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).

    LENGTH

    = 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 absent

    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

    c

    d

    = ('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

    FN*P(D-|-)-|-TN*P(D-)

    Results

    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

    -6time [months]

    0

    ATTACHMENTLEVEL (mm)

    RADIOGRAPHIC1.2miii CHANGE

    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 Oidinale veranschcni-licht das Niveau desEpithelansatzes einerjcden Region.Auf der Abzisse ist die Versuc/iszeil in Monalen abge-setzt, wobei 0 den Zeitpunkt des nach 6 MonatenerstcUien RoiUgenbildes angibt. Die 2. Rontgenaufnah-me wurde zu dem Zeitpiinki angejertigt, der am Endeder Skizze angegeben ist. Der kon.statierte, durch dasRontgenbiid ermittelte, Verlust wird zusammen initdenPfeilen angegeben, die das Messintervall bezeichnen.Me.siires du niveau d'attache et changement radiogra-phicjue de 4 sites interproximaux. L'ordonnee represen-te le niveau d'attaehe mesurc dans chaque site. L'abscis-se indique le temps en mois. 0 etant le moment de la priseradiographique a 6 mois. La seconde radiographie a eteeffeetuee au moment indique en fin dc traec. La perteosseuse lue a la radiographie est indiquee par des flechesdefinissant aussi t'intervalle de temps.

  • ATTACHMENT LOSS AND BONE LOSS 353

    Table 2. Magnitude of change of the measured radio-graphic bone height compared to the maximum at-tachment level changeVergleich zwischen Verandenmgcn rontgenologisch er-mitleller Hohe des aheolaren Knochenkammes undmaximalen Verdnderungen der Hohe des Atlacluncnl-niveaus (der Hohe des Epilhelansalzes)Ampleur de la perte osseuse lue sur la radiographiecomparee au changemeni maximal de niveau d'attache

    Radiographieloss (mm)

    1.201.171.040.840.600.560.560.560.560.5

    r=0.76 mm

    Attachment levelchange (mm)

    5.04.05.04.03.54.05.55.02.56.0

    r=4.5 mm

    level change to predict radiographie bone losscan be evaluated from the data of Table 3. Foran attachment loss of 1 or 2 mm, neither priornor coincident relationship had predictive abilityas indicated by high false positive ratios and lowlikelihood ratios ( T P / F P ) . For attachment levellosses of 3 mm or greater measured prior to theradiographie measurement interval, predictionimproved as indicated by lower FP ratios andhigher likelihood ratios. In contrast, attach-

    ment loss measured over the same time frame asradiographie analysis had consistently poorability to predict radiographie loss. These rela-tionships are illustrated in Fig. 3 where it can beseen that for all false positive values less than50%, attachment loss measured prior to aradiographie monitoring period was a betterpredictor of bone loss than coincident attach-ment loss.

    The relationship between prior and coinci-dent attachment loss measurement and theprediction of bone loss was also seen in the post-test probabilities (Table 4). Considering that thebest estimate of the probability of significantbone loss was 0.061 in the group studied (TableI), knowledge of attachment loss of 1 or 2 mmonly slightly increased the probability that agiven site would exhibit bone loss either duringor following the attachment loss. However, anattachment loss of 3 mm or more prior to theradiographie measurement interval eonsider-ably increased the probability of subsequentbone loss to 0.8 with 5 mm of attachment lossand decreased the probability of a false negativeresult. In contrast, attachment loss coincidentwith the radiographie analysis interval had littleeffect on any of the post-test probabilities.

    Discussion

    If two events A and B, oecurred sequentially in aseries, one would expect that:

    Table J. Attachment loss as a predictor of radiographie bone lossAltachmentverlust (Hohenverlust des Epithelansatzes) als Pradiktor rontgenologisch ermittellen Knochenschwiin-desPerte d'attache preeedant la perte osseuse radiographique (TP: positif vrai, FP: positif faux)

    Attachment losscutoff (mm)

    12345

    TPratio

    0.800.700.600.600.40

    Prior toradiographie loss

    FPratio

    0.760.420.190.050.01

    TP/FP

    1.051.673.16

    12.040.0

    TPratio

    0.900.800.500.200.20

    Coincident withradiographie loss

    FPratio

    0.930.530.280.150.10

    TP/FP

    0.971.511.791.332.0

  • 354 GOODSON, HAFFAJEE AND SOCRANSKY

    IOOT

    TRUE POSITIVE

    RATIO 50

    ATTACHMENT LEVELMEASURED PRIORRADIOGRAPHICCHANGE

    ATTACHMENT LEVEL. MEASURED COINCIDENT WITH

    RADIOGRAPHIC CHANGE

    50FALSE POSITIVE RATIO

    100

    Fig. 3. Prediction of bone loss from attachment loss(receiver-operating-characteristic, ROC). The ;^-axisrepresents the true positive ratio and the x-axisrepresents the false positive ratio, both expressed as a%. Points and curves represent computed values oftrue positive and false positive ratios for varyingdegrees of attachment loss. Closed circles representvalues for attachment level measured prior to radio-graphic change and open circles for attachment levelmeasured coincident with radiographic change. TheROC curves indicate that attachment level measure-ments made prior to radiographic change are superiorpredictors of bone loss for all values of false positiveratio less than 50%.

    Die Voraussagc des Knochenschwundes dwell Beob-achtung des Attachment (Epithelan.satz)-vcrhistes.(Receiver operating characteristic - ROC). Die Ordi-nate veranschaulicht die wahrepositive, unddie Abzissediefaischepositive Verhaltniszahi, beide in Prozentwer-ten ausgedrUckt. Die Punkte und Kurven bezeichnen diewahren positiven und die falschcn positiven Verhaltnis-werte bei Epithelansatzveriust versehiedenen Grades.Die geschlossenen Kreise bezeichnen die Werte desAttachmentniveaus vor der im Rontgenbild konstatier-ten Verdnderung des Knochenniveaus und die offenenKreise die Attachmentniveaus, die mit der rontgenolo-

    gischen Veranderung zusammenfieien. Die ROC-Kur-ven zeigen, dass die Messung des Attachmentniveausvor der rontgenologisch konstatierbaren Veranderungdes Knochenniveaus fiir alie faischen positiven Werteunder 50%, ais Pradiktoren des Knoehenschwundesiiberlegen sind.Prediction de la perte osseuse a partir de la perted'attaehe. L'ordonnee represente le % de positif-vrai eti'abscisse le pourcentage de positif-faux. Les points etcourbes sont ies vaieurs integrees des proportions depositif-vrai et positif-faux pour des degres variables deperte d'attaehe. Las points fonces representent lespertes d'attaehe enregistrces avant les changementsradiographicjues et les elairs eelles coincidant avec Iesehangements radiographiques. Les courbes montrcntque les mesures dc perte d'attaehe effectuees avant leschangements radiographiques sont de meilleurs predic-teurs de perte osseuse pour toutes les vaieurs de propor-tion positif-faux inferieure a 50%.

    (1) event A would be observed to precede B inmost if not all cases;(2) the occurrence of A would predict B withhigh probability;(3) the occurrence of B would fail to predict A.

    In 7 out of 10 of the sites for which bothradiographic and attachment level measure-ments were available, a major attachment levelchange preceded the period over which radio-graphic bone loss was detected. In these cases,radiographic evidence of bone loss occurredduring a period when attachment level hadreturned to a more coronal, stable level. There-fore, the most common observed pattern wasthat in which an attachment level change pre-

    Table 4. Post-test probabilities ' .Wahrseheinlicher Verlauf nach dem TestProbabilites consecutives aux tests (Tj de I'existenee ou non de perte osseuse (D + /) avec ou sans perted'attaehe (T+/-)

    Attachment losscut-off (mm)

    Prior toradiographic loss

    /'(D-I-IT-I-) /'(D + lT

    Coincident withradiographic loss

    P(D-t-lT-l-) P(D-l-lT-)0.0710.1090.1870.4610.800

    0.0590.0360.0350.3000.042

    0.0670.1000.1160.0910.132

    0.0900.0300.0490.0650.061

  • ATTACHMENT LOSS AND BONE LOSS 355

    ceded radiographic evidence of bone loss byseveral months (Fig. 2).

    An attachment change of 4 mm predictedsubsequent bone loss in 60% ofthe cases with afalse positive error of 0.05 (Table 3). By com-parison, an attachment change of 4 mm oc-curring during the radiographic monitoringinterval "predicted" only 20% of the instanceswhere radiographic loss was measured. Goodpredictive ability would correctly identify alarge proportion of sites with radiographicevidence of bone loss without including siteswhich did not exhibit bone loss. The likelihoodratio ( T P / F P ) , a measure of predictive ability, isgreater at all cutoff levels for attachmetit lossmeasured prior to radiographic bone loss thanmeasurements made at coincident times (Table3). This relationship is also shown in post-testprobability (Table 4). Given that the probabili-ty of bone loss in the group of subjects studiedwas 0.061 (Table 1), an attachment loss of 4 mmincreases the probability that bone loss willfollow to 0.461 with 0.03 probability that boneloss will occur without an attachment loss ofthat magnitude. Note that an attachment loss of5 mm is associated with near certainty (/) = 0.80)that bone loss will follow at a later time (Table3). In contrast, post-test probability of coinci-dent attachment and bone loss is only slightlyimproved over the initial probability of 0.061.Therefore, attachment loss predicts bone losswith a high probability, but only when theattachment loss measurement precedes thebone loss measurement.

    The final point, failure of B to predict A isillustrated by the observation that none of thesites which lost bone predicted subsequentattachment loss over the 1-year monitoringperiod. Thus, the true positive ratio of bone lossto predict attachment loss was 0% and the falsepositive ratio was 100%. This surprising ob-servation requires some explanation. Siteswhich became shallower from the beginning ofthe measurement period have been termed"gain" in attachment. It seems clear now thatthese sites were those which entered the study in

    a disease active state and spontaneously under-went remission during the monitoring period.In this subject group, sites exhibiting significant"gain" were 9.6% by running medians and11.6% by regression (Table 1). Most sites (7 outof 10) which exhibited bone loss were among thesites which were classified in a previous com-munication (Goodson et al. 1982) as exhibitingattachment level gain.

    These observations suggest that periodontalattachment loss precedes radiographic evidenceof bone loss by several months. For those sitesshown in Fig. 2, if the initial attachtnent changeof 4 to 6 mm as illustrated was used to indicatedisease activity, diagnosis of active disease byradiographic analysis would have been delayedby 7 to 16 months, indicating that radiographicanalysis of periodontal disease by means used inthis study does not appear to be capable ofdetecting early disease changes. Furthermore,the attachment level measurements at the timeof the second radiograph would suggest that thelesion had undergone a considerable degree ofrepair by that time and the disease may havealready subsided.

    The inability of the radiographic methodused in this study to provide early detection ofperiodontal disease activity relates primarily tothe conventional use of clinical radiographs fordiagnosis of periodontal disease. Methods in-volving densitometric changes (Hausmann etal. 1979, Grondahl et al. 1982) would presum-ably have a greater potential for early detectionof bone loss due to active periodontal disease.

    There is reason to question whether attach-ment level measurements have any direct rela-tionship to bone loss. In a comparative study ofseveral measures of periodontal destruction,Renvert et al. (1981) found that the correlationbetween attachment level and probing bonelevel or attachment level and entry/re-entrybone height was good (^ = 0.81 and 0.75, re-spectively). However, correlation between at-tachment level and radiographic bone heightwas much weaker (R = 0.45). The magnitude ofmaximum change in attachment level observed

  • 356 GOODSON, HAFFAJEE AND SOCRANSKY

    in our study was consistently greater than thatof the measured radiographie change (Table 2).On average, for disease active sites, attachmentlevel measurements changed by 4.6 mm, whileradiographie crestal bone height changed by0.76 mm.

    It seems likely that the large changes inattachment level measured reflect a large under-lying change in bone which is not detected bythe radiographie measurements of crestal boneheight. This has been suggested by studies onradiopharmaeeutical uptake in beagle dogswith periodontal disease (Jeffeoat et al. 1980,1983). In these studies, a high uptake of techne-tium-99m-diphosphonate at periodontal sitescorrelated significantly with radiographie evi-dence of bone loss measured 8 months later(^ = 0.85). This observation suggests that a highlevel of localized bone metabolism occurs sever-

    al months before radiographie evidence of boneloss can be seen.

    It has been demonstrated that complete re-moval of medullary bone produces little changein the radiographie appearance of a periodontalsite (Lang and Hill, 1977). In this connection,it is instructive to eonsider the ease history eitedby Haffajee et al. (1983) in which an infrabonydefeet undeteetable by eonventional radio-graphie analysis and assoeiated with an increaseof 5 mm in the attachment level measurementwas demonstrated by direct surgical access. In astudy of the pattern of periodontal osseouslesions in dried mandibles, Stoner (1972) foundthat small, crater-like defects often oecurred inthe center of the alveolar crest. These defectswere located at a midpoint between the bueealand lingual cortieal plates whieh obseured theirradiographie deteetion. Thus, it appears that

    DISEASE AenVITY RECOVERY

    Fig. 4. Relationship between attachment loss and radiographie bone loss. This figure illustrates possibleattachment level and alveolar bone changes during a period of active destructive periodontal disease. Theearliest phase results in medullary bone loss with an accompanying increase in probing attachment level (centralfigure). During this phase, radiographie evidence of bone loss is not apparent, since the cortieal bone heightremains unchanged. At the end of the acute burst of active destructive disease, the probing attachment depthresumes a stable level and the underlying bone remodels. At that tinie (right figure), radiographie evidence ofbone loss is detected due to a decrease in the level of crestal alveolar bone.Die Beziehung zwischen dem Attachmentverlust (Hohenverlust des Epithelansatzes) und dem rontgenologischkonstatierbaren alveolaren Knochenschwund. Diese Abbildung veranschaulicht die unterschiedlichen Moglichkei-ten von Niveauhohen des Epithelansatzes bei Veranderungen des alveolaren Knochenkammes wdhrendeiner aktivenParodontalkrankheitsperiode. In der einleitenden Phase kommt eszum Schwundmarkreichen Knoehengewebes beigleichzeitig erhohter sondierbarer Taschentiefe (mittlere Abbildung). Wdhrend dieser Phase liegen keineeindeutigen Zeichenfiir das Vorliegen von Knochenschwund vor, da die kortikale Knochenhohe unverdndert bleibt.Gegen Ende des akuten Schubes der aktivdesiruktiven Krankheitsphase stabitisiert sich die Hohe des Attaehmentni-veaus und der darunter befindliche Knochen remodelliert. Zu diesem Zeitpunkt (rechte Abbildung) wird derKnochenschwund aufgrund der Senkung des Knochenkammniveaus rontgenologisch sichtbar.Relation entre perte d'attaehe et perte osseuse radiographique. Cette figure illustre les ehangements possibles deniveau d'attache et d'os alveolaire durant une periode de parodontite active. La phase primaire resulte en une perteosseuse medullaire avec sondage plus profond (centre). La perte osseuse n'est pas visible a la radiographie puisque lahauteur de I'os cortical n'a pas varie. Apres cet acees aigu de parodontite active, le niveau d'attache reste stable maisI'os environnant se remodete. C'est a ce moment (droite) que la perte osseuse est detectee a la radiographie.

  • ATTACHMENT LOSS AND BONE LOSS 357

    existence of intact cortical plates serves toobscure medullary bone loss and that radio-graphic evidence of bone loss is primarilyrelated to a change in the vertical dimension ofthe cortical bone plates.

    These observations suggest an associationbetween attachment level change and bone lossas illustrated in Fig. 4. This figure suggests thatan early bone lesion associated with attachmentloss occurs during the exacerbation phase of aperiodontal disease activity cycle. At that time,bone destruction proceeds along the lines ofleast resistance to reduce medullary bone andcollagenous tooth attachment so that the peri-odontal probe encounters less resistance there-by resulting in a larger probing attachment levelmeasurement. Since cortical bone is largelyunaffected by this early process, clinical radio-graphs taken at this time do not show detectablechange. At some period several months follow-ing this initial attack on the periodontal connec-tive tissue, as a result of host defense mecha-nisms or other changes in the local environ-ment, the lesion begins to undergo remission.Connective tissue is reformed thereby reducingthe probing attachment level, and the alveolarbone recontours to fill the medullary defect. Atthis time, radiographic evidence of bone loss isdetected as a loss in vertical height of thealveolar crest as measured from a fixed toothlandmark.

    It cannot be said that the sequence describedis true of all cases. A rapid bone loss conditionhas been associated with periodontal diseaseconditions such as juvenile periodontitis inwhich radiographic evidence of bone loss andattachment loss appear to occur simultaneous-ly. None of the subjects in this study hadjuvenile periodontitis. However, 2 of the 10cases identified in this study had significantbone loss and attachment loss in the same timeinterval.

    At our current state of understanding, asignificant change in attachment level appearsto be the earliest detectable event with radio-graphic evidence of bone loss following by

    several months. However, attachment levelchange is not the first event in the series leadingto periodontal destruction. Elucidation of thosebiological events which relate to the time frameof attachment loss and bone loss will be achallenge for the future.

    Acknowledgements

    This work was supported in part by grant #DE-04881 from the National Institute of DentalResearch.

    Zusammenfassung

    Die Beziehung zwischen dem Attachmentver/ust undalveolarem KnoehenverlustBei 22, an destruktiver Parodontitis erkrankten,unbehandelten Patienten wurdcn ein Jahr lang regel-massig die Zahnfleisehtaschen gemessen, sowie stan-dardisierte Rontgenaufnahmen angefertigt.

    0, 6 und 12 Monate nach dem Versuchsbeginnwurden vorher bestimmte Regionen rontgenograph-isch untersucht. Attachmentniveaumessungen wur-den monatlich vorgenommen. Das Ausmessen derRontgenbilder erfolgte auf Projektionsbildern in 7-facher Vergrosserung. Die Hoiie des alveolarenKnochenkammes in Bezug auf die Schmelz-Zement-grenze wurde durch Multiplikation der mittlerenWurzellange mit der Verhaltniszahi zwischen denMesstrecken von der Schmelz-Zementgrenze zumKnochenkamm, und von der Schmelz-Zementgrenzezur Wurzelspitze, errechnet. Jedes Rontgenbild wurdevon den Untersuchenden 2 X vermessen. Regionenmit nicht erkennbaren Messpunkten, bei denen dieStandarddeviation der 4 Messungen den Messirrtumbei wiederholten Bestimmungen um 0.16 mm Ciber-schritt, wurden nicht ausgewertet.

    Als kritischer 3-Sigma Wert fur signifikantenKnoehenverlust wurde 0.48 mm bestimmt.

    Die Veranderungen des Attachmentniveaus wur-den fur Zeitabschnitte vor und wahrend der 6-12Monate andauernden rontgenographischen Messpe-riode berechnet.

    Von diesen kritischen Werten ausgehend, wurdebei 6.1% der 231 rontgenfotografierten Regionensignifikanter Knoehenverlust konstatiert. Analog da-zu wurde bei 5.7% der 1155 sondierten Regionensignifikanter Attachmentverlust festgestellt. Bei kei-ner der Regionen mit signifikantem Knoehenverlustlag jedoch gleichzeitig ein sichergestellter Attach-mentverlust vor. Im allgemeinen ging ein 6-8 Monatelang konstatierbarer, signifikanter Attachmentver-lust dem alveolaren Knochenschwund voraus.

  • 358 GOODSON, HAFFAJEE AND SOCRANSKY

    Ein Attachmentverlust vom 4 mm zeigte bei wahrerpositiver Abhangigkeit von 60% und einem falschenpositiven Abhangigkeitsverhaltnis von 5%, hochgra-dig voraussagendes Diskriminationsvermogen fur zuerwartenden alveolaren Knoehenverlust an. DieseBeobachtungen zeigen, dass wiihrend der Periodenparodontaler Krankheitsaktivitat, der Attachment-verlust dem durch das Rontgenbild nachweisbarenalveolaren Knoehenverlust vorausgeht.

    Resume

    Relation entre perte d'attache et perte osseuseDes radiographies reproductibles et des sondages depoehe rcpctes ont ete effeetues au cours d'une anneesur 22 sujets non traltes atteints de parodontite. Desradiographies de sites selectionnes (>4mm) ont eteprises a 0, 6 et 12 mois et les mesures des niveauxd'attache tous les mois. Les mesures radiographiquesont ete faites sur des images projetces agrandies 7 X.La hauteur alveolaire osseuse par rapport a lajonc-tion email-eement (JEC) a ete integree en multipliantla longueur moyenne de la racine par la fractiondistance JEC - os sur distanee JEC - apex. Chaqueradiographie a ete mesuree a 2 reprises par 2 cher-eheurs. L'ceart-type de l'erreur de lecture osseuse surde bonnes radiographies etait de 0.16 mm, et les sitesaux points de repere imprecis et ou I'ecart-type des 4leetures etait superieur a 0.16 mm ctaient elimines.Une valeur eritique 3 sigma de 0.48 mm a eteseleetionnee pour une perte osseuse significative. Lesvariations de niveau d'attache ont etc intcgrees pourles intervalles de la periode de mesures radiographi-ques de 6-12 mois et antcrieurs a celle-ci.

    Bases sur ces valeurs critiques, 6.1% des 231radiographies montraient une perte osseuse significa-tive. De meme, 5.7% des 1155 sites sondes aceusaientune perte d'attache significative. Cependant aucundes sites avee perte osseuse significative ne presentaitde perte d'attaehe significative durant la meme peri-ode. En general, une perte d'attache significativepreeedait la perte os.seuse de 6 a 8 mois. Avee uneperte d'attache de 4 mm, une perte osseuse subsequen-te pouvait etre predite avec 60% de positif-vrai et 5%de positif-faux, ce qui constitue une predietion tressure. Ces observations indiquent que la perte d'atta-che precede l'evidence radiographique de perte os-seuse lors des parodontites aetives.

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