You are on page 1of 10

Periodontology 2000, Vol.

39, 2005, 30–39 Copyright  Blackwell Munksgaard 2005


Printed in the UK. All rights reserved PERIODONTOLOGY 2000

Clinical parameters: biological


validity and clinical utility
ANDREA MOMBELLI

Periodontal diagnosis and monitoring rely upon probing depth and attachment level, the percentage
clinical parameters to a large extent. Clinical diag- of deep periodontal pockets or sites bleeding upon
nosis directly affects decisions to initiate therapy, to probing).
select methods, and to outline the topographical area
of application. Dentists also evaluate the outcome of
What do we measure?
therapy, and attempt long-term prognosis based on
clinical parameters. Finding the Ôbottom of the pocketÕ by inserting a
This paper will specifically focus on the biologic blunt instrument between the tooth and the gums
validity and utility of clinical parameters assessed until it meets resistance seems to be a straight-
with the periodontal probe. forward procedure. Various technical and biological
factors, however, determine how a probe tip advan-
ces and where it finally stops. Up close, this proce-
Biological validity dure is surprisingly complex, and the data it
generates need some interpretation. Firstly, the shape
Pocket formation and loss of attachment are pathog- and the diameter of the probe matter, as they deter-
nomonic for periodontal disease. The reduction of mine the pressure of the instrument on ⁄ in the peri-
periodontal pocket depth and gain of attachment are odontal tissues at any given probing force (47). Probe
thus obvious clinical goals of periodontal therapy, and design was a discussion topic for a long time (95).
pocket probing appears as the evident method for The periodontal probes mostly used today in practice
diagnosing the disease and evaluating therapy. The and clinical research are slightly tapered metal cyl-
primary parameters assessed by periodontal probing inders with horizontal marks, with a rounded tip
are probing pocket depth (the distance between the 0.4–0.5 mm in diameter. These types of probes have
gingival margin and the bottom of the sulcus ⁄ pocket), been used in the majority of clinical trials to record
gingival recession (the distance between the cemento- pocket probing depth and clinical attachment level
enamel junction and the gingival margin), and clinical on a millimeter scale.
attachment level (the distance between the cemento- To discuss the biological significance of perio-
enamel junction and the bottom of the sulcus ⁄ pocket). dontal probing, we need to briefly review the
Measuring probing depth, recession, and attachment anatomic structure of the Ôperiodontal pocketÕ and its
level at the same time is redundant, since with any two histologic components interfering with probe inser-
of these parameters the third is also established tion. Under ideal conditions of periodontal health,
(Fig. 1). Periodontal probing also generates informa- the lateral wall of the gingival unit is lined by the
tion regarding bleeding on probing and suppuration sulcular epithelium in the coronal part and the
from the periodontal pocket. In addition, the perio- junctional epithelium in the apical part. The junc-
dontal probe is commonly used to determine the tional epithelium tapers apically, and its free surface
roughness of the tooth surface and to detect subgin- lines the bottom of the sulcus in the region of the
gival calculus. These two aspects are not expressed cemento-enamel junction. An attachment apparatus
numerically. Periodontal probing is site specific; consisting of a basement lamina and hemides-
secondary parameters on the level of the patient can be mosomal junctions, termed epithelial attachment,
generated using data from several sites (e.g. mean provides a union between the epithelium and the

30
Clinical parameters

Baseline Month 2 Month 6 Month 12


0
1.3
1 2.0 Gingival Recession 1.6
2.2

4 Probing Pocket Depth


4.4 4.8
mm

4.8
5 7.4 Fig. 1. Gingival recession, probing
depth, and clinical attachment level
6
gain in deep periodontal pockets of
7 subjects treated with scaling and
2.3 Clinical Attachment Gain 2.3
root planing and adjunctive sys-
8 1.7 temic antibiotics. 0 mm corresponds
to the cemento-enamel junction
9 (data from 64).

tooth surface (87). With the development of perio- examination (quite the opposite is probably done by
dontal disease, the epithelium progresses apically many clinicians).
from the cemento-enamel junction to follow the Apart from biological properties of the periodontal
receding connective fiber attachment. An inflam- tissues, the insertion of a periodontal probe may be
matory infiltrate extends apically and laterally into influenced by factors which change due to treatment,
the connective tissues. Periodontal therapy reduces but are not the object of the measurement: the
inflammation and gingival swelling and increases the roughness of the root surface, or patient comfort
firmness of the tissues (10). Histologically, a reduc- (tendency to lighter probing if a patient signals dis-
tion of the inflammatory infiltrate and the formation comfort to mechanical irritation).
of a new epithelial attachment can be demonstrated
(89).
Several studies have indicated that periodontal
probes easily fail to identify the apical termination of
Reproducibility and longitudinal
the junctional epithelium, or the coronal level of the
monitoring of clinical attachment level
connective tissue attachment (2, 4, 23, 27, 34, 56, 61,
and pocket probing depth
77, 83, 86, 88). The error by which the probe misses Information about dynamic phenomena may be
these histological landmarks is variable. Probe tips gained by combining data from repeated assess-
penetrate differently in diseased and healthy pockets ments. The potential to record loss or gain of clinical
(4, 20, 26, 42, 61, 83, 91). In untreated periodontal attachment is limited by the resolution of probing
disease, probe tips inserted with a force of 0.5 N and depends on the reproducibility of a single
penetrated through the junctional epithelium, and measurement. Probing with a manual probe has a
stopped in the connective tissue, approximately resolution of 1 mm. Electronic probes have been
0.5 mm away (23). In smokers, due to reduced proposed that may have a resolution up to 0.2 mm,
inflammation, the probe tips seemed to penetrate making it theoretically possible to detect smaller
less easily and approached nearer to the actual changes in probing depth or clinical attachment level
attachment than in nonsmokers (13). After treatment, over time (43, 69). Thirty to forty percent of perio-
probes tended to stop between the junctional epi- dontal pockets that are re-probed with a manual
thelium and the tooth, at a distance of approximately probe after 1–3 weeks may show a positive or neg-
0.7 mm coronal to its apical termination (23). Thus, ative deviation in clinical attachment level or probing
gain of clinical attachment, observed by probing after depth of ± 1 mm (41, 67). The standard deviation of a
treatment, cannot be solely explained by the forma- single measurement of an average periodontal pocket
tion of new connective tissue attachment to the root has been reported to be in the range of 0.8–1 mm (1,
surface. If the aim of periodontal probing were to 7, 33, 62, 73, 74). Consequently, in an existing peri-
locate the apical termination of the junctional epi- odontal defect, true changes in probing depth or
thelium, one would actually have to apply higher clinical attachment level can hardly be discriminated
forces for probing after therapy than at an initial from probing error in practice unless they exceed

31
Mombelli

2 mm. Shallow periodontal sites have a narrower determined attachment level would seem to be
range in probing depths and therefore show better identical with the location of the gingival margin. If
reproducibility (69). Analytical procedures have been therapy produces shrinkage of the gingival tissues,
designed to test for significant changes in clinical the use of such a slight probing force would lead to
attachment level on the basis of pairs of attachment the false conclusion that treatment has produced
level measurements, taken 1 week apart, and repea- attachment loss. On the other hand, since scaling and
ted at 2-month intervals over 1 year (33). These root planing induce a significant reduction of probing
procedures have been helpful in clinical research to depth as well, there is a crossover of the depth-force
test the prognostic capability of simpler means to plots obtained before and after treatment when they
detect active disease. One-time assessments of pro- are superimposed. This is illustrated in Fig. 3, where
bing depth, clinical attachment level, bleeding on the mean depth values obtained at 0.25, 0.50, 0.75,
probing or suppuration, used alone or in combina- 1.00, and 1.25 N are used together with the mean
tion, were unable to indicate a state of activity as levels of the gingival margin (intercept with y-axis)
determined by these procedures (32, 33). To improve before and after treatment to project depth-force
reproducibility of probing, especially in untreated curves. Crossover is located at about 0.1 N in this
patients where the presence of subgingival calculus graph (70). Thus, a probing force of 0.1 N would
may interfere with probe insertion, it has been sug- indicate no change in clinical attachment level.
gested to measure each site twice using a Ôdouble- Even lower forces would indicate mean attachment
passÕ method (73, 74). loss, and higher forces would indicate attachment
gain. Beyond the crossover area, lighter forces may
yield more attachment gain than higher forces,
Probing force and probing depth
because the newly formed long junctional epithelium
Early studies showed that forces used by clinicians for may not resist probe penetration at higher probing
periodontal probing varied considerably. Forces forces.
differed between examiners, and when different The phenomenon described above appears quite
regions of the mouth were probed (24, 25, 36). Force clearly in the results of a study by Proye et al. (78).
controlled probes have been proposed to reduce these Using standardized probing forces of 0.15, 0.25, and
possible sources of error (12, 14, 15, 28, 60, 77, 93, 96). 0.50 N, these authors evaluated the effect of a single
By recording probe penetration into a periodontal episode of root planing. They reported a mean apical
pocket as a function of probing force (Fig. 2) it can be shift of 0.84 mm of the gingival margin, and found no
demonstrated that probing depth depends upon the attachment level alterations with a probing force of
force applied to the instrument (65, 69). Since depth- 0.15 N but a significant attachment gain when the
force curves have the characteristics of saturation effects of treatment were evaluated at higher force
curves, which flatten with increasing probing force, levels.
small changes of probing force have a greater impact Although not all studies have demonstrated signi-
on the reproducibility of depth readings in the low ficant improvements in probing reproducibility
force range. In other words, deviations in probing when using force controlled periodontal probes (77,
depth are generally more likely to occur if one uses 90, 97), standardization of probing force has been
light forces (e.g. 0.25 N) for probing than heavier advocated because it reduces the possibility of
ones. Thus, if high reproducibility is the primary goal, operator bias. A more important source of error may
one should use a high probing force level. be probe positioning, which is difficult to standard-
Comparing depth-force curves recorded before and ize under practical conditions (36, 99). Splints have
after periodontal therapy, it has been found that the been used in some trials (41, 98) to secure probe
force range chosen for repeated probing influences insertion pathways and to provide vertical reference
the amount of attachment level change determined points for depth readings. There may be some jus-
(68, 70). As depth-force curves may have different tification for the use of these tools in clinical re-
shapes before and after treatment, the measurable search, but they are too complicated to be useful in
outcome of a treatment, expressed as the difference clinical practice.
in probing depth and attachment level, depends on
the force chosen for probing. In theory, if the inser-
Bleeding on probing
tion pressure is smaller than the initial resistance of
the marginal tissues, the probe tip will not penetrate The characteristics of the gingival tissues associated
into the sulcus. In this extreme case, the clinically with bleeding after probing were investigated histo-

32
Clinical parameters

Probing force (N)


0.00 0.25 0.50 0.75 1.00 1.25
0

0.5

1
Probing depth (mm)

1.5

2.5

3.5 Fig. 2. Mean depth force curves


obtained from probing measure-
4 ments with a probing device
recording depth and force simulta-
4.5 neously (data from 69).

Probing force (N)


0.00 0.25 0.50 0.75 1.00 1.25
0

2
Depth (mm)

Fig. 3. Mean depth values obtained


4 at 0.25, 0.50, 0.75, 1.00, and 1.25 N
are used together with the mean
levels of the gingival margin (inter-
5
cept with y-axis) to project mean
depth-force curves. Crossover of the
before and after treatment curves is
located at about 0.1 N (data from
6 70).

logically (30). Specimens from sites bleeding after to probing with high force as a possible reason for
probing with 0.25 N showed a significantly increased bleeding in the absence of disease. Probing with
percentage of cell-rich and collagen-poor connective controlled forces not exceeding 0.25 N was thus
tissue, but no increase of blood vessel lumens. recommended. Controlled forces were recommended
Experiments in periodontally healthy subjects dem- already in earlier studies to increase the reproduci-
onstrate that occasional bleeding upon probing can bility of bleeding on probing, but at a much higher
occur even in the absence of disease (51). In subjects force of 0.75 N (90). It is quite obvious that the
with a reduced but healthy periodontium, a nearly reproducibility of bleeding on probing can be
linear relationship has been found between the per- improved by either increasing or lowering the
centage of sites bleeding on probing and probing probing force level (eventually, either all, or no, sites
force (46). These studies pointed to tissue trauma due will bleed reproducibly).

33
Mombelli

Clinical utility established on the subject level, much less is known


about specific local factors.
The utility of a diagnostic parameter depends on its Monitoring untreated disease by recording pocket
ability to answer a concrete diagnostic question and probing depth, clinical attachment level, or bleeding
on the clinical context in which this question is on probing has a limited value for indicating present
asked. Diagnostic tasks in periodontics may include activity or predict future attachment loss (32, 33, 35).
the identification of people and dental sites at risk of However, in a population of elderly subjects, teeth
developing periodontitis, the detection of early stage with reduced attachment levels had an increased
disease in apparently asymptomatic individuals, the probability of being lost during the next 5 years. In
classification of disease categories, the delineation addition, teeth that actively lost attachment during
and local assessment of the disease in affected sub- an observation period were more likely to be lost
jects, the prediction of the likely response to a spe- during the following period than were teeth with a
cific therapy, monitoring of treatment efficacy, and stable clinical attachment level in the first period
finding recurrent disease. The utility of a diagnostic (11). As it is characteristic for periodontal disease that
parameter may not be the same in every one of these not all parts of the dentition are affected with equal
situations – it therefore needs to be determined severity, is it thus indispensable to monitor all sites
separately each time. For example, if a parameter has regularly? The answer to this question would be
been confirmed to indicate a risk for further attach- affirmative if the distribution and temporal occur-
ment loss in previously treated subjects, it is not rence of periodontal lesions were entirely random. If
automatically a proven useful diagnostic tool to the distribution and occurrence is, however, struc-
detect early stage disease in a large population. tured, a limited assessment in certain areas, and at
specific time points, may be sufficient to obtain
diagnostically useful information. Using data from
comprehensive assessments in the entire dentition,
Risk assessment and screening
we estimated the influence of symmetry on the
The issue of periodontal risk factors has been dis- variance of clinical and microbiological parameters
cussed in detail in recent years. Risk factors may in 56 patients with chronic periodontitis (66). The
influence a subject in general, or may affect perio- impact of contralateral conditions was determined
dontal tissues locally (for review, see 81). Individual on the level of the site, the tooth (Fig. 4), and the
variability in periodontal tissue destruction, docu- quadrant. Significant correlations were detected in
mented longitudinally in untreated populations (59), probing depth, recession, clinical attachment level,
calls for diagnostic procedures for the early identifi- total cultivable bacterial counts, and the plaque
cation of subjects at high risk for severe periodontal index, recorded on the right and left side on all levels
disease. While the paramount roles of smoking and of analysis. Given this amphichiral nature, the diag-
systemic diseases, notably diabetes, have been clearly nostic advantage of full mouth recordings over partial

17 27
16 26
15 25
14 24
13 23
12 22
11 21
41 31
42 32
43 33
44 34
45 35
46 36
47 37

10 8 6 4 2 0 2 4 6 8 10
Probing pocket depth (mm)
Fig. 4. Symmetrical behavior of tooth-specific mean probing depths in one subject (data from [66]).

34
Clinical parameters

assessments should be evaluated carefully in various necessarily current, disease. Since periodontal tissue
clinical situations. Correlations other than symmetry damage accumulates over time, the disease may
should also be explored for their potential to improve appear more severe in elderly patients than in young
the utility of clinical (and other) parameters. ones, although in terms of disease progression, the
Attention has been focused in the past on the contrary may be the case. For a further discussion of
possibility that periodontal disease may not be a this, the reader is referred to the article of Hujoel in
continuous process, but may be characterized by this volume (40).
episodes of activity, followed by periods of relative Decades of clinical experience and well documen-
quiescence. As has been discussed above, the ted longitudinal studies have shown that all clinically
potential of detecting an active episode of perio- distinguishable forms of periodontal disease respond
dontitis by simply probing a previously measured site favorably to a nonspecific reduction of the subgin-
after a few weeks or months is limited. On the other gival bacterial mass (52, 53, 71, 72, 75, 84, 85). How-
hand, the true impact of short bursts of activity on ever, studies have also indicated that certain
the accumulated loss of periodontal tissues over time circumstances, identifiable by periodontal probing,
also remains to be determined, and may have been may justify specific forms of therapy.
overestimated (31, 80). Slow continuous attachment • Calculus removal is accomplished less often in
loss may have considerable consequences in the deeper periodontal pockets (19, 79). Calculus
long run, although it is undetectable in studies lim- removal in deep pockets has been found to be
ited to a few months’ duration. Given the inaccuracy more efficient if a surgical access is provided for
of periodontal probing, the detection of a continuous root instrumentation (16, 18, 19).
disease process leading to 6 mm attachment loss • Deep periodontal pockets showed more pocket
over 60 years would require a minimal study period reduction following surgical procedures (54, 55, 75,
of 20 years (subsequent measurements must yield a 76).
difference of at least 2 mm in order to distinguish • Sites with shallow initial probing depth have a
tissue destruction from measurement error with tendency to lose attachment (8, 54).
sufficient confidence). • In patients with deep periodontal pockets, sys-
temic antibiotics in conjunction with scaling and
root planing can be of additional benefit compared
Classification and treatment planning
with scaling and root planing alone (38).
The historical perspective and potential problems
with the current classification are discussed in a
Monitoring
broader context by van der Velden in this volume
(92). The present chapter confines itself to a discus- The paramount question when evaluating the success
sion of the impact of clinical parameters on the of periodontal therapy is whether further interven-
classification process. Eight classes of periodontal tions are necessary or whether the therapeutic phase
diseases and conditions are currently distinguished. can be concluded. In general, this decision is based on
Among them are chronic periodontitis, aggressive a comparison of clinical attachment level, probing
periodontitis, and periodontitis as a manifestation of depth, and radiographs taken before and after treat-
systemic diseases (3). Although these three forms are ment. This means that the prognosis for future tissue
all associated with an increased probing depth and changes is based on clinically observed reactions
clinical attachment level, their differentiation is not appearing as a result of treatment. Monitoring of 1688
based on criteria derived from the periodontal pocket sites in 49 patients over 24 months indicated that the
chart. The diagnostic key elements include the outcome of nonsurgical therapy in proximal surfaces
patient’s age, systemic health, and the occurrence of of nonmolar teeth was not compromised by the
similar problems in the family – information essen- severity of the initial soft tissue or bony lesion (9). The
tially obtained by assessing the medical and dental value of clinical and microbiological data assessed
history. shortly after the completion of nonsurgical perio-
The clinical periodontal examination thus does not dontal therapy to predict the outcome several months
classify causes, it classifies destruction patterns. A later is limited (17, 22). The key parameters of probing
major limitation of periodontal probing is its inability depth and clinical attachment level may continue to
to distinguish previous tissue loss from current improve over a period of 6 months (45). It would be
disease activity. Clinical attachment level and pocket desirable to have a set of parameters for an early
probing depth reflect the extent of prior, but not evaluation of treatment success in order to be able to

35
Mombelli

decide rapidly whether additional or alternative Certain circumstances, identifiable by periodontal


therapy is necessary. probing, may justify specific forms of therapy. Teeth
Longitudinal studies on successfully treated with reduced attachment or with evidence of having
patients show that the results of conventional peri- actively lost attachment recently are at greater risk of
odontal treatment can be maintained over many being lost. In deep pockets, calculus removal is more
years if an efficient recall system is provided (5, 6, efficient after surgical access and systemic antibiotics
48, 53, 57, 85). In well-maintained populations, can offer an additional benefit. Furthermore, residual
recurrent disease seems to be limited to a few probing depth is predictive of future disease pro-
individuals. In these subjects, however, several sites gression.
are often affected at the same time (29, 39, 63). Since the distribution and temporal occurrence of
Clearly, these individuals need to be identified early periodontal disease is not entirely random, a limited
on. Very tight recall systems require an expensive assessment of clinical parameters in certain areas,
work force and are a nuisance to the patients, not to and at specific time points, may be sufficient to obtain
mention the tissue damage caused by repeated diagnostically useful information in many situations.
instrumentation. This indicates a need for diagnostic Correlations between parameters (37, 58) should be
tools to select the optimal recall interval for each explored to reduce redundancy and improve the
patient individually and to decide which sites need utility of multiple or repeated measurements.
retreatment in excess of what regular prophylaxis
implies. Clinical indices assessed during the main-
tenance phase are poor prognosticators of attach- References
ment loss (44, 50, 94). In one study (49), 41 patients
were monitored after periodontal therapy for 1. Abbas F, Hart AAM, Oosting J, van der Velden U. Effect of
bleeding on probing for 2 1 ⁄ 2 years in a mainten- training and probing force on the reproducibility of pocket
depth measurements. J Periodontal Res 1982: 17: 226–234.
ance program. The sensitivity of frequent bleeding
2. Aguero A, Garnick JJ, Keagle J, Steflik DE, Thompson WO.
to predict clinical attachment loss > 1 mm was only Histological location of a standardized periodontal probe
29%, and the specificity 88%. On the other hand, in man. J Periodontol 1995: 66: 184–190.
continuous absence of bleeding on probing had a 3. Armitage GC. Development of a classification system for
predictive value of 98% for stability. Using the periodontal diseases and conditions. Ann Periodontol 1999:
4: 1–6.
methodology of the systematic review an attempt
4. Armitage GC, Svanberg GK, Löe H. Microscopic evaluation
was made to assess the predictive value of residual of clinical measurements of connective tissue attachment
probing depth, bleeding on probing, and furcation levels. J Clin Periodontol 1977: 4: 173–190.
involvement in determining further loss of attach- 5. Axelsson P, Lindhe J. Effect of controlled oral hygiene
ment following initial cause related therapy (82). procedures on caries and periodontal disease in adults.
Results after 6 years. J Clin Periodontol 1981: 8: 239–248.
After a detailed review of 47 publications, only one
6. Axelsson P, Lindhe J. The significance of maintenance care
study fulfilled all inclusion criteria. That study (21) in the treatment of periodontal disease. J Clin Periodontol
included 16 subjects reviewed over 42 months and 1981: 8: 281–294.
demonstrated that residual probing depth was pre- 7. Badersten A, Nilvéus R, Egelberg J. Reproducibility of pro-
dictive of further disease progression, whereas per- bing attachment level measurements. J Clin Periodontol
1984: 11: 475–485.
sisting bleeding on probing was not.
8. Badersten A, Nilvéus R, Egelberg J. Effect of nonsurgical
periodontal therapy. VI. Localization of sites with probing
attachment loss. J Clin Periodontol 1985: 12: 351–359.
Conclusions 9. Badersten A, Nilvéus R, Egelberg J. Effect of nonsurgical
periodontal therapy (VIII). Probing attachment changes
Reduction of pocket probing depth and clinical related to clinical characteristics. J Clin Periodontol 1987:
14: 425–432.
attachment level gain are the obvious clinical goals of
10. Beardmore HD. Tonus of marginal gingiva. J Periodontol
periodontal therapy. Gain of clinical attachment is 1963: 34: 31–40.
largely due to increased tissue firmness and epithelial 11. Beck JD, Sharp T, Koch GG, Offenbacher S. A 5-year study
attachment, and cannot be explained solely by the of attachment loss and tooth loss in community-dwelling
formation of new connective tissue attachment. If the older adults. J Periodontal Res 1997: 32: 516–523.
12. Bergenholtz A, al-Harbi N, al-Hummayani FM, Anton P,
aim of periodontal probing were to locate the apical
al-Kahtani S. The accuracy of the Vivacare true pressure-
termination of the junctional epithelium, one would sensitive periodontal probe system in terms of probing
actually have to apply higher forces for probing after force. J Clin Periodontol 2000: 27: 93–98.
therapy than at an initial examination.

36
Clinical parameters

13. Biddle AJ, Palmer RM, Wilson RF, Watts TL. Comparison of 33. Haffajee AD, Socransky SS, Goodson JM. Comparison of
the validity of periodontal probing measurements in smo- different data analyses for detecting changes in attachment
kers and non-smokers. J Clin Periodontol 2001: 28: 806–812. level. J Clin Periodontol 1983: 10: 298–310.
14. Birek P, McCulloch CAG, Hardy V. Gingival attachment 34. Hancock EB, Wirthlin MR. The location of the periodontal
level measurements with an automated periodontal probe. probe tip in health and disease. J Periodontol 1981: 52: 124–
J Clin Periodontol 1987: 14: 472–477. 129.
15. Borsboom P, ten Bosch JJ, Corba N, Tromp J. A simple 35. Harley A, Floyd P, Watts T. Monitoring untreated perio-
constant force probe. J Clin Periodontol 1981: 52: 390–391. dontal disease. J Clin Periodontol 1987: 14: 221–225.
16. Brayer WK, Mellonig JT, Dunlap RM, Marinak KW, Carson 36. Hassell TM, Germann MA, Saxer UP. Periodontal probing:
RE. Scaling and root planing effectiveness: the effect of root interinvestigator discrepancies and correlations between
surface access and operator experience. J Periodontol 1989: probing force and recorded depth. Helv Odontol Acta 1973:
60: 67–72. 17: 38–42.
17. Brochut P, Marin I, Baehni PC, Mombelli A. Predictive 37. Hausmann E, Allen K, Norderyd J, Ren W, Shibly O,
value of clinical and microbiological parameters for the Machtei E. Studies on the relatinship between changes in
treatment outcome of scaling and root planing. J Clin radiographic bone height and probing attachment. J Clin
Periodontol 2005: 32: 695–701. Periodontol 1994: 21: 128–132.
18. Buchanan SA, Robertson PB. Calculus removal by 38. Herrera D, Sanz M, Jepsen S, Needleman I, Roldán S. A
scaling ⁄ root planing with and without surgical access. systematic review on the effect of systemic antimicrobials
J Periodontol 1987: 58: 159–163. as an adjunct to scaling and root planing in periodontitis
19. Caffesse RG, Sweeney PL, Smith BA. Scaling and root pla- patients. J Clin Periodontol 2002: 29: 136–159.
ning with and without periodontal flap surgery. J Clin 39. Hirschfeld L, Wasserman B. A long-term survey of tooth
Periodontol 1986: 13: 205–210. loss in 600 treated periodontal patients. J Periodontol 1978:
20. Caton J, Greenstein G, Polson AM. Depth of periodontal 49: 225–237.
probe penetration related to clinical and histological signs of 40. Hujoel PP, Cunha-Cruz J, Selipsky H, Saver BG. Abnormal
gingival inflammation. J Periodontol 1981: 52: 626–629. pocket depth and gingival recession as distinct phenotypes.
21. Claffey N, Egelberg J. Clinical indicators of probing Periodontol 2000 2005: 39: 22–29.
attachment loss following initial periodontal treatment in 41. Isidor F, Karring T, Attström R. Reproducibility of pocket
advanced periodontitis patients. J Clin Periodontol 1995: depth and attachment level measurements when using a
22: 690–696. flexible splint. J Clin Peridontol 1984: 11: 662–668.
22. Claffey N, Loos B, Gantes B, Martin M, Egelberg J. Probing 42. Jansen J, Pilot T, Corba N. Histologic evaluation of probe
depth at re-evaluation following initial periodontal therapy penetration during clinical assessment of periodontal
to indicate the initial response to treatment. J Clin attachment levels. An investigation of experimentally
Periodontol 1989: 16: 229–233. induced periodontal lesions in beagle dogs. J Clin Perio-
23. Fowler C, Garrett S, Crigger M, Egelberg J. Histologic probe dontol 1981: 8: 98–106.
position in treated and untreated human periodontal tis- 43. Jeffcoat MK, Reddy MS. A comparison of probing and
sues. J Clin Periodontol 1982: 9: 373–385. radiographic methods for detection of periodontal disease
24. Freed HK, Gapper RL, Kalkwarf KL. Evaluation of perio- progression. Curr Opin Dent 1991: 1: 45–51.
dontal probing forces. J Periodontol 1983: 54: 488–492. 44. Kaldahl WB, Kalkwarf KL, Patil KD, Molvar MP. Relation-
25. Gabathuler H, Hassell T. A pressure-sensitive periodontal ship of gingival bleeding, gingival suppuration, and
probe. Helv Odontol Acta 1971: 15: 114–117. supragingival plaque to attachment loss. J Periodontol
26. Garnick JJ, Keagle JG, Searle JR, King GE, Thompson WO. 1990: 61: 347–351.
Gingival resistance to probing forces. II. The effect of 45. Kaldahl WB, Kalkwarf KL, Patil KD, Molvar MP, Dyer JK.
inflammation and pressure on probe displacement in Long-term evaluation of periodontal therapy. I. Response to
Beagle dog gingivitis. J Periodontol 1989: 60: 498–505. 4 therapeutic modalities. J Periodontol 1996: 67: 93–102.
27. Garnick JJ, Spray JR, Vernino DM, Klawitter JJ. Demon- 46. Karayiannis A, Lang NP, Joss A, Nyman S. Bleeding on
stration of probes in human periodontal pockets. probing as it relates to probing pressure and gingival health
J Periodontol 1980: 51: 563–570. in patients with a reduced but healthy periodontium. J Clin
28. Gibbs CH, Hirschfeld JW, Lee JG, Low SB, Magnusson I, Periodontol 1992: 19: 471–475.
Thousand RR, Yerneni P, Clark WB. Description and clinical 47. Keagle JG, Garnick JJ, Searle JR, King GE, Morse PK. Gingival
evaluation of a new computerized periodontal probe – the resistance to probing forces. I. Determination of optimal
Florida Probe. J Clin Periodontol 1988: 15: 137–144. probe diameter. J Periodontol 1989: 60: 167–171.
29. Goldman MJ, Ross IF, Goteiner D. Effect of periodontal 48. Knowles JW, Burgett FG, Nissle RR, Shick RA, Morrison EC,
therapy on patients maintained for 15 years or longer. A Ramfjord SP. Results of periodontal treatment related to
retrospective study. J Periodontol 1986: 57: 347–353. pocket depth and attachment level. Eight years. J Period-
30. Greenstein G, Caton J, Polson AM. Histologic characteris- ontol 1979: 50: 225–233.
tics associated with bleeding after probing and visual signs 49. Lang NP, Adler R, Joss A, Nyman S. Absence of bleeding on
of inflammation. J Periodontol 1981: 52: 420–425. probing. An indicator of periodontal stability. J Clin
31. Gunsolley JC, Best AM. Change in attachment level. Periodontol 1990: 17: 714–721.
J Periodontol 1988: 59: 450–456. 50. Lang NP, Joss A, Orsanic T, Gusberti FA, Siegrist BE.
32. Haffajee AD, Socransky SS, Goodson JM. Clinical parame- Bleeding on probing. A predictor for the progression
ters as predictors of destructive periodontal disease activ- of periodontal disease? J Clin Periodontol 1986: 13:
ity. J Clin Periodontol 1983: 10: 257–265. 590–596.

37
Mombelli

51. Lang NP, Nyman S, Senn C, Joss A. Bleeding on probing as 69. Mombelli A, Mühle T, Brägger U, Lang NP, Bürgin WB.
it relates to probing pressure and gingival health. J Clin Comparison of periodontal and peri-implant probing by
Periodontol 1991: 18: 257–261. depth-force pattern analysis. Clin Oral Implants Res 1997:
52. Lindhe J. Treatment of localized juvenile periodontitis. In: 8: 448–454.
Genco RJ, Mergenhagen SE, editors. Host–parasite Inter- 70. Mombelli A, Mühle T, Frigg R. Depth-force patterns of
actions in Periodontal Diseases. Washington, D.C.: Ameri- periodontal probing. Attachment gain in relation to pro-
can Society for Microbiology, 1982: 382–394. bing force. J Clin Periodontol 1992: 19: 295–300.
53. Lindhe J, Nyman S. The effect of plaque control and sur- 71. Nyman S, Lindhe J, Rosling B. Periodontal surgery in plaque-
gical pocket elimination on the establishment and main- infected dentitions. J Clin Periodontol 1977: 4: 240–249.
tenance of periodontal health. A longitudinal study of 72. Nyman S, Rosling B, Lindhe J. Effect of professional tooth
periodontal therapy in cases of advanced disease. J Clin cleaning on healing after periodontal surgery. J Clin
Periodontol 1975: 2: 67–79. Periodontol 1975: 2: 80–86.
54. Lindhe J, Socransky SS, Nyman S, Haffajee A, Westfelt E. 73. Osborn J, Stoltenberg J, Huso B, Aeppli D, Pihlstrom B.
ÔCritical probing depthsÕ in periodontal therapy. J Clin Comparison of measurement variability using a standard
Periodontol 1982: 9: 323–336. and constant force periodontal probe. J Periodontol 1990:
55. Lindhe J, Westfelt E, Nyman S, Socransky SS, Haffajee AD. 61: 497–503.
Long-term effect of surgical ⁄ non-surgical treatment of 74. Osborn JB, Stoltenberg JL, Huso BA, Aeppli DM, Pihlstrom
periodontal disease. J Clin Periodontol 1984: 11: 448–458. BL. Comparison of measurement variability in subjects
56. Listgarten MA, Mao R, Robinson PJ. Periodontal probing with moderate periodontitis using a conventional and
and the relationship of the probe tip to periodontal tissues. constant force periodontal probe. J Periodontol 1992: 63:
J Periodontol 1976: 47: 511–513. 283–289.
57. Listgarten MA, Slots J, Rosenberg J, Nitkin L, Sullivan P, 75. Pihlstrom BL, McHugh RB, Oliphant TH, Ortiz-Campos C.
Oler J. Clinical and microbiological characteristics of trea- Comparison of surgical and nonsurgical treatment of per-
ted periodontitis patients on maintenance care. J Period- iodontal disease. A review of current studies and additional
ontol 1989: 8: 452–459. results after 6.5 years. J Clin Periodontol 1983: 10: 524–541.
58. Lobene RR, Mankodi SM, Ciancio SG, Lamm RA, Charles CH, 76. Pihlstrom BL, Oliphant TH, McHugh RB. Molar and non-
Ross NM. Correlations among gingival indices: a metho- molar teeth compared over 6 1 ⁄ 2 years following two
dology study. J Periodontol 1989: 60: 159–162. methods of periodontal therapy. J Periodontol 1984: 55:
59. Löe H, Anerud A, Boysen H, Morrison E. Natural history of 499–504.
periodontitis in man. Rapid, moderate and no loss of 77. Polson AM, Caton JG, Yeaple RN, Zander HA. Histological
attachment in Sri Lankan laborers 14–46 years of age. J Clin determination of probe tip penetration into gingival sulcus
Periodontol 1986: 13: 431–445. of humans using an electronic pressure-sensitive probe.
60. Magnusson I, Clark WB, Marks RG, Gibbs CH, J Clin Periodontol 1980: 7: 479–488.
Manouchehr-Pour M, Low SB. Attachment level measure- 78. Proye M, Caton J, Polson A. Initial healing of periodontal
ments with a constant force electronic probe. J Clin pockets after a single episode of root planing monitored by
Periodontol 1988: 15: 185–188. controlled probing forces. J Periodontol 1982: 53: 296–301.
61. Magnusson I, Listgarten MA. Histological evaluation of 79. Rabbani GM, Ash MM Jr, Caffesse RG. The effectiveness of
probing depth following periodontal treatment. J Clin subgingival scaling and root planing in calculus removal.
Periodontol 1980: 7: 26–31. J Periodontol 1981: 52: 119–123.
62. Mayfield L, Bratthall G, Attstrom R. Periodontal probe 80. Ralls SA, Cohen ME. Problems in identifying ÔburstsÕ of per-
precision using 4 different periodontal probes. J Clin iodontal attachment loss. J Periodontol 1986: 57: 746–752.
Periodontol 1996: 23: 76–82. 81. Rees TD. Periodontal risk factors and indicators. Period-
63. McFall WT. Tooth loss in 100 treated patients with perio- ontol 2000 2003: 32: 9–135.
dontal disease in a long-term study. J Periodontol 1982: 53: 82. Renvert S, Persson GR. A systematic review on the use of
539–549. residual probing depth, bleeding on probing and furcation
64. Mombelli A, Brochut P, Plagnat D, Casagni F, Giannop- status following initial periodontal therapy to predict fur-
oulou C. Enamel matrix proteins and systemic antibiotics ther attachment and tooth loss. J Clin Periodontol 2002: 29
as adjuncts to non-surgical periodontal treatment: clinical (Suppl. 3): 82–89; 90–91.
effects. J Clin Periodontol 2005: 32: 225–230. 83. Robinson PJ, Vitek RM. The relationship between gingival
65. Mombelli A, Graf H. Depth-force patterns in periodontal inflammation and resistance to probe penetration. J Peri-
probing. J Clin Periodontol 1986: 13: 126–130. odontal Res 1979: 14: 239–243.
66. Mombelli A, Meier C. On the symmetry of periodontal 84. Rosling B, Nyman S, Lindhe J. The effect of systematic
disease. J Clin Periodontol 2001: 28: 741–745. plaque control on bone regeneration in infrabony pockets.
67. Mombelli A, Minder CE, Gusberti FA, Lang NP. Repro- J Clin Periodontol 1976: 3: 38–53.
ducibility of microscopic and cultural data in repeated 85. Rosling B, Nyman S, Lindhe J, Jern B. The healing potential
subgingival plaque samples. J Clin Periodontol 1989: 16: of the periodontal tissues following different techniques of
434–442. periodontal surgery in plaque-free dentitions. A 2-year
68. Mombelli A, Mühle T, Brägger U. Probing force depend- clinical study. J Clin Periodontol 1976: 3: 233–250.
ence of attachment level measurement in the assessment 86. Saglie R, Johansen JR, Fløtra L. The zone of completely and
of effects of surgical periodontal treatment with or without partially destructed periodontal fibres in pathological
NSAID. Acta Med Dent Helv 1996: 1: 34–39. pockets. J Clin Periodontol 1975: 2: 198–202.

38
Clinical parameters

87. Schroeder HE, Listgarten MA. Monographs in Develop- 94. Vanooteghem R, Hutchens LH, Garrett S, Kiger R, Egelberg
mental Biology. Fine Structure of the Developing Epithelial J. Bleeding on probing and probing depth as indicators of
Attachment of Human Teeth. Basel: S. Karger, 1971. the response to plaque control and root debridement.
88. Spray JR, Garnick JJ, Doles LR, Klawitter JJ. Microscopic J Clin Periodontol 1987: 14: 226–230.
demonstration of the position of periodontal probes. 95. Vartoukian SR, Palmer RM, Wilson RF. Evaluation of a new
J Periodontol 1978: 49: 148–152. periodontal probe tip design. J Clin Periodontol 2004: 31:
89. Stern IB. Current concepts of the dentogingival junction: 918–925.
the epithelial and connective tissue attachments to the 96. Vitek RM, Robinson PJ, Lautenschlager EP. Development of
tooth. J Periodontol 1981: 52: 465–476. a force controlled periodontal probing instrument. J Peri-
90. van der Velden U. Influence of probing force on the odontal Res 1979: 14: 93–94.
reproducibility of bleeding tendency measurements. J Clin 97. Wang S-F, Leknes KN, Zimmerman GJ, Sigurdsson TJ,
Periodontol 1980: 7: 421–427. Wikesjö UME, Selvig KA. Reproducibility of periodontal
91. van der Velden U. Location of probe tip in bleeding and probing using a conventional manual and an automated
non-bleeding pockets with minimal gingival inflammation. force-controlled electronic probe. J Periodontol 1995: 66:
J Clin Periodontol 1982: 9: 421–427. 38–46.
92. van der Velden U. Purpose and problems of perio- 98. Watts T. Constant force probing with and without a stent in
dontal disease classification. Periodontol 2000 2005: 39: 13– untreated periodontal disease: the clinical reproducibility
21. problem and possible sources of error. J Clin Periodontol
93. van der Velden U, de Vries JH. Introduction of a new per- 1987: 14: 407–411.
iodontal probe: the pressure probe. J Clin Periodontol 1978: 99. Watts TLP. Probing site configuration in patients with
5: 188–197. untreated periodontitis. J Clin Periodontol 1989: 16: 529–533.

39

You might also like