PEDIATRIC /Copyright ° 1981 by The American Academy of Pedodontics Vol. 3, Special Issue

Epidemiology and indices of gingival and Dr. Poulsen Sven Poulsen, Dr Odont

Abstract Validity of an index indicates to what extent the This paper reviews some of the commonly used indices index measures what it is intended to measure. Deter- for measurement of and periodontal disease. mination of validity is dependent on the availability Periodontal disease should be measured using loss of of a so-called validating criterion. attachment, not pocket depth. The reliability of several of Pocket depth may not reflect loss of periodontal the indices has been tested. Calibration and training of attachment as a sign of periodontal disease. This is be- examiners seems to be an absolute requirement for a cause gingival swelling will increase the distance from satisfactory inter-examiner reliability. Gingival and periodontal disease is much more severe in several the to the bottom of the clinical populations in the Far East than in Europe and North pocket (pseudo-pockets). Thus, depth of the periodon- America, and gingivitis seems to increase with age resulting tal pocket may not be a valid measurement for perio- in loss of periodontal attachment in approximately 40% of dontal disease. 15-year-old children. Apart from the validity and reliability of an index, important factors such as the purpose of the study, Introduction the level of disease in the population, the conditions under which the examinations are going to be per- Epidemiological data form the basis for planning formed etc., will have to enter into choice of an index. and evaluation of dental care programs throughout Since these factors vary considerably from one study the world. When epidemiological data have been col- to another, no single index will be appropriate for all lected, the amount of disease found has to be quanti- types of studies. fied by using indices. It is the purpose of this paper to (1) review some of Measurement of Gingivitis the more commonly used indices for the study of gin- Four indices commonly used in recent studies on gival and periodontal disease, and (2) describe some of gingival inflammation in children and young adults the epidemiological trends in the natural history of are presented in Table 1. gingivitis and periodontal disease in children. The diagnostic criteria employed in three of these indices are described in Tables 2 to 4. In the index de- Selection of Indices scribed by Ainamo & Bay," only absence or presence of An index is a numerical value describing the rela- bleeding after gentle probing is recorded. tive status of the population on a scale with definite Both the index described by Lbe & Silness17 and the upper and lower limits'. The use of indices permits index described by Suomi & Barbano3 as modified by comparison between different populations classified Suomi,4 are based on a combination of criteria. As an by the same criteria and methods. example, score 1 in Suomi & Barbano's index (Table 4) A large number of gingival and periodontal indices is based on changes in color, volume, and texture, as have been described in the dental literature. In order well as presence or absence of stipling. to evaluate different indices it is important to esti- An example of an index which is based on only one mate two parameters: reliability and validity. symptom is the bleeding index used by Miihleman and Reliability is the ability of a given test to give the coworkers. The criteria for the Papillary Bleeding In- same result when applied twice to the same object. In dex5 are described in Table 4. As seen from this table, the case of gingival and periodontal indices, reliability bleeding is the only symptom which is recorded. An can be estimated by having an examiner examine the increasing score is assigned according to an increased same patient twice. tendency of the gingival tissue to bleed.

EPIDEMIOLOGY AND INDICES 82 Poulsen The index described by Ainamo & Bay,6 considers formed in the Scandinavian countries during recent only presence or absence of bleeding on gentle probing years. The diagnostic criteria -- bleeding or no bleed- of the gingival tissue. Thus, this index represents a ing w are assumed to be relatively easy to interpret. simplification of the index developed by Miihleman Therefore this index is assumed to be relatively and coworkers {Table 4). Whencompared to the index insensitive to examiner differences. described by LSe & Silness (Table 3), you can see that it represents score 2 and 3 in this index. The index de- Measurementsof Periodontal Disease scribed by Ainamo& Bay has proved to be useful in a Those indices described up to now only consider number of epidemiological and clinical trials per- gingival inflammation. Recording of loss of periodon- tal attachment is not included in any of them. The diagnostic criteria for the Periodontal Index Table1. Fourindices commonly used in recentstudies on gingival ~9 inflammationin children and young adults. (PI) developed by Russell, are based on gingival in- flammation and loss of periodontal attachment (Table 5). This index has been used mainly for epidemiologi- Name(abbreviation) Reference cal purposes, and a variety of different populations in developing countries have been examined using this Gingival Index (GI) ~ L~e& Silness 1963 index. Gingivitis Index Suomi & Barbano 19688 Suomi19684 Papillary Bleeding Index {PBI) Saxer & M~ihlemann19755 Gingival~ Bleeding Index (GBI) Ainamo& Bay 1976 Table4. Diagnosticcriteria for the PapillaryBleeding Index developed~ by Saxer& MiJhlemann.

Table~,7 2. Diagnosticcriteria for theL~e & Silness gingival index. ScoreCriteria

Score Criteria Nobleeding. Bleedingsome seconds after probing. Bleeding immediatelyafter probing. Normalgingiva. spreading towards the mar- Mild inflammation-- slight changein color, slight ginal gingiva. edema. Nobleeding on probing. Moderate inflammation -- redness, edema and glazing. Bleedingon probing. Severe inflammation -- marked redness and 8’~ edema. Tendencyto spontaneous bleeding. Ulcera- Table5. Diagnosticcriteria described byRussell. tion. Score Criteria

Table3. Diagnosticcriteria for thegingival index developed by 3 6 0 Negative. There is neither overt inflammation in Suomi&Barbano andlater modifiedby Suomi. the investing tissues nor loss of function due to de- struction of supportingtissue. Score Criteria Mild gingivitis. There is an overt area of inflamma- tion in the free gingivae which does not circum- scribe the tooth. 0 Absenceof inflammation-- gingiva is pale pink in Gingivitis. Inflammationcompletely circumscribes color and firm in texture. Swelling is not evident the tooth, but there is no apparent break in the and usually can be noted. epithelial attchment. Presence of inflammation-- a distinct color change Gingivitis with pocket formation. The epithelial at- to red or magentais evident. There maybe swell- tachment has been broken and there is a pocket ing, loss of stippling and the gingiva maybe spongy {not merelya deepenedgingival crevie due to swell- in texture. ing in the free gingivae). Thereis no interference Presence of severe inflammation-- a distinct color with normalmasticatory function, the tooth is firm changeto red or magentais evident. Swelling, loss in its socket, andhas not drifted. of stippling and a spongyconsistency can be noted. Advanceddestruction with loss of masticatory There is either gingival bleeding upon gentle prob- function. The tooth maysound dull on percussion ing with the side of an explorer or the inflamma- with a metallic instrument; maybe depressible in tion has spread to the attached gingiva. its socket.

PEDIATRICDENTISTRY 83 Volume3, SpecialIssue When comparing the criteria proposed by Ram- Tablem] 6. Diagnosticcriteria described by Ramfjo~rd. fjord’°,’’ (Table 6) to the criteria developed by Russell we find that the criteria for score 1 and 2 are almost Score Criteria identical in the two indices. In those cases where no loss of attachment is recorded, Ramfjord’s Periodon- tal Disease Index (PDI) is equivalent to the gingivitis Absenceof signs of inflammation. score. If the gingival crevice extends apically to the Mild to moderate inflammatory gingival changes, cemento-enamel junction, the tooth is assigned a not extending around the tooth. Mild to moderately severe gingivitis extending all higher Periodontal Disease Index score and the gingi- around the tooth. vitis score for the same tooth is then disregarded. Severegingivitis characterized by marked redness, Both the index proposed by Russell and the index swelling,tendency to b]eedand ulceration. proposed by Ramfjord have criteria based on gingi- val inflammation as well as loss of periodontal scored as 1 decreased slightly, while the number of attachment. gingival units scored as 2 increased slightly from the Another possibility is to distinguish between gin- first examination to the second. Several explanations gival inflammation and periodontal disease and record gingivitis and loss of attachment separately. may be available for this phenomenon. The authors suggest that the first examination increased the tend- Whenrecording periodontal disease, a distinction should be made between pocket depth and loss of at- ency of the gingival units to bleed. Another explana- tachment;2 Pocket depth is the distance from the gin- tion may be a shift in diagnostic criteria. Probably gival margin to the bottom of the clinical pocket. both explanations are partly valid. The fact is, how- Since swelling of the gingival tissue due to inflamma- ever, that reliability of gingival indices is a difficult parameter to estimate, since the object being meas- tion may increase the depth of the pocket in cases where no loss of attachment has taken place, pocket ured is not constant. depth may not be a valid measurement of periodontal One of the only ways of comparing the performance disease. of different indices is to apply several indices in the Loss of attachment is the distance from the same study. The experimental gingivitis model has cemento-enamel junction to the bottom of the clinical been used extensively in studies on the plaque- and TM pocket. Both pocket depth and loss of attachment are gingivitis-preventive effects of a variety agents. Re- analysis of data from one of these trials. ’9 showedthat measured using a , and usually the gingival index developed by LSe & Silness ~ was recorded to the nearest millimeter. more sensitive than the Papillary Bleeding Index de- veloped by MiJhlemann and his co-workers2 Further- Reliability,Sensitivity and Statistical Analysis of Indicesof more, the Gingival Exudate Measurement~ proved to Gingivitis andPeriodontal Disease be more sensitive than the Gingival Index. The same study showed that only slight reduction The reliability of the various indices for gingival in the sensitivity of the LSe & Silness Gingival Index and periodontal disease have been studied to some ex- was observed if the scale was reduced from a 4-point tent in the literature. Lack of inter-examiner reliabil- scale to a 2-point scale using bleeding as the criterion. ity has been demonstrated by, among others, Davies Similar findings have been made by other groups;’ et al; ~ as part of an epidemiological training course. In The non-parametric nature of many indices of gin- this study the index proposed by Russell was used and the results clearly indicate that without any calibra- gival and periodontal disease prohibits statistical analysis using regular parametric statistical methods. tion or training the inter-examiner reliability was low. One possible solution is to apply statistical methods Later studies conducted by Smith et al., ’4 Alexander et ~6 which have been designed to analyse non-parametric al./5 and Shaw & Murray have shown that training data. = Another possibility is to tabulate the frequency programs can be effective in reducing inter-examiner with which the different scores are found. This type of as well as intra-examiner agreement in recording measurement is parametric in nature and can be gingivitis. analysed using parametric statistics. Whenevaluating the reliability of gingival indices remember that the first examination might influence Epidemiologyof Gingivaland Periodontal Disease the results of the following examination. This was in- dicated in a study by Birkeland & Jorkjend/7 where an Epidemiology has been defined as the study of dis- examiner examined the same children twice at two ease distribution and determinants in man.= A number hour intervals. The analysis showed that no differ- of reviews on the epidemiology of gingival and perio- ences were found between the number of gingival dontal disease have already been published in the lit- units recorded as 0. The number of gingival units erature, u,~.u The present review is limited to the preva-

84 EPIDEMIOLOGYAND INDICES Poulsen lence of gingivitis and periodontal disease in children already present during the first years of life. In one of with respect to such commonly used epidemiological these studies ~ three-year-old children from four differ- background variables as age, sex and geography. ent geographical areas in Denmarkwere examined. Of a total of 80 gingival units, 15 to 20 units were bleed- GeographicalVariation in Prevalenceof Gingival and ing on gentle probing. The accumulation of plaque was PeriodontalDisease also relatively high, 30 to 40 tooth surfaces out of 80 = were covered with a layer of plaque, which could be Russell and coworkers demonstrated that wide seen with the naked eye after careful drying (score variations in periodontal disease in a given age-group according~ to Silness & LSe). exists across the world. Similar conclusions were ~ A recent longitudinal Swedish study can be used to reached by Ramfjord et al. and Barmes." The general describe the situation from the age of three through trend was that some populations, especially in the Far school age. ~ In this study 162 children were followed East, were more likely to be affected by periodontal longitudinally and examined when they were three, disease than Europeans and North Americans. This four, and five years of age. has been substantiated by a series of epidemiological This study seems to indicate that the level of gin- studies performed in Sri Lanka during the last decade. ~ gival inflammation decreases through preschool age, In 1969 Waerhaug presented data which documented but preventive dental care programs now established a very high prevalence of periodontal disease in a in many Scandinavian municipalities may explain this sample of several thousand persons ranging in age decrease: the age-trend observed in this study may from 13 to over 60. When the data were compared to partly be due to better with increasing data for Norwegian students, periodontal disease was age. shown to be much more severe in Sri Lanka. When the One of the few surveys which includes data from same analysis was performed after adjustment for early childhood to the late teen-ages was published by differences in oral hygiene however, very small differ- Parfitt. ~ The PMA-index~ was used in a modified ences were found. form. A steady increase in the severity index was In a longitudinal survey conducted by LSe and co- noted from the age of three until the age of 13. From workers the baseline examination showed that the the age of 13 until the age of 17 a decrease in the number of gingival units with a score of 2 or more was severity of gingivitis was noted. almost seven times higher in Sri Lanka than in Nor- way.~ The same study showed that before the age of A large survey of a communityin the southern part of Sweden~ showed that in three-year-old children, 5% 20, loss of periodontal attachment was considerably of all surfaces showedbleeding gingiva on gentle prob- higher in Sri Lanka than in Norway. Whenthe annual rate of attachment loss was studied on a longitudinal ing. This percentage increased through the teen-ages and reached a level of about 35%at the age of twenty. basis, the individuals from Sri Lanka tended to lose Part of the explanation for the increase in gingivitis two to three times as much periodontal attachment during childhood may be found in data published re- per~ year as the individuals from Norway. cently by Mackler & Crawford~ and by Matsson; 9 In One of the explanations for the high prevalence of Matsson’s study six four-to five-year-old children and periodontal disease in early age in many developing six 23- to 29-year-old adults were studied. Before the countries could be a higher tendency toward initiation of the study, intense oral hygiene proced- formation. A recent epidemiological study of more than 600 6- to 15-year-old schoolchildren in one of the ures were practiced. This reduced the frequency of major cities in Sri Lanka showed that calculus was bleeding units to a very low level. During the study all found as early as age 6. 31 At the age of 15 more than oral hygiene procedures were stopped, and the devel- half of the six surfaces scored for calculus were cov- opment of plaque and gingivitis studied. In the chil- dren, no gingival inflammation developed over a ered by calculus. No data which would allow a direct twenty-one day period with no oral hygiene, while comparison with European or American populations marked gingivitis developed during the same period of seems available, but the general impression is that cal- culus is not found as frequently in these populations. time in the adults. A number of different explanations for this finding can be found, including different host responses to . Future studies should fur- Prevalenceof Gingivaland Periodontal Disease in Relationto Ageand Sex ther clarify this interesting aspect of the etiology of in children. Most of the early studies on the epidemiology of Some studies have shown less gingivitis in girls gingival and periodontal disease were limited to adult than in boys of similar age, while other studies have populations. This led to the view that periodontal dis- shown the opposite trend. Whether these differences ease is a disease of adulthood. More recent studies, are truly related to sex, or whether they only reflect however, have clearly demonstrated that gingivitis is the difference in oral hygiene or oral cleanliness be-

PEDIATRICDENTISTRY 85 Volume3, SpecialIssue Table7. Summaryof clinical studies on periodontitis in children and young adults.

Author Pocket Loss of Agein years (year) Population depth attachment 11-14 15 16 17

Sheiham4~ English ¯ 3 mm -- 11% 21% 28% 36% (1969) Downer~ English 24% ------(1970) Negro or ¯ 3 mm 45% ------mixed Axelsson~ et al. Swedish 4 mm -- -- 17% -- -- (1975) Bowden~ et al. English -- > 1 mm -- 47% -- -- (1973) Lonnon~ et a]. English -- 41% -- -- (1974) Non-European -- ¯ 1 mm -- 84% -- -- tween the two sexes~ seems open for discussion. were re-examined three years later, 44 to 68% of Gingivitis studies are important because this condi- the individuals showed loss of alveolar bone on tion may lead to irreversible breakdown of the perio- radiographs. Further studies seem to be indicated in dontal tissues. Since we are not, at the present time, this area. able to determine whether a given level of gingival in- Summary flammationin a given child will result in loss of perio- dontal attachment, our efforts at preventing periodon- 1. An index of gingivitis should be simple, easy to tal disease must be to obtain a general reduction in communicate to professionals, as well as laymen, the level of gingivitis. Thus, epidemiological data on and be amenable to simple statistical analysis. In- frequency of periodontal disease in individuals below dices which consider bleeding as the only diagnostic the age of twenty becomes important. criteria seem to fulfill these criteria and have The literature contains studies in which the pocket proven valid in a number of recent epidemiological depth has been recorded, studies where loss of attach- studies and clinical trials conducted on children. ment has been recorded and studies where bone-loss 2. Periodontal disease is most clearly expressed as loss has been determined on radiographs. Table 7 is a sum- of periodontal attachment measured from the mary of some of the more extensive epidemiological cemento-enamel junction to the bottom of the clini- studies published in the literatureY ,4~4~ As always, cal pocket: pocket depth should not be confused when data from various epidemiological studies are with loss of periodontal attachment. compared, due regard should be given to the inter-ex- 3. Gingival inflammation has been shown to increase in aminer reliability, and to the different criteria used. In prevalence and severity with increasing age. The rea- general, we can conclude that pockets of three to four sons for this are not well known now. Permanent, millimeters or more are found in 20 to 30%of 11 to 15- Table8. Summaryof radiographic studies on alveolar bone loss year-old children. in children. True loss of periodontal attachment has been re- corded in two British studies, also summarized in Prevalence of Table 7. Both studies included 15-year-old children, periodontal and the frequency of children with loss of attachment Author (year) Population bone loss of one millimeter or more was 40 to 47%.a.~ Three studies are available in which radiographic examination45, of loss of alveolar bone was performed. Hull*~ et al. 14 years 51% ,.,7 Similar diagnostic criteria in the diagnosis of bone (1975) English loss on bite-wing radiographs seem to have been em- Blankenstein 13-15 years ployed and the study populations seemed to be similar et~ al. English and Danish in many respects. However, prevalence of loss of al- (1978) veolar bone, varied from 1 to 51%of the individuals Davies4~ et al. 11-12 years 19-37% (Table 8). (1978) English When the individuals examined by Davies et alY

EPIDEMIOLOGYAND INDICES 86 Poulsen irreversible loss of periodontal attachment has been mutanase, Scand J Dent Rex, 86:93-102, 1978. recorded in up to 20% of 15-year-old children. 19.Poulsen, S., Holm-Pedersen, P. & Kelstrup, J.: Comparison of different measurements of development of plaque and gingivitis 4. When the influence of such factors as sex, socio- in man, Scand JDent Rex, 87:178-183, 1979. economic background, medical disorders etc., on 20. L~e, H. & Holm-Pedemen, P.: Absence and presence of fluid gingival inflammation are to be studied, due regard from normal and inflamed gingivae, Pedodontics, 3:171-177, should be given to oral cleanliness. Comparing dif- 1965. ferent population groups should be done only for 21. Barbano, J. P. & Clemmer, B. A.: A comparison of analysis of individuals with the same level of plaque. dichotomous and severity data of clinical trials using dental data, JPedodont Rex, 9:129-142, 1974. 5. Loss of periodontal attachment is always preceded 22. Conover, W. J.: Practical non-parametric statistics, NewYork, by gingival inflammation, therefore the ultimate London, Sydney, Toronto,: John Wiley & Sons, 1971. goal of preventing gingival inflammation is to pre- 23. MacMahon, B. & Pugh, T. F.: Epiderrdology: Pdncicplex and vent irreversible break-down of the periodontal Methods, Boston: Little, Brown and Co., 1970. Lb’e, H.: Epidemiology of periodontal disease. An evaluation of structures. 24. the relative significance of the etiological factom in the light of recent epidemiological research, Odont T, 71:480-503, 1963. Dr. Poulsen is head of the Department of Pedodontics and Pre- 25. Russell, A. L.: World epidemiology and oral health, In: ventive Dentistry, Royal Dental College, Vennelyst Boulevard, Kreshover, S. J. & McClure, F. J.: Environmental va~ablex in KD-8000 Aarhus C, Denmark. oral disease, Washington, American Association for the Advancementof Science, pp 21-39, 1966. References 26. Ramfjord, S. P., Emslie, R. D., Greene, J. C., Held, A.-J. & Waer- 1. Russell, A. L.: Epidemiology and the rational bases of dental haug, J.: Epidemiological studies of periodontal diseases, AmJ Publ Hoslth, 58:1713-1722, 1968. public health and dental practice, In Young & Striffler, The , His Practice, and His Community, London, Toronto: 27. Barmes, D. E.: Epidemiology of dental disease, J Clin Pedodont, W. B. Saunders Company,Philadelphia, 1969, pp 35-62. 4: 80-93, 1977. 2. L~e, H. & Silness, J.: Periodontal disease in . I Preva- 28. Waerhaug, J.: Prevalence of periodontal disease in Ceylon, Acta lence and severity, Acta Odont Scand, 21:533-551, 1963. Odont Scoand, 25:2005-231, 1967. 3. Suomi, J. D. & Barbano, J. P.: Patterns of gingivitis, J Pedodon- 29. L~ie, H., Anerud, A., Boysen, H. & Smith, M.: The natural his- tel, 39-71-74, 1968. tory of periodontal disease in man, J Pedodont Rex, 13:550-562, 4. Suomi, J. D.: Periodontal disease and oral hygiene in an institu- 1978. o o tionalized population: Report of an epidemiological study, 30. Lge, H., Anerud, A., Boysen, H. & Smith, M.: The natural his- J Periodontol, 40:5-10, 1969. tory of periodontal disease in man, J Pedodontol, 49:607-620, 5. Saxer, U. P. & Miihlemann, H. R.: Motivation und AufklhLrung, 1978. Schweiz Monatsschr Zahnheilkd, 85:905-919, 1975. 31. Amaratunge, A.: Oral health in a group of schoolckdldren resid- 6. Ainamo, J. & Bay, I.: Parodontalindices for og i praksis, Tand- ing in Kandy, Sd Lanka, Thesis, University of Sri Lanka 1980. laegebladet, 80:149-152, 1976. 32. Poulsen, S. & M~ller, I. J.: The prevalence of dental caries, 7. L~e, H.: The Gingival Index, the Plaque Index and the Reten- plaque and gingivitis in 3-year-old Danish children, Scand J tion Index Systems, J Pe~odontol, 38:610-616, 1967. Dent Rex, 80: 94-103, 1972. 8. Russell, A. L.: A system of classification and scoring for preva- 33. 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Pedodontol,38:592-598, 1967. 13. Davies, G. N., Kruger, B. J. & Homan,B. T.: An epidemiological 37.Axelsson,P., G~iland, U., Hugoson, A., Koch, G., Paulander,G., training course, Aust Dent J, Feb.:17-28, 1967. Pettersson,S., Rasmussen,C.-G., Schrnidt, G. & Thilander,H.: 14. Smith, L. W., Suomi, J. D., Greene, J. C. & Barbano, J. P.: A Tancll/~soti]lst~ndethosi000 personer i ~Idrarna3 till70 ~tr study of intra-examiner variation in scoring oral hygiene status, inomJb’nkgpings kommun, Tandl’~ikartidningen, 67:656-666, gingival inflammation and epithelial attachment level, J Pedo- 1975. dontol, 41-:11-14, 1970. 38.Mackler,S. B. & Crawford,J. J.:Plaque development and gingi- 15. Alexander, A. G., Leon, A. R., Ribbons, J. W. & Morganstein, S. vitisin theprimary dentition, JPeriodontol, 44:18-24, 1973. 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PEDIATRICDEI~ITISTRY 87 Volume3, Special Issue 43. Bowden, D. E. J., Davies, R. M., Holloway, P. J., Lennon, M. A. 46. Blankenstein, R., Murray, J. J. & Lind. O. P.: Prevalence of & Rugg-Gunn, A. J.: A treatment need survey of a 15-year-old in 13- to 15-year-old children. A population, Brit Dent J, 134:375-379, 1973. radiographic study, J C1in Periodontol, 5:285-292, 1978. 44. Lennon, M. A. & Davies, R. M.: Prevalence and distribution of 47. Davies, P. H. J., Downer, M. C. & Lennon, M. A.: Periodontal alveolar bone loss in a population of 15-year-old schoolchildren, bone loss in English secondary school children. A longitudinal J Clin Perlodontol, 1:175-182, 1974. radiological study, J ClJn Periodontol, 5:278-284, 1978. 45. Hull, P. S., Hillam, D. G. & Beal, J. F.: A radiographic study of the prevalence of chronic periodontitis in 14-year-old English schoolchildren, J Clin Periodontol, 2:203-210, 1975.

EPIDEMIOLOGYAND INDICES 88 Poulsen