Radiographic Assessment of Peri-Implant Vertical Bone Loss: DICRG Interim Report No. 9

J OralMaxiliofac Surg 55:62-71, 1997, Suppl 5

Radiographic Assessment of Peri-Implant Vertical Bone Loss: DICRG Interim Report No. 9 MICHAEL C. MANZ, DDS, MPH* Vertical bone loss is being assessed radiographically as part of the Dental Implant Clinical Research Group studies through direct measurements on study radiographs taken longitudinally at surgery and recall appointments. Preliminary results and trends for the period between implant placement and 6 months after implant uncovering show more bone loss in implants that are 1) not coated with hydroxyapatite; 2) placed in the maxilla; 3) placed in anterior regions of the jaws; 4) in completely edentulous cases; and 5) placed in bone scored as having lower quality. Confounding relationships between predictor variables will require controlled statistical analyses when data collection is completed. being conducted at 32 Department of Veterans Affairs (DV A) medical centers and university research clinics. One aspect of these studies is the evaluation of changes in bone height around placed implants. Establishing the expected pattern and extent of bone loss around implants under varying conditions is an important component of the expanding knowledge on the effects of dental implant treatment. This knowledge can be used to maximize the probability of success of implant treatment through proper planning and selection of patients, restorative components, and procedures. In the DICRG studies, changes in bone height are primarily evaluated through measurements on radiographs that are taken at implant placement, implant uncovering, prosthesis placement, 6 months after implant uncovering, 12 months after uncovering, and yearly thereafter. Radiographic bone changes are followed to quantify and describe the extent, rate, and distribution patterns of vertical bone loss around the endosseous implants. Analysis of radiographic bone loss data will also be conducted to determine risk factors correlated with such bone loss to aid the decisionmaking process on whether and how to best provide dental implant treatment. Such information can be used to maximize the probability of successful dental implant treatment and improve care provided to patients.

With the relatively recent surge in the development and use of dental implants, a concomitant need for controlled clinical studies to validly assess the safety and efficacy of different dental implant systems has arisen. Such studies can also investigate the relationships of patient and treatment variables to identify risk factors in providing such treatment, allowing for better treatment planning and improved patient care. The summary National Institutes of Health Consensus Development Conference Statement (1988) stated the need for long-term studies that compare different types of implants and include evaluation of radiographic evidence of tissue health as part of studying and characterizing wound repair and tissue adaptation in the periimplant region. I Two concurrent multicenter clinical studies of dental implants, titled' 'The Influence of Implant Design, Application, and Site on Clinical Performance and Crestal Bone," are being conducted by the Dental Implant Clinical Research Group (DICRG). These studies are • Research Fellow. Department of Veterans Affairs Medical Center, Ann Arbor, MI; Department of Periodontics, Prevention, and Geriatrics, University of Michigan School of Dentistry, Ann Arbor. MI; Program in Dental Public Health, University of Michigan School of Public Health, Ann Arbor, MI. Address correspondence and reprint requests to Dr Morris: Department of Veterans Affairs Medical Center, Dental Research (154), 2215 Fuller Rd, Ann Arbor, M148105.

Background

This Is a US government work. There are no restrictions on its use.

The anatomy, physiology, histology, and embryology of the bone in the oral cavity have been described

0278·2391/97/5512-5002$0.00/0

62

63

MICHAEL C. MANZ

extensively by many authors."? The specific relationship of these biologic properties of oral bone to dental implant treatment has also been addressed.' Tatum and Lebowitz" discussed the specific differential biologic reactions of bone to dental implant treatments depending on individual characteristics of the patient and the general anatomic and physiologic characteristics of bone in different areas of the maxilla and mandible. Fagan" has described specific anatomic features of the maxilla and mandible and a classification scheme of the variations in anatomy that a clinician may encounter in the course of dental implant treatment. Osseointegration of implants has long been the advocated goal in dental implant treatment. Although researchers have disagreed on the exact nature and definition of osseointegration, descriptions of bone reaction and osseointegration have been provided. 10.1I Chiarenza" pointed out that differences in histology and bone reaction at the bone-implant interface are present around a single implant, depending on the type of bone (eg, cortical or trabecular) approximating the implant at a given site. Widera et al" discussed the differential effects that periodontal membrane thickness, cortical bone thickness, differential external stresses, implant shape, type of bone, possible connective tissue encapsulation, and differing mechanical properties of implants and teeth can have on the interactive mechanical effects and the response of bone to dental implants. The authors further discussed the advantages of a surrounding membrane and the differences in stress patterns between natural teeth and implants.':' Boyne et al'" described the alveolar bone response to hydroxyapatite (HA) replica implants in beagle dogs, and Meffert et al 15 described the differences in the anatomic and histologic healing of bone in the presence of HA-coated versus non-HA-coated titanium implants. The importance of microscopic surface characteristics and surface preparation on the bone-implant interface has also been addressed.l'"!? Weiss" has discussed the evaluation of the natural resorption of the maxillary and mandibular ridges before dental implant treatment and the retarding of ridge resorption that results from such treatment. Scheer and Boyne!" have advocated the use of bone graft substitutes and HA implants for osseointegration and preservation of alveolar bone after tooth loss. PERI-IMPLANT VERTICAL BONE

Loss

Albrektsson et al 20 proposed criteria, which are widely cited and used, for the evaluation of dental implant success, including the criterion that vertical bone loss should be less than 0.2 mm annually after the first year of service of an implant. Criteria for dental implant success proposed in a book edited by

Schnitman and Shulman" in 1979 included bone loss not greater than one third of the height of the implant. Vertical bone loss around implants has been studied and quantified by many investigators. Kapur et al 22 followed bone loss in a carefully designed study of blade-type implants. Weber et al 23 found no statistically significant change in bone level between 1 and 2 years after placement of nonsubmerged implants. Baseline measurements were not made, but the authors estimated bone loss of about 0.6 mm around mandibular implants and 1.1 mm around maxillary implants in the first year after implant placement." Branemark et al 24 reported bone loss of less than 0.1 mm annually for implants that they determined to be osseointegrated and that had been in function for 1 year before initiating the assessment. No information on the first year after implant placement was reported. Malmqvist and Sennerby" reported a high proportion of implants, followed for up to 4 years, having vertical bone loss of more than 2 mm, and many with bone loss greater than one third the length of the implant. Pilliar et al 26 reported differing vertical bone loss with different implant designs and surface characteristics. These varying results on vertical bone loss around dental implants highlight the need for further studies in this area. RADIOGRAPHIC MEASUREMENT OF VERTICAL BONE Loss

Although direct clinical measurements of bone height can be made at implant insertion and implant uncovering appointments, subsequent evaluation requires that radiographic measurements be used to avoid further tissue trauma. Measurements using radiographs require the visual determination of the position of the alveolar crest. As the lamina dura is observed radiographically from the apex coronally, there is usually an abrupt decrease in opacity. The crest of the alveolar bone is normally located I to 1.5 mm below the level of the cementoenamel junction (CEJ) when natural teeth are present. Bone loss around teeth can therefore be approximated by subtracting about 1 mm from the measured distance between the CEJ and the crest of the alveolar bone." In the case of implants, there is no CEJ to use as a landmark for establishing a baseline of bone level. Therefore, a baseline measurement must be made at the time of implant insertion. This measurement is made by measuring the distance from the level of bone to some point of reference on the implant. Subsequent measurements, using the same point of reference, can then be compared with the baseline measurement to estimate the amount of bone loss that has occurred subsequent to implant insertion. Figure I shows an example of radiographic bone level at implant insertion and subsequent bone loss at a followup appointment.

64

FIGURE I. Radiographs showing change in the bone level. A, Bone level at implant insertion. IJ, Bone loss around implants at a follow-up evaluation.

For large studies, indices with specially designed proportional measurement rulers have been developed to speed the measurement process and address the problem of nonstandardized radiographs.i"?" These methods. although providing proportional bone loss assessment. do not allow for determination of the actual amount of bone loss, Based on their investigation. Kaimenyi and Ashley" recommended the use of direct measurements as opposed to proportional measurements when studying bone loss using panoramic radio-

PERI-IMPLANT RADIOGRAPHIC BONE LOSS

graphs. Direct measurements can also be easily converted to proportional measurements (eg, the percentage of an implant in direct contact with bone), if desired. Measurement of intrusion or extrusion of the implant relative to the crestal bone at the time of placement also may be important in long-term studies evaluating bone change. Many investigators have compared the accuracy of bone loss measurements from different types of radiographs. Douglass et al 32 found no difference in periodontal disease diagnosis sensitivity for panoramic versus periapical and bitewing radiographs. However, another study found that, along with generally high interexaminer variability, bone loss was underestimated by 13% to 32% in panoramic radiographs, 11% to 23% in bitewing radiographs. and 9% to 20% in periapical radiographs." Gettleman et al" suggested a combination of assessment of radiographic bone height and pocket depth for determining implant condition, because of difficulties in judging quantitative changes from radiographs. Many factors affecting the quality of information obtained from radiographic measurements have been investigated. with subsequent recommendations made. The effect of radiographic angulation on bone height measurements has been thoroughly investigated." For radiographic evaluation of the periodontium, bitewing radiographs have been recommended as a complement to panoramic radiographs." For detecting small amounts of bone loss, Benn 37 pointed out the need for standardized film holders. an accurate reproducible measuring technique. and an automated computerbased measuring system. Much attention has been given to the application of computer-assisted assessment of periodontal bone as a means of further improving the quality of information derived from radiographs. Many computer procedures to aid accurate and reproducible analysis of radiographs have been described.i''?" The methods and advantages of digital subtraction radiography as a sped fie mode of computer-aided radiographic analysis of bone changes have been discussed.i':" Findings from many studies on alveolar bone changes using these computeraided analysis techniques have appeared in the literature. 43-46 However, the advantages of digital imaging have been accompanied by some cautionary commerits." D1CRG

DENTAL IMPLANT STUDIES

The objectives of the DICRG studies are to assess the effects of implant design, application (partial/full denture, removable/fixed, multiple/single tooth), and location (maxillary/mandibular. anterior/posterior) on clinical performance and crestal bone. Cases will be followed for 6 years after implant uncovering. The

65

MICHAEL C. MANZ

studies will assess implant survival along with specific complications and adverse responses associated with dental implant treatment. Other aspects of treatment, including plaque and calculus accumulation, soft tissue response, and patient satisfaction, will be monitored. Some special considerations usually apply when conducting dental-related clinical research. Most studies of dental outcomes of interest are by necessity lengthy. Caries and periodontal disease are slow in progression, and therefore long periods are required to evaluate preventive or treatment regimens. Similarly clinical evaluation of restorations-or, as in these studies, dental implants-requires sufficiently long periods to follow physiologic changes and evaluate longevity. Additionally, large sample sizes are required in situations in which safety is already well established and when studies are planned to investigate marginal differences.

Methods STUDY POPULATION

The subjects for these studies have been recruited from 32 sites, 30 of which are DVA medical centers with patients recruited and treated in the Dental Services of these centers. The other two sites, the University of Louisville and the University of Pennsylvania, are university-based dental implant research clinics. Patients are initially screened for general health or oral conditions that disqualify them from participation in the studies; patients who meet the study criteria and agree to participate are entered into the studies. Several study case types are being investigated, including mandibular and maxillary fully and partially edentulous cases, and maxillary anterior single tooth replacement cases. Depending on the case type, different implant designs from the Spectra-System implant system (Core-Vent Corporation, Las Vegas, NV) are randomly assigned to the sites for implantation in each case. The appropriate length and diameter for the implants are determined by the surgeon placing the implants. If alterations are made that deviate from defined study treatments, the cases are assigned to an alternate study stratum for separate analysis. Sample sizes for the DlCRG studies were calculated to ensure sufficient power to test the main hypotheses of the DICRG study. Final patient accrual goals for the studies were set using these calculations for minimum sample size requirements as a guide, More than one study case can be initiated and followed in a single study patient if conditions allow. The studies have accumulated a large number of study patients and cases, with recent totals exceeding 700 study patients and 1,000 study cases.

Table 1. Bone Level Relative to Top of Implant by Study examination (In mllllmetersJ Examination

N

1,354 Implant insertion Implant uncovering 1.233 897 Six-month follow-up

Minimum Maximum Mean SO

o o

0.1

5.6 12.2 9.3

0.5 I.5

2.6

0.6

1.2 1.2

DATA COLLECfION

Direct bone level measurements are made at implant insertion and implant uncovering appointments because the bone is exposed in completing the surgical procedures. These direct measurements can be used to check the reliability of measurements made from the radiographs taken at these appointments, Radiographs are also taken when the final prosthesis is inserted and at follow-up appointments, which are scheduled for all study patients based on the date of implant uncovering, These appointments are scheduled at 6 months, at I year, and then yearly thereafter for a period of 6 years. Direct measurements are not made at the time of prosthesis placement and at the follow-up appointments to avoid further tissue trauma and possible compromise of the peri-implant tissues, which may, in tum, increase the chances of implant complications or failure. Radiographs of the implant cases are sent to the project director's office, where they are labeled and catalogued. The radiographs are then mounted on a flat viewbox and measurements are made to the nearest 0.1 mm using vernier calipers, Vertical measurements of bone level adjacent to the implants are made from the top of the implant, which provides a fixed reference point (Fig 2). Measurements taken from the .radio- , graphs at implant uncovering are used as the baseline for radiographs taken at subsequent follow-up evaluations. Although generally the implant should be inserted so that its top is flush with the level of the crestal bone, deviations often occur. These deviations must be accounted for when determining the change in bone level at subsequent appointments. In determining actual bone loss from radiographic measurements, particularly on panoramic radiographs that generally provide an enlarged image of teeth and implants, calibration of the measured increments of bone change is required. Calibration is the process of correcting and standardizing measurements in radiographic analysis so that accurate and valid measurements of changes in bone over time may be made. The measurement from the top of the implant to the point of bone-implant interface is calibrated using the known and the radiographically measured length of the implant. This calibration involves multiplying the bone height measurements by the ratio of the known to the

66

PERI-IMPLANT RADIOGRAPHIC BONE LOSS Frequency

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Vertical Bone Change (mm)

FIGURE 2. Radiographic measurement sites and formulas used for analysis, Measurement average of bone from top of implant = (A + Bl/2. Actual average distance = (A + B) (known length)l2C. Proportion of implant not directly apposed to bone = (A + B)/2C.

measured implant length. Formulas used for calibration appear in Figure 2. The calibrated (ie, actual) distance at the time of implant uncovering is subtracted from all subsequent calibrated vertical bone measurements for a given implant in determining bone height changes. Negative values are not assigned in cases in which the bone level is above the level of the implant, because the amount of implant-bone contact is considered to be the factor of primary importance. DATA ENTRY

Measurements and bone pattern assessments are entered onto paper forms. These forms, which include case information, arc generated by the FoxPro data management software (Microsoft Corporation, Redmond, WA) using databases with information entered from study forms sent to the DICRG Data Management Center (Ann Arbor, MI). The measurements, along

FreqUtncy

700 , . . . . - - - - - - - - - - - - - - - -

FIGURE 4. Frequency distribution for bone loss measurements: Implant uncovering to 6-month follow-up.

with the other case-related information, are then entered into a data set using the Epi Info (USD, Inc, Stone Mountain, GA) data management and analysis package. Entry is double-checked to ensure that no entry errors have been made. The investigator rechecks measurements, data entry, and the resulting data set to ensure clean, accurate data. ANALYStS OF DATA

The Epi Info program provides data analysis capabilities. Certain aspects of the data analysis are completed using this program. However, the raw data tile created in Epi Info is also converted into a SAS (SAS Institute Inc., Cary, NC) data set for complete analysis. Variables are created and transformed as needed for analysis. The use of appropriate methods of data analysis is an important aspect of these studies. However, at this interim stage in the studies, data collection is far from complete. The results presented in this article are there-

Proportion

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FIGURE 3. Frequency distribution for bone loss measurements: Implant placement to implant uncovering.

nm..

Evaluation Contactl.!'Vbon!-. Not contacting bone

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0.955 0.045

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FIGURE 5. Direct implant-to-bone apposition as a proportion of total implant surface.

67

MICHAEL C. MANZ

• HA. non-HA

mm

• Anterior. Posterior

mm

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Stage 1 to 2 Stage2 to 6 mo. Evaluation Time Intervala

FIGURE 6. Mean peri-implant vertical bone change for study intervals: HA vs non-HA.

fore primarily descriptive and intended only to provide indications of trends seen in the data to this point. Data from the two D1CRG studies were pooled to simplify the presentation of these preliminary findings. Results are presented on bone loss overall. and on bone loss stratified by various predictor variables. As the database on radiographic bone loss becomes more complete. a more comprehensive analysis of the data will be conducted.

Results The mean actual bone levels calculated from the calibration formulas for the different study examination appointments are shown in Table I. For data collected to this point. the overall average bone loss between implant insertion and implant uncovering is 0.94 mm. Average overall bone loss between implant uncovering and 6 months after uncovering is 1.14 mm. The distributions of bone change measurements for the two study intervals are shown in Figures 3 and 4.

mm

• Mandible • Maxilla

1.4....-----------------, 1.21------------

o

Stage 1 to 2 Stage 2 to 6 mo. Evaluation Time Im-rv."

FIGURE 8. Mean peri-implant vertical bone change for study intervals: Anterior vs posterior.

The average proportion of the implant that radiographically appears to be in direct contact with bone at the different study evaluation points is shown in Figure 5. The top portions of the bars indicate the mean proportion of the implants not in direct contact with bone. providing an indication of vertical bone loss relative to the length of the implant. The mean proportion. of the implants not in direct contact with bone as evaluated radiographically. increases from about 4.5% at implant insertion to 21.2% at the 6-month follow-up. The remainder of the results primarily show the bivariate relationships of various predictor variables in the studies to radiographic bone loss. Vertical bone changes for HA-coated versus non-HA-coated implants are compared for the two study intervals in Figure 6. Non-HA-coated implants show more vertical bone loss at both intervals. Figure 7 shows average vertical bone loss for implants placed in the maxilla compared with bone loss for implants placed in the mandible. For the two study intervals shown in the figure, there is more average • Mandible • Maxilla

mm

2.-----------------..

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0.8 0.6 D...

0.5

0.2

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Stage 1 to 2 St8ge 2 to 6 mo. Evaluation Time I'*"'a"

FIGURE 7. Mean peri-implant vertical bone change for study intervals: Mandible vs maxilla.

o

Ant

Post

Stage 1102

Ant

Post

Stage 2 tD 8 mo.

FIGURE 9. Mean peri-implant vertical bone change for study intervals by arch location.

68

PERI-IMPLANT RADIOGRAPHIC BONE LOSS

mm

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mm

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• BoneScore =1 • BoneScore 2 BoneScore 4

o BoneScore =3 •

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FIGURE 10. Mean peri-implant vertical bone change for study intervals by HA vs non-Ha and mandible vs maxilla.

vertical bone loss around implants placed in the maxilla thun around those placed in the mandible. There is also more bone loss in both study intervals for implants placed in anterior regions of the maxilla and mandible than in posterior regions (Fig 8). Figure 9 shows a further breakdown by jaw location. For the two study intervals, the tendencies for more bone loss in the maxilla than the mandible. and more bone loss in anterior regions than posterior regions. generally hold. Figure 10 displays the comparison of b.one los~ between implants with and without HA coating stratified by arch. The figure shows a trend of more bone loss in noncoated implants and implants placed in the maxilla up to 6 months after uncovering. Figure 11 displays mean vertical bone loss between implant placement and implant uncovering by case type. More bone loss is seen in compl~tely edent~lous cases for both the maxilla and mandible. The figure also shows that mea~ bone loss for the different manmm

1.4.-----------------, 1.21--------1 0.8

o.e2

0.8

....

Stlge 2 to 8 mo.

FIGURE 12. Mean peri-implant vertical bone change for study intervals by bone quality score.

dibular case types are all intermediate between completely edentulous maxillary cases and the other ty~es of maxillary cases. Vertical bone loss by bone quality, as evaluated at the implant placement surgery, is shown in Figure 12. The figure shows a slight tendency t~r more vertical bone loss with the increasing numeric designations for bone quality type. particularly between the implant uncovering and the 6-month followup examination. Figure 13 shows bone change between implant placement and uncovering for the different implant designs being studied. For this study stage. the least amount of bone loss is seen with the Bio- Vent design. followed by Micro-Vent, Screw-Vent (titanium alloy). Screw-Vent (HA-coated), Core-Vent, and Screw-Vent (commercially pure titanium).

Discussion Overall. the implants in this study experienced about 1 mm bone loss between implant insertion and implant mm

2.----------------,

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0.4

0.2

o

0.5 LCE LRP LLP

M.ndlbul.r c•••

UCE URP ULP UST

Maxlll.ryC....

FIGURE II. Mean peri-implant vertical bone change by case type: Implant insertion to implant uncovering. LCE, lower completely edentulous; LRP. lower right posterior; LLP, lower left posterior; UCE, upper completely edentulous; URP, upper right posterior; ULP, upper left posterior; UST, upper single tooth.

FIGURE 13. Mean peri-implant vertical bone change by implant design:implant insertion to implant uncovering.

MICHAEL C. MANZ

uncovering, and another millimeter of bone loss between implant uncovering and 6 months post-uncovering. It is difficult to compare bone loss in these early stages of the DICRG studies with other studies because publications from other studies generally have not reported on bone loss occurring during these early stages. Although the data collection to this point is not sufficient to report findings, preliminary indications are that, after the initial stages, the rate of vertical bone loss around DICRG study implants declines substantially. As the DICRG studies continue, data will show whether the bone loss seen in these later study intervals falls in the range of bone loss reported in other studies.2J-26 Direct comparisons with other studies will be made when data collection is more complete. The distribution of bone change measurements for the two study intervals up to 6 months after uncovering are seen in Figures 3 and 4. These figures show the distribution of bone loss measurements for those implants on which measurements were completed for both the beginning and ending study appointments for the intervals. The distribution of measurements for bone change between implant insertion and implant uncovering is skewed toward higher values of bone loss, with most measurements falling between 0 and I mm. The measurements for the interval between implant uncovering and 6 months after uncovering shift slightly away from 0 and appear to be somewhat more normally distributed and less severely skewed. Higher measurement values, which cause skewing of the distributions, act to pull up the means for the interval measurements. The medians provided in the distribution figures are lower than the means for the two study intervals (medians of 0.7 and 0.99 vs means of 0.94 and 1.14). The normality of measurement distributions must be considered in future data analysis. These measurement distributions indicate that in the early stage after implant insertion most implants show little loss of bone, with a small proportion of implants having substantially more bone loss. Continuing research in this and other studies should investigate the variables associated with those implants showing rapid early vertical bone loss. Figure 5 relates the same information on overall bone loss in a different way. The upper sections of the bars indicate the average proportion of the implants that do not appear radiographically to be in direct approximation to bone, providing an indication of vertical bone loss relative to implant length in the study evaluations. On average, about 95.5% of the study implants appear radiographically to be in direct contact with bone at implant insertion. This proportion drops to 87.5% at implant uncovering, and 78.8% at 6 months after uncovering. This information can be evaluated and related to current ideas on the percentage of direct bone-implant contact necessary to bear the mechanical

69 stress and loading forces placed on dental implants when prosthetic restoration has been completed. The results shown in Figures 6 through 13 show various and overlapping relationships of different study variables to vertical bone loss around implants. More bone loss is associated with non-HA-coated implants than with HA-coated implants (Fig 6) in the early study intervals. It is possible that these findings may relate to the immediate biologic reaction to the implant surface at implant placement. Whether the trend for greater bone loss with non-HA implants in these studies remains after a period of healing and stabilization of the implants will be evaluated as follow-up results continue to be gathered. Overall, more vertical bone loss appears to be associated with implants placed in the maxilla than the mandible, and with implants placed in anterior regions than with those in posterior regions (Figs 7 and 8). Unlike the HA versus non-HA comparison, smaller differences were noted in the interval between implant placement and implant uncovering, with the greatest differences appearing in the interval between implant uncovering and 6 months after uncovering for these implant location variables. The further categorization of implant location in Figure 9 shows bone change results stratified by arch and anterior/posterior location. Generally, in the earlier study intervals the greatest vertical bone loss is seen around implants placed in the maxillary anterior region, followed by the mandibular anterior region, with posterior regions in both arches showing the least amounts of vertical bone loss. Whether bone loss differences by arch location are mostly confined to the initial stages after implant insertion will continue to be evaluated as data collection continues. Figure 10 shows results for HA-coated versus noncoated implants stratified by arch. The same' basic trends described for the bivariate relationships of arch to bone loss and HA coating to bone loss are stilI apparent in this figure. In both study intervals, less bone loss is associated with HA-coated implants and with implants placed in the mandible. From these results, the relationship of HA coating and arch to bone loss is still apparent and would appear to be additive. The results shown in Figure I I provide an indication of a more complex interrelation of the different predictor variables in these studies. From this figure it is evident that the tendency for greater bone loss in the maxilla than in the mandible (Fig 7) for the interval between implant insertion and implant uncovering is entirely accounted for by bone loss around implants in completely edentulous' cases. Maxillary implants for partially edentulous and single tooth cases actually show less bone loss on average than implants for any of the different types of mandibular cases. The greater vertical bone loss seen in the completely edentulous cases for both arches might be related to the

70 placement of implants for these cases in anterior locations, where more bone loss was seen (Fig 8), whereas implants for the partially edentulous cases were placed in posterior areas of the jaws. However, the maxillary single tooth cases show similar bone loss to the other types of partially edentulous maxillary cases and less bone loss than the mandibular case types, even though they are placed in the maxillary anterior region, where the most bone loss was seen in study implants overall. Bone loss related to case type might actually be related to the underlying conditions requiring implant treatment rather than just the location where the implants are placed. The factors that led to complete edentulism in a patient also might contribute to bone loss around dental implants. The results for vertical bone loss associated with bone quality scores (Fig 12) provide another example of the possible interrelations of predictor variables in these studies. Bone quality hall been stated to be associated with the arch and anterior/posterior location in the arch." The differing distributions of bone quality by arch and anterior/ posterior location for the DICRG study have been reported previously." Vertical bone loss results reported by arch and anterior/posterior position may therefore actually be reflecting the relation between such bone loss and bone quality. Conversely, there may be factors associated with jaw location other than bone quality that affect bone loss around implants, and may be reflected in results reported by bone quality type. These types of confounding relationships need to be evaluated and accounted for in analysis of study data. The interrelationships between the different study variables also must be considered when evaluating the results for bone loss by implant design (Fig 13). The different implant designs were not used in all locations and applications in the DICRG studies. Core-Vent implants were only placed in mandibular cases, MicroVent implants were only placed in the maxillary single tooth and partially edentulous cases, and titanium alloy Screw-Vent implants were placed only in mandibular fully edentulous cases, whereas HA-coated and commercially pure titanium Screw-Vent implants were placed in maxillary fully edentulous cases. Bio-Vent implants were placed in partially edentulous mandibular cases and in fully edentulous cases in both arches. Any comparisons by implant type must therefore control for the potential confounding effects of the different applications and jaw locations in which the different types of implants were placed. The DICRG radiographic bone loss data sets have other characteristics besides possible confounding relationships of predictor variables that affect the choice of statistical methods to be used in the analysis of data for these studies. The primary outcome of interest in the DICRG studies is success (or failure) of the placed prostheses and, secondarily. success of the implants supporting the prostheses. Survival analysis techniques

PERI-IMPLANT RADIOGRAPHIC BONE LOSS

are readily applied using measures of time to an event of interest. However, the assessment of vertical bone loss involves continuous data measurement and is not suitable for survival analysis methods. Additionally, the longitudinal analysis (repeated measures) of continuous data from vertical bone loss measurements over time must account for the correlation of measurements within study cases and study patients. Different methods of analysis of data from longitudinal studies of radiographic bone loss have been described, including generating results of mean bone loss, mean bone loss per year, correlation among independent variables, linear regression, and multiple logistic regression methooS.49.50 Wennstrom" has pointed out the importance of evaluating the individual variation of extent and severity of bone loss by analytical methods beyond the calculation of means. Methods of analysis specific to repeated measures over time have been described." Although all values of mean bone change reported in this article are in the direction of bone loss, there are numerous instances of individual implants where radiographic measurements indicated an increasing bone level from one evaluation point to the next. Measurement error can obviously be responsible for such findings but, as bone gain is seen in periodontal evaluations around natural teeth, bone gain around implants is certainly plausible. The potential for bone gain in the bone-implant interrelationship is another area for investigation in the future. If bone gain does appear to be occurring, future data analyses will focus on the conditions present around implants where bone gain is seen. By determining the factors that affect the bone support of dental implants, the planning of treatment methods and materials ean be modified to increase the probability of successful dental implant treatment.

References I. National Institutes of Health: National Institutes of Health consensus development conference statement on dental implants. June 13-15, 1988. J Dent Educ 52:824. 1988 2. Brescia NJ: Applied Dental Anatomy. St Louis. MO. Mosby. 1961 3. Provenza DV: Fundamentals of Oral Histology and Embryology (ed 2). Philadelphia, PA, Lea & Febiger, 1988 4. Bodecker CF: Fundamentals of Dental Histology and Embryology Including Clinical Applications. New York. NY. School of Dental and Oral Surgery, Columbia University. 1940 5. Beust TB: Dental Histology and Embryology. Philadelphia. PA. Saunders, 1934 6. Brand RW, Isselhard DE: Anatomy of Orofacial Structures (cd 4). St Louis, MO, Mosby, 1990 7. Lake FT: Basic bone biology in implantology. in McKinney RV (ed): Endosteal Dental Implants. St Louis, MO, Mosby Year Book, 1991 8. Tatum OH, Lebowitz MS: Anatomic considerations for dental implants. J Oral Implantol 17:16, 1991 9. Fagan MJ: New Concepts in Implant Dentistry "Implantodontics" (ed 4). Atlanta. GA, Dental Practice Plan. 1972 10. Weiss CM: Short- and long-term bone maintenance surrounding

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II.

12. 13.

14. 15. 16. 17. 18. 19. 20.

21. 22.

23. 24. 25.

26. 27. 28. 29.

fibro-osteal and osteal integrated dental implants. 1 Oral Irnplanto116:12,1990 Branemark P-I: Introduction to osseointegration, in Branemark P-I, Zarb GA, Albrektsson T (eds): Tissue-Integrated Prostheses: Osseointegration in Clinical Dentistry. Chicago, IL, Quintessence, 1985, pp 11-76 Chiarenza AR: Retrospective observations on the influence of bone type in determining the nature of bone implant interface. Int 1 Oral Implantol 6:43, 1989 Widera GEO, Tesk lA, Privitzer E: Interaction effects among cortical bone, cancellous bone, and periodontal membrane of natural teeth and implants. 1 Biomed Mater Res 10:613, 1976 Boyne PI, Rothstein SS, Gumaer KI, et al: Long-term study of hydroxylapatite implants in canine alveolar bone. 1 Oral Maxillofac Surg 42:589, 1984 Meffert RM, Block MS, Kent IN: What is osseointegration? Int 1 Periodontics Restorative Dent 7:9, 1987 Baier RE, Mayer AE: Future directions in surface preparation of dental implants. 1 Dent Educ 52:788, 1988 Smith DC: Future directions for research on materials and design of dental implants. 1 Dent Educ 52:815, 1988 Weiss CM: Dental implants: Differential diagnosis and treatment planning. NY State Dent 1 47:12, 1981 Scheer P, Boyne PI: Maintenance of alveolar bone through implantation of bone graft substitutes in tooth extraction sockets. 1 Am Dent Assoc 114:594, 1987 Albrektsson T, Zarb G, Worthington P, et al: The long-term efficacy of currently used dental implants: A review and proposed criteria of success. Int 1 Oral Maxillofac Implants I: I I, 1986 Schnitman PA, Shulman LB: Recommendations of the consensus development conference on dental implants. 1 Am Dent Assoc 98:373, 1979 Kapur KK, Participants of CSP No 86: Veterans Administration Cooperative Dental Implant Study-Comparisons between fixed partial dentures supported by blade-vent implants and removable partial dentures. Part II: Comparisons of success rates and periodontal health between two treatment modalities. 1 Prosthet Dent 62:685, 1989 Weber HP, Buser 0, Fiorellini IP, et al: Radiographic evaluation of crestal bone levels adjacent to nonsubmerged titanium implants. Clin Oral Implants Res 3:181, 1992 Branemark P-I, Adell R, Albrektsson T, et al: Osseointegrated titanium fixtures in the treatment of edentulousness. Biornaterials 4:25, 1983 Malmqvist IP, Sennerby L: Clinical report on the success of 47 consecutively placed Core-Vent implants followed from 3 months to 4 years. Int 1 Oral Maxillofac Implants 5:53,1990 Pilliar RM, Deporter PA, Watson PA, et al: Dental implant design: Effect on bone remodeling. 1 Biomed Mater Res 25:467, 1991 Wuehrmann AH, Manson-Hing LR: Dental Radiology (ed 4). St Louis, MO, Mosby, 1977 Schei 0, Waerhaug 1, Lovdal A, et al: Alveolar bone loss as related to oral hygiene and age. 1 Periodontol 30:7, 1959 Bjorn H, Holmberg K: Radiographic determination of periodontal bone destruction in epidemiological research. Odont Rev 17:232, 1966

71 30. Bjorn AL: Dental health in relation to age and dental care. Odont Rev 25:8, 1974 (suppl 29) 31. Kairnenyi IT, Ashley FP: Assessmentof bone loss in periodontitis from panoramic radiographs. 1 Clin Periodontol 15:170, 1988 32. Douglass CW, Valachovic RW, Wijesinha A, et al: Clinical efficacy of dental radiography in the detection of dental caries and periodontal diseases. Oral Surg Oral Med Oral Pathol 62:330, 1986 33. Akesson L, Hakansson 1, Rohlin M: Comparison of panoramic and intraoral radiography and pocket probing for the measurement of the marginal bone level. 1 Clin Periodontol 19:326, 1992 34. Gettleman L, Schnitman PA, Kalis P, et 81: Clinical evaluation criteria of tooth implant success. 1 Oral Irnplantol 8:12. 1978 35. Hausmann E, Allen K, Christersson L, et al: Effect of x-ray beam vertical angulation on radiographic alveolar crest level measurement. 1 Periodont Res 24:8, 1989 36. Stenstrom B, lulin P, Lavstedt S: Comparison between panoramic radiographic techniques. Part II: Marginal bone level interpretability with Status-X and Orthopantomograph, model OP 3. Dentomaxillofac Radiol 11:37. 1982 37. Benn OK: A review of the reliability of radiographic measurements in estimating alveolar bone changes. J Clin Periodontol 17:14,1990 38. Dunn SM, Kantor ML: Digital radiology facts and fictions. 1 Am Dent Assoc 124:39, 1993 39. Van der Stelt PF: Modern radiographic methods in the diagnosis of periodontal disease. Adv Dent Res 7:158. 1993 40. Brllgger U: Digital imaging in periodontal radiography. 1 Clin Periodontol 15:551, 1988 41. leffcoat MK: Radiographic methods for the detection of progressive alveolar bone loss. 1 Periodontol 63:367. 1992 42. leffcoat MK, Reddy MS: Digital subtraction radiography for longitudinal assessment of peri-implant bone change: Method and validation. Adv Dent Res 7:196, 1993 43. Braegger U, Litch 1, Pasquali L, et al: Computer assisted densitometric image analysis for the quantitation of radiographic alveolar bone changes. 1 Periodont Res 22:227, 1987 44. Brllgger U, Pasquali L, Komman KS: Remodelling of interdental alveolar bone after periodontal flap procedures assessed by means of computer-assisted densitometric image analysis (CADIA). 1 Clin Periodontol 15:558, 1988 45. Benn OK: A computer-assisted method for making linear radiographic measurements using stored regions of interest. 1 Clin Periodontol 19:441, 1992 46. Hausmann E, Dunford R, Wikesjo U, et al: Progression of untreated periodontitis as assessed by subtraction radiography. 1 Periodont Res 21:716, 1986 47. Misch CE: Progressive loading of bone with implant prostheses. 1 Dent Symp 1:50, 1993 48. Orenstein IH. Synan WI, Truhlar RS, et al: Bone quality in patients receiving endosseous dental implants: DICRG interim report no. I. Implant Dent 3:90, 1994 49. Albander 1M, Rise 1, Gjermo P, et al: Radiographic quantification of alveolar bone level changes: A 2-year longitudinal study in man. 1 Clin Periodontol 13:195, 1986 50. Albander 1M: Some predictors of radiographic alveolar bone height reduction over 6 years. 1 Periodont Res 25:186, 1990 51. Wennstrom lL: Interpretation of radiographic data on longitudinal loss of periodontal support. 1 Periodontol 61:459, 1990 52. Wallenstein S, FIeiss lL, Kingman A: Repeat measurements analysis of dental data. 1 Dent Res 59:2021. 1980