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In recent years, much interest has been of periodontal health rather than the sig- healing period of 1 month, reevaluation
focused on the evaluation of existing nificance of presence of BOP for the was carried out and periodontal surgery
routinely used periodontal diagnostic recurrence or progression of disease. using the modified Widman flap pro-
parameters for their accuracy to be used The purpose of this prospective clin- cedure (Ramfjord & Nissle 1974) was
as predictors for progression of perio- ical trial was to determine the predictive performed in areas where pocket prob-
dontal disease or disease recurrence fol- value of absence of "bleeding and prob- ing depths of 5 mm or more remained
lowing periodontal therapy. In this con- ing" for the maintenance of periodontal (less than 50% of the patients). At least
text, the predictive value of bleeding on health and to test the feasibility of such 1 month (up to 3 years) following the
probing (BOP) has been tested in a few a clinical parameter in a private practice surgical procedure, the patients were re-
clinical studies (e.g., Badersten et al. situation. evaluated and baseline data for this
1985, Lang et al. 1986). The results of study obtained. The baseline data for
these studies revealed that BOP yielded the patients who did not need surgical
rather low predictive values for disease Material and Methods therapy were obtained at various time
progression and/or recurrence. One of 50 patients were selected for this clinical points following the completion of the
the reasons for this finding, however, trial on the basis of the presence of hygienic phase but during ongoing
could have been that the studies were periodontal disease and the patients maintenance. None of the patients were
carried out in patients enrolled in a availability for maintenance visits fol- aware of their participation in the clin-
maintenance care program following lowing active periodontal therapy. At ical trial.
treatment, and repeated instrumen- the completion of the study, 14 males Maintenance visits were scheduled at
tations of all sites exhibiting bleeding and 27 females, 20 to 60 years of age, regular intervals varying between 2 and
on probing were performed for ethical were available for final evaluation be- 6 months. Hence, within the designed
reasons. These repeated interferences cause of their compliance with the main- observation period of the present study
with the subgingival microbiota may tenance schedule, while 9 patients had 2-2'/2 years), the patients had presented
have contributed to an improvement of to be excluded from evaluation because for maintenance therapy at least 5 times
the periodontal conditions, thereby ob- of irregularities (Fig. 1). Initially, all pa- (Table 1).
scuring the predictive value of BOP for tients presented with moderate to ad-
disease progression. Ideally, the predic- vanced periodontal disease with at least
tive value of BOP for disease pro- one advanced lesion (i.e., pocket prob- Ciinicai procedures
gression should be determined in a sys- ing depth > 6 mm and loss of alveolar All maintenance care was performed by
tem without the interference of regular bone >40% of the root length) in each the same experienced dental hygenist
maintenance care. Since such a study quadrant. Initial treatment comprised and supervised by the same general den-
cannot be done for ethical reasons, it motivation and instruction in oral hy- tist with special post graduate training
appears logical to study the importance giene measures and scaling and root in periodontics (RA). At the beginning
of absence of BOP for the maintenance planing of all tooth surfaces. After a of each maintenance visit, the con-
Absence of bleeding 715
10 - Data analysis
(D
For the purpose of simplicity, only data
E based on normalized BOP-frequencies
3 are presented in this report.
Sites in which complicating factors,
such as furcation involvements, restora-
tions or adjacent extractions performed
20-29 30-39 40-49 50-59
during the maintenance phase, could in-
Age (baseline) fluence gingival bleeding were excluded
Eig. 1. Age and sex distribution and number of patients at basehne prior to the maintenance from analysis. Also, all sites of third
program. molars were disregarded. Of these rea-
sons 369 sites (9%) were excluded, and
a total of 3807 (91 %) sites in 41 patients
Table 2. Actually scored BOP frequencies were available for statistical analysis.
Normalized frequency of BOP Separate calculations of interproxi-
Actual number of mal sites (i.e., exclusion of buccal and
maintenance visits 0 1 2 3 4 6
lingual sites) in order to avoid the influ-
5 0 1 2 _ 3 4 5 ence of possible trauma from tooth
6 0 1 2 3 4 5 6 brushing were also performed. Because
7 0 1 2 3/4 5 6 7 of anatomical differences in different in-
0 2/3 4 5/6 8 terproximal areas, premolar and molar
9 0 1 2/3 4/5 6/7 8 9 interproximal sites (side teeth) were also
group rarely occasionally frequently analyzed separately.
Progression of periodontal disease
Example (circled in Table 2). A patient who was seen at 8 maintenance visit: a site having a
normalized BOP frequency of 5 (out of 6) actually scored 7 out of 8, and a site having a
was defined by scoring both > 1 mm
normalized BOP frequency of 1 (out of 6) actually scored 1 out of 8. and > 2 mm ofprobing attachment loss
716 Lang et al.
H -
uu - " "
values exceeding 31% (Fig. 3). When
analyzing single sites, 58% of the sites
80 - bled rarely and 12% yielded frequent
bleeding (Fig. 4). These percentages are
H
slightly higher than those encountered
.1 60 - BOP - Prevaience
D Oof 6
in a previous study in a university en-
o vironment (Lang et al. 1986) and may
40 -
Blliililil'" 1 of 6
refiect the standard of a prophylactical-
2 of 6
3 of 6 ly oriented semi-rural practice. Also,
4 of 6 during the observation period of 2.5
20 -
5 of 6 years it was found that 2.4% of all sites
6 of 6 lost > 2 mm of probing attachment.
0 - This is substantially more than the 0.8%
Total Reduced Stable Increased of tooth surfaces which lost similar
amounts of attachment during the
3807 41 3735 31 Sites
course of 14 years in a study on perio-
Fig. 8. Difference in probing depth >2 mm during the observation time in relation to BOP dontal maintenance care (Lindhe and
prevalence.
Nyman, 1984). However, the finding
that 2.1 % of all sites yielded >2 mm of
gingival recession in the present study
^^^
and that only 0.8% of the surfaces
showed increased probing depths sug-
gests that the loss of attachment en-
uu - countered may partly have been the ef-
fect of an overzelous toothbrushing.
80 - About 25% (19) of all recessions (81)
mnnnon
affected buccal surfaces, most of them
BOP - Prevalence without clinical signs of gingival inflam-
a> Rn -
mation (13 sites did not bleed at any
., n Oof 6
1 of 6 recall visit, 4 sites bled once, 2 sites bled
40 - ED 2 of 6 2 times). Nevertheless, the fact that
3 of 6 there was a higher number of sites with
4 of 6 recession that sites with increased prob-
20 -
5 of 6 ing depth emphazises the importance of
6 of 6 regular surveillance of toothbrushing
0- techniques during periodontal mainten-
Total Gain Stable Loss ance.
3807 64 3652 91 Sites In 46 sites (1.2%) which scored 6-9
Fig. 9. Difference in attachment level >2 mm during the observation time in relation to BOP mm probing depth at the completion of
prevalence. ' - . . the study, bleeding on probing was quite
Absence of bleeding 719
frequently observed (Fig. 5). Over 60% pockets > 4 mm appear to bleed more should be instrumented at all recall
of these sites bled 5 or 6 times out of 6 frequently on probing than sites with visits in order to ehminate gingival in-
maintenance visits. In contrast, in the probing depths of less than 4 mm. This fiammation (Lang et al. 1986).
86% of sites (3268) with 1-3 mm prob- may indicate a higher risk for deep The characteristics of diagnostic tests
ing depth, BOP was observed rarely or pockets to lose further attachment than are generally expressed in terms of sensi-
at irregular intervals. This documents shallow sites and would also suggest tivity and specificity as well as positive
that sites with residual periodontal that pockets with deep probing depth and negative predictive value for disease
progression (Fig. 2). In the present
study, these characteristics for BOP as
a diagnostic test have been calculated
for different standards to indicate dis-
E ease progression as well as different
CM threshold levels for a positive diagnostic
Al test. In this respect, loss of attachment
of > 1 mm or > 2 mm respectively were
selected as standards for disease pro-
D All teeth gression, while a positive diagnostic test
H m+d, all teeth of BOP was assessed for both a BOP
^ m+d, side teeth frequency of > 2 or a BOP frequency of
a> > 5 out of 6 maintenance visits. The
'55 results of these calculations showed,
that the sensitivity of BOP as a diagnos-
tic test was influenced both by the selec-
tion of the standard for disease pro-
0 to 1 2 to 4 5 to 6 gression and by the selection of the
Bleeding prevalence (6 recalls) threshold level for a positive test. On
Fig. 10. % of sites with > 2 mm loss of attachment in relation to the BOP prevalence. the other hand, it was noted that the
specificity of BOP as a diagnostic test
was only influenced by the selection of
the threshold level for a positive test
E (Table 3). The highest sensitivity
E (66.7%) was observed when the stan-
20 - dard for disease progression was se-
Al lected to be > 2 mm of loss of attach-
ment and the threshold level for a posi-
o D All teeth tive test was chosen to be a BOP
m+d, all teeih prevalence > 2 out of 6 maintenance
10 - m+d, side teeth visits. For the practitioner, the determi-
nation of the sensitivity and specificity
o of a diagnostic test may be of limited
4-*
value, since these characteristics gener-
"55 ally refiect the probability to have ob-
tained a positive or negative result of
0 to 1 2 to 4 5 to 6 the test under the prerequisite that the
actual status of the patient is known.
Bleeding prevalence (6 recalls) The practioner may, therefore, be more
Fig. 11. % of sites with > 1 mm loss of attachment in relation to the BOP prevalence. interested in the so-called predictive
values of a test, since these refiect the
probability of a disease to progress or
Table 3. % with different standards and test-threshold values. to remain stable. Predictive values pre-
dominantely depend on the selection of
Standard for disease progression LOA > 1 mm LOA > 2 mm
the standard for disease progression.
Positive test: BOP frequency >2 >5 >2 >5
For instance, the positive predictive
true positive 7.5 2.4 1.6 0.7 value in the present study varied be-
false positive 34.4 9.6 40.3 11.3 tween 3.8-5.8%, when a loss of attach-
false negative 9.8 14.9 0.8 1.7 ment of > 2 mm was chosen as the stan-
true negative 48J 73.1 57.3 86,3
dard for disease progression. However,
prevalence 17.3 17.3 2.4 2,4 selecting a standard of > 1 mm loss of
accuracy 55.8 75.5 58.9 87,0 attachment to indicate disease pro-
sensitivity 43.4 13.9 66.7 29,2 gression, positive predictive values of
specificity 58.4 88.4 58.7 88,4 17.9 and 20.0% respectively were found.
5.8 Since predictive values primarily de-
positive predictive value 17.9 20.0 3.8
83.1 98.6 98.1 pend on the prevalence of a disease, it
negative predictive value 83.1
720 Lang et al.
is evident that choosing a standard of Lang et al. (1986) demonstrating that positiven und negativen Voraussagewerte
> 1 mm loss of attachment as a stan- the positive predictive value of BOP (predictive values) beurteilt. Wahrend eine
dard of disease progression covers a generally did not exceed 30%. Higher diagnostische Empfmdlichkeit (sensitivity)
much greater number of sites (17.3%) positive predictive values may probably von nur 29% fiir haufig vorkommendes Blu-
ten beim Sondieren (BOP) berechnet wurde,
than if a loss of attachment > 2 mm is have been achieved in the present pro- betrug die Spezifitat (specificity) 88%. Die
chosen (2.4%). However, in the latter spective study if the patients had been Tatsache, dass der positive Voraussagewert
case, the chance for detecting true loss left untreated. However, because of ethi- (predictive value) fur die Progression der La-
of attachment and thereby coming cal reasons, such data could not be ob- sion nur 6%, der negative Voraussagewert
closer to the "gold standard" is in- tained. On the other hand, the results (predictive value) dagegen 98% betrug, be-
creased, since the measurement error in- of the study clearly show that absence deutet, dass die andauernde Abwesenheit von
herent in pocket probing is most likely of bleeding on probing demonstrated a "Bluten beim Sondieren" ein zuverlassiger
by-passed (Armitage et al. 1977). On the very high probability for the mainten- Pradiktor fur die Erhaltung der parodonta-
other hand, minute loss of attachment ance of periodontal health and hence, len Gesundheit ist.
will be disregarded in this case, which this parameter may be recommended
in turn may explain the low positive for use in daily practice.
predictive value of BOP as a diagnostic When using BOP as a clinical par- Resume
test. It is, therefore, reasonable to dis- ameter for tissue evaluation, especially
cuss the clinical relevance of the nega- during maintenance care, the results of Absence de saignement au sondage. Un indica-
teur de la stabilite parodontale
tive predictive value of BOP as a diag- the present study suggest that non- Suite au traitement parodontal actif, 41 pa-
nostic test. bleeding sites do not need further treat- tients ont eu des rappels tous les 2 a 6 mois
Hence, in the present study, it was ment, while bleeding sites will be over- pendant deux ans et demi. Au debut de cha-
found that BOP had a high negative treated in 4 out of 5 cases when instru- que visite de maintien, les tissus parodontaux
predictive value for disease progression. mented. However, from a clinical point ont ete evalues en utilisant le saignement au
This was clearly reflected by the nega- of view, overtreatment of bleeding sites sondage (BOP). Un nouveau lissage radicu-
tive predictive value of 98.1% found for may be acceptable in patients whit a laire n'a ete effectue qu'au niveau des sites
the frequently bleeding sites (BOP history of periodontal disease. saignant au sondage. Cependant, la plaque
et le tartre sus-gingivaux ont toujours ete en-
prevalence: 5/6 or 6/6), when a "stan-
leves. Les profondeurs de poche et les niveaux
dard" for disease progression of > 2 d'attache au sondage ont ete enregistres suite
mm was chosen. This in turn means that au traitement actif ainsi qu'a la fm de Fetude.
the absence of BOP is a good indicator Acknowledgements La progression de la maladie parodontale a
for the maintenance of periodontal sta- This study has been supported by the ete defmie lorsqu'il y avait une perte d'atta-
bility. Chnical Research Foundation (CFR), che d'au moins 2 mm. La fiabihte du test
Although the sensitivity and positive University of Berne, Switzerland. BOP en tant que signe avant-coureur a ete
predictive value of BOP for loss of evaluee en calculant la sensibilite, la specifi-
attachment was rather low in this study, cite, la precision et les valeurs de presage
positif et negatif. Alors que seulement 29%
this might have been influenced nega- de sensibilite etait calculee comme saigne-
tively even more if the BOP-scoring Zusammenfassung ment frequent, la specificite etait de 88%. Le
would have been performed strictly ac- fait que la valeur de presage positif de la
cording to the method of Ainamo & Abwesenheit von Bluten beim Sondieren. Fin progression de la maladie etait seulement de
Bay (1975) (probing in the gingival crev- Indikator der parodontalen Stabilitdt 6% et que la valeur de presage negatif etait
ice and not to the bottom of the pocket). Nach durchgefiihrter aktiver Parodontalthe- de 98%, rend I'absence continue de BOP un
rapie wurden 41 Patienten wahrend 2 1/2 Jah-
The possibihty of false negative values ren in ein Betreuungsprogamm einbezogen. signe avant-coureur fiable pour le maintien
for BOP would have been even greater Die Abstande zwischen den Prophylaxebesu- d'un parodonte sain.
in pockets with deeper probing depth chen variierten zwischen 2-6 Monaten. Zu
than in more shallow sites. However, Beginn jeder Prophylaxesitzung wurde das
all sulci or pockets were probed to the Vorkommen von "Bluten beim Sondieren" References
bottom of the pocket at each recall visit (BOP) registriert, um den Zustand der paro-
thereby minimizing the change for false dontalen Gewebe zu heurteilen. Wiederholtes Ainamo J & Bay I (1975) Problems and Pro-
negative values. Nevertheless, probing Scaling und Wurzelglatten wurde nur an den posals for recording gingivitis and plaque.
Zahnwurzelflachen durchgefuhrt, welche Journal of Periodontology 25, 229-235,
forces were not standardized in the pres- "Bluten beim Sondieren" zeigten. Supragin-
Armitage GC, Svanberg GK & Loe H (1977)
ent study and hence, some variations in givale Plaque und Zahnstein wurden jedoch
Microscopic evaluation of clinical meas-
probing forces might have been used at immer entfernt. Sondierungsmessungen der urements of tissue attachment levels. Jour-
the different assessment. It was attempt- Taschen und Bestimmen des klinischen At- nal of Clinical Periodontology 4, 173-190.
ed to control this riks for variability in tachmentniveaus wurden nach durchgefuhr- Badersten A, Nilveus R & Egelberg J (1985)
the number of false negatives by letting ter aktiver Parodontaltherapie und beim Effect of nonsurgical periodontal therapy.
the same calibrated dental hygienist per- Abschluss der Studie aufgenommen. Eine VIL Bleeding, suppuration and probing
form all the BOP-examinations Verringerung des sondierbaren Attachment- depth in sites with probing attachment
niveaus um 2 mm oder mehr wurde als Pro- loss. Journal of Clinical Periodontology 12,
throughout the study.
gression der parodontalen Lasion gedeutet. 432-440.
Under the circumstances of this clin- Die Zuverlassigkeit des "Bluten beim Sondie-
Bass, C. C. (1954) An effective method of
ical trial, the positive predictive value of ren" (BOP)-Test, als ein Voraussager wurde personal oral hygiene. Journal of the Loui-
BOP for disease progression was low durch die Berechnung der diagnostischen siana Medical Society 106, 57-73, 101-
to moderate. This corrobarates results Empfindlichkeit (sensitivity), Spezifitat (spe- 112.
presented by Badersten et al. (1985) and cificity), Genauigkeit (accuracy) sowie der Fletcher RH, Fletcher SW & Wagner EH
Absence of bleeding 721
(1982) Clinical epidemiology; the essentials, a predictor for the progression of perio- Address:
chapter 3, 41-57. Williams & Wilkins, dontal disease? Journal of Clinical Period-
Baltimore. N.RLang ^^
ontology 13, 590-596.
Fowler C, Garett S, Crigger M & Egelberg J University of Berne
Lindhe J & Nyman S (1984) Long-term main-
School of Dental Medicine
(1982) Histologic probe position in treated tenance of patients treated for advanced
Freiburgstmsse 7
and untreated human periodontal tissues. periodontology. Journal of Clinical Period-
CH-3010 Berne
Journal of Clinical Periodontology 9, ontology 11, 504-514.
Switzerland
373-385. RamQord, S. P. & Nissle, R. R. (1974) The
Lang NP, Joss A, Orsanic T, Gusberti FA & modified Widman flap. Journal of Period-
Siegrist BE (1986) Bleeding on probing - ontology 45, 601-608.