Disease Activity

46 CHAPTER 4. DISEASE ACTIVITY Section 1. Bleeding Upon Probing

CHAPTER 4.DISEASE ACTIVITY

Section 1. Bleeding Upon ProbingAssessment of bleeding upon probing (BOP) is an im-

portant part of the periodontal examination. Bleeding hasbeen demonstrated in clinical and histological studies to bea more sensitive sign of gingival inflammation than visualalterations. Meitner et al. (1979) examined 6,990 gingivalsurfaces visually, then probed for bleeding 1, 2, and 3months following prophylaxis. At the first exam, 1,678 sites(24%) demonstrated a combined absence of visual inflam-mation and BOP. One month later, only 766 of these sur-faces were still healthy. Data from surfaces that hadchanged since the first examination showed that there werea significantly greater number of surfaces which bled uponprobing compared to either a color change only or a com-bination of color change and BOP. The authors concludedthat gingival indices based upon BOP are more accuratethan those using visual changes.

BLEEDING INDICESInterdental bleeding following stimulation with wooden

interdental cleaners forms the basis of the Eastman Inter-dental Bleeding Index (EIBI), while bleeding followingsweeping a probe in the sulcus from the line angle to theinterproximal contact forms the basis of the Papilla Bleed-ing Index (FBI). Caton et al. (1988) compared visual eval-uation, FBI, and EIBI in 82 subjects not currentlyundergoing periodontal therapy. Visual signs of inflamma-tion were seen at 71% of the sites, EIBI was positive at65%, and FBI was positive at 42% of the sites. At sitesrated visually as non-inflamed, almost twice as many in-flammatory lesions were detected by EIBI versus FBI. Theauthors concluded that the Eastman Interdental BleedingIndex was a more reliable clinical indicator for detectinginterdental inflammation than the Papilla Bleeding Index.

HISTOLOGY OF BLEEDING SITESHistological studies have verified the presence of signif-

icantly more inflammation in the bleeding sites comparedto non-bleeding sites. Greenstein et al. (1981) evaluated 60gingival biopsies for visual presence or absence of bleedingafter probing using a pressure-controlled probe set at 25g.Sites which bled on probing exhibited a significantlygreater percentage (28.7% versus 19.9%) of cell rich-col-lagen poor connective tissue than non-bleeding sites with-out an increase in blood vessel lumens. Other studies havecharacterized the histopathological features of active peri-odontal lesions using bleeding as one of the criteria of dis-

ease activity. Davenport et al. (1982) found that thepercentage of infiltrated connective tissue was consistentlylarger in bleeding lesions with suppuration than in non-bleeding lesions with suppuration. Significant differenceswere observed between bleeding and non-bleeding sites interms of the mean percent volume occupied by plasma cells(68% versus 24%) and mononuclear cells (5.5% versus22%). The pocket epithelium of bleeding lesions demon-strated thinned and ulcerated areas along with proliferationof rete pegs.

Passo et al. (1988) examined the histological features ofbleeding sites with and without suppuration. They reportedthat the percentage of collagen-poor area in bleeding (butnot suppurating) sites was similar (27.7%) to the abovefinding of Greenstein et al. (1981), but was higher in thesuppurating area. However, suppuration was not always as-sociated with extensive inflammation, and intense inflam-mation was also seen in non-suppurating sites. Thus,suppuration did not appear to be a specific indicator of adestructive periodontal lesion. Reinhardt et al. (1988) ex-amined the lymphocyte subpopulation in periodontal activelesions characterized by bleeding and progressive attach-ment loss.

Polymorphonuclear leukocytes (PMNs) were seen onlyin 3.7% of the sulcular third of stable sites and in 5.6% to8.3% of the sulcular third of active sites. Lymphocyte den-sity was greater in the sulcular thirds than in the oral thirds.When compared to stable sites, active sites showed an in-creased number of plasma cells and a reduced T/B ratio.The T helper/T suppressor ratio did not vary significantlybetween blood and gingival tissue of any disease group butseemed to follow a trend toward lower numbers of T helpercells. These results indicated that active periodontal lesionscharacterized by bleeding and attachment loss displayed el-evated B cell population and abnormal immune regulationpossibly involving the T helper cell subset.

Badersten et al. (1990) studied the longitudinal effectsof non-surgical therapy on nonmolar teeth. The diagnosticvalue of clinical scores of plaque, bleeding, suppuration,and probing depth in predicting probing attachment lossduring the maintenance phase was investigated. A combi-nation of linear regression and end-point analysis was usedto determine probing attachment loss over the 0 to 60month period. The authors found that all of the investigatedscores were associated with clinical attachment loss andthat improved diagnostic predictability was noted with anincreased length of time in recording scores. The positivepredictive value (Pv+) of accumulated plaque or accumu-

Section 1. Bleeding Upon Probing CHAPTER 4. DISEASE ACTIVITY 47

lated bleeding scores reached a maximum of about 30%,corroborating the findings of Lang et al. (1986). A residualprobing depth of > 7 mm had about a 50% Pv+ while in-creased probing depths > 1.0 mm reached 80% Pv+ after60 months. This led to the conclusion that an increase inprobing depth, as opposed to the presence of bleeding onprobing, was most valuable in predicting probing attach-ment loss (our "gold standard" of disease activity?). Theuse of lower probing pressure (< 0.75 Newton [N]) usedin this study) and selection of only those sites with markedbleeding might have improved the predictive value ofbleeding upon probing. Suppuration only reached a maxi-mum of 20% positive predictive value, probably because itwas a rare occurrence.

Claffey et al. (1990) did a parallel study which includedmolars. For 42 months following periodontal therapy,plaque, bleeding, suppuration, and probing depth were re-corded for 17 subjects. A probing force of 0.50 N was usedand 4 of the subjects received no subgingival instrumen-tation during the 42 months of maintenance. Similar resultsto Badersten et al. (1990) were obtained: 1) accumulatedplaque scores had low Pv+; 2) 41% of sites that bled onprobing at 75% or more of the examinations between 3 to42 months had undergone probing attachment loss; 3) sup-puration on probing reached a Pv+ of 40 to 50% but wasnot a frequent finding; and 4) increase in probing depth ofgreater than 1 mm reached a Pv+ of 68% at 42 months.The combination of increasing probing depth with bleedingfrequency at 75% or more of examinations yielded a pre-dictability score of 87% at 42 months. The best positivepredictive value was found using a combination of bleedingupon probing and an increased probing depth of 1 mm ormore. A comparison of this group with that of Baderstenet al. (1990) revealed higher plaque and bleeding scores inthis group of patients. Furcations showed the highest inci-dence of probing attachment loss. The authors conclude thatlonger observation periods are needed if the commonlyused clinical signs such as BOP and suppuration are toreach meaningful diagnostic values.

In another longitudinal study of maintenance patients,Kaldahl et al. (1990) investigated the relationship of bleed-ing, suppuration, and presence of supragingival plaque toattachment loss during the second and third years followingactive therapy which included either coronal scaling, rootplaning, modified Widman surgery, or flap with osseousresection. A probing force of 25 grams was used to detectbleeding on probing, while an increased pressure of 50grams was used to record the probing attachment level.They found that as the frequency of bleeding on probingincreased, the sensitivity decreased (0.82 to 0.15), the spec-ificity increased (0.20 to 0.88), and positive and negativepredictive values remained constant (Pv+ = .15-. 18; Pv�= .86). For suppuration, sensitivity was extremely low butspecificity was nearly 1.0 while positve predictive valueincreased (from 0.27 to 0.50) because of the low frequency

of suppuration in the population. For supragingival plaque,as the frequency of presence of plaque increased, the sen-sitivity decreased (0.67 to 0.15), the specificity increased(0.40 to 0.87), and the positive and negative predictive val-ues remained constant (Pv+ = .16-17; Pv- = .87-.S6).The authors conclude that bleeding and plaque are not goodprognosticates while suppuration is a weak prognosticatorover the 2-year maintenance period. The bleeding symptomassociated with a non-aggressive state (gingivitis) is prob-ably much more frequent and therefore may mask bleedingassociated with an aggressive inflammatory state (periodon-titis).

Greenstein and Caton (1990) published a critical assess-ment of periodontal disease activity concepts. Several im-portant issues were addressed, including the fact that at anygiven moment, there is no practical clinical test to deter-mine if disease activity is occurring. Longitudinal monitor-ing is required. If a 3 mm increase in probing attachmentloss is used, as selected by Haffajee et al. (1983), as equiv-alent to 3 times the standard deviation association with dif-ference between replicate probing measurements, androunded upward, clinically significant loss may occur be-fore initiating therapy. In this instance, the sensitivity of thetest will be low and the specificity high, resulting in a highnumber of false-negatives and possible undertreatment.Conversely, if a 1 mm increase in probing depth is used asthe standard for disease activity, variability in probing ac-curacy may produce significant numbers of false-positiveresults, with subsequent overtreatment.

REFERENCESBadersten A, Nilveus R, Egelberg J. Scores of plaque, bleeding, suppu-

ration and probing depth to predict probing attachment loss. 5 yearsof observation following nonsurgical periodontal therapy. J Clin Per-iodontol 1990;17:102-107.

Caton J, Poison A, Bouwsma O, Blieden T, Frantz B, Espeland M. As-sociations between bleeding and visual signs of interdental gingivalinflammation. J Periodontol 1988;59:722-727.

Claffey N, Nylund K, Kiger R, Garrett S, Egelberg J. Diagnostic predict-ability of scores of plaque, bleeding, suppuration and probing depthfor probing attachment loss. 3 1/2 years of observation following in-itial periodontal therapy. J Clin Periodontol 1990;17:108-114.

Davenport RH, Simpson DM, Hassell TN. Histometric comparison of ac-tive and inactive lesions of advanced periodontitis. J Periodontol 1982;53:285-295.

Greenstein G, Caton J, Poison AM. Histologic characteristics associatedwith bleeding after probing and visual signs of inflammation. J Per-iodontol 1981;52:420-425.

Greenstein G, Caton J. Periodontal disease activity: A critical assessment.J Periodontol 1990;61:543-552.

Haffajee AD, Socransky SS, Goodson JM. Clinical parameters as predic-tors of destructive periodontal disease activity. J Clin Periodontol1983;10:257.

Kaldahl WB, Kalkwarf KL, Patil KD, Molvar MP. Relationship of gin-gival bleeding, gingival suppuration, and supragingival plaque to at-tachment loss. J Periodontol 1990;61:347-351.

Lang NP, Joss A, Orsanic T, Gusberti FA, Siegrist HE. Bleeding on prob-ing. A predictor for the progression of periodontal disease. J ClinPeriodontol 1986;13:590-596.

48 CHAPTER 4. DISEASE ACTIVITY Section 2. Gingival Crevicular Fluid

Meitner SW, Zander II, Iker, Poison A. Identification of inflamed gingivalsurfaces. J Clin Periodontol 1979;6:93-97.

Passo SA, Reinhart RA, DuBois LM, Cohen DM. Histological character-istics associated with suppurating periodontal pockets. J Periodontol1988;59:731-740.

Reinhardt RA, Bolton RW, McDonald TL, DuBois LM, Kaldahl WB. Insitu lymphocyte subpopulations from active versus stable periodontalsites. J Periodontol 1988;59:656-670.

Section 2. Gingival Crevicular Fluid

DEFINITIONGingival Crevicular Fluid (GCF): Tissue fluid that

seeps through the crevicular epithelium. It is increased inthe presence of inflammation.

It has been reported that the flow of GCF can be detecteda few days before other clinical signs of inflammation areevident. Crevicular fluid appears during altered states ofvascular permeability which may accompany gingival in-flammation (Abbott and Caffesse, 1977). On this basis, itsmeasurement has been proposed as an indicator of perio-dontal disease activity.

METHODS OF COLLECTION ANDMEASUREMENT

GCF may be collected by two basic techniques: filterpaper strips and capillary micropipettes. Measurements areaccomplished by ninhydrin stain assessment or by use ofthe Periotron (measures filter strip wetness impedance).GCF collection methods using filter paper strips may bedivided into the intracrevicular and extracrevicular tech-niques:

IntracrevicularThe Brill (1962) technique includes placement of a filter

strip into the gingival sulcus until resistance is felt. After 3minutes in place, the strips are removed, dried, and stainedwith ninhydrin (stains proteins). Loe and Holm-Pedersen(1965) proposed a method involving minimal irritation tothe gingival sulcus, in which the paper strip is placed at theentrance of the crevice.

ExtracrevicularBrill and Krasse (1959) and Loe and Holm-Pedersen

(1965) also employed an extracrevicular collection tech-nique. The strips were closely adapted to the buccal sur-faces of the teeth, across the gingival margin and onto theattached gingiva.

GCF collected with capillary pipettes permits the meas-urement of fluid volume; however, to assure accurate meas-urement, relatively large volumes have to be collected. Thishas the disadvantage of requiring a considerable amount oftime in order to obtain a sample, rendering the techniqueimpractical for clinical use. A more precise method is theuse of micropipettes which determines the actual volumeof GCF (Kaslick, 1970).

The Periotron employs an electronic transducer to meas-ure GCF. This instrument measures electrical capacitance,as the insulating properties of the filter paper strip varyaccording to the quantity of fluid absorbed within the strip(Suppipat, 1977). The instrument evaluates the flow of cur-rent based on the wetness of the strip (impedance). A digitalreadout registers the area wetted and is indicative of thevolume of fluid collected on the paper strip.

QUANTITATIVE ASSESSMENTHancock et al. (1979) studied crevicular fluid and gin-

gival inflammation, reporting weak correlations betweenGCF and clinical or histologic parameters. They concludedthat the quantity of fluid may have potential as a clinicalindicator of presence but not severity of gingival inflam-mation. Shapiro et al. (1979) found no statistically signifi-cant correlation between the amount of GCF and thehistological degree of inflammation. However, there was apositive correlation between the GCF and the clinical as-sessment of inflammation. Cimasoni (1983), in reviewingthis subject, noted that a "positive correlation was alwaysfound between the clinical appreciation of gingival inflam-mation and the amount of gingival fluid." He also reportedthat the correlation between gingival crevicular fluid flowand histological inflammatory changes was poor.

It is generally agreed that gingival crevicular fluid re-flects vascular permeability and thus gingival inflammation.It may indicate the presence of gingival inflammation butthere is no evidence showing that it can predict periodontalbreakdown or disclose the degree of inflammation. Factorssuch as circadian periodicity, hormonal alteration, and dif-ferences in collection technique may provide sources of er-ror, making interpretation of findings difficult.

QUALITATIVE ASSESSMENTHydrogen sulfide is a cytotoxic metabolite of bacterial

origin. Solis-Gaffer et al. (1980) proposed that the level ofGCF hydrogen sulfide could be an indication of periodontaldisease and used a quantitative method to determine theproduction of hydrogen sulfide from 240 GCF samples col-lected with paper strips. A strong positive correlation be-tween hydrogen sulfide production and the degree ofgingival inflammation was shown. Horowitz and Folke(1973) analyzed hydrogen sulfide production in patientswith gingival health (probing depth 2 mm or less), perio-dontitis (PD > 4 mm), and surgical treatment (pocket elim-ination). Results indicated that hydrogen sulfide generationincreased with sulcular depth and that toothbrushing failedto reduce hydrogen sulfide production in periodontal pock-ets. These findings appear to favor pocket reduction sur-gical procedures.

PMN RESPONSE TO CHEMOTACTICCHALLENGE

Neutrophils (PMNs) are the predominant cell type in thegingival sulcus during the initiation and progression of per-

Section 3. Bacterial Flora CHAPTER 4. DISEASE ACTIVITY 49

iodontal disease (Attstrom, 1971; Page and Schroeder,1976). These cells are responsive to a number of chemo-tactic factors produced by the gingival microflora and byactivated products of the complement system. Most studieshave indicated that neutrophils play a protective role in per-iodontal tissues (Van Dyke et al., 1980). PMN dysfunction(especially defective chemotaxis) has been observed inmany cases of severe periodontal disease. It has been shownthat PMNs migrate through the gingival connective tissueand junctional epithelium into the gingival sulcus (VanDyke et al., 1980). Monitoring crevicular PMNs has beenadvocated as a means of assessing periodontal disease ac-tivity.

Golub et al. (1981) described a technique (the sulculartechnique) for assessing neutrophil chemotaxis in vivo.Singh et al. (1984) utilized this method to monitor patientswith gingivitis, chronic periodontitis, and LJP. In gingivitisand chronic periodontitis, the response to the chemotacticagent (casein) was similar to normal subjects except thatthe peak cell count was greater. LJP patients showed anabnormal response with two leukocyte peaks comparedwith a single peak in controls. This in vivo assay of neu-trophil response could be useful in determining suscepti-bility to periodontal breakdown and individual treatmentregimens.

Lamster et al. (1985) studied enzymatic profiles in gin-gival fluid. Arylsulfatase and B-glucuronidase were se-lected as indicators of the breakdown of connective tissueground substance. Evidence suggests that ground substanceintegrity is important for maintenance of the collagen com-ponent of the connective tissue. The authors found that theground substance degrading enzyme activity in crevicularfluid plateaued 2 to 3 weeks after the initiation of experi-mental gingivitis. The authors observed that this peak inenzyme activity corresponded with the established lesion ofgingivitis. Similarly, Oshrain et al. (1984) found greaterarylsulfatase volume activity in patients with gingivitis andperiodontitis than in normal subjects.

Elevation of serum levels of aspartate aminotransferaseis frequently used as a diagnostic indicator of myocardialinfarction and as a quantitative measure of the extent oftissue destruction. Chambers et al. (1984) hypothesized thatcell death during active periodontitis would release aspar-tate aminotransferase into the crevicular fluid. They studiedthe levels of this enzyme in GCF in a ligature-induced per-iodontitis model in the beagle dog. Results showed signif-icant increases in aspartate aminotransferase levels 2 weeksafter ligation. The authors suggested that this peak repre-sented the acute destructive episodes of active periodontaldisease.

Lamster et al. (1988) performed a longitudinal evalua-tion of GCF levels of B-glucuronidase, arylsulfatase, andlactate dehydrogenase in patients with chronic adult perio-dontitis. They determined that increased GCF levels of B-glucuronidase (a marker for primary granule release from

PMNs) was a very strong predictor of impending clinicalattachment loss. In contrast, neither arylsulfatase nor lactatedehydrogenase was able to predict attachment loss.

REFERENCESAbbott B, Caffesse R. Crevicular fluid: Origin, composition, methods of

collection, and clinical significance. J West Soo Periodontol PeriodontAbstr 1977;25:164-178.

Attstrom R. Studies on neutrophil polymorphonuclear leukocytes at thedento-gingival junction in gingival health and disease. J PeriodontolRes 1971;8(Suppl.):l-15.

Brill N, Krasse B. Effect of mechanical stimulation on flow of tissue fluidthrough gingival pocket epithelium. Acta Odontol Scand 1959; 17:115-130.

Brill N. The gingival pocket fluid. Studies of its occurrence, composition,and effect. Acta Odontol Scand 1962;113(Suppl. 20):1-10.

Chambers DA, Crawford JM, Mukherjee S, Cohen RL. Aspartate ami-notransferase increases in crevicular fluid during experimental perio-dontitis in beagle dogs. J Periodontol 1984;55:526-530.

Cimansoni G. Crevicular Fluid Update, 2nd ed. Basel: Karger; 1983.Golub LM, lacono VJ, Nicoll G, Ramamurthy N, Kaslick RS. The re-

sponse of human sulcular leukocytes to a chemotactic challenge. Anew in vivo assay. J Periodont Res 1981;16:171-179.

Hancock EB, Cray RJ, O’Leary TJ. The relationship between gingivalcrevicular fluid and gingival inflammation. A clinical and histologicstudy. J Periodontol 1979;50:13-19.

Horowitz A, Folke L. Hydrogen sulfide production in the periodontal en-vironment. J Periodontol 1973;44:390-395.

Kaslick AS, Chasens Al, Bressman E, et al. Investigation of periodontosiswith periodontitis: Ultra microanalysis of gingival fluid, gross exam-ination of periodontal ligament and approach to treatment. J Perio-dontol 1971;42:428-34.

Lamster IB, Hartley LJ, Vogel RI. Development of a biochemical profilefor gingival crevicular fluid. J Periodontol 1985;56(Suppl.)13-21.

Lamster IB, Oshrain RL, Harper DS, Celenti RS, Hovliaris CA, GordonJM. Enzyme activity in crevicular fluid for detection and predictionof clinical attachment loss in patients with chronic adult periodontitis.J Periodontol 1988;59:516-523.

Loe H, Holm-Pedersen. Absence and presence of fluid from normal andinflamed gingivae. Periodontics 1965;3:171�177 .

Oshrain RL, Lamster IB, Hartley LJ, Gordon JM. Arylsulfatase activityin human gingival crevicular fluid. Arch Oral Biol 29:399, 1984;29:399-402.

Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal dis-ease. A summary of current work. Lab Invest 1976;34:235�249 .

Shapiro L, Goldman H, Bloom A. Sulcular exudate flow in gingival in-flammation. J Periodontol 1979;50:301-309.

Singh S, Golub LM, lacono VJ, Ramamurthy NS, Kaslick R. In vivocrevicular leukocyte response in humans to a chemotactic challenge.Effects of periodontal diseases. J Periodontol 1984;55:l-8.

Solis-Gaffar MC, Rustogi KN, Gaffer A. Hydrogen sulfide productionfrom gingival crevicular fluid. J Periodontol 1980;51:603-606.

Suppipat W, Suppipat N. Evaluation of an electronic device for gingivalfluid quantitation. J Periodontol 1977;48:388-394.

Van Dyke TE, Horoszewicz HW, Cianciola LJ, Genco RJ. Neutrophilchemotaxis dysfunction in human periodontitis. Infect Immun 1980;27:124-132.

Section 3. Bacterial FloraIn recent years, traditional clinical assessments of dis-

ease progression have been questioned. Haffajee et al.(1983) demonstrated that common clinical assessments ofinflammation (gingival erythema, bleeding on probing, and

50 CHAPTER 4. DISEASE ACTIVITY Section 3. Bacterial Flora

suppuration) were poor predictors of progression in an un-treated population. Similar results were reported by Bad-ersten et al. (1985) and by Lang et al. (1986) who showedthat repeated measurements (4/4) of bleeding on probing atmaintenance visits was followed by a loss of attachment atonly 30% of possible sites. These and other studies suggestthat since it is impossible to clinically detect sites whichare actually undergoing attachment loss, treatment of allinflamed sites is necessary.

Although bacterial plaque has long been accepted as theprimary etiology of periodontal disease, there is some de-bate over the exact etiologic mechanism of disease activity.The "non-specific plaque" hypothesis proposes that the eti-ologic mechanism in periodontitis is related to total plaquemass, therefore, reducing the amount of plaque will curtaildisease activity. According to the "specific plaque hypoth-esis," periodontal disease activity is related to specific bac-terial species and their products. The latter theory suggeststhat identification and eradication of putative periodonto-pathogens should be the goal of treatment. Microbial mon-itoring is based on the specific plaque hypothesis. In reality,mechanisms mediating periodontal diseases probably relateto both hypotheses or theories. The non-specific theory maybe more relevant to chronic adult periodontitis, whereas thespecific plaque theory may be more applicable to distinctiveperiodontal disorders; e.g., localized juvenile periodontitis(Listgarten, 1988).

Since clinical tests are currently unable to provide ade-quate disease assessment and predictability and since spe-cific microbiologic species seem to be related to diseaseactivity, microbiologic tests were sought as viable alterna-tives or adjuncts to clinical parameters.

COMPOSITION OF SUBGINGIVAL FLORA TODISEASE ACTIVITY

Analysis of Bacterial Morphotypes (DarkfieldMicroscopy [DFM])

With DFM, light enters the microscopic field peripher-ally so that microorganisms are obliquely illuminated andglow against a dark background.

Listgarten and Hellden (1978) described a technique forclassifying bacterial samples on the basis of constituentshape, size, and motility. Two diseased and two healthysites from 12 patients with severe periodontitis were stud-ied. Clinical parameters (gingival fluid flow, gingival index[GI], periodontal index [PI], and probing depth) were re-corded and plaque samples obtained from apical sites ofeach crevice. Samples were diluted and observed with dark-field microscopy; bacteria were categorized into 9 morpho-types. Results indicated significant differences betweenflora at healthy and diseased sites. At healthy sites, coccoidcells predominated (74.4% versus 22.3%), while diseasedsites presented a greater number of motile rods, curvedrods, and spirochetes. The ratio of motile to non-motilecells at healthy sites was 1:49, while at diseased sites the

ratio increased to 1:1. The authors suggest that this tech-nique may be used to predict sites with active disease basedon percentages of certain bacterial morphotypes.

Listgarten and Levin (1981) studied the correlation be-tween proportions of subgingival spirochetes and motilebacteria and susceptibility of subjects to periodontal dete-rioration. At baseline and every 2 months for 1 year, clin-ical and microbiological parameters were recorded for 20patients treated for moderate-advanced periodontitis. Mi-crobial samples from the deepest pocket in each quadrantwere pooled for analysis using DFM. Microbial forms wererecorded as coccoid, motile rods, spirochetes, or others.When probing depth at any surface exceeded baseline by >3 mm, the tooth was exited from the study. A significantpositive correlation was found between proportions of mo-tile rods and PI and GI scores. Also, a positive correlationbetween PD and proportions of spirochetes was observed.Spirochetes and/or motile rods predominated in subjectswho had 2 or more teeth exited from the study, whereascoccoid forms predominated in sites without exited teeth.The authors concluded that the proportion of spirochetes isa good predictor of periodontal deterioration within the up-coming year.

Armitage et al. (1982) correlated the percentage of mo-tile bacteria with clinical assessments of inflammatory per-iodontal disease. Two sites were selected from each of 60subjects and categorized into 6 disease categories, rangingfrom health to advanced periodontitis. These findings werecompared to DFM analysis of subgingival plaque from eachsite. Bacterial morphotypes were classified as non-motiles,spirochetes, or other motiles. The authors reported that se-verity of disease correlated significantly with an increase inthe percentage of spirochetes, although no such relationshipwas observed for other motile bacteria. There was also asignificant correlation between each clinical parameter (PI,GI, BOP, PD, gingival exudate, attachment loss) and thepercentage of spirochetes at individual sites. Bleeding onprobing and/or probing depth or loss of attachment > 3mm were the parameters most closely related to the per-centage of spirochetes. In fact, there was an 80% correla-tion between BOP and high levels (2 to 3 fold increase) ofspirochetes. Due to the high correlation of clinical para-meters with DFM findings, the need for microbiologic as-sessment of subgingival flora was questioned.

Rosenberg et al. (1981) examined composite bacterialpopulations before, during, and after various stages of per-iodontal therapy. Eighteen (18) patients with moderate per-iodontitis were scored for PI, GI, and PD. The tooth surfacewith the deepest pocket in each sextant (per patient) waschosen as the microbial sampling site. Subgingival plaquesamples were obtained at baseline, after initial preparation,and at various times after surgical therapy. A pooled samplefrom each patient was studied by DFM for each time pe-riod. There was a significant increase in the mean percent-age of coccoid cells and significant decrease in the

Section 3. Bacterial Flora CHAPTER 4. DISEASE ACTIVITY 51

proportions of spirochetes and motile rods from baseline topost-initial therapy and from post-initial therapy to post-surgery. In spite of continued improvements in microbio-logical parameters, little or no change in clinical indiceswas noted after the surgical phase. Two of 18 patients ex-hibited increases in motile rods and spirochetes, accompa-nied by a deterioration of clinical parameters during thetreatment period. The authors suggest that despite treatmentrendered, microflora of these sites were related to increaseddisease susceptibility rather than periodontal health.

Evian et al. (1982) correlated proportions of bacterialmorphotypes at different diseased sites within the samemouth, determining the extent of correlation with the clin-ical parameters of periodontitis in 14 patients with untreatedmoderate to advanced disease. After clinical indices (PD,PI, GI) were recorded, microbial samples were obtainedfrom the deepest pocket in each sextant and examined in-dividually by DFM. Bacterial morphotypes were catego-rized as cocci, motile rods, spirochetes, or others. Propor-tions of morphotypes among the 6 sites in any individualmouth varied considerably. In accordance with earlier stud-ies, the mean percentage of spirochetes varied directly withincreased PD, PI, and GI scores. However, no significantcorrelations could be determined when measurements of in-dividual sites were analyzed. The authors suggest that dif-ferences in disease activity among sites as well asvariability due to the sampling process may account for theresults. The authors suggest that by pooling samples fromindividual patients, it may be possible to minimize sam-pling errors and still yield useful information about sites atrisk.

CULTURAL STUDIESTanner et al. (1979) characterized the microbial flora at

the apical region of advancing periodontitis lesions. Criteriaof disease activity in 8 subjects with advanced periodontitisconsisted of at least 2 mm of radiographic bone loss in theprevious year. Anaerobic bacterial samples were obtainedand cultured. Correlations between bacterial and clinicalparameters were statistically evaluated. Microbiota of 2young adult patients with generalized bone loss and inflam-mation were dominated by Porphyromonas gingivalis andActinobacillus actinomycetemcomitans. Sites of 2 patientswith extensive bone loss but minimal inflammation weredominated by Prevotella intermedia, Eikenella corrodens,and fusiform-shaped Bacteroides (probably Bacteroidesforsythus). Sites of the remaining 4 patients had moderateinflammation with continued bone loss and demonstratedhigh levels of P. gingivalis, F. nucleatum, "fusiform" Bac-teroides, and anaerobic Vibrios. Sites with minimal diseaserevealed higher proportions of Gram-positive organisms.The authors concluded that significant differences do existin the apical plaque of adult periodontitis patients and thatit seems likely that specific groups of organisms are relatedto certain clinical diseases.

RAPID IDENTIFICATION OF POTENTIALPATHOGENS

Investigators have attempted to develop methods for rap-idly identifying certain bacteria or disease activity based onbacterial antigenic profiles (DNA probes, latex agglutina-tion), enzymatic activity (B-glucuronidase, collagenase,etc.), metabolic end products and/or antibody liters. Reviewarticles by Armitage (1987) and Greenstein (1988) discusssome of the advantages and disadvantages of various rapididentification techniques.

DNA Probes. These are comprised of radio-labeledDNA fragments of specific bacteria such as P. gingivalis.Theoretically, when the labeled fragments are added to adigested plaque sample adhering to nitrocellulose, they willcombine with any analogous fragments (P. gingivalis ifpresent), allowing identification and quantification of thespecific organism if present. This method is site specificand simple, but disadvantages include decay of the label,inter-reaction of labeled fragments, and cross-reactivitywith DNA of other species.

Latex Agglutination. In this technique, plaque samplesare mixed with latex beads that are coated with antibodiesspecific for certain periopathogens. If the pathogen is pres-ent in the plaque sample, cross-bridging of the antibody-pathogen-antibody results in visibly detectableagglutination of the beads. This technique has potential, butis not widely used.

Flow Cytometry. This technique involves reaction ofplaque with fluorescein-tagged antibodies specific for se-lective pathogens. The sample is then dispersed and’ ’tagged’’ pathogens are counted as they flow past a spec-trometer. Disadvantages include equipment expense and aninadequate data base related to plaque microbe determina-tion.

Use of ELISA. In this enzyme-linked immunosorbentassay, plaque samples are diluted and attached to a poly-styrene plate to which pathogen specific antibodies (taggedwith enzyme substrate) are added. Unattached antibody isthen washed off and the plate reacted with an enzyme thatis specific for the substrate tag. The remaining antibodieswhich are attached to the pathogens can be detected byspectrophotometry for color change.

Direct Immunofluorescence (IF). In this technique, flu-orescein tagged antibodies are reacted with plaque dilutionsand specific staining of organisms is observed using a flu-orescent microscope.

Indirect IF. Here untagged antibodies are initially com-plexed with the antigen. The second step involves additionof fluorescein-tagged antibodies which will react with ("pig-gybacking") the first antibody (antisera). This gives a muchhigher fluorescein signal and has been used successfully todetect specific microbes in plaque samples (good for quali-tative analysis, time consuming for quantitative analysis).Disadvantages: monoclonal antibodies are so specific theymay overlook some of the organisms and polyclonal anti-

52 CHAPTER 4. DISEASE ACTIVITY Section 4. Indices Used in Assessment of Periodontal Status

bodies may cross-react with other species. Indirect immu-nofluorescence is probably not clinically feasible.

When complex mixed infections make it difficult to sin-gle out individual pathogens, increased antibody titers toparticular organisms may suggest pathogenicity. The prob-lem with measuring serum antibody titers is that high levelsare not always associated with disease progression, andnon-specific cross-reactivity may occur. Titers are some-times low in the presence of disease progression. This isexplained by the fact that the systemic response (blood se-rum antibodies) may lag behind disease initiation. This lagmay continue well beyond resolution of diseased sites andmay also influence antibody titers to specific organisms.

RELEVANCE AND CONCERNSInitially, darkfield studies appeared to offer a means for

relating disease activity to proportions of motile bacteria,especially spirochetes. Evian et al. (1982), however, sug-gested that spirochetes are so ubiquitous in nearly all formsof periodontal disease that their mere presence in bacterialsample is of limited diagnostic value.

The initial study by Listgarten and Levin (1981) wasencouraging, because it suggested that spirochetes and mo-tile rods could be used to identify subjects at risk for futurebreakdown. In a subsequent study, however, Listgarten etal. (1984) were unable to use the percentage of spirochetesin a subgingival sample to identify specific sites at risk forbreakdown. In addition, a separate study by the same group(Listgarten et al., 1986) was unable to effectively use mi-croscopic monitoring to prevent recurrence of periodontitisby altering maintenance regimens. When pooled subgingi-val samples from a patient were examined for spirocheteprevalence, levels of spirochetes tended to correlate withdisease activity although site of the activity is not identifiedby this method. However, when levels of spirochetes at sim-ilar (> 6 mm) sites within a patient are examined, a corre-lation between disease activity and number of spirochetescould be shown. Other factors discouraging the use of DFMto monitor disease activity are that the major putative per-iodontopathogens (e.g., P. gingivalis, A. actinomycetemcom-itans, and P. intermedia are non-motile and would bediscounted by a method based solely on bacterial motilityand/or number of spirochetes (Slots and Listgarten, 1980).

Technical difficulties associated with cultural studies in-clude: 1) location of plaque sample; 2) tendency of variousmethods of dispersing bacterial plaque to favor growth ofone species over another; and, 3) unavailability of a singleculture media/method capable of recovering all bacterialspecies in subgingival plaque. Selective media may disin-franchise important species and purportedly "non-selectivemedia" may "select" for different segments of microbiota.These 3 factors may be partially responsible for the varietyof microbiological findings reported by different laborato-ries. Furthermore, probing accuracy may present a problemwhen attempting to associate cultural findings with probing

depth. The time and expense associated with culturing pres-ently limit its use to that of a periodontal research diag-nostic tool.

REFERENCESArmitage G, Dickerson WR, Jenderseck RS, Levine SM, Chambers DW.

Relationship between the percentage of subgingival spirochetes andthe severity of periodontal disease. J Periodontol 1982;53:550-556.

Armitage GC. Diagnosing periodontal disease and monitoring the re-sponse to periodontal therapy. In: Perspectives on Oral AntimicrobialTherapeutics. 1987;47-60.

Badersten A, Nilveus R, Egelberg J. Effect of nonsurgical periodontaltherapy. VII. Bleeding, suppuration and probing depth in sites withprobing attachment loss. J Clin Periodontol 1985;12:432-440.

Evian C, Rosenberg E, Listgarten M. Bacterial variability within diseasedperiodontal sites. J Periodontol 1982;53:595-598.

Greenstein G. Microbiologic assessments to enhance periodontal disease.J Periodontol 1988;59:508-515.

Haffaje A, Socransky S, Goodson J. Clinical parameters as predictors ofdestructive periodontal disease activity. J Clin Periodontol 1983;10:527-565.

Lang NF, loss A, Orsanic T. Bleeding on probing. A predictor for theprogression of periodontal disease. J Clin Periodontol 1986;13:590-596.

Listgarten MA, Hellden L. Relative distribution of bacteria at clinicallyhealthy and periodontally diseased sites in humans. J Clin Periodontol1978;5:115-132.

Listgarten MA, Levin S. Positive correlation between the proportions ofsubgingival spirochetes and motile bacteria and susceptibility of hu-man subjects to PD. J Clin Periodontol 1981;8:122-138.

Listgarten MA, Levin S, Schiffer C, et al. Comparative differential dark-field microscopy of subgingival bacteria from tooth surfaces with re-cent evidence of recurring periodontitis and from nonaffected surfaces.J Periodontol 1984;55:398-405.

Listgarten M, Schiffer CC, Sullivan P. Failure of a microbial assay toreliably predict disease recurrence in a treated periodontitis populationreceiving regularly scheduled maintenance. J Clin Periodontol 1986;13:768-773.

Listgarten M. The role of dental plaque in gingivitis and periodontitis. JClin Periodontol 1988;15:485-487.

Rosenberg E, Evian C, Listgarten M. The composition of the subgingivalmicrobiota after periodontal therapy. J Periodontol 1981;52:435^41.

Slots J, Listgarten M. Bacteroides gingivalis, Bacteroides intermedius andActinobacillus actinomycetemcomitans in human periodontal disease.J Clin Periodontol 1988;15:85-93.

Tanner ACR, Haffer C, Bratthall GT. A study of the bacteria associatedwith advancing periodontitis in man. J Clin Periodontol 1979;6:278-307.

Section 4. Indices Used inAssessment of Periodontal Status

DEFINITIONIndex: A relative or arbitrary system of measurement

which describes or quantitates a condition. Such indices areappropriate for use in an individual patient or for epide-miological studies.

PURPOSEPeriodontal indices are designed to assess disease prev-

alence and/or incidence within a population or a given pa-

Section 4. Indices Used in Assessment of Periodontal Status CHAPTER 4. DISEASE ACTIVITY 53

tient. Prevalence is denned as the number of existing casesin the population at a specific point in time, while incidenceis the number of new cases of a disease from one time pointto another. The long latent period of periodontal diseasemakes it difficult to determine a definite time of diseaseonset, a fact needed to establish incidence rates. Prevalenceof disease is usually the main determinant in populationhealth need surveys. For periodontal disease, the degree andseverity of inflammation must be determined in order todetermine treatment needs. All periodontal indices in cur-rent use measure morbidity. However, none are designedto measure tooth mortality related to periodontal disease.

TYPESIndices may be reversible, irreversible, or composite

(See Tables 1 through 8) (Barnes et al., 1986). An irre-versible index measures the permanent tissue damagecaused by disease. Indices which record radiographic boneloss and attachment loss are considered irreversible. Re-versible indices assess active disease and allow for changesin periodontal health status. Examples are: Russell’s peri-odontal index (PI), Ramfjord’s periodontal disease index(PDI), and Greene and Vermillion’s oral hygiene index(OKI), and OKI-simplified. The PI and PDI indices havereversible and irreversible components and are consideredto be composite indices.

Loe (1967) described the gingival index, the plaque in-dex, and the retention index systems. The gingival index(GI) describes qualitative changes in the gingival soft tissueat 4 areas on the tooth (buccal, mesial, distal, and lingual).A score of 0 to 3 is given for each area based on visualcharacteristics of inflammation after drying of the tissuesand the presence or absence of bleeding when a probe isrun along the soft tissue wall of the entrance of the gingivalcrevice. The GI may be used to determine a GI for the tooth(sum of the 4 areas divided by 4), a GI for a group of teeth(grouping scores of incisors, premolars, molars), or a GIfor the individual (adding the indices for the teeth and di-viding by the total number of teeth examined). Criteria forthe GI are: 0 = normal gingiva; 1 = mild inflammation-slight change in color, slight edema, no bleeding on prob-ing; 2 = moderate inflammation-redness, edema, andglazing with bleeding on probing; 3 = severe inflamma-tion-marked redness and edema, ulceration, and spontane-ous bleeding.

The plaque index (PI) describes the thickness of the softdebris aggregates in the gingival area of the tooth surfaces,and no attention is paid to the coronal extension of theplaque. A score from 0 to 3 is given for the same areasevaluated in the GI, but is based on the amount of softmatter detected following drying of the tissues and runninga probe across the tooth surface at the entrance of the gin-gival crevice. PI should precede GI when the two indicesare used together. Criteria for the PI are: 0 = no plaque inthe gingival area; 1 = a film of plaque adhering to the free

gingival margin and adjacent area of the tooth, recognizedby running a probe across the tooth surface; 2 = moderateaccumulation of soft deposits within the gingival pocket,on the gingival margin and/or adjacent tooth surface whichcan be seen by the naked eye; 3 = abundance of soft matterwithin the gingival pocket and/or on the gingival marginand adjacent tooth surface. The retention index describesthe quality of the tooth surface as it relates to the presenceof retentive factors such as calculus, ill-fitted margins, andcarious lesions. Criteria are: 0 = no caries, no calculus, noimperfect margin of dental restoration in gingival location;1 = supragingival cavity, calculus, or imperfect margin ofrestoration; 2 = subgingival cavity, calculus, or imperfectmargin of restoration; 3 = large cavity, abundance of cal-culus or grossly insufficient marginal fit of restoration in asupra- and/or subgingival location.

Chaves et al. (1993) evaluated the association betweengingival index (GI) bleeding (GI = 2 or 3) and bleedingon probing (BOP) in 125 gingivitis patients (19 to 62 yearsold). Clinical parameters included GI and PI with a manualprobe, probing depth (PD), and BOP with a Florida probe.BOP was considered present if bleeding occurred within 20seconds of probing. PD ranged from 0.1 to 5.9 mm; 98.6%of depths were 0.1 to 4 mm. Mean GI bleeding was 35.3%and mean BOP bleeding was 40.9%. When sites were eval-uated, BOP showed a positive correlation with PD as didGI with PI. There was a good overall correlation betweenGI and BOP, and agreement varied with PD. Highest agree-ment between GI and BOP bleeding was for PD > 4 mm(85.4%) and PD > 2 mm (72.3%). In shallow pockets (0.1mm to 2 mm), the highest percent agreement was for siteswith GI = 0 or 1, or negative BOP (77.7%). When therelationship between BOP and visual signs of inflammationwas related to PD, the percent BOP increased with increas-ing PD.

Muhlemann and Son (1971) concluded that bleedingfrom the sulcus is the earliest clinical symptom of gingivitisand that it precedes discoloration and swelling of gingivalunits. Sulcus bleeding index (SBI) was scored at time in-tervals over 17 days in 13 dental students refraining fromoral hygiene measures. SBI was determined using a perio-dontal probe (diameter 0.5 mm) placed in the sulcus parallelto the tooth long axis at facial/lingual sites and directedtowards the col at interproximal sites. A score of 1 repre-sented a bleeding point which occurred up to 30 secondsafter probing in the absence of gingival swelling or colorchange. At the start of the test period, 738 gingival unitsappeared healthy and did not bleed upon sulcus probing(score 0). After 17 days without hygiene, 264 apparentlyhealthy units (score 0) remained. The number of score-1units (bleeding upon gentle probing in the absence of colorchange or swelling) increased from 88 to 470. At this time,score-2 units (bleeding with change of color) increasedfrom 6 to 89, while only 9 gingival units were slightlyswollen (score 3). Using SBI, 64.2% of gingival units at


TABLE 1. INDICES USED TO EVALUATE SIGNS, SYMPTOMS, AND ETIOLOGIC FACTORSASSOCIATED WITH DENTAL DISEASE (PLAQUE AND HYGIENE)

Index(source)

Oral hygiene index(OHI) (Greene andVermillion)

Oral hygiene indexsimplified (OHI-S)(Greene andVermillion)

OHI-S debrismodification (Glass)

Hygiene analysis index(HAI) (Love et al.)

Patient hygieneperformance (PHP)(Podshadley andHaley)

Plaque index(Lennox andKopczyk)

Plaque index(Quigley and Hein)

Measures

Debriscalculus

Debriscalculus

Debris

Plaque

Plaque

Plaquebleeding

Plaque

Soft tissuearea or

Scored by teeth examined

Segments All except 3rdmolars

Teeth Max (R) 1stmolar

Max (R) centralincisor

Max (L) 1stmolar

Mnd (L) 1stmolar

Mnd (L) centralincisor

Mnd (R) 1stmolar

Teeth Same as OHI-S

Teeth All

Teeth Same as OHI-S

Teeth All

Teeth All except 3rdmolars

Aspect orsurfacesexamined

Buccal,lingual

BuccalFacialBuccalLingualFacialLingual

Same asOHI-S

Mesial, distal,facial,lingual

Same asOHI-S


Buccal,lingual

Presence orseverity

measured

Severity

Severity

Severity

Presence/absence

Severity

Presence/absence

Severity

Uses

Epidemiologicsurveys, clinicaltrials,monitoring,individualpatient

Epidemiologicsurveys


Patient motivation,monitoringpatient progress


Patient motivation,monitoringpatient progress

Clinical trials,epidemiologicsurveys

TABLE 2. INDICES USED TO EVALUATE SIGNS, SYMPTOMS, AND ETIOLOGIC FACTORSASSOCIATED WITH DENTAL DISEASE (CALCULUS)

Index(source) Measures

Calculus Surface Index Calculus(CSI) (Ennever et al.)

Probe Method Calculus Calculusassessment (Volpeet al.)

Marginal Line Calculus CalculusIndex (MLC)(Muhlemann andVilla; Villa et al.)

Soft tissuearea or

Scored by teeth examined

Teeth Mandibularcentral andlateral incisors

Teeth All mandibularincisors andcuspids

Teeth Mandibularcentral andlateral incisors



Lingual (andlingualaspects ofinter-proximals)

Lingual

Presence orseverity

measured

Presence/absence

Severity

Severity

Uses

Clinical trials

Clinical trials,epidemiologicsurveys

Clinical trials,patientprogress,patientmotivation


TABLE 3. INDICES USED TO EVALUATE SIGNS, SYMPTOMS, AND ETIOLOGIC FACTORSASSOCIATED WITH DENTAL DISEASE (BLEEDING AND GINGIVAL)

Index(source)

Gingival BleedingIndex (GBI)(Carter and Barnes)

Sulcus Bleeding Index(SBI)(Muhlemann andMajor; Muhlemannand Son)

PMA Index papillary,marginal, attachedgingiva(Massler et al.;Schour and Massler)

Gingival Index (Gl)(Soumi and Barbano)

Gingival Index (Gl)(Loe; Loe andSilness)

Plaque Index (usedwith Gl)(Loe)

Retention Index (usedwith Gl)(Loe)

Measures

Bleeding

Bleeding,gingival,colorchange,edema

Gingivalinflamma-tion(edema,bleedingnecrosis,recessionpocketformation)

Gingivalinflamma-tion

Inflamma-tion (colorchanges,edema,bleeding,ulcera-tion)

Debris andplaque

Calculus,caries,over-hangingrestora-tions,otherretentiveagents

Scored by

Teeth

Teeth

Papillarymarginalandattachedgingivalunits

Segmentsandteeth(papil-lary andmarginalgingivalunits)

Teeth

Teeth

Teeth

Soft tissuearea or

teeth examined

All exceptbetween 2ndand 3rdmolars

All maxillary andmandibularcentralincisors,lateralincisors,cuspids, and1st bicuspids

Around all teethexcept 3rdmolars

All

Gingival, plaqueand retentionindices areintended to beused togetheras a system.All use thesame teethand samesurfaces.

Max (R) 1stmolar

Max (R) lateralincisor

Max (L) 1stbicuspid

Mnd (L) 1stmolar

Mnd (L) lateralincisor

Mnd (R) 1stbicuspid

Aspect or Presence orsurfaces severityexamined measured

Interproximal Presence/absence

Mesial, distal, Presence/facial, absencelingual and

severity

Facial, lingual Severity andpresence

Facial, lingual Severity

Mesial, distal, Severityfacial,lingual

Uses

Clinical trials,patientprogress,patientmotivation

Clinical trials,epidemiologicsurveys, patientprogress,patientmotivation


Epidemiologicsurveys, clinicaltrials, patientprogress

Epidemiologicsurveys, clinicaltrials,monitoringpatient progress


TABLE 4. INDICES USED TO EVALUATE SIGNS, SYMPTOMS, AND ETIOLOGIC FACTORSASSOCIATED WITH DENTAL DISEASES (PERIODONTAL)

Index(source)

Periodontal DiseaseRate Index (PDR)(Sandier and Stahl)

Periodontal Index (PI)(Russell)

Periodontal Disease In-dex (PDI)(Ramfjord)

ScoredMeasures by

"Periodontal TeethDisease":inflamma-tioncrevicedepth, mo-bility, alve-olar boneresorption

Inflammation Teethpocketdepth toothmobility

Pocket depth, Teethcrevicedepth (fromCEJ)

Soft tissuearea or

teeth examined

All

All

Max(R) 1stmolar

Max (R) lateralincisor


Mesial, distal,facial, lin-gual, (usesradio-graphs)

Facial, lin-gual, me-sial, distal

Mesial, facial

Presence orseverity

measured

Presence/absence

Severity

Severity

Uses

Crude epidemio-logic surveys


Epidemiologicsurveys, clinicaltrials

Max(L) 1st bi-cuspid

Mnd (L) 1stmolar

Mnd (L) lateralincisor

Mnd(R) 1st bi-cuspid

Gingival Index (a partof PDI)(Ramfjord)

Plaque Index (usedwith PDI)(Ramfjord [Shick andAsh Modification])

Calculus Index (usedwith PDI)(Ramfjord)

Periodontal screeningexamination(O’Leary)

Includes:Gingival IndexPeriodontal IndexIrritant Index

Inflammation, Teeth Same as PDIbleeding,edema, ul-ce ration

Plaque Teeth Same as PDI

Calculus Teeth Same as PDI

Gingival In- Segments Alldex: inflam-mation

Periodontal Segments AllIndex:pocket Segmentsdepth

Irritant Index: Allplaque, cal-culus, over-hangingrestora-tions, unfil-led

Mesial, facial



Gingival in-dex, facial,lingual, in-terproxi-mals

Periodontalindex, me-sial, lineangle

Irritant index:all toothsurfaces

Severity

Presence andseverity

Severity

Severity

Severity

Severity




Monitor patientprogress, epide-miologic sur-veys


TABLE 5. COMPARISON OF SCORES IN FREQUENTLY USED PLAQUE AND DEBRIS INDICES

Scores

Index

Greene and Vermil-lion OHI-S DebrisIndex

Glass modification ofOHI-S

Loe Plaque Index

Ramfjord Plaque In-dex

Quigley and HeinPlaque Index(modified)

Podshadley and Ha-ley PHP

Lennox and KopczykPlaque Index

Love Hygiene Analy-sis Index

0 1

No debris or Soft debrisstain covering not

more than onethird of the toothsurface

No visible de- Debris visible atbris gingival margin,

but discontinu-ous. Lessthan 1 mm in

heightNo plaque in A film of plaque

the gingival adhering to thearea free gingival

margin and ad-jacent area ofthe tooth. Theplaque may onlybe recognizedby running aprobe across thetooth surface

No plaque Plaque present onsome but not allinterproximalbuccal and lin-gual surfaces ofthe tooth

No plaque Separate flecks ofplaque at thecervical marginof the tooth

No plaque The tooth surfaceif mentally di-vided into 5areas. Plaque inonly one area

Plaque severityis notscored; onlypresence orabsence onfour toothsurfaces.

2

Soft debriscoveringmore than onethird, but notmorethan two thirdsof the exposedtooth surface

Debris continuousat gingival mar-gin. Greater than1 mm in height

Moderate accumu-lation of soft de-posit is withinthe gingival mar-gin, which canbe seen by thenaked eye

Plaque present onall interproximal,buccal and lin-gual surfaces,but coveringless than onehalf of thesesurfaces

A thin continuousband of plaque(up to 1 mm) atthe cervical mar-gin

Plaque in two ar-eas

3 4

Soft debris

covering morethan two thirdsof the exposed

tooth

Debris involving Debris generallyentire gingival scattered overthird of tooth tooth surface

Abundance of softmatter within the

gingival pocketand/or on thegingival margin

Plaque extendingover all inter-

proximalbuccal andlingual surfaces,but coveringmore than onehalf of thesesurfaces

A band of plaque Plaque covering atwider than 1 mm least one thirdbut covering but less thanless than one two thirds of the

third of crown crownPlaque in three Plaque in four ar-

areas eas

5

Plaque coveringtwo thirds ormore of crown

Plaque in five ar-eas

Plaque severity is not scored; only presence or absence on four tooth surfaces

58 CHAPTER 4. DISEASE ACTIVITY Section 4. Indices Used in Assessment of Feriodontal Status

TABLE 6. COMPARISON OF SCORING SYSTEM IN FREQUENTLY USED CALCULUS INDICES

Greene andVermillion

OHI-SCalculus

Scores Scores

0 No calculuspresent

1 Supragingivalcalculuscovering notmore thanone third ofthe exposedtooth sur-face

2 Supragingivalcalculuscovering onethird to twothirds of theexposedtooth sur-face and/orflecks ofsubgingivalcalculus

3 Supragingivalcalculuscoveringmore thantwo thirds ofthe exposedtooth sur-face and/ora continuousband of sub-gingival cal-culus

RamfjordCalculus Index

No calculus

Supragingivalcalculus ex-tending onlyslightly be-low the freegingivalmargin

Moderateamount ofsupra- andsubgingivalcalculus orsubgingivalcalculusalone

An abundanceof supra-and subgin-gival calcu-lus

Ennever et al.

Calculus CalculusSurface SurfaceIndex Severity Index

Has no sever- No calculusity compo- presentnent. Scores16 tooth sur-faces forpresence orabsence ofcalculus

Calculus ob-servable, butless than0.5 mm inwidth and/orthickness

Calculus notexceeding1.0 mm inwidth and/orthickness

Calculus ex-ceeding 1 .0mm in widthand/or thick-ness

Volpe andManhold probe

method ofcalculus

assessment

Uses a perio-dontal probeto measurethe heightand width ofcalculus de-posits ontooth sur-face. Re-sults arereported inmillimeters

Muhlemannand Villa

marginal linecalculus index

Uses a probeto measureheight ofcalculus de-posits ontooth sur-faces. Re-sultsreported inpercentageof surfacecovered (0,12.5, 25, 50,75, and100%)

O’LearyIrritant Index

No detectableplaque, or cal-culus, eitherSupragingivalor subgingivalis found onany tooth inthe segment

A slight amountof plaque orSupragingivalcalculus notextendingmore than 2mm from thegingival mar-gin is foundon any toothin the seg-ment

Plaque or Supra-gingival calcu-lus covers upto one half theexposed clini-cal crown onany tooth inthe segment

Plaque or Supra-gingival calcu-lus coversmore thanone half theclinical crownor subgingivalcalculus de-posits or over-hanging ordeficient res-torations aredetectable byprobing


TABLE 7. COMPARISON OF SCORES IN FREQUENTLY USED GINGIVAL AND BLEEDING INDICES

Scores

Index

Schour and MasslerPMA IndexPapillae

Marginal

Attached gingiva

Loe and SilnessGingival Index

Ramfjord Gingival In-

dex

O’Leary Gingival

Score

Muhlemann and Major,Muhlemann andSon Sulcus Bleed-ing Index

Soumi and BarbanoGingival Index

Carter and BarnesGingival BleedingIndex

0

Normal: no inflam-mation

Normal; no inflam-

mation visible

Normal; pale rose;stippled

Normal gingiva

Absence of signs ofinflammation

Normal gingiva

Healthy appearance,no bleeding onsulcus probing

Absence of inflam-mation. Gingiva ispale pink in colorand firm in texture.Swelling is not ev-ident and stippling

can usually benoted

1

Mild papillary en-gorgement; slightincrease in size

Engorgement; slightincrease in size;no bleeding

Slight engorgementwith loss of stip-pling; change incolor may or maynot be present

Mild inflammation,slight change incolor, slightedema. No bleed-ing on probing

Mild to moderate in-flammatory gingi-

val changes, notextending aroundthe tooth

Slight to moderateinflammation notsurrounding anyteeth

Apparently healthy Pand M showing nochange in colorand no swelling,but bleeding from

sulcus on probing

Presence of severeinflammation. Adistinct colorchange to red ormagenta is evi-dent. There maybe swelling andloss of stippling.The gingiva maybe spongy in tex-ture

2

Obvious increase insize of gingivalpapilla: hemor-rhage on pressure

Obvious engorge-ment; bleedingupon pressure

Obvious engorge-ment of attachedgingiva withmarked increasein redness. Pocketformation present

Moderate inflamma-tion, redness,edema and glaz-ing. Bleeding onprobing

Mild to moderatelysevere gingivitisextending allaround the tooth

Slight to moderateinflammation sur-rounding one ormore teeth

Bleeding on probingand change ofcolor due to in-flammation. Noswelling, macro-scopic edema

Presence of severeinflammation. Adistinct colorchange to red ormagenta: swelling,loss of stipplingand a spongy con-sistency. Gingivalbleeding upongentle probing.The inflammationhas spread to theattached gingiva

3

Ecessive increase insize with sponta-neous hemorrhage

Swollen collar; spon-taneoushemorrhage; be-ginning infiltrationinto attached gin-giva

Advanced periodon-titis. Deep pocketsevident

Severe inflamma-tion�marke d red-ness and edema.Ulceration. Spon-taneous bleeding

Severe gingivitischaracterized bymarked redness,swelling, tendencyto bleed and ulcer-ation

Marked inflammationulceration, sponta-neous bleeding,loss of surfacecontinuity, clefts ofgingival tissue

Bleeding on probing,change in colorand slight edema-tous swelling

Bleeding severity is not scored. Only the presence or absence of bleeding from a maximum

recorded.

4 5

Necrotic papilla Atrophy and loss ofpapilla (throughinflamma-tion)

Necrotic gingivitis Recession of thefree marginal gin-giva below theCEJ due to in-flammatorychanges

Bleeding on prob- Bleeding on probinging, change in and spontaneouscolor obvious bleeding andswelling change in color,

marked swellingwith or without ul-ceration

of 28 gingival units following flossing is


TABLE 8. COMPARISON OF SCORES IN FREQUENTLY USED PERIODONTAL INDICES

ScoresRussell

Periodontal Index

RamfjordPeriodontal Disease Index

(Crevice Depth)O’Leary Periodontal

Screening Examination Scores

Negative. There is no overtinflammation

Mild gingivitis. There is anovert area of inflammationin the free gingiva whichdoes not circumscribe thetooth

Gingivitis. Inflammationcompletely circumscribesthe tooth, but there is noapparent break in theepithelial attachment

Gingivitis with pocketformation. The epithelialattachment has beenbroken and there is apocket. There is nointerference with normalmasticatory function, thetooth is firm in its socket

Advanced destruction withloss of masticatory function

If the gingival crevice in noneof the measured areasextends apically to theCEJ, the gingival score isthe PDI score for that tooth(it can range from 0 to 3)

The gingival crevice extendsapical to the CEJ, but notmore than 3 mm

The gingival crevice extendsapically from 3 to 6 mm inrelation to the CEJ

The gingival crevice extendsmore than 6 mm apically tothe CEJ

Upon probing of the gingivalcrevices, a score of 0 isgiven if the probe does notextend 1 mm apical to theCE Junction of any tooth inthe segment and there isno exposure of the CEJ onany surface of any tooth inthe segment

The probe extends up to 3mm apical to the CEJ ofany tooth in the segment

The probe extends from 3 to6 mm apical to the CEJ ofany tooth in the segment

The probe extends 6 mm ormore apical to the CEJ ofany tooth in the segment

34

risk (score 0 at baseline) revealed inflammation. Withoutusing SBI and with visual inspection alone (GI), only11.9% of units would have been detected as having becomeinflamed. Bleeding from the gently probed sulcus precedesthe appearance of gingival color changes and is the leadingand first clinical symptom of marginal gingivitis. The au-thors conclude that the higher sensitivity of SBI makes itpossible to use non-hygiene periods of a reasonable lengthof time (2 to 3 weeks) in areas with moderate gingivitisactivity. Characteristics of the SBI which differentiate itfrom the GI are: 1) inflammation is diagnosed only if bleed-ing occurs upon gentle probing of the sulcus; 2) apparentlyhealthy gingival units without color changes or swelling arediagnosed as inflamed (score 1) if the bleeding occurs upongentle probing; and 3) resulting SB scores are roughly 1unit higher.

Quirynen et al. (1991) examined 5 plaque indices (Har-rap index, Quigley and Hein index, Navy plaque indexmodified by Clemmer and Barbano, Navy plaque indexmodified by Hancock and Wirthlin, planimetrical plaqueindex) to determine which could best discriminate the dif-ference in the rate of plaque formation associated withhealthy tissue (phase I) versus with gingival inflammation(phase II) where plaque was allowed to accumulate over a96-hour period. Significant differences between phase I andphase II plaque accumulations could not be detected usingthe Harrap index and the Navy index (Hancock and Wirth-lin). The Navy index (Clemmer and Barbano) detected adifference at 82 hours while the Quigley and Hein indexdetected a phase I and phase II difference at 72 hours. Theplanimetrical index detected a significant difference at 36hours. The planimetrical plaque index demonstrated the


highest discriminating power; the Harrap and Navy index(Hancock and Wirthlin) was the least discriminating. Al-though the planimetrical index is highly reproducible, it istime consuming and difficult to use. The Quigley and Heinor Navy index (Clemmer and Barbano) seem to be the bestalternative of those indices studied if the planimetrical in-dex is not feasible. Each index has its own advantages anddisadvantages and the aim of study should determine theplaque index chosen.

Almas et al. (1991) evaluated the capacity of the com-munity periodontal index of treatment needs (CPITN) toreflect the clinical periodontal status in 52 patients as rep-resented by the standard clinical indices of PI, GI, papillableeding index (FBI), and PD. CPITN scores determinedfor each sextant are as follows: code 4 = pathologic pock-ets 6 mm or more; code 3 = pathologic pockets 4.0 to 5.5mm; code 2 = supra-or subgingival calculus; code 1 =gingival bleeding after probing; and code 0 = none of theabove signs present. PD was assessed using a pressure-sen-sitive probe with 0.34 mm tip and 0.25 N force. CPITNwas assessed using a (WHO 612) CPITN probe with a ballend of 0.5 mm and 0.25 N force. Six sites per tooth wererecorded. CPITN did not correlate with the amount ofplaque present, number of sites affected in a given sextant,or GI. There was a tendency for an association between theCPITN and both the PD and the FBI. In spite of the abovecorrelations, extreme ranges for all indices were foundwithin a sextant regardless of the CPITN code; 25% of siteshad pockets > 6 mm deep and 70% of sextants had aCPITN score of 4. This study demonstrated that the CPITNfunctions as an epidemiologic tool for population planningand treatment needs but is not indicated for assessment ofindividual treatment needs.

Kaldahl et al. (1990) evaluated gingival suppuration andsupragingival plaque following 4 modalities of periodontaltherapy: coronal scaling (CS) only; coronal and subgingivalscaling and root planing (RP); root planing followed by mod-ified Widman surgery (MW); root planing followed by flapreflection with osseous surgery (FO). Clinical assessmentswere made at baseline (exam 1), 4 weeks following oralhygiene instruction (OHI) and CS or Sc/RP (exam 2), 10weeks following respective therapies (exam 3), and annuallyprior to maintenance therapy appointments (exams 4 and 5).This assessment included presence of supragingival plaque,gingival suppuration, probing depth, and clinical attachmentlevel. Patients were seen every 3 months for 2 years formaintenance therapy. The authors found that the prevalenceof supragingival plaque between the groups except for FO-treated sites showed more plaque accumulation after surgicaltherapy. The presence or absence of supragingival plaque atspecific sites was dynamic, frequently converting to a newstatus between 2 examinations. Sites that were not suppu-rating at 1 exam but were suppurating at the subsequentexam or at both exams had a less favorable response in bothprobing depth and probing attachment level.

USESThere are 4 ways in which a periodontal index may be

used: 1) clinical trials; 2) epidemiologic surveys; 3) eval-uation of patient progress; and 4) motivation of the patientto improve hygiene. The ideal index should: 1) be simpleto use; 2) require minimum time; 3) require minimum ar-mamentarium; 4) be clear, understandable, and reproduci-ble; 5) be amenable to statistical analysis; 6) be equallysensitive throughout its scale of variable measure; and 7)be acceptable to the patient (Barnes et al., 1986).

CONSIDERATIONSWhen using indices or evaluating studies using indices,

the following should be considered: 1) studies conductedwith different indices should be compared only as to gen-eral findings rather than specific details; 2) an index shouldbe selected according to its ability to best evaluate the var-iable (i.e., presence/absence of plaque rather than quantityof plaque); 3) index methodology should not be modified;4) those that measure presence or absence of plaque aremore applicable to motivation at assessment while thosemeasuring quantity may be more suited for clinical trialsand epidemiologic surveys; 5) full-mouth scoring should bereserved for clinical use, a single patient or small popula-tion groups, while simplified indices are more useful forepidemiologic surveys and large clinical studies; 6) exam-iner intra- and inter-reliability should be established priorto use and repeated throughout the study time period.

REFERENCESAlmas K, Bulman J, Newman H. Assessment of periodontal status with

CPITN and conventional periodontal indices. J Clin Periodontal 1991;18:654-659.

Barnes G, Parker W, Lyon T, Fultz R. Indices used to evaluate signs,symptoms and etiologic factors associated with diseases of the perio-dontium. J Periodontol 1986;57:643-651.

Carter HG, Barnes GP. The gingival bleeding index. J Periodontol 1974;45:801-805.

Chaves E, Wood R, Jones A, Newbold D, Manwell M, Kornman K. Re-lationship of "bleeding on probing" and "gingival index bleeding"as clinical parameters of gingival inflammation. / Clin Periodontol1993;20:139-143.

Ennever J, Sturzenberger OP, Radike W. The calculus surface indexmethod for scoring clinical calculus studies. J Periodontol 1961;32:54-57.

Glass RL. A clinical study of hand and electric toothbrushing. J Perio-dontol 1965;36:322-327.

Greene JC, Vermillion JR. The oral hygiene index: a method for classi-fying oral hygiene status. J Am Dent Assoc 1960;61:172-179.

Greene JC, Vermillion JR. The simplified oral hygiene index. J Am DentAssoc 1964;68:7-13.

Kaldahl W, Kalkwarf K, Patil K, Molvar M. Evaluation of gingival sup-puration and supragingival plaque following 4 modalities of periodon-tal therapy. J Clin Periodontol 1990; 17:642-647.

Lennox JA, Kopczyk RA. A clinical system for scoring a patient’s oralhygiene performance. J Am Dent Assoc 1973;86:849-852.

Loe H. The gingival index, the plaque index and the retention index sys-tems. J Periodontol 1967;36:610-616.

Loe H, Silness J. Periodontal disease in pregnancy. Acta Odontol Scand1963;21:532-551.


Loe H, Theilade E, Jensen S. Experimental gingivitis in man. J Perio-dontol 1965 ;36:177-187.

Love WD, Ramirez JM, Fultz RP. An oral hygiene measurement systemfor possible research and clinical use. J Public Health Dent 1975;35:227-230.

Manhold JH, Volpe AR, Hazen SP, et al. In vivo calculus assessment.Part II. A comparison of scoring techniques. J Periodontol 1965;36:299-304.

Massler M. The P-M-A index for the assessment of gingivitis. J Perio-dontol 1967;38:592-601.

Massler M, Rosenberg HM, Carter W, Schour I. Gingivitis in young adultmales. Lack of effectiveness of a permissive program of toothbrushing.J Periodontol 1957;28:111-124.

Massler M, Schour I, Chopra B. Occurrence of gingivitis is suburbanChicago school children. J Periodontol 1950;21:146-164.

Muhlemann HR, Major ZS. Gingivitis in Zurich school children. HelvOdontolActa 1958;2:3-12.

Muhlemann HR, Son S. Gingival sulcus bleeding� a leading symptom ininitial gingivitis. Helv Odontol Acta 1971;15:107-113.

Muhlemann HR, Villa P. The marginal line calculus index. Helv OdontolActa 1967;! 1:175-179.

O’Leary TJ. Instruction Manual For the Periodontal "Screening" Pro-cedure, USAF School of Aerospace Medicine (AFSC), Brooks AFB,Texas, April 1963.

O’Leary TJ. The periodontal screening examination. J Periodontol 1967;38:617-624.

Podshadley AG, Haley JV. A method for evaluating oral hygiene per-formance. Public Health Rep 1968;83:259-264.

Quigley G, Hein J. Comparative cleansing efficiency of manual and powerbrushing. J Am Dent Assoc 1962;65:26-29.

Quirynen M, Dekeyser C, van Steenberghe D. Discriminating power offive plaque indices. J Periodontol 1991;62:100-105.

Ramfjord S. Indices for prevalence and incidence of periodontal disease.J Periodontol 1959;30:51-59.

Ramfjord S. The periodontal disease index. J Periodontol 1967;38:602-610.

Russell AL. A system of classification and scoring for prevalence surveysof periodontal disease. J Dent Res 1956;35:350-359.

Russell AL. The periodontal index. J Periodontol 1967;38:585-591.Sandier HC, Stahl SS. Measurement of periodontal disease prevalence. J

Am Dent Assoc 1959;58:93-97.Schour I, Massler M. Prevalence of gingivitis in young adults. J Dent Res

1948;27:733.Shick RA, Ash MM. Evaluation of the vertical method of toothbrushing.

J Periodontol 1961;32:346-353.Suomi JD, Barbano JP. Patterns of gingivitis. J Periodontol 1968;39:71-

74.Turesky S, Gilmore N, Glickman I. Reduced plaque formation by the

chloromethyl analogue of victamine C. J Periodontol 1970;41:41-43.Villa P, Brakas GM, Muhlemann HR. A comparison of various calculus

incidence indices. Helv Odontol Acta 1967;11:180-188.Volpe AR, Kupczak LJ, King WJ. In vivo calculus assessment. Part III.

Scoring techniques, rate of calculus formation, partial mouth examsvs. full mouth exams, and intra-examiner reproducibility. Periodontics1967;5:184-193.

Volpe AR, Manhold JH. A method of evaluating the effectiveness of po-tential calculus inhibiting agents. NY State Dent 1962;28:289-290.

Volpe AR, Manhold JH, Hazen SP. In vivo calculus assessment. Part I.A method and its examiner reproducibility. J Periodontol 1965;36:292-298.

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