Periodoiltology 2000, Val.

2, 1993, 57-71 Printed in Denntnrk All rights reserved

PERIODONTOLOGY 2000
ISSN 0906-6713

Prevalence, extent, severity and progression of periodontal disease

L. JACKSON BROWN & HARALD LOE

Introduction
Epidemiology is the science concerned with the factors that influence the distribution and occurrence of health, disease and mortality among groups of individuals. Groups of interest range in size from small populations (such as local communities, worksites or schools) to large subnational aggregates (such as states, regions, occupations or socioeconomic strata) to entire countries. A frequent measure of disease used in epidemiological studies is prevalence (49, 54, 57, 63, 109). It is the proportion of individuals in a group who exhibit the condition at a point in time. The total number of individuals with the condition is frequently referred to as the prevalence also but should be distinguished from the proportion. Prevalence is estimated from cross-sectional surveys. The periodontal status of an individual, much less a group, is difficult to describe concisely. To thoroughly characterize periodontal status, epidemiological studies assess numerous sites throughout both arches on several clinical conditions for each individual. Epidemiological assessment of a group of individuals requires a summary of the periodontal status over individual sites in the mouth. Development of summaries must deal with the thorny issues of case definition as well as the number and types of sites to assess (14, 30, 41). The effect of fallible measurement techniques is also an important issue and is discussed elsewhere in this volume. Before the prevalence of periodontal disease can be described, a case of disease must be defined. This requires consideration of severity (such as amount of inflammation or attachment loss) as well as the extent (the percentage or number of affected sites). Although all epidemiological studies use some combination of the concepts of prevalence, extent and

severity to describe the periodontal status of a population, various studies have assessed and combined these concepts differently. It is difficult to compare the results from studies that use different measurement methods or case definitions, and comparison can be misleading if the effects of the different methods are ignored. Cross-sectional surveys identify previous tissue destruction from past disease. Identification of disease progression requires repeated measures of clinical attachment level (27, 33, 34, 95, 98). The average rate of progression or percentage of sites that progress are two usual outcome measures. The length of time between measurements is an important issue in the design of longitudinal studies. Studies that examine subjects at yearly or longer intervals can assess the average rate of disease progression or the percentage of sites that progress, but the intervals may be too long to conclusively identify specific patterns of disease activity (119). Selection of the sites around the dentition with which to calculate summary measures is another important methodological issue. Since the number of sites that could be measured is large, a judicious selection of sites that minimizes loss of information from partial recording is often necessary. Although a number of studies have compared various combinations of sites to indicate overall periodontal status, additional research is needed to better assess the information lost from various partial recordings. It is currently known that prevalence is potentially underestimated with partial recording. However, the degree of underestimation varies widely, depending on factors such as the severity level at which the disease is assessed and its true distribution within and between individuals (23, 52). Compared with prevalence, the estimates of extent or severity are less influenced by partial recording.

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Brown & Loe

This chapter reviews the summary measures that have been used in epidemiological studies and describes the epidemiology of gingivitis and periodontitis and the progression of periodontitis. The methodological issues discussed here should be kept in mind when the results of the various studies are evaluated.

Brief review of periodontal disease measures

Early studies of periodontal disease did not have well defined criteria for measuring variations in periodontal conditions (74, 94, 95). Beginning in the late 1940s and early 1950s indices were developed that established some uniformity in the classification of gingival and periodontal status. Massler et al. (80, 81) developed the PMA Index, which uses the sum of papillary, marginal and attached gingival units affected with inflammation to characterize the gingival status of an individual. The average PMA score is used to describe a population. By counting the number of sites, the PMA introduced the concept of extent of disease as part of the assessment of gingivitis. More recently, Loe & Silness (68, 75) developed the Gingival Index as a further refinement of gingival assessment. The Gingival Index incorporates assessment of both the extent (number of sites) and the severity of inflammation to describe gingivitis. Four areas are scored for each tooth: the distofacial papilla, the facial margin, the mesiofacial papilla and the entire lingual margin. Inflammation is scored at 3 levels of severity, based on visual signs as well as bleeding assessed with a probe. Bleeding on probing has proved to be a popular method for assessing gingival inflammation because it is an early sign of gingival inflammation (31, 32,90) and is a relatively objective measure of outcome. The Gingival Index is sensitive to rather small variations in gingival status and allows calibration of examiners against well defined criteria. Two widely used indices of overall periodontal status are the Periodontal Index (110) and the Periodontal Disease Index (103, 105). With the Periodontal Index, each tooth is visually assessed for gingivitis and periodontitis. Gingivitis is scored at two levels, based on the extent of inflammation around a tooth. Inflammation that does not completely circumscribe a tooth is scored as 1; a score of 2 represents completely circumscribing inflammation. Severity, as indicated by the degree of inflammation at

a site, is not scored. A score of 6 indicates a tooth with a periodontal pocket and 8 indicates advanced periodontal destruction. The site around the tooth where the pocket is located is not identified. With the Periodontal Disease Index, Ramfjord introduced the measurement of clinical attachment level into epidemiological indices. Six teeth, chosen because they are believed to adequately represent the periodontal status of the overall dentition, are assessed. Gingivitis is scored visually from 0 to 3, depending of the extent and severity of gingival inflammation. Clinical attachment level is measured with a periodontal probe, usually at 4 sites around each tooth. Two separate measurements are taken at each site: one from the crest of the gingiva to the cementoenamel junction and the second from the crest of the gingiva to the bottom of the gingival sulcus. Attachment loss is calculated indirectly from those measures. The gingivitis score is not used if attachment loss is 3 mm or greater. Both the Periodontal Index and the Periodontal Disease Index combine assessment of gingivitis and periodontitis into a single index. Gingivitis is scored for teeth without periodontitis but is not recorded for teeth with periodontitis. The underlying assumption is that gingivitis progresses to periodontitis unless treated and periodontitis does not occur without gingivitis. Combining the measurement of the 2 diseases is no longer considered appropriate, given current understanding of the disease process. With both indices, average scores are calculated to describe the individual. These averages are averaged to describe the population. Over the past decade, most major epidemiological studies in the United States have included separate clinical measurements for gingivitis and periodontitis. Recent national surveys conducted by the US National Institute of Dental Research (NIDR) and the US National Center for Health Statistics used bleeding elicited by gentle probing to indicate gingivitis (68) and the method of indirect measurement of clinical attachment level with a periodontal probe to assess periodontitis (85). This approach allows more flexibility in deriving separate measures of prevalence, extent and severity of periodontitis and gingivitis. Nevertheless, case definitions are still required. For example, a recent estimate of the prevalence of early or incipient periodontitis based on the NIDR survey required at least one site with clinical attachment loss of 2 2 mm before the person is considered a case (85).Other recent estimates of prevalence are based on clinical attachment loss of 2 1 mm, 2 3 mm and 2 5 mm (11). The

58

Prevalence, extent, severity and progression

severity and extent of disease required for a case influence estimates of prevalence, extent and average severity of affected sites. Some forms of periodontal disease require consideration of the pattern of clinical conditions as well as the extent and severity. Case definitions of rapidly progressing adult periodontitis require multiple sites of moderate to severe attachment loss throughout the dentition (69).Localized juvenile periodontitis requires severe clinical attachment loss (4-5 mm or greater) at interproximal sites of first molars andlor incisors, whereas generalized juvenile periodontitis requires extensive clinical attachment loss on teeth other than first molars and incisors (24, 72). In practice, textbook cases are rarely observed; subtle variation in attachment loss patterns are common, with the result that some individuals are difficult to classify. Several advances in the measurement of periodontal disease are under development. Probes that apply a controlled amount of force to the tissues when inserted into the periodontal sulcus are available (45, 77, 93). Another probe under development will automatically detect the cementoenamel junction and measure the distance from the junction to the bottom of the sulcus (43). The results of studies using these probes will be published soon. Also being developed are techniques to take repeated radiographs from positions that are in almost identical geometric relation to the dentition (44,55,92). These radiographs can be digitized on computers and used to calculate the bone loss occurring between repeated radiographs with much better accuracy than possible with routine radiographs. Analysis of the constituents of gingival crevicular fluid holds promise for a more refined characterization of sites with subclinical disease and activities for the development of an etiological basis for the classification of periodontal disease (19, 59, 60, 88, 89, 102). Harvesting gingival crevicular fluid constituents from saliva will be possible one day, further simplifying collection. Such advances will improve the validity and reliability of disease measurement and the accuracy of estimates from epidemiological studies.

Epidemiology of gingivitis
Prevalence and extent Early epidemiological studies of gingivitis were mostly conducted on children. Estimates of prevalence varied widely. In a 1933 survey of schoolchildren aged 6 to 14 in the United States reported by Messner

et al. (84), less than 9.0% of the children had gingivitis. Brucker (121, in the early 1940s, reported a similar estimate of the prevalence of gingivitis among children aged 4 to 16 in Newark, New Jersey. In contrast, during the 1930s, Westin et al. (129) reported that nearly 90% of Swedish children had gingivitis. King & Francklyn (51) reported a 1941 study that found wide variation in severe gingivitis among London children. Thirty-four percent of children evacuated to London from Gibraltar during the Second World War exhibited gingivitis as compared with only 9% of London children. In 1949, Marshall-Day and Shourie (78) reported nearly universal gingivitis in Indian boys under 17 years of age. These early studies were conducted without probability sampling techniques and with only crude criteria for case definition. Given these methodological limitations, little can be concluded about the relative validity of these studies except that the variation in prevalence estimates is more likely due to differences in methods than to actual variation in disease. Beginning in the early 1950s, studies were reported using criteria that established some uniformity to the classification of cases of gingivitis and a little more consistency to the results. Several studies using well defined criteria for gingival assessment were conducted on subnational United States populations, mostly children. In the early 1950s, Massler et al. (80, 81) used the PMA Index to study gingivitis in children aged 2 to 16 years in Chicago and Philadelphia. With the PMA Index, Massler et al. (80, 81) reported not only that around 80% of children in Chicago exhibited gingivitis compared with 60% of children in Philadelphia, but also that, on average, 9 sites were affected in children in Chicago compared with 5 sites in children in Philadelphia. Jamison (42) used the Periodontal Disease Index to measure the periodontal status of deciduous teeth among children aged 5 to 14 years in Tecumseh, Michigan. Over 70% of the children had gingivitis. Broken down by pattern, 27% had localized, 20% had generalized and 28% had scattered gingivitis. It was unknown whether the gingivitis around deciduous teeth resulted from microbial plaque or from the natural process of exfoliation of the deciduous dentition followed by the eruption of permanent replacements. Ayers et al. (1)found a prevalence of gingivitis of less than 15% among very young children (aged 2-5 years) who had not begun their mixed dentition. In 1976-1977, the oral health of North Carolinians was surveyed (39). Because probability sampling was used, the participants were considered representative of the population of the state. The ages of those

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Brown & Loe

examined ranged from 5 years to over 70 years, allowing periodontal status to be reported for adults as well as children. The Periodontal Index was used to measure the periodontal status. Gingivitis was defined as being present when at least one tooth scored 1 or 2 and none of the teeth scored 6 or 8 on the Periodontal Index. The prevalence of gingivitis ranged from 20% to over 50%, varying by age, gender and race. Since the gingival score was not recorded for the teeth with periodontitis, the prevalence of gingivitis was probably underestimated. Over the years, several European studies of gingivitis have also been reported. McHugh et al. (82) reported that 99% of 13-year-old children in Dundee, Scotland had gingivitis. Gibson et al. (25) reported a prevalence of marginal gingivitis of nearly 50% among children aged 5 years in England. Muhlemann & Mazor (86),in 1958, reported that the prevalence of gingivitis among 13-year-old children in Switzerland was 93%. Curilovic et al. (18) reported a similar prevalence for children in Switzerland in 1977. In a 1969 report, Bjorby & Loe (6) used the Gingival Index to determine that only 4 of a sample of 1038 children in Sweden aged 9 to 16 years were free of gingivitis. Some years later, Hugoson et al. (40)reported prevalence rates of gingivitis of 35% and 64% among 3- and 5-year-old children in Sweden, respectively. A national survey in Denmark in 1981 examined a sample of 3020 people who represented Danes aged 16 to 80 years. Using this survey data, Kirkegaard et al. (53) reported that about 50% of the population had gingivitis. About 5% of assessed gingival units were inflamed. Outside of the United States and Europe, high prevalences of gingivitis have also been reported, both in industrialized and developing countries. Cutress et al. (21) found that over 96% of a sample in New Zealand aged 15-19,25-29 and 35-44 had gingivitis. Gingivitis was reported at 34% of all sites scored. Gingivitis was exhibited by 79% of those aged 15 to 19 years. Spencer et al. (118) reported an 85% prevalence of gingivitis among 5- and 6-year-old children in Australia. Among developing countries, gingivitis was nearly universal in Israel (108), Sri Lanka (128) and India (29, 104) and extremely prevalent in Ethiopia (671, Nigeria (116) and Tanzania (62). National probability oral epidemiological surveys of the United States were conducted in 1960-1962, 1966-1970, 1971-1974, 1980, 1981, 1985-1986 and 1986-1987. These surveys provide the most comprehensive data on the periodontal status of the United States population. The Health Examination Survey, conducted from 1960 to 1962, sampled and examined

7400 survey participants, representing over 24 million children in the United States aged6-11 years. Russells Periodontal Index was used to assess periodontal status. Using data from the survey, Kelly & Harvey (46) reported that the average Periodontal Index scores for the children ranged fromO.O to over 2.0. Approximately 60% of the children had an average Periodontal Index of zero, indicating that they were free of periodontal disease. About 37% of the children had mild gingivitis, as estimated by a Periodontal Index score between 0.1 and 1.0 (47). Another sample of 7710 adults aged 18to 79 years, representing approximately 90 million people, were also examined as part of the Health Examination Survey. Across all ages, about 48% of adults had gingivitis (48). From 1966-1970, the US National Center for Health Statistics conducted a national probability survey of the oral health of youths 12 to 17 years. Once again, the Periodontal Index was used to assess periodontal status. A sample of 7514 participants were examined, representing around 23 million youths in the United States. From these data, Sanchez (111) reported that 62% exhibited gingivitis, as indicated by Periodontal Index scores between 0.1 and 1.0. This is almost double the prevalence found in 1960-1962 among children aged 6 to 11 years but comparable to the prevalence of gingivitis among 18to 24-year-old adults examined in 1960-1962. The US National Center for Health Statistics conducted the National Health and Nutrition Examination Survey I from 1971 to 1974. Approximately 20,000 people, representing almost 194 million people in the United States aged 1-74 years, were examined. Twenty-four percent of people aged 6 to 74 years exhibited gingivitis. According to age, 14% of children 6-11 years old and 32% of youths 12-17 had gingivitis. The percentage of adults with gingivitis ranged from 29% for the youngest to 13%for the oldest people. Douglass et al. (22) reanalyzed the periodontal data on adults from the Health Examination Survey and the National Health and Nutrition Examination Survey I and concluded that the prevalence of adult gingivitis had declined between the two surveys. The decrease in gingivitis resulted almost entirely from the increase in the percentage of adults who were free of periodontal disease. The percentage of persons exhibiting periodontitis was about the same in both surveys. The authors noted that the decline could represent a real improvement in gingival health or could result from systematic differences in the measurement of gingival inflammation in the two surveys.

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Prevalence, extent, severity and progression

n No Disease t 4 Gingivitis
EPeriodontitis

11731

Table 2. Percentage of schoolchildren with at least one site with gingivalbleeding by age and sex, United States, 1986-1987. Source: Bhat (5) Age hears) Male Female Total
14 15 16 17 64.9 63.0 60.6 57.4 61.5 58.4 55.3 54.3 56.3 56.0 61.7 59.2 57.5 56.9 58.8

All

Age, 19-44

45-64

65

All

Fig. 1. Distribution of periodontal disease by the percentage of people and the most severe condition according to age in the United States in 1981 (data from the 1981 US Health Resources and Services Administration study on dental

health outcomes related to prepayment)

In 1981, the US Health Resources and Services Administration (HRSA) conducted a national probability household survey to assess dental prepayment, utilization and oral health status. A sample of 2428 households with 7078 individuals, representing approximately 206 million people in the United States aged 3 years or older, was selected. Russells Periodontal Index was modified to assess gingivitis and periodontal pocket depth separately. Gingivitis was assessed with the usual visual criteria and was recorded for every tooth. Pocket depth was measured with a probe at the mesiofacial site of each tooth. Using the data from that survey, Brown et al. (10) reported that gingivitis without accompanying periodontitis (no pockets 2 4 mm) was detected in 50% of the adults aged 19 years or older (Fig. 1).Gingivitis declined with age from 54% among people 19 to 44 years old to 44% among people 45 to 64 years old to 36% among people 65 years or older. Only 15% of the

population aged 19 or older had neither gingivitis nor periodontitis. As for the extent of gingivitis, 60% of the population had 6 or more teeth affected (Table 1). Thirty-six percent had 11 or more teeth affected, and 22% had 16 or more teeth affected. People 19 to 44 years old had the highest percentage of individuals with extensive gingivitis. The NIDR conducted the National Survey of Oral Health of US Employed Adults and Seniors in 1985-1986. A final probability sample consisted of 15,132 people, representing approximately 100 million employed people in the United States. Gingivitis was determined by gently inserting a periodontal probe no more than 2 mm into the gingival sulcus just distal to the midpoint of the tooth and moving it into the mesial interproximal area. Brown et al. (11) reported that approximately 44% of the employed population between 18 and 64 years old had gingivitis. Gingivitis tended to decrease slightly with age and occurred at an average of 2.6 sites per person, which is less than 6% of all sites scored. Only 3.3% of sites with gingivitis also had periodontal pockets 2 4 mm, and 11.6% of gingivitis sites also exhibited gingival recession. Bhat (5) described the periodontal health of 14- to 17-year old people who were examined in the NIDR National Survey of Oral Health in US Schoolchildren conducted in 1986-1987. Gingivitis was assessed using the same method used in the 1985-1986 NIDR

Table 1. Extent of gingivitis: percentage of people by number of teeth with gingivitis by age in the United States. Source: Brown et al. (10) (data from the 1981 US Health Resources and Services Administration study on dental health outcomes related to prepayment) Age group (years) Number of teeth 1944 45-64 265 All ages
0 1-5 6-10 11-15 216

18.5 (3.9) 20.0 (2.7) 23.2 (2.3) 13.4 (1.9) 25.0 (4.1)

15.6 (3.2) 28.2 (3.5) 24.2 (2.5) 15.6 (2.6) 16.4 (3.8)

19.5 (4.8) 22.1 (5.6) 25.1 (3.5) 16.8 (3.9) 16.5 (6.0)

17.9 (3.2) 22.3 (2.3) 23.6 (1.5) 14.4 (1.5) 21.9 (3.0)

Teeth with periodontal pockets 4 mm or deeper are classified as having periodontitis and are not counted as having gingivitis. Standard errors adjusted for sample design are in parentheses.

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Brown & Liie

survey. The prevalence of gingivitis was close to 62% for all ages (Table 2). Approximately 6% of all sites scored had gingivitis, which was most common in the molar areas in the maxilla and the incisor areas in the mandible (Table 3). Traditionally, the prevalence of gingivitis has been thought to increase with age until adulthood, possibly registering a jump during the pubertal years. Among adults, gingivitis was thought to decrease slowly with age (42, 81, 86). An apparent reciprocal relationship between the prevalence of gingivitis and periodontitis across the age spectrum led to the assumption that gingivitis typically progressed to periodontitis (94). Using National Health and Nutrition Examination Survey 1 data, Kelly & Harvey (46) reported that 14% of children aged 6-11 in the United States had gingivitis without pockets. The presence of gingival inflammation increased to 32% among those aged 12-17 vears and then declined with increasing age among adults. The findings from the National Dental Caries Prevalence Survey conducted by NIDR in 1979-1980 suggest that 92% of all schoolchildren age 5 to 17 years had mild or moderate gingival inflammation that would benefit from improved oral hygiene or professional care (125). The percentage with gingivitis remained relatively stable from the youngest to the oldest children; however, the severity of gingivitis increased slightly with age. National probability survey data from the mid1980s indicated that the prevalence of gingivitis in people 14 to 17 years old varied around 60% without a clear relation to age (5). Among employed adults in 1985-1986, the prevalence of gingivitis decreased slightly, from around 50% of people aged 18-24 years to about 40% in people aged 40 years or older (85). Among people aged 65 or older, gingivitis affected just under 50% of the population, regardless of age. The percentage of sites (extent) with gingivitis varied little with age. About 6% of sites were inflamed in people aged 14 to 17 vears and among employed adults aged 18 to 65 or older (5, 85). The percent of
Table 3. Percentage of sites with gingival bleeding in schoolchildren by age and sex, United States, 1986-1987. Source: Bhat (5)

sites inflamed among people aged 65 years or older was slightly larger, around 10%. Males had a higher prevalence of gingivitis than females regardless of age. Among youths, the difference was only slight. Among employed adults aged 18-65, almost 10% more men than women had gingivitis, the difference being more pronounced in the older age groups. Similarly, almost 10% more men than women had gingivitis among these 65 years or older. In other words, in both employed adults and elderly people, gingivitis was slightly more extensive among men. According to data from the 1986-1987 NIDR survey (51, non-white youths, mostly blacks, had a higher prevalence of gingivitis than white youths in each age and gender group. Among employed adults aged 18 years and older, 52% of blacks compared with 42% of whites exhibited gingival inflammation at one or more sites. Racial differences in prevalence were apparent in most age groups, from youngest to oldest. However, notable differences in the extent of gingivitis were not observed between employed blacks and whites; about 5% of gingival sites were inflamed among employed whites of all ages and about 1% more gingival sites were inflamed among blacks. A consistent racial difference in the prevalence of gingivitis was not apparent between elderly blacks and whites; however, elderly blacks had significantly higher percentages of inflamed sites.

Summary National probability surveys in the United States and Denmark found that gingivitis affected about 60% of teenagers and 40-50% of adults. Only about 5-6% of gingival sites were inflamed. Different measurement methods as well as other methodological factors, including partial recording, could have influenced these estimates. Despite methodological differences, the findings are rather consistent and lend confidence to the results of the surveys as a body of knowledge. Earlier estimates of prevalence, based on studies of subnational populations from the 1950s through 1960% were somewhat higher, on the whole, than estimates from the national surveys. Whether these differences represent improvement in gingival health or reflect different measurement and sampling techniques is unknown. Oral hygiene has certainly improved in most industrialized countries, lending credence to the notion that actual improvement may have occurred. However, many measurement issues

Age (vears)
14 15 16 17 All

Male 6.9
6.6 6.6 6.2 6.6

Female 5.5
~ ~~~~

Total 6.2
5.7
5.9 5.6 5.8

4.7 5.1 5.0 5.1

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Prevalence, extent, severity and progression

remain, and more precise estimates of gingivitis have to await improved methods of assessment. Surprisingly little variation in the prevalence of gingivitis by age is apparent from the recent national surveys in the United States. The earlier belief that gingivitis increased with age until the teenage years and then slowly decreased in a reciprocal relationship to the increase in the prevalence of periodontitis is not supported by data from the national surveys. Data from the United States surveys do indicate that a higher percentage of men have more extensive gingivitis than women and a higher percentage of blacks have more extensive gingivitis than whites. The picture may be very different in developing countries. Recent data, based on national probability surveys, are not available. The studies reported suggest that gingivitis may be highly prevalent, extensive and severe throughout much of the developing world.

Epidemiology of early-onset periodontitis

According to the American Academy of Periodontology (87), early-onset periodontitis is distinguished from adult periodontitis by its onset before the age of 35 years, rapid rate of progression, defects in host defense and the composition of its microbial plaque. Prepubertal periodontitis, juvenile periodontitis and rapidly progressive periodontitis are all considered forms of early-onset periodontitis.

Prevalence
Prepubertal periodontitis is a recently described form of periodontitis (97, 100, 117, 122, 128). The disease is rare and exhibits both a generalized and a localized pattern of attack (97). The generalized form affects deciduous and permanent teeth and is thought to start soon after the eruption of the deciduous dentition. The localized form affects only the deciduous dentition and is less aggressive. To date, information about these diseases has been derived from clinical cases. Little is known about the prevalence or distribution of these diseases in the general population. Juvenile periodontitis is a relatively infrequent periodontal disease. It first occurs in adolescents around puberty and is characterized by gingival inflammation and severe angular bony defects, resulting in pronounced loss of periodontal attachment

during adolescence (13, 28, 73, 74, 96, 114). The very rapid rate of periodontal destruction often results in tooth loss before the age of 20 years. Although substantial progress has been made in understanding the microbial and immunological mechanisms of the disease (2, 16, 24, 50, 64, 83, 89, 1011, clinical diagnosis is usually made by the distribution of bone loss and age of onset. Two forms of the disease have been identified (15, 24, 100, 125). Localized juvenile periodontitis is characterized by bone loss around the incisors, first molars and the mesial surface of the second molars. A more generalized pattern of periodontal destruction, involving teeth other than incisors and first molars, is recognized as generalized juvenile periodontitis (38). Estimates of the prevalence of juvenile periodontitis vary greatly (20, 66, 74). Recent epidemiological studies of Nordic populations reported prevalence rates of 0.2% for Norway (35), 0.1% for Finland (115) and 0.1% for Denmark (37). Blankenstein et al. (8) reported 0.06% in children in England and Denmark, and Van der Velden et al. (126) reported between 0.1% and 0.2% for children in the Netherlands. Two studies of populations in Nigeria reported prevalence rates of 0.75% and 0.8% in children 12 to 20 years old (36, 76). A prevalence of 3.7% was estimated for children 15-16 years old in Brazil (26). Kowashi (56) reported a prevalence rate of 0.47% for university students in Japan aged 19 to 28 years. Barnett et al. (3) found that 2.4% of patients aged 13 to 30 years at a United States dental school had juvenile periodontitis. Cianciola et al. (17) reported juvenile periodontitis among 9.8% of insulin-dependent diabetes mellitus patients and 1.7%of non-diabetic controls at an outpatient dental clinic of a large childrens hospital. Lacy & Brasher (58) estimated a prevalence of 0.4% among a United States military population. These previous studies vary in the diagnostic criteria used (patterns and severity of attachment loss, microbial and immunological assay), clinical methods for measuring the periodontal attachment (visual assessment, radiographs and probing), the types of population studied (patients, schoolchildren, military and young adults), the ages of the individuals assessed and the sample selection method (convenience versus probability). Any combination of these differences could explain the variation in the prevalence rates. Loe & Brown (72) estimated the prevalence of both localized and generalized juvenile periodontitis, based on a national survey of the oral health of United States children aged 5-17 conducted by the

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NIDR during the 1986-1987 school year. The sampling frame for the survey consisted of all children in grades kindergarten through 12 enrolled in public or private schools. A multi-stage probability sample was selected to represent 43 million children in these age groups. A total of 11,007 individuals aged 14-17 years were periodontally assessed and used in the analysis. Their patterns of loss of periodontal attachment, as assessed by probing at mesial sites, were used to classify children as cases of juvenile periodontitis. Missing teeth were not included as part of the classification. The criteria were similar to those used by Loe et al. (701, with some adjustments for the young age of the population. An individual was classified as a case of localized juvenile periodontitis if at least one first molar and at least one incisor or second molar and two or fewer cuspids or premolars had 2 3 min loss of attachment. An individual was classified as a case of generalized juvenile periodontitis if 4 or more teeth had 2 3 mm loss of attachment and if 2 affected teeth were second molars, cuspids or premolars. Juvenile periodontitis was rare among United States schoolchildren aged 14-17 years. Of 11,007 schoolchildren, 50 were classified as cases of localized juvenile periodontitis and 14 were classified as having generalized juvenile periodontitis (Table 4 ) . Approximately 0.5% of adolescents nationwide were estimated to have localized juvenile periodontitis and 0.13% were estimated to have generalized juvenile periodontitis. Although these prevalence rates

were small, the total number of children affected was not trivial. Close to 70,000 adolescents in the United States were estimated to have localized juvenile periodontitis in 1986-1987. More destructive generalized juvenile periodontitis effected a n estimated 17,000 children. From these prevalence data, Loe & Brown (72) estimated that the incidence of localized juvenile periodontitis between 14 and 15 years of age was 1.3 per 1000 people at risk. Case series have generally found that girls are more likely than boys to have juvenile periodontitis by ratios of approximately 2.5 : 1. Some population studies also report a higher prevalence among girls than boys (3, 38). One reason may be that puberty starts earlier in girls, which may lead to a n earlier onset of juvenile periodontitis and greater prevalence rates in young age groups (114). However, marked differences in gender-specific prevalence rates have not been confirmed in studies with well-defined diagnostic criteria carried out with probability samples (112). A racial association has been observed in several populations. For example, a survey of children in England found the prevalence of juvenile periodontitis to be 0.1% for whites, 0.2% for Asians and 0.8% for blacks (113). Studies of populations in Africa report a prevalence in the 0.8% range (36, 76). Based on a 1986-1987 NIDR survey of the oral health of United States children, the percentage of adolescents with localized juvenile periodontitis increased until age 16 years (72). Generalized juvenile periodontitis did not show a n association with age.

Table 4. Prevalence of periodontitis in children 14-17 pears of age, United States (NIDR 1987).Source: Loe & Brown
(72)

Number Population Classification in sample estimate Localized juvenile periodontitis 50 69,748 (29,228)' Generalized juvenile periodontitis 14 16,781 (8,689) Incidental loss of attachment 175 212,386 (53,439) *Standard errors, adjusted for complex sample design, are in parentheses.

Percentage of people 0.53 (0.22) 0.13 (0.066) 1.61 (0.41)

Table 5. Prevalence of periodontitis in children 14-17 years of age by race, United States (NIDR 1987). Source: I,Oe & Brown (72) Crude estimated prevalence odds ratio black :white* 15.1 (8.2-28.2) 24.6 (6.0-101.1) 5.5 (4.0-7.4)

Classification Localized juvenile periodontitis Generalized juvenile periodontitis Incidental loss of attachment *95% confidence intervals are listed in parentheses.

Black 2.05
0.59 4.63

White
0.14

0.03
0.91

Prevalence, extent, severity and progression

The percentage of boys and girls with localized juvenile periodontitis or generalized juvenile periodontitis were not statistically different. Blacks were 15 times more likely than whites to have localized juvenile periodontitis and 22 times more likely to have generalized juvenile periodontitis (Table5). Hispanic children were 2.4 times more likely to have localized juvenile periodontitis than non-Hispanics.

Summary
Localized juvenile periodontitis is a rare disease affecting 1 or 2 adolescents per 1000. The generalized form of the disease is even more rare. Studies of community populations do not distinguish an increased risk for juvenile periodontitis, based on gender. Blacks, however, are several times more likely to have both patterns of the disease than whites.

Epidemiology of adult periodontitis

Prevalence, extent and severity Early studies provided wide ranges in estimates of the prevalence of adult periodontitis. Most studies have found that periodontitis affects a significant percent of individuals before the age of 20. The studies reported that the prevalence and average severity of periodontitis increased with age for groups of individuals until virtually all middle-aged people had the disease. In 1918, Black (7) assessed alveolar bone resorption from radiographs on 600 Chicago residents. Thirteen percent of those aged 20-24 exhibited evidence of bone loss. The percentage with bone loss was close to 70% among individuals in their thirties and close to 90% in those older than 50 years. Marshall-Day & Shourie (78) also used radiographs to detect periodontitis in younger adults in India and concluded that prevalence increased with age. A few years later, Marshall-Day et al. (79) found that 43% of children in the United States had periodontitis and 9 of 10 adults had the disease by the age of 40. Bossert & Marks (9) reported that 18-33% of New York City residents under age 40 exhibited periodontitis. In the 1976-1977 North Carolina survey, periodontitis was scored with the Periodontal Index (39). Using average Periodontal Index scores to characterize the periodontal status of groups, the findings from North Carolina indicated that incipient periodontitis occurred among whites mostly after the age of 40;

established periodontitis was uncommon before age 60. For black males, the onset of periodontitis occurred at a younger age and progressed rapidly. Turning to United States national probability surveys, Kelly & Van Kirk (48) reported data from the 1960-1962 Health Examination Survey that indicated that the average Periodontal Index for each age group increased steadily from less than 1.0 for people aged 18-24years to 2.91 for people aged 75-79 years. Average Periodontal Index scores between 1.0 and 2.0 are considered to represent incipient periodontitis, and those between 2.0 and 4.0 represent established periodontitis. Thus, the older the person, the higher were both the prevalence and severity of periodontitis. Findings from the 1971-1974 National Health and Nutrition Examination Survey I showed that the average Periodontal Index remained under 1 (in the gingivitis range) for persons under 45 years old. It then increased to 1.57 among people aged 46-64 years, indicating what Russell called incipient periodontitis. An average Periodontal Index of over 2.0 among elderly people suggested that established periodontitis was prevalent in that age group. The percentage of people with pathological pockets in 1971-1974 was estimated to be very low for people under 18 years. About 15% of people aged 1 8 4 4 years had deepened pockets as determined by the Periodontal Index, whereas almost 40% of people aged 45-64 and 50% of those 265 years were listed as having pockets. Until the 1980% epidemiological studies usually
U
All Pockets c4 mm 1or More Pockets >6 mm

Z 3 1 or More Pockets 4-6 mm

19-44

45-64
Age, Years

65+

Fig. 2. Severity of periodontitis by the percentage of people and the deepest pocket according to age in the United States in 1981 (data from the US Health Resources and Services Administration study on dental health outcomes related to prepayment)

65

Brown & Loe

assessed periodontal status either visually or with unstandardized dental radiographs. Both of these methods have pronounced limitations. Visual assessment is inherently subjective, making calibration of examiners difficult. Researchers continue to debate whether the Periodontal Index tends to underestimate or overestimate periodontal disease. Standard radiographs can only assess interproximal sites (107). They are not accurate in detecting early periodontitis and tend to underestimate the amount of bone loss
(61, 121, 123). In the 1980s, national oral epidemiological surveys

in the United States began using a periodontal probe to measure pocket depth and clinical attachment level. Although not without its problems, this more objective measurement method largely has replaced the visual assessment of periodontitis. The remainder of the discussion concentrates on the results of these more recent national surveys. Analyzing data from a 1981 national probability survey described earlier, Brown et al. (10) reported the prevalence of periodontitis (at least one mesial site with a periodontal pocket 2 4 mm) of 36% for the adult United States population (Fig. 1). The prevalence increased with age; 29% of people aged 19 to 44 years had periodontitis and close to 50% among people 45 years or older. The prevalence of periodontitis in elderly people was also around 50%. Moderate periodontitis, defined as at least one mesial pocket 4-6 mm in depth, occurred in 28% of all people, and 8% had advanced disease (at least one mesial pocket 2 6 mm) (Fig. 2). The prevalence of both moderate and advanced periodontitis increased with age. Only 3% of those under 45 years had advanced periodontitis compared with 15% of those aged 45 or older. The prevalence of moderate periodontitis was 28% among people aged 19 to 44 years, whereas it was present in 44v0 of those 45 years or older. When present, periodontitis was not extensive.

Twenty-five percent of the population had two or more teeth with pockets depths 4-6 mm; only 9% had 6 or more teeth with pockets that deep. Less than 4% of the population had 3 or more pockets 2 6 mm in depth. Brown et al. (11) also reported estimates of periodontitis from the 1985-1986 NIDR survey of employed adults aged 18 to 64 years. In that survey, clinical attachment loss was measured with a periodontal probe at the mesiofacial and midfacial sites on all teeth except third molars in a randomly selected half-mouth design, consisting of a maxillary and a mandibular quadrant. Loss of clinical attachment of 2 1 mm at one or more sites was found in around 99% of employed adults (Table 6). Thirty-five percent of measured sites exhibited that much attachment loss. Approximately 44% of the sample had loss of attachment of 2 3 mm at less than 4% of the measured sites. More severe attachment loss of 2 5 mm was found in slightly less than 13% of people at less than 1% of all measured sites. Clearly, most people had some loss of clinical attachment, but only a small percentage had severe enough attachment loss to raise concern about function or tooth mortality. Periodontal pockets 4-6 mm deep were observed in slightly less than 14% and deep pockets ( 2 7 mni) in less than 1% of the sample (Table 7). When present, moderate and deep periodontal pockets were not extensive. About l%of all measured pockets were 4-6 mm deep, for an average of less than 1 per person. Less than 1 in 3300 measured sites had pockets 2 7 mm. A general finding from many studies is that the prevalence of periodontitis among adults is higher among older people. Brown et al. (10) reported that 29% of those aged 19-44 years had periodontitis, defined as at least one mesial pocket 24 mm, whereas the prevalence was close to 50% for those 45 years or older. Only 3% of those younger than 45 years had advanced periodontitis (one or more pockets 2 6 mm

Table 6. Prevalence, severity and extent of loss of attachment in employed adults in the United States, 1985-1986. Source: Brown et al. (11) 21 n i m loss of attachment 2 3 nim loss of attachment 2 5 mm loss of attachment Prevalence Extent Prevalence Extent Prevalence Extent Age (?D people) (years) (% people) (no of sites)* (% people) (no. of sites)* (no. of sites)
11\11

18-24 25-34 35-44 45-54 55-65

99.7 (0.01) 99.0 (0.04) 99.9 (<0.01) 99.7 (0.02) 100.0 (<0.01) 99.6 (0.03)

34.5 (0.06) 32.8 (0.09) 35.7 (0.06) 34.9 (0.07) 34.1 (0.07) 33.5 (0.07)

43.8 15.7 34.5 48.6 67.1 77.3

(0.07) (0.11) (0.12) (0.14) (0.18) (0.15)

3.4 (0.05)

0.7 2.1 3.8 5.9 8.2

(0.01) (0.02) (0.02) (0.03) (0.04)

12.8 (0.05) 1.9 (0.05) 6.0 (0.06) 13.5 (0.10) 24.9 (0.15) 35.0 (0.15)

0.7 <0.1 0.3 0.8 1.4 2.0

(<0.01)

(<0.01) (<0.01) (<0.01) (0.01)

(0.02)

*Half-mouth scores are multiplied by 2. Standard errors, adjusted for complex sample design, are in parentheses.

Prevalence, extent, severity and progression

Table 7. Prevalence, severity, and extent of periodontal pockets in employed adults in the United States, 1985-1986 4-6 mm pocket depth 2 7 mm pocket depth Prevalence Extent Prevalence Extent (Wpeople) (no. of sites)* (Wpeople) (no. of sites)* Age (years) 0.6 (0.03) 0.01 (0.01) 13.4 (0.05) 0.6 ((0.01) All
18-24

5.7 (0.09)

0.2 ((0.01)

<0.1 (<0.01)

<0.01 (0.01)

0.5 (<0.01) 0.01 (0.01) 0.5 (<0.01) 25-34 11.7 (0.09) 0.6 (0.02) 0.02 (0.01) 16.6 (0.08) 0.8 (0.01) 3544 0.8 (0.01) 0.9 (0.02) 0.03 (0.01) 18.3 (0.12) 45-54 1.1 (0.04) 0.03 (0.01) 0.8 (0.01) 55-65 18.1 (0.11) *Half-mouthscores are multiplied by 2. Standard errors, adjusted for complex sample design, are in parentheses.

in depth) compared with 15% of people 45 years or older. Similar patterns are observed for loss of clinical attachment. The percentage of people with 2 3 mm attachment loss was about 15%for those aged 18-24 years but increased regularly with age to over 77% of people aged 55-64 (11). The prevalence of advanced periodontitis (2-7 mm loss of attachment) was virtually nonexistent among people under 25 years but increased to 35% for those 55-64 years. For all ages, men were 1.5 times more likely to have pockets 2 4 mm than women (11). Blacks were twice as likely to have pockets that deep as whites, and about 10% more blacks than whites (51% to 42%) had attachment loss 2-3 mm (91). The racial difference persisted in all age groups. A higher percentage of people with less than 12 years of schooling had attachment loss of 2 3 mm and pockets 2 4 mm. Summary Recent national surveys estimated that moderate periodontitis affected about one half of the United States population. More advanced periodontal destruction ( 2 5 mm loss of attachment in one site) affected only about 1 in 8 people. Advanced destruction was almost nonexistent among younger adults but increased with age, reaching a prevalence of over one third among people aged 55-64 years. These estimates, based on the 1985-1986 NIDR survey, are probably lower than the actual prevalence due to the impact of partial recording. The amount of the underestimate is unknown, but even if the true prevalence is double the estimate, only 25% of the population had advanced periodontitis in 1985-1986. Periodontitis may not be as widespread as once thought, and perhaps we are entering an era when almost everyone can maintain their dentition throughout their life.

Progression of periodontal disease

Four issues are central to the discussion of progression of periodontal disease. Does gingivitis progress to periodontitis? Does untreated periodontitis progressively destroy the periodontium? Are rates of periodontal destruction different in groups with better oral hygiene and access to professional care? Is the pattern of progression continuous or episodic? Early studies led to the belief that gingivitis progresses in time to periodontitis and that untreated periodontitis progressively destroys the periodontium, ultimately leading to tooth loss (4,42, 106, 120). The relationship between the prevalence and severity of gingivitis and the onset of adult periodontitis has recently been questioned (27, 100). Clearly, not all gingivitis progresses to periodontitis; however, most believe that periodontitis must be preceded at some point by gingivitis (74). The proportion of gingival lesions that convert to periodontitis is currently unknown, but is probably rather small. More importantly, the factors that cause the conversion are not well understood. Since gingival lesions that will convert to periodontitis cannot currently be distinguished from those that will not, the conservative approach to management is to try to prevent or treat all gingivitis. Evidence from both cross-sectional and longitudinal studies indicate that the prevalence of adult periodontitis increases with age. Longitudinal studies of untreated periodontal disease confirm that more of the periodontium is destroyed as a person ages (69, 71). As documented in both rapidly and moderately progressing disease groups of tea workers in Sri Lanka, periodontitis continued until the entire periodontium was affected and teeth were lost (70). The mean rate of loss of attachment in this population was between 0.1 and 0.3 mm per year (Fig. 3). At the higher

67

Brown & Loe

Sri Lanka Tea Laborers

1970-77

mm 7
6

Mean rate of loss of attachment in buccal (B)and mesial (M surfaces of the anterior (1,2, 1 and posterior (4,5,67) teeth of the right upper and iower jaws between 17 and 37+ years

mm
- 7
-6

5
4

Maxilla

3
2
1

0
0

treated patients and found that periodontal destruction progressed in all cases. Progression was also studied in patients with mild to moderate attachment loss over 6 years and in patients who did not receive treatmentfor advanced destruction for one year (33, 65). The findings indicated that progression at any given site occurs only slowly. Rapid progression is limited to a small proportion of individuals. Progression of untreated periodontal disease as described in studies that examined subjects at relatively long intervals is not incompatible with rapid, but relatively infrequent bursts of destruction followed by periods of stability (70). Regardless of the pattern of destruction over short time periods, both cross-sectional data and extended longitudinal observation indicate that untreated periodontitis progresses to further destruction. Hopefully, further research will permit the prediction of which sites will progress. Then it will be possible to tailor treatment to individual sites.

0
1

References
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3
4
5

3
4

5 Mandible

6
rnm

mn

Fig. 3. Mean rate of loss of attachment among tea laborers in Sri Lanka, 1970-1973

rate of progression, clinical attachment would be mostly destroyed in less than 30 years. Since attachment loss began as early as the teenage years, little of the periodontiurn was left in the middle-aged study subjects. A longitudinal study in Norway demonstrated that periodontal lesions progress slowly among well educated people living in developed countries, practicing adequate oral hygiene and seeking periodic professional care (69). The rate of progression in Norway ranged from 0.05 to 0.1 rnm per year, several times slower than the rates observed in the untreated Sri Lankans. Becker et al. (4) followed a small group of un-

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Prevalence, extent, severity and progression

~~~ ~

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32. Greenstein G, Caton J, Polson AM. Histologic characteristics associated with bleeding after probing and visual signs of inflammation. J Periodontol 1981: 52: 420-425. 33. Haffajee AD, Socransky SS, Goodson JM. Clinical parameters as predictors of destructive periodontal disease activity. J Clin Periodontol 1983: 10: 257-265. 34. Haffajee AD, Socransky SS, Goodson JM. Periodontal disease activity. J Periodont Res 1982: 17: 521-522. 35. Hansen BF, Gjerrno P, Bergwitz-Larsen KR. Periodontal bone loss in 15-year-old Norwegians. J Clin Periodontol 1984: 11: 125-131. 36. Harley AF, Floyd PD. Prevalence of juvenile periodontitis in schoolchildren in Lagos, Nigeria. Community Dent Oral Epidemiol 1988: 16: 299-301. 37. Hoover JN, Ellegaard B, Attstrom R. Periodontal status of 14-16-year-old Danish schoolchildren. Scand J Dent Res 1989: 89: 175-179. 38. Hormand J, Frandsen A. Juvenile periodontitis: localization of bone loss in relation to age, sex, and teeth. J Clin Periodontol 1979: 6: 407-416. 39. Hughes JT, Rozier RG, Ramsey DL. Natural history of dental diseases in North Carolina. 1976-77. Durham, NC: Academic Press, 1982. 40. Hugoson A, Koch G, Hallonsten A, Ludivigsson M, Lundgren D, Rylander H. Dental health 1973 and 1978 in individuals aged 3-20 years in the community of Konkoping, Sweden. Swed Dent J 1980: 4: 217-229. 41. Imrey PB. Consideration in the statistical analysis of clinical trials in periodontitis. J Clin Periodontol 1986: 13: 517-528. 42. Jamison HC. Prevalence of periodontal disease in the deciduous teeth. J Am Dent Assoc 1963: 66: 207-215. 43. Jeffcoat MK, Jeffcoat RL, Jens SC, Captain K. A new periodontal probe with automated cemento-enamel junction detection. J Clin Periodontol 1986: 13: 276-280. 44. Jeffcoat MK, Reddy MS, Webber RL, Williams RC, Ruttimann UE. Extraoral control of geometry for digital subtraction radiography. 7 Periodont Res 1987: 22: 396-402. 45. Karim M, Birek P, McCulloch CA. Controlled force measurements of gingival-attachment level made with the Toronto automated probe using electronic guidance. J Clin Periodontol 1990: 17: 594-600. 46. Kelly JE, Harvey CR. Basic data on dental examination findings of persons 1-74 years, United States, 1971-74. Washington, DC: US Government Printing Office, 1979. 47. Kelly JE, Sanchez MJ. Periodontal disease and oral hygiene among children. Washington, DC: US Government Printing Office, 1972 (National Center for Health Statistics. Vital and Health Statistics, Series ll, No. 117). 48. Kelly JE, Van Kirk LE. Periodontal disease in adults, United States 1960-62. Washington, DC: US Government Printing Office, 1965 (National Center for Health Statistics, Vital Health Statistics, PHS Publication No. 2000, Series 22, No. 12). 49. Kelsey JL, Thompson WD, Evans AS. Methods in observational epidemiology. New York Oxford University Press, 1986. 50. Kinane DF, Johnston FA, Evans CW. Depressed helperto-suppressor T-cell ratios in early-onset forms of periodontal disease. J Periodont Res 1989: 24: 161-164. 51. King JD, Francklyn AB. Gingival disease in Gibraltar evacuee children. Lancet 1944: April: 4955498. 52. Kingman A, Morrison E, Loe H, Smith J. Systematic errors

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in estimating prevalence and severity of periodontal disease. J Periodontol 1988: 59: 707-713. 53. Kirkegaard E, Borgnakke WS, Grobaek L. Oral health status, dental treatment need, and dental care habits in a representative sample of the adult Danish population survey of oral health of Danish adults. Copenhagen: Odontologisk Boghandel. 1986. 54. Neinbaum DG. Kupper LL, Morgenstern H. Epidemiologic research. New York: Van Nostrand Reinhold, 1982. 55. Kornman KS. Nature of periodontal diseases: assessment and diagnosis. J Periodont Res 1987: 22: 192-204. 56. Kowashi Y. Prevalence of juvenile periodontitis among students at Nagasaki University. Adv Dent Res 1988: 2: 395-396. 57. Kramer MS. Clinical epidemiology and biostatistics. New York Springer-Verlag, 1988. Periodontosis: incidence and find58. Lacy ED, Brasher WJ. ings in a military population. J Oregon Dent Assoc 1977: 46: 4-6. 59. Lamster IB, Hartley LJ, Vogel RI. Development of a biochemical profile for gingival crevicular fluid. Methodological considerations and evaluation of collagen-degrading and ground substance-degrading enzyme activity during experimental gingivitis. J Periodontol 1985: 56 (spec issue): 13-21. 60. Lamster IB, Vogel RI, Hartley LJ, DeGeorge CA, Gordon JM. Lactate dehydrogenase, beta-glucuronidase and arylsulfatase activity in gingival crevicular fluid associated with experimental gingivitis in man. J Periodontol 1985: 56: 130-148. 61. Lang NP, Hill RW. Radiographs in periodontics. J Clin Periodontol 1977: 4: 1 6 2 4 . 62. Lembariti BS. Pilot T. Periodontal diseases in urban and rural populations in Tanzania. Dar es Salaam, Tanzania: University Press, 1983. 63. Lilienfeld AM, Lilienfeld DE. Foundations of epidemiology. New York: Oxford University Press, 1980. 64. Liljenberg B, Lindhe J. Juvenile periodontitis: some microbiological. histopathological and clinical characteristics. J Clin Periodontol 1980: 7: 48-61. 65. Lindhe J, Haffajee AD, Socransky SS. 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Prevalence, extent, severity and progression

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