J. Periodontal Res. 12: 148-159, 3977

A genetic and epidemiologic study of periodontaI disease in Hawaii I. Racial and other epidemiologic factors C. S. CHtJNG, M. C. W. KAO, S. S. C . CHUNG AND S. A. SCHENDEL

School of Public Health and the Pacific Biomedical Research Center, University of Hawaii, Honolulu, Hawaii and Division of Dental Health, Hawaii State Department of Health, Honolulu, Hawaii Using a modification of the Ramfjord procedure, 939 individuals aged 14 years or above of six racial groups were examined for periodontal disease to study the effects of genetic and epidemiologic factors with special emphasis on inbreeding and race. Other factors studied included sex, age, years of edacation, frequency of toothbrushing, smoking, tooth malalignment, and medical history. Among six racial groups, two distinct clusters were discernible even when relevant concomitant variables including years of education and oral hygiene practice were adjusted for. Caucasians, Japanese, and «Others» had cleariy higher levels of periodontal health status than Hawaiians or part-Hawaiians, Samoans, and Filipinos. The difference in Samoans and Fflipinos may be explained in part by cultural and socioeconomic factors associated with their recent immigration to Hawaii. Inbreeding was not related to any indicator of periodontal disease showing inconsistency with the hypothesis of significant role of recessive genes in the etiology of the disease. Smoking was found to have adverse effect on periodontal health status, whereas no clear-cut association was noted with tooth malalignment. The principal component analysis on eight periodontal disease variables led to the extraction of two major factors, destructive periodontal disease and plaque accumulation. (Accepted for publication July 7, 1976)

Three-fourths of the adult population of the Utiited States are known to suffer from periodontal disease and one-third of those with the disease have destructive periodontal disease (Kelly & Van Kirk 1965). Yet the etiology of the condition still remains unknown. Numerous epidemiologic studies have been done in search of etiologic factors for this insidious disease. McMillan and Wolff (1969) and Waerhaug (1971) reviewed the

recent status of the epidemiology of the disease. Among many epidemiologic factors studied, several are widely accepted as closely associated with the risk of periodontal disease. These are oral hygiene status, age, socioeconomic status, and sex. The relationship between other epidemiologic factors and periodontal disease is either less well known or controversial. Among these variables are malocclusion (Glickman 1967, Stallard 1969, Ainamo 1972, Buckley 1972, Geiger et al. 1972), smoking (Arno et al. 1959, Lilienthal, Ame-

PERIODONTAI

DISEASE

rena & Gregory 1965, Summers & Oberman 196S, Preber & Kant 1973), diabetes (Mackenzie & Millard 1963, Benveniste, Bixler & Conneally 1967, Finestone & Boorujy 1967, Glavind, Lund & Loe 1968, Kelly & Eogel 1969, Bernick et al. 1975), and other systemic diseases (McMillan & Wolff 1969). Although the literature contains a number of epidemiologic studies of periodontal disease on different racial groups of the world, it is difficult to compare them due to differences in sampling method of subjects and examination procedure involved. Nevertheless, populations of Asia and Africa were observed to have generally poorer periodontal health status than those of the United States and Western Europe (Waerhaug 1971). More is known about United States whites and blacks. The studies by Russell & Ayers (1960) and Kelly & Van Kirk (1965) showed that whites have better periodonta] health than blacks in the United States. However, remaining to be answered is the question of whether or not the racial difference can be explained fully by the differences in socioeconomic status and oral hygiene status between the two groups. Chung et al. (1970) observed that among schoolchildren in Hawaii individuals of Hawaiian ancestry had higher PI scores (Russell 1956) than other racial groups even when concomitant variables were adjusted for. The role of heredity is virtually unknown though there is a suggestion that recessive genes may be involved in the etiology of periodontal disease. This is based on the observations that pariodontal disease responded adversely to inbreeding of the subject in Japan (SchuU & Neel 1965) and favorably to racial hybridity in Hawaii (Ch\m%etal. 1970). The present investigation was designed to critically examine racial differences along with other epidemiologic factors in Hawaii, where the multiracial composition of the

IN

HAWAII

149

population offers a unique opportunity. This study is considered as an extension of the earlier population study (Chung et al. 1970) and will be followed by a genetic study based on family data (Chung et al. 1976). Materials and Methods

Subfects: Selection of subjects for this study wag based on the general criterion that both natural parents with at least one child aged 14 or above are available for dental examination. The volunteer subjects were obtained primarily from two sources. The first group of subjects was derived from volunteers who were participating in a project of the Behavioral Biology Laboratory to study variation of cognitive ability, which imposed the same requirement for age and family composition. Additional requirement for the study was that subjects could read and write English. The volunteers responded to advertisements published in city, community, and school newspapers and other bttUetins. The second group of subjects was obtained through social workers associated with the State Health Department, who were familiar with the commttnity under their responsibility. Initial contacts were made by telephone by the social workers. The criteria of minimum age and completeness of family composition were the same as for the first group. Belonging to the second group were a small number of volunteers from personnel and their families of the Schofield Barracks. Thus there were a total of 939 suhjects who were included in the study. Table 1 shows the breakdown of these subjects by age, race, and sex. Dental Examination: The evaluation of the periodontal condition of the individuals was made according to the method described by Ratnfjord (1959) with slight modification. The Ramfjord procedure scores gingivitis, depth of periodontal pocket, calculus.

150

CHUNG,

KAU,

CHUNG

AND

S O H E N D E L

Table 1

Breakdown of subjects by age, race, and sex Age Race

20

21-.30 F

M

F

M

Caucasian Japanese Filipino Hawaiian or part-Hawaiian Samoan

54 27

71

1

17

2

37

25

36

34

17

24

Other

30 201

Total

31-40

41-50

M

F

6

25

38

2

2

«

7

7

7

13

21

2

8

10

4

6

8

4 9

32

0 1 1

5

3

4

203

12

26

61

81

contact, attrition,, mobility, and plaque. The modification involved was in the observation of periodontal pocket depth. Instead of deriving a periodontal score from observations on periodontal pocket depth and gingivitis score, the present study used the raw measurement of pocket depth in milinjcters independent of gingivits score. The pocket depth was measured apically from the cementum-enamel junction on the four surfaces (buccal, lingual, mesial, and distal) around the six teeth specified by Ramfjord without removing calculus. A score of 0 was assigned when the pocket did not extend apically to the level of the cementumenamel junction. The periodontal pocket depth of an individual was represented fay the mean of means of the examined teeth and will be referred to as average pocket depth. Gingivitis was scored according to the method of Ramfjord but was treated separately from pocket depth in our study. In addition the measurement of deepest periodontal pocket in millimeters was recorded and used in the analysis. All other variables were scored strictly according to the procedure of Ramfjord. Tooth maialignment was expressed by the total number of malaligned teeth (both major and minor types) following the method used in the eariier study (Chung et al. 1971).

M

Total

61 +

51-60

IF

M

F

M

F

60

54

15

S

1

1

334

24

32

8

e

3

134

25

14

5

7

0 1

169

3

4

0

1

1

103

2 7

2

2

0

12

13 11

2

1

3

S8 111

13iB

138

50

26

15

6

939

Dental examinations were performed principally hy two dentists (M.C.W.K. and S.S.C.C.) with periodic calibrations in the scoring technique between them. During the cotirse of study, the data obtained by the two examiners were monitored through a computerized procedure for a possible consistent discrepancy. Suhjects were assigned to each examiner at random with respect to age, sex, and race. The two dentists exatnined approximately equal number of subjects. Questionnaire Information: Each subject was asked to provide information on sociological, biological, medical,, and dental variables prior to the dental examination. The questions were on birth date, sex, race, occupation, number of years of education, consanguinity of the parents, smoking history, and frequency of toothbrushing per day. Medical and dental questions dealt with histories of blood or heart disease, diabetes, aUergy, tooth extraction, and periodontal disease. Method of Analysis: Analysis of associations of epidemiologic factors with periodontal disease was carried out in two ways. Firstly, all of the periodontal disease variables were treated individually in relation to epidettii-

P E R I C D O N T A L

DISEASE

ologic and racial variables. The periodontal disease variables considered were gingivitis, mean pocket depth, deepest pocket depth, calculus, contact, attrition, mobility, and plaque. Secondly, these variables were subjected to a principal component analysis (see Kendall 1957, Morrison 1967) in order to reduce the dimensions of the eight disease variables to a smaller but meaningful number. This approach led to the formation of a composite index derived from all of the variables considered above. This method has been employed successfully in the analysis of malocclusion (Chung et al 1971). The analysis used the correlation matrix derived from the pooled sums of squares and products formed within the six racial groups to be described. Statistical analysis was carried out in several steps. This procedure was followed because of logical grouping of those epidemiologic factors as related to the periodontal disease variables. At the first stage, a periodontal disease variable v^as regressed stepwise on a group of demographic variables, which consisted of sex (0 = female, 1 = male), age in years, age squared, years of education, and years of education squared. This group of variables represent those whose effects are usually recognized and should be adjusted for in testing the effects of other factors of interest. This analysis was performed within racial grotips by using the pooled sums of squares and products. The quadratic terms were included to detect a possible non-linear relationship. The second stage involved stepwise regression analysis of the periodontal disease variables in relation to genetic, medical, and dental variables within racial groups after fitting the demographic variables proved significant in the preceding analysis. This group of variables are listed in Table 2. At the final stage the racial effects were tested by introduction of design variables by the regression method after fitting the variables

IN

HAWAII

151

Table 2 Description of genetic, medical and dental variables studied VariabJe

Description

inbreeding coefficient

Coefficient of Wright (1922| derived from consangiiiini'ty of ihe parents Present = 1, absent = 0 Present = 1, absent = 0 Present = 1, absent = D' Present = 1, absent = 0 Yes = 1. mo = 0 Number of cigarettes smoked' per day Frequency per day Positive = 1, negative = D

Blood' disease Heart disease Diabetes Allergy Pregnancy Smoking Toothbrushing History of orthodontic treatment: History of canker sores Tooth maialignment

Positive = 1, negatiive =: 0 Total number of malalignment

found significant at the two preceding tests. Differences of racial means in the periodontal disease variables were tested further by the multiple range test (Duncan 1955) after the means were adjusted for significant covariates noted above. For the purpose of studying racial effects, the subjects were classified into Caucasian, lapanese, Filipino, Hawaiian or part-Hawaiian, Samoan, or Other. Because of a small number of unmixed Hawaiians, this group of individuais were pooled with partHawaiians and will be referred to as Hawaiins or part-Hawaiians. The last category of "Other" includes individuals of other unmixed or mixed racial origin. This classification of race gave rise to five design variables as shown in Table 3 to be used for the test of racial differences. Thus the racial effects were first tested as deviation from the Caucasian base. Differences among Filipinos, Hawaiians or part-Hawaiians,, and Samoans were tested by introducing a new variable in which the Filipino variable was nested and the effects of the other two races were studied as deviation from the mean of the common variable. The difference be-

152

CHUNG,

KAU,

CHUNG

Table 3 Dummy variables designed to test racial differences Race combination

X,

X.

Caucasian Japanese Filipino Hawaiian or pairt-Hawaiian Samoain Other

0 1 0

0 0 1

0 0 0

0 0 0

X4

K5

0 0 0

0 0 0

0 0 0

1 D 0

0 1 0

0 0 1

tween Hawaiians or part-Hawaiians and Samoans was examined similarly. Not all of these analyses were done simultaneously. Finally, average pocket depth, which is the single most informative variable for periodontal health status, was subjected to further specific analysis. In this regression analysis calculus and plaque scores were treated as covariates along with other significant demographic and epidemiologic variables. This step was taken to further evaluate net racial differences after controlling the ethnic variation in oral hygiene practice not necessarily of biologic origin. Results

Table 4 shows the results of regression analysis of the periodontal disease variables as a function of two sets of independent variables. The first set represents demographic characteristics of the individual, namely sex, age and number of years of education. The significant partial regression coefficients of these variables are shown at the upper part of Table 4. As expected from nutnerous other studies,, our data showed a clear adverse effect of advancing age on all of the variables except for plaque score. The number of years of education was significantly associated with the variables of periodontal health such that the more education one had, the better was his periodontal condition. This finding is again consistent

AND

S C H E N D E L

with the results of other studies which related socioeconomic status to periodontal disease (Russell 1957, Russell & Ayers 1960, Kelly & Van Kirk 1965). Males were shown to have higher risk than females in major periodontal disease indicators such as gingivitis, average pocket depth, calculus, and plaque, being consistent with the findings of other studies (Russell 1957, Kelly & Van Kirk 1965). In general significant variables among the five demographic factors explained 8 % to 39 % of the variations of the periodontal disease indicators as seen by the multiple correlations squared (R*) in Table 4. Higher percentages (21 % to 39 %) were noted in pocket depth, calculus, and attrition. The lower part of Table 4 shows the result of the regression analysis of those independent variables given in Table 2 after fitting the demographic variables found significant in the preceding analysis. The table lists only those factors which exhibited significant association with at least one of the periodontal disease variables. Amount of smoking was found to be positively associated with major periodontal variables including gingivitis, average pocket depth, deepest pocket, and calculus. The adverse effect of smoking confirms the earlier findings (Arno et al. 1959, Summers & Oberman 1968). The relationship between perio-

NUMBER OF CIGARETTES SMOKED PER' ,my Fig. 1. Average poci