The relationship between attachment level loss and alveolar bone loss
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Journal of Clinieal Periodontology 1984: 11: 348-359Key words; Pcrindoittal disvasc - auachmeni loss ~ bone toss.Acccplcd for publication June 15, 1983
The relationship between attachment ieveiioss and aiveoiar bone ioss
J. M. GooDsoN, A. D. HAFFAJEE AND S. S. SOCRANSKY
Forsyth Dental Center, Boston, Mass., USA
Abstract Standardized radiographs and repeated periodontal probe measurements were made on 22untreated subjects with destructive periodontal disease monitored for 1 year. Radiographs of selectedsites were taken at 0, 6 and 12 months. Measurements of attachment level were made monthly.Radiographic measurements were made on 7X magnified projected images. Alveolar bone height fromthe CEJ was computed by multiplying the average length of the root times the measured ratio of CEJ toalveolar bone over CEJ to root tip. Each radiograph was measured twice by 2 investigators. Sites wereexcluded as having indistinct anatomical landmarks in which the standard deviation of the 4measurements exceeded 0.16 mm, the measurement error for repeat determination of bone height onhigh quality radiographic images. A 3 sigma critical value for significant bone loss was selected as 0.48mm. Changes in attachment level were computed for the intervals preceding and during the 6-12 monthradiographic measurement period. Based on these critical values, 6.1% ofthe 231 radiographed sitesshowed significant bone loss. Similarly, 5.7% of the 1155 probed sites showed significant attachmentloss. However, none of the sites with significant bone loss exhibited significant attachment loss over thesame time period. In general, significant attachment loss preceded bone loss by 6 to 8 months. At 4 mm,attachment loss was found to predict subsequent bone loss with a true positive ratio of 60% and a falsepositive ratio of 5%, indicating a high degree of predictive discrimination. These observations indicatethat attachment loss precedes radiographic evidence of crestal alveolar bone loss during periods ofperiodontal disease activity.
2 primary clinical assessments serve to indicatethe presence of periodontal disease; attachmentloss by probe measurement and bone loss byradiographic measurement. It has often beenassumed that these diagnostic procedures aredirectly related. However, the association be-tween attachment loss and bone loss has notbeen demonstrated beyond the obvious correla-tion between deep periodontal pockets andradiographic translucency.
A major factor which must be taken intoconsideration when examining the interrela-tionship between attachment level change andalveolar bone loss is the phenomenon of theepisodic nature of periodontal disease activity.Based on clinical experience, histologic evi-
dence, periodontal probing, and clinical radio-graphs, several dental investigators have sug-gested that human periodontal disease proceedsthrough a series of recurring exacerbations(Black 1915, Stanley 1955, Hirschfeld & Was-serman 1978, Selikowitz et al. 1981, Page &Schroeder 1982). Similar suggestions have beenmade to explain experimental findings in stud-ies of periodontal disease in monkeys (Heijl etal. 1976) and rats (Garant 1976). In addition,the observation that individuals with advancedperiodontal lesions can exist in a state ofremission which can last for periods of 6 to 10years has been documented (Moskow 1978,Vandesteen et al. 1981).
The hypothesis that periodontal disease pro-
ATTACHMENT LOSS AND BONE LOSS 349
ceeds through a series of exacerbations has beensubstantiated by repeated meastirements ofradiographic density and attachment levelchange at individual periodontal sites. Radio-graphic density measurements by ' ' i absorp-tiometry (Hausmann & McHenry 1982) indi-cate that bone density exhibits cyclic variationsunder disease conditions. Likewise, statisticallysignificant changes in attachment level mea-surements have been demonstrated which occurover short periods of time at individual period-ontal sites (Goodson et al. 1982, Haffajee et al.1983). These observations indicate that net lossof both attachment and bone may occur byrepeated cycles of loss and incomplete recovery.Thus, periodontal destruction does not appearto be a continuous process, but is characterizedby periods of episodic activity (Haffajee et al.1982). A disease model has been described(Socransky et al. 1983) in which periodontaldisease is seen to proceed in bursts of activitywhich occur randomly at periodontal sitesthroughout the mouth. Following these de-structive bursts, periodontal sites then remainquiescent for an undetermined period of time.In this study, "periodontal disease activity"will be used to describe statistically significantloss in periodontal attachment as detected byrepeated longitudinal attachment level mea-surements (Haffajee et al. 1983). The temporalrelationship between cyclic variations in attach-ment level and radiographic evidence of boneloss is of interest in the elucidation of sequentialsteps in the disease process and the evaluationof these measurements for early diagnosis ofdisease activity. In this paper, we will presentdata indicating that radiographic evidence ofperiodontal bone loss generally follows attach-ment change by periods of 6 months or moreand occurs during the period of remission ofattachment loss.
Material and Methods
The subject population in this study was thatdescribed in preceding papers on disease activ-
ity (Goodson et al. 1982) and definition ofperiodontal disease syndromes (Socransky et al.1982), where the characteristics of this groupare described in detail. Probeable attachmentlevel measurements to the nearest 0.5 mm weretaken monthly at 2 sites on each tooth usingMichigan "0" periodontal probes (Goodson etal. 1982, Haffajee et al. 1983).
Radiographs were standardized for angula-tion and film-source distance using film holders(Rinn Corp., Elgin, IL 52780) with occlusalregistration (Polygel, L.D. Caulk Co., Milford,DE 19663). Film holders were constructed atthe first appointment and used to re-positionfilms at subsequent time periods. Stability of thepolyether impression material was determinedby measuring radiographs of skull specimenstaken at 6-week intervals for a period of 6months. The average standard deviation ofrepeated measurements from the CEJ to crestalbone made on the skull radiographs was0.00820.0023 mm (Duckworth et al. 1983).Films were developed in an automated process-ing system (Peri-Pro automatic film processor.Air Techniques Inc., #70 Cantiague Rock Rd.,Hicksville, NY 11801) at room temperature.The developer and fixer were changed eachweek.
4 areas with pockets greater than 4 mm wereselected in each subject's mouth for radiograph-ie analysis. Periapical films were taken atthese 4 areas at 0, 6 and 12 months. Differencesbetween the radiographic measurement of al-veolar bone height in the radiographs taken at 6and 12 months were used to determine bone lossin association with attachment level changesoccurring prior to and coincident with theradiographic measurement interval.
Radiographic measurements (Fig. 1) weremade on 7X enlarged images projected on thesurface of an X-Y plotter/digitizer (Tektronix4662) connected to a computer (Tektronix4052). A pointer attached to the pen carriagewas used to locate and define the coordinates ofthe projected image of 3 points; the CEJ, thealveolar bone crest and the root tip. The linear
350 GOODSON, HAFFAJEE AND SOCRANSKY
distances A and B (Fig. 1) were computed by thefollowing algorithm (in Tektronix BASIC)based on the Pythagorean theorem.
Program statement Comment
DIM X(3), Y(3)
FOR 1=1 TO 3
POINTER DO, DO,D$
DIMENSION COOR-DINATE ARRAYSENTER 3 COORDI-NATE VALUESWAIT FOR A-GRAPHIC INPUT(DUMMY VARI-ABLES)INPUT COORDI-NATE VALUES
NEXT IK1 = X(1)-X(2)K2=Y(1)-Y(2)A = SQR(Kr2XKr2) CEJ TO BONEK3 = X(2)-X(3)K4 = Y(2)-Y(3)B = SQR(K3-2 + K4-2) CEJ TO APEXR=A/B IMAGE RATIO
The ratio R is the image distance from the CEJto the alveolar crestal bone (A) divided by theimage distance from the CEJ to the root tip (B).To express these measurements in mm, thecomputed image ratio R was multiplied by theaverage length of that tooth root (Wheeler,1950). This value represents the distance fromthe CEJ to the alveolar bone crest.
Each site on the radiographs was measuredtwice by 2 investigators from coded radio-graphs. The method had a standard deviation of0.16 mm as determined by repeat measurementsof radiographs of high quality with distinctCEJs and crestal alveolar bone. Sites wereexcluded where the standard deviation ofthe 4measurements (2 by each investigator) wasgreater than 0.16 mm. As a result, 12.2% ofthetotal number of sites which could be seen in theradiographic survey were excluded. A signif-icant change in radiographic alveolar boneheight was taken as the 3 sigma critical value of0.48 mm. Significant changes in attachment
level measurements are listed for the regressionmethod as previously reported (Goodson et al.1982) and in addition, computed using themedian smoothed method described by Haffa-jee et al. (1983), considering a change of 2 mm inthe median smoothed value to be statisticallysignificant.
5 derived values were computed to expressthe ability to predict bone loss from attachmentlevel change.
(1) The true positive ratio (TP, the propor-tion of sites with attachment level change whichalso exhibited bone loss).
= ilLVEOLAR BONE HEIGHT
Fig. I. Measurement of alveolar bone height fromstandardized periapical radiographs. The 7 X mag-nified image distance from the CEJ to the root tip(B) and from the CEJ to the alveolar bone height (A)was computed from coordinates ofthe CEJ, alveolarcrest and root tip (see text). The ratio/4//f multipliedby the mean root length of the tooth provided a mea-sure of alveolar bone height from the CEJ.Messungen der Hohe des alveolaren Knoehenkammesauf standardisierten Rontgenbildern. Der 7-faeh ver-grosserte Abstand von der Schmelz-Zementgrenze zurWurzelspitze (T3j und von der Schmelz-Zementgrenzezum alveolaren Knoehenkamm (A) wurde mit Hilfe dervon der Schmelz-Zementgrenze, vom alveolaren Kno-ehenkamm und von der Wurzelspitze ausgehendenKoordinaten vermessen (siehe weiler im Text). DasResultat des mit der mittleren Wurzellange multiplizier-ten Verhaltnisses A/B ergab das Mass fur die alveolareKnochenhohe in Bezug auf die Schmelz-Zementgren-ze.
Mesure de la hauteur osseuse alveolaire a partir deradiographies apicales standardisees. Les imagesagrandies 7 X de la distance entre la jonetion email-cement (JEC) et I'apex (B), et entre JEC et sommetalveolaire (A) ont ete integrees a des enregistrements deJEC, sommet alveolaire et apex. Le rapport A / BtnultipUe par la longueur radiculaire moyenne donne lamesure de la hauteur osseuse alveolaire vi.s-a-vis de laJEC.
ATTACHMENT LOSS AND BONE LOSS 351
(2) The false positive ratio (FP, the propor-tion of sites with attachment loss which did nothave bone loss).
(3) The likelihood ratio ( T P / F P ) .(4) The post-test probability of a site with
attachment loss (T+) being associated withbone loss (D + ), P(D + lT + ).
(5) The post-test probability of a site with noattachment loss (T ) being associated withbone loss, P(D-l-lT-).
These probabilities were computed from thedecision matrix defining outcomes of the mea-sure considered the test (attachment levelchange) and the measure considered the dis-ease (significant radiographic evidence of boneloss). The decision matrix for these quantitieswas constructed as follows (McNeil et al. 1975).
Test results(attachment change)
Presence of disease(bone loss)
present I aabsent , b
true positive ratio(T-t-lD-f)false positive(T + l D - )true negative(T-ID-)false negative(T-ID + )fraction of sites with bone loss
= ('D + ) =
fraction of sites without bone /oss = P(D )= 1-
Probability of correctly predicting bone lossfrom attachment loss:
Probability of failing to predict bone loss froman attachment loss:P(D- | - IT-)= F
A total of 231 radiographic sites were measuredin which the standard deviation of the 4 repeat-ed measurements was within the cutoff value of0.16 mm. 14 sites in this group exhibitedsignificant bone loss equal to or exceeding thesignificance criterion of 0.48 mm. Table 1indicates the % of sites with significant radio-graphic change. These data are compared withattachment level changes in the same subjectsand literature values from 2 other groups. The% of sites with significant bone loss by radio-graphic measurement (6.1 %) was similar to the% of sites exhibiting significant attachment loss(5.7% by regression and 3.9% by mediansmoothing). However, none of the sites whichshowed radiographic evidence of bone loss werethe same sites which exhibited evidence ofsignificant attachment loss during the 1-yearmonitoring period.
Attachment level measurements were madeat 146ofthe231 radiographed sites including 10of the 14 sites which showed significant boneloss. With one exception, all of the sites showingradiographic bone loss exhibited a significantattachment level change at some time duringthe attachment level monitoring period. Theprevalent pattern, seen in 7 of the 10 sites withsignificant bone loss, was an attachment mea-surement which started at the beginning of themeasurement interval with some degree ofattachment loss and subsequently gained inprobable attachment level prior to radiographicdetection of bone loss. This is shown in Fig. 2,where the attachment level measurements of 4such sites are illustrated. 2 of the sites showingsignificant bone loss exhibited a cyclic attach-ment loss followed by recovery during theperiod of radiographic monitoring. The attach-ment level measurements of one site did notchange significantly over the total time period;however, the measurement interval started only1 month before the first radiograph was taken.
The magnitude of radiographic change mea-sured at each of the 10 sites and the maximum
352 GOODSON, HAFFAJEE AND SOCRANSKY
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attachment level change measured at the samesite is illustrated in Table 2. In each case, theattachment level change was greater than theradiographic change. The average maximumattachment level change was nearly 6 times themeasured radiographic change.
Based on the 146 sites where both measure-ments were taken, the ability of attachment
Fig. 2. Attachment level measurements and radio-graphic change of 4 interproximal sites. The j-axisrepresents attachment level measured at each site. TheX-axis is the time in months, 0, being the lime of the 6-month radiograph. The second radiograph was takenat the time indicated by the end of the trace. Measuredradiographic loss is given along with arrows definingthe measurement interval.Messungen des Attciclunent (Epithclcmsatz)-niveaus undder iin Rtmtgenhild kon.slalierlcn Veriinderungen in 4interapproximalen Regionen. Die Oidina...