
Observers'assessments of mandibular sections with a mean TTBV £ 40%
Dense Dense/sparse Sparse Total
Dense 2 5 4 11 Dense/sparse 1 19 6 26 Sparse 0 9 4 13
Total 31 33 14 50~
130 DISCUSSION
The classification of the jaws with regard to jaw bone quality as proposed by
Lekholm and Zarb12 is well established. However, when interpreting periapical radiographs prior to treatment with implants we found it difficult to apply, especially in the posterior region of the mandible. Dense trabeculation and sparse trabeculation were found to be representative image features but the surrounding cortical bone was not visualized in the periapical radiographs. Furthermore, for some regions the trabecular bone pattern was varying and a single feature was not sufficient. Therefore, a class describing the trabecular pattern as alternating dense and sparse was included in our classification. Another feature of the trabecular bone which might be distinguishable in periapical radiographs is the thickness of the bone trabeculae. Inclusion of this feature would have led to a minimum of two subgroups, thin and thick bone trabeculae, to each of the three classes of our system. As such a classification might be too complicated and less efficient to use in clinical practice, we found it not relevant to incorporate this feature in our classification.
The prerequisite for assessment of accuracy is that external evidence, i.e. evidence entirely separate from information obtained via the system under study16, can be established. In this study morphometric measurements of the total trabecular bone volume were used as the gold standard for periapical radiography. Although these measurements were performed with the aid of radiography, the measure of the total trabecular bone volume of thin slices obtained perpendicular to the sections imaged by periapical radiographs should be regarded as an objective analysis of the
131 bone tissue. No other classification system used for implant treatment has been compared to a gold standard. The classification proposed by Lekholm and Zarb12 is mainly based on personal experience and the opinion of the surgeon, which might be subjective. Trabecular bone volume was correlated to bone mineral density by quantitative computed tomography17, which is another method to describe bone characteristics.
When choosing reference images, the two radiographs showing the highest mean
TTBV values were excluded as they depicted anterior mandibular sections. Only eight of the 26 radiographs assessed by the observers were from anterior regions.
As anterior sections in general showed a denser trabecular pattern than those of the posterior region, it was considered inappropriate to use one of the two above as a reference image. Most of the radiographs of the posterior sections would then have been classified as imaging sparse trabeculation and the three classes of the classification would have been insufficiently used.
Seven observers were selected because very little is generally to be gained by going beyond about seven16. The same observers took part throughout the study.
Written instructions with details of the purpose of the study, the material and the region to be assessed in the periapical radiographs were provided and intended as a form of calibration of the observers. In addition to this, oral explanations were given if wanted. Observer agreement was described both as Kappa index and as estimated probability of agreement between and within the observers. The Kappa index was chosen because this is the most widely accepted measure of agreement when considering data from nominal or ordinal scales18. However, the Kappa
132 coefficients are usually not sufficient to demonstrate the qualities of the methods
studied19. Therefore, the estimated probability of agreement between and within
observers was calculated as well, taken into account that six of the images
occurred twice in the material.
The radiographic assessment of bone tissue prior to implant treatment differs from
most other diagnostic tasks. Generally, image reading is a matter of identifying a
signal (the radiologic abnormality) against a noisy background of structures and of
combining the features meaningfully to discriminate between two alternatives,
disease and no disease. The diagnosis schemata are then based on the assignment
of features to normal-anatomy schemata and to features "left over" presenting
possible abnormalities20. Furthermore, an appropriate clinical history is known to
improve perceptual performance21 on image features that ought to be present or
absent in order for the disease category to be confirmed or rejected. When the
bone tissue is assessed prior to endosseous implant treatment, the described
circumstances do not exist. The observer has to deal with normal variations when
categorizing the normality into three or four groups rather than to conceptualize the signal into an abnormal/normal call. Although the observers were experienced
in the interpretation of periapical radiographs, they were outside their domains of
expertise as they did not know beforehand the significant features of the present
assessment.
There was quite a difference between accuracy for images with dense trabeculation, being 78% and for images with sparse trabeculation being, 28%.
The accuracy for images presenting alternating dense and sparse trabeculation was
133 in between, 57%. This might indicate that the images with dense trabeculation were so-called clear-cut cases, whereas the images with sparse and alternating dense and sparse trabeculation were more difficult to separate. In the assessment of a method, it is important to be aware that if only clear-cut cases are included a reasonably good method will be labelled 'very good'. On the other hand, if unclear cases make up the series of cases, the method will be labelled 'poor' or 'fair'19. Our result indicated that we had selected a mixture of clear-cut and unclear cases, which accordingly is an advantage in the evaluation of the diagnostic outcome of our methods. The reference images resulted in a slight increase of accuracy, especially for images with alternating dense and sparse trabeculation.
The use of reference images has been shown to increase both inter- and intraobserver agreement22-23. This is not consistent with our results. Judged from the results on both the inter- and intraobserver agreement, the classification without reference images was the best method, calculated as the estimated probability of agreement between and within observers. When the the classification by Lekholm and Zarb12 was applied there was a low agreement between the observers in there way to define bone quality. In 30% of the assessments one observer classified the bone trabeculae to be dense (classes 1,2 and 3, see Figure 2), whereas another observer classified the same mandibular section to display a sparse trabeculation (class 4, see Figure 2). The clinical implication of such an observer difference might be a variation in treatment decision, i.e. one observer will propose implant treatment, whereas another will not. Based on the Kappa index, all three classifications were comparable, 'fair' according to Landis and Koch15, as regards interobserver agreement. The
134 intraobserver agreement was 'good' for the majority of assessments with and
without reference images, but varied substantially using the Lekholm and
Zarb12classification. Mostly only two classes of this classification were applied by
the observers, a fact that actually should have increased the observer agreement.
The fact that the reference images did not increase the observer agreement, which
was also found in a study by Thanyakarn et al.24, indicated that it is difficult to
change the judgement of the observer, who is a unique individual with his or her
own references for the assessments. This was illustrated by the two observers who
are both experienced radiologists and who clearly expressed the confusion they felt
when using the reference images. Both achieved higher accuracy with the aid of
reference images but they were obviously not aware of the guidance. Another
reason why the observer agreement did not increase with the reference images
could be that the observers did not find the grading of the reference films to be
discriminating enough, a fact stressed by Cockshott and Park22.
The bone pattern of the four illustrations of the classification proposed by Lekholm
and Zarb12 was not possible to compare with that presented by the contact
radiographs. The illustrations show an even layer of compact bone surrounding a
core of homogeneous trabecular bone with high or low density. It was obvious
from the contact radiographs, however, that the trabecular bone varied in structure
and that the compact layer surrounding the trabecular bone was of varying thickness. The mandibles in our study were from normal individuals with no history of disease or medical treatment that may have influenced bone metabolism.
Therefore, our findings are probably valid in general. The observations are consistent with the results of Parfitt25, that jaw bone trabeculae have a great normal
135 variation in shape, size and thickness. Furthermore, the compact bone was mostly
thin at the top of the alveolar crest. This finding stresses the importance of the
trabecular bone tissue in implant surgery, especially in the posterior regions of the
mandible, where it is impossible to anchor the fixture in the compact bone of the
mandibular base unless a nerve reposition is performed. In clinical practice the classification by Lekholm and Zarb12 is mostly used to evaluate the bone quality of the entire jaw. Bone properties vary within small areas26'27 and when using a
classification it would be more appropriate to classify individual sites of the jaws.
Until now the clinical impact of a radiographic assessment of bone trabecular
pattern on the planning, performance and prognosis of implant treatment has not been studied in an unbiassed analysis. A classification of the trabecular bone tissue
with known diagnostic properties should form the basis for such an analysis. We
propose a new classification to assess the bone trabecular pattern with the aid of
periapical radiographs. The classification, which is based on qualitative evaluation
of jaw bone prior to implant treatment, is presented with and without reference
images. We recommend the classification with reference images as this system
resulted in the highest diagnostic accuracy. It remains to be proved if the
classification will improve clinical decision-making and thereby the management of the patient.
136 ACKNOWLEDGEMENT
We wish to express our gratitude to Professor Jan Lanke, Department of Statistics, Lund University, for statistical analysis.
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