608
Early Onset Periodontitis
in the United
States of America* Harald Löe and L. Jackson Brown
A national survey of the oral health of U.S. children aged 5 to 17 was conducted by the National Institute of Dental Research during the 1986-87 school year. Eleven thousand and seven adolescents aged 14 to 17 years received a periodontal assessment. Their patterns of loss of periodontal attachment as assessed by probing at mesial sites were used to classify adolescents as cases of early onset Periodontitis. Approximately 0.53% of adolescents nation-wide were estimated to have localized juvenile Periodontitis (UP), 0.13% to have generalized juvenile Periodontitis (GJP), and 1.61% to have incidental loss of attachment (LA) (>3 mm on 1 or more teeth). The total number of adolescents affected were not trivial. Close to 70,000 adolescents in the U.S. were estimated to have LIP in 1986-87. More destructive GJP affected an estimated 17,000 adolescents. Another 212,000 adolescents were estimated to have incidental LA. Blacks were at much greater risk for all forms of early onset Periodontitis than whites. Males were clearly more likely (4.3 to 1) to have GJP than females when other variables were statistically controlled. Gender associations were more complicated for LJP because gender interacted with race. Black males were 2.9 times as likely to have UP as black females. In contrast, white females were more likely than white males to have the disease by about the same odds. When interactions among demographic variables exist, caution must be taken in comparing results from different studies. / Periodontal 1991; 62:608616.
Key Words: Periodontitis, juvenile/epidemiology; oral health surveys; adolescents.
Juvenile Periodontitis first occurs around puberty and is characterized by gingival inflammation and severe angular bony defects, resulting in pronounced loss of periodontal attachment during adolescence.16 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,714 clinical diagnosis is usually made on the basis of the distribution of bone loss and age of onset. Two forms of the disease have been identified.14"17 Localized juvenile Periodontitis (UP) is characterized by bone loss around the incisors, molars, and the mesial surface of the second molars. A more generalized pattern of periodontal destruction, involving teeth other than or in addition to incisors and first molars, is recognized as generalized juvenile Periodontitis (GJP).18 Estimates of the prevalence of juvenile Periodontitis vary greatly.2,19'20 Scandinavian studies reported prevalence of 0.2% for Norwegian,21 0.1% for Finnish,22 and 0.1% in Danish subgroups of children.23 Blankenship et al.24 reported 0.06% in groups of English and Danish children,
'Epidemiology and Oral Disease Prevention Program, National Institute of Dental Research, National Institutes of Health, Bethesda, MD.
and Van der Veiden et al.25 reported between 0.1% and 0.2% for a special group of Dutch children. Two studies of 12 to 20 year old children in Lagos, Nigeria reported prevalence of 0.75% and 0.8%.26'27 A prevalence of 3.7% was estimated for a group of Brazilian children 15 to 16 years old.28 Kowashi reported a prevalence rate of 0.47% for Japanese university students aged 19 to 28 years.29 Barnett et al.30 found 2.4% of patients aged 13 to 30 years examined at a U.S. dental school had juvenile Periodontitis. Cianciola et al.31 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 children's hospital. Lacy and Brasher32 estimated a prevalence of 0.4% among a U.S. military population. Case series have generally found females more likely than males to have juvenile Periodontitis by ratios of approximately 2.5:1. Studies of smaller dental school populations also report a higher prevalence among females than males.4'18'30 Puberty starts earlier in females which may lead to an earlier onset of this disease. However, marked differences in gender specific prevalence rates have not been confirmed in studies with well-defined diagnostic criteria carried out with probability samples.33 A racial association has been observed in several popu-
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lations. For example, a survey of English children found the prevalence of juvenile Periodontitis to be 0.1% for whites, 0.2% for Asians, and 0.8% for blacks.34 Studies of African populations report prevalence in the 0.8% range.26-27 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, various periodontal indices, and probing), the types of population studied (patients, school children, military, young adults), the ages of the individuals assessed, and the sample selection method (convenience vs. probability). Any combination of these differences could explain the variation in the prevalence rates. This paper reports the first estimates of the prevalence of juvenile Periodontitis based on a national probability sample of school children in the U.S.A. Bivariate and multivariate associations of age, gender, race, and Hispanic background with the prevalence of different forms of juvenile Periodontitis are described. Percentages of individual teeth affected are also reported. MATERIALS AND METHODS
Sample Selection and Field Methods A national survey of U.S. children from kindergarten through grade 12 was conducted by the National Institute of Dental Research (NIDR) during the 1986-87 school year to assess oral health. The sampling frame for the survey consisted of all public and private schools in the United States, except Alaska. A multi-stage probability sample was selected representing 45 million children. All children in selected classes, whose parents gave written consent for their participation in the survey, were given a standardized visual-tactile examination for dental caries, dental fluorosis, gingivitis, periodontal disease, and soft tissue lesions. Of the 196 school districts selected for the survey, 163 participated. Ninety-one percent of the 664 schools selected in the initial sample participated in the survey. The sample was augmented with 11 school districts and 107 schools to replace those schools and districts that did not participate. A total of 52,289 students were in the selected classes, 41,623 agreed to be examined, and 40,694 were examined. Overall, 78% percent of sampled students received a complete examination. Field staff for the survey consisted of 13 coordinating teams and 12 examination teams. Examination teams were trained and calibrated by NIDR and contractor staff according to standardized written diagnostic criteria. The NIDR probe was used to measure the loss of periodontal attachment (LA) in buccal and mesial sites. The distance (in mm) from the free gingival margin (FGM) to the cemento-enamel junction (CEJ) and the distance from the FGM and the bottom of the sulcus or pocket was measured at each site. Gingival assessment at each buccal and mesial site was measured by absence or presence of bleeding on probing.
LÖE, BROWN
609
Table 1. Distribution of Demographic Characteristics of U.S. School Children Age 14-17 (NIDR 1987)
Characteristic
Age* 14 15 16 17
Population
in Millions
Percent
Sample Size
3.15 3.46 3.55 3.01
23.9 26.2 27.0 22.9
2686 2708 2888 2725
6.70 6.47
50.9 49.1
5179 5828
Gender* Male Female Race Blade* White
2.38 10.77
18.1 81.8
(2.93) (2.96)
1408 9590
Hispanic Background Hispanic Non-Hispanic
(0.38) (0.40)
1.30 11.86
(0.09) (0.11)
9.9 90.1
(0.72) (0.72)
1114 9884
9.63 3.55
(0.24) (0.24)
73.1 26.9
(1.84) (1.84)
5875 5132
0.70 1.97 2.95 3.53 1.34 0.75 1.93 13.17
(0.03) (0.02) (0.01) (0.02) (0.02) ( 3 mm LA. Generalized Juvenile Periodontitis classified if first criteria were not met and if 4 or more teeth had > 3 mm LA and at least 2 affected teeth were second molars, cuspids, or
premolars.
Incidental Loss of Periodontal Attachment Individuals who did not meet the first 2 criteria, but had 1 or more teeth with > 3 mm LA showed evidence of advanced LA at an early age. Seventy-one percent of those individuals had only 1 affected site; 97% had 3 or fewer affected sites. The few sites with advanced periodontal destruction could indicate incipient cases of frank juvenile Periodontitis or could be incidental to other factors. These persons were classified as exhibiting incidental LA which was advanced for their age. The classification should not be interpreted as a
distinct clinical
entity.
Statistical Analysis Estimates of the prevalence rate and the number of persons with disease (prevalence) were weighted to reflect the total number of U.S. children attending school. Standard errors were adjusted for the complex sample design and are included in the tables.38 Associations between individual demographic attributes and the presence of LJP or GJP are estimated with odds ratios of diseased to non-periodontal diseased individuals. Bivariate analysis was used to estimate the crude (unadjusted) odds ratios between single demographic variables and the different forms of juvenile Periodontitis. Multivariate analysis, logistic regression, was used to estimate the association (adjusted odds ratios) between LJP and GJP and several demographic attributes considered simultaneously.39,40 Logistic regression allowed a determination of the extent to which the associations between individual demographic variables and the presence of juvenile Periodontitis were independent of one another. Interactions between the demographic attributes were also assessed. For logistic regressions, each demographic variable was
50 14
175
Population Estimate
69,748
Percent of Persons 0.53
(29,228)*
(0.22)
(8,689)
(0.066)
(53,439)
(0.41)
16,781
212,386
0.13 1.61
adjusted for complex sample design, are in parentheses.
entered as a dummy variable, taking the value "one" if the person had the attribute and "zero" otherwise.41 The antilogs of the coefficients for the dummy variables indicate the odds of persons with the attribute having juvenile Periodontitis compared to persons who do not have the attribute. Odds ratios are indicators of the strengths of association between demographic variables and the different forms of juvenile Periodontitis. A ratio of one (1.0) indicates no association. Only tables of odds ratios are reported; logistic regression results may be requested from the authors. RESULTS Prevalence
Early onset Periodontitis was rare among the children stud-
ied. Of 11,007 school children examined, 50 individuals classified as cases of localized juvenile Periodontitis; 14 were classified as general juvenile Periodontitis; and another 175 had incidental LA (Table 2). Sampling weights were applied to the sample to estimate the prevalence of the diseases for the U.S. population. Nationwide, 0.53% of 13 million U.S. adolescents 14 to 17 years old were estimated to have LJP, 0.13% to have GJP, and 1.61% to have incidental LA (> 3 mm on 1 or more teeth). Altogether, 2.27% of adolescents were classified as exhibiting advanced loss of attachment for their ages, while close to 97.73% were classified as normal. While these prevalences were small, the total numbers of children affected were not trivial. Close to 70,000 of U.S. adolescents were estimated to have LIP in 1986-87. More destructive GJP affected an estimated 17,000 adolescents. Another 212,000 adolescents were estimated to have incidental LA. were
Distribution of LA Among Individual Types of Teeth Patterns of LA among individual teeth varied greatly among the adolescents in the different disease classifications. Among persons with LJP, 13.7% of teeth (an average of approximately 4 mesial sites per person) had LA of > 3 mm. As expected, first molars were most commonly affected; slightly over 40% demonstrated LA of > 3 mm, ranging from 72% in the upper right quadrant to nearly 23% in the lower right (Fig. 2). Twenty-one percent of second molars (mostly in the maxillary arch) and 10% of incisors were affected. Premolars and cuspids were not greatly affected.
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LÖE, BROWN Percent
611
Percent 100
100
75 50
Upper
Upper 25 0
0 25
50
50
Lower
Lower
Right
75
75
100
100
Left
Figure 2. Localized juvenile Periodontitis: Percent mm or greater loss of attachment by site.
Right
of mesial sites with 3
Percent 100
50
Upper 25
7654321
Lower
25
1234567
"MM Right
' Left
Figure 3. Generalized juvenile Periodontitis: Percent 3 mm or greater loss of attachment by site.
of mesial sites with
Among individuals classified as GJP, one-third of teeth (over 9 mesial sites per person) had LA of > 3 mm. Attachment loss was widely distributed among tooth types (Fig. 3); 37% premolars and 33% of molars were affected. Attachment loss among anterior teeth occurred primarily in
the mandibular arch where over 50% of the incisors were affected. Among individuals classified with incidental LA, 5% of teeth (1.4 mesial sites per person) had > 3 mm LA. Attachment loss occurred rather evenly among maxillary teeth although molars were slightly more frequently affected (Fig. 4). Mandibular molars and premolars did not exhibit substantial LA. For comparison, LA of similar severity was virtually absent among normal adolescent children. Bivariate Associations With Demographic Variables The percent of adolescents with LJP increased until age 16 years while the percent with the GJP and incidental LA did not increase after age 15 (Table 3). All 3 conditions were rare for each age group. The odds ratio for adolescents 16 years old compared
Left
Figure 4. Incidental loss of attachment: Percent of mesial sites with 3 mm or greater loss of attachment by site. those 14 years old was estimated to be 4.5, indicating that individuals in the older age group were four and onehalf times more likely to have LJP than those in the younger age group (Table 3). The odds ratio for LJP comparing children 17 and 14 years old was 3.8. The 95% confidence intervals (CI) for both odds ratios did not include the number one (1.0), indicating a very high confidence that the true odds ratios were greater than one. An association between GJP and age could not be detected. Except for children 15 years old, odds ratios were near 1.0. None of the GJP odds ratios approached statistical significance at the 5% level. Odds ratios for incidental LA for different ages varied between 1.6 and 1.2. Only the odds ratio for children 15 years old compared to those 14 years old was significant at the 5% level. However, the lower boundaries of the CIs for the other 2 odds ratios were close to 1.0, indicating substantial probability of a weak bivariate association. Table 4 displays the percent of males and females with each disease classification. Only small differences were apparent between the genders. Males were slightly more likely to exhibit all three disease classifications. Odds ratios ranged from 1.3 to 2.7. Although none were significant at the 5% level, each was close to 1.0, indicating substantial probability of a weak bivariate association between males and juvenile periodontal disease. Race was strongly associated with the disease classification (Table 5). The percentage of blacks with disease were several times larger than the percentage of whites (which included small percentages of Asians and American Indians) in all three classifications. Odds ratios ranged from 5.5 for incidental LA to 15.1 for UP and 24.6 for GJP. The 95% CIs indicate a very small probability that these findings were due to sampling variation. Hispanic children were 2.4 times more likely to have UP than non-Hispanics (Table 6). They were slightly more likely to exhibit incidental LA also. An association between Hispanic background and GJP could not be statistically detected. to
612
J Periodontol October 1991
EARLY ONSET PERIODONTITIS IN THE UNITED STATES OF AMERICA
Table 3. Prevalence of Periodontitis in U.S. Children 14-17 Years of Age, NIDR 1987
Classification Localized juvenile
Periodontitis Generalized juvenile Periodontitis Incidental loss of attachment
14 0.19
Percent 15 16 0.32 0.86
Crude Prevalence Odds Ratio of Older Children Compared to 14 Year Olds Estimate* 17 0.73
0.09
0.23
0.11
0.08
1.27
1.96
1.43
1.79
15_16_17 1.7
(0.6
2.7
5.1)
4.5
3.8
(1.7 11.9)
(1.4 10.3)
1.3
-
(0.6
12.3)
1.6
(0.2
-
(1.01
1.2
are
Table 4. Prevalence of Periodontitis in U.S. Children 14-17 Years of
Age, by Gender (NIDR 1987)
Classification
Percent Male Female
Localized juvenile
0.60
Periodontitis Generalized juvenile Periodontitis Incidental loss of attachment
Crude Prevalence Odds Ratio Male to Female Estimate*
0.45
0.18
0.07
1.78
1.43
1.3
(0.8 2.3) 2.7 -
(0.8 9.0) 1.3 -
(0.9 1.7) -
*95% confidence intervals
listed in
are
parentheses below
the estimates.
Table 5. Prevalence of Periodontitis in U.S. Children 14-17 Years of Age, by Race (NIDR 1987)
Classification Localized juvenile
Periodontitis Generalized juvenile Periodontitis Incidental loss of attachment
Percent Black White
2.05
Crude Prevalence Odds Ratio Black to White Estimate*
0.14
0.59
0.03
4.63
0.91
15.1
(8.1
28.2)
24.6 -
listed in
2.4)
(0.7
7.4)
Table 6. Prevalence of Periodontitis in U.S. Children 14-17 Years of
Age, by Hispanic Background (NIDR 1987) Classification Localized
Hispanic Non-Hispanic
juvenile Periodontitis Generalized juvenile
Periodontitis
Incidental loss of attachment
1.02 0.06
2.36
0.43 0.14 1.50
Crude Prevalence Odds Ratio Black to White Estimate* 2.4
(1.2 4.7) 0.4 -
(0.03 5.5) 1.6 -
(1.05 2.4) -
*95% confidence intervals
Multivariate
are
listed in
1.4
6.2)
-
1.8)
(0.9
-
2.2) -
parentheses below the estimates.
Table 7. Odds Ratios and 95% Confidence Intervals Comparing Children With LJP to Normal Children (NIDR 1987)
Variables
Main Effects 15 to 14 years 16 to 14 years 17 to 14 years
Hispanic to non-Hispanic
Urban to rural Atypical examiners to other examiners Interactions Black to White
Females, not Region IV Females, Region IV Males, not Region IV Males, Region IV
Male to Female Whites Blacks Region IV to the rest of the country Whites Blacks
Odds Ratio
95% CI Lower
Upper
1.3 3.4 3.3 4.0 1.5
0.4 1.3 1.2 1.9 0.7
4.0 9.4 9.3 8.6 3.5
11.6
6.0
22.5
1.7 35.4 13.4 282.4
0.5 2.5 3.2 17.5
5.8 506.7 56.1 4567.8
0.4 2.9
0.1 1.4
1.2 5.8
0.2 1.7