Archs oral Bid.
Vol.
15. pp. 1231-1244,
1970. Pergamon
Press.
Printed in Gmt
Britain.
EPIDEMIOLOGY OF PERIODONTAL DISEASE IN WESTERN NIGERIANS IN RELATION TO SOCIO-ECONOMIC STATUS C. 0. E~wo~vu* Department
and J. C. EDOZIEN
of Nutrition, Massachusetts Institute of Technology, Cambridge, Mass. 02139, U.S.A.
Summary-An epidemiological survey was carried out in the Yoruba ethnic group of Western Nigeria in 1965. The survey was undertaken to determine the relation of periodontal health to socioeconomic status, and included 941 persons. The age groups between 5 and 19 yr comprised 53 per cent and 95 per cent of the low and high socioeconomic communities respectively. Russell’s Periodontal Index (PI) and the Simplified Oral Hygiene Index (OHI-S) comprising the Debris and Calculus Indices @I-S and CI-S) were recorded. Evaluation of the nutritional status of the communities was carried out by studies of the dietary intakes and the biochemical estimation of blood haemoglobin, serum proteins and serum ascorbic acid levels. In both communities, CI-S and age were closely correlated with PI. At all ages, the same level of CI-S was associated with a higher PI score in the low than in the high socioeconomic group. Multiple correlation analysis indicated some residual variation in PI not accounted for by age, CI-S and DI-S, and this was more evident in the low socio-economic group. Clinical, dietary and biochemical studies suggested marked deficiencies of essential nutrients in the low socioeconomic group. The survey showed that, in addition to the oral hygiene, due attention should be paid to the host state and his environment in planning prophylactic measures for periodontal lesions especially in malnourished populations. INTRODUCTION
CONSIDERABLE variation exists in the prevalence and severity of periodontal disease throughout the world (WHO, 1961). Broad epidemiological surveys indicate extremely high prevalence in all age groups examined in the developing countries in Africa and Asia (GREENE, 1960; RAMFJORD,1961; EMSLIE, 1966). Similar findings have been reported in Nigerians (EMSLIE,1963; SHEIHAM,1966). In the Yoruba tribe of Western Nigeria, extensive pocket formation with destruction of the supporting tissues of the teeth was seen in 82.5 per cent of individuals aged 25 yr and over (SHEIHAM,1966) while EMSLIE(1963) noted that the severity of periodontal disease in Nigerian children was greater than reported findings (GREENE,1960) for similar age groups in India. Most of the reported studies of periodontal health in Nigerians have been concerned mainly with the disease-producing agents and have not taken an adequate ecologic approach which should recognize in addition, the vital role of the host and his environment. A thorough study of the victim on whom the disease-producing agents act as + Present address: Department of Oral Biology, University of Washington, Seattle, Washington 98105, U.S.A. 1231
1232
C. 0.
ENWONWU AND J. C. EDOZIEN
well as his conditions of life, social, economic, and educational, is an important step towards a better understanding of the disease process. Malnutrition is an immense problem in Nigeria, with extreme variations prevailing within and between different ethnic groups. In an attempt to examine the possible role of nutritional imbalances in the pathogenesis of periodontal lesions, we have in this study paid attention to the major indices of socio-economic status in the assessment of prevalence and severity of periodontal disease within a single ethnic group in Nigeria. MATERIALS
AND METHODS
Selection of study sample
Since socio-economic status is a vague, nonspecific terminology, it was necessary to determine and define the criteria to be adopted in the classification of the samples. These criteria should be such as would bring out distinctly any effects of the gross disparity in living standards of the population groups studied. Material items have been previously regarded as the best indicator of living standards in the Yoruba tribe of Western Nigeria (GALLETTI,BALDWINand DINA, 1956). Preliminary observation of the Yoruba communities in Ibadan, the capital city of Western Nigeria, indicated that this was not a reliable index since the worst conditions of environmental hygiene and malnutrition were seen in many homes where the most modern material comforts were to be found. Such apparently wealthy groups were mainly uneducated cocoa farmers who do not absorb the values of the social stratum to which they might be entitled, but rather tend to live like their tribal counterparts in the less developed rural areas. This observation questions the validity of arbitrary classification of population groups in Africa into rural and urban communities in studies aimed at elucidating the role of socio-economic factors in desease prevalence and severity. In this study, we adopted such criteria as educational attainments, dietary habits, child health and infant mortality as the essential indices of socio-economic status. The low socio-economic group was drawn from Osegere village, a relatively static rural Yoruba tribal community of just over 3000 people, and situated 16 miles northeast of Ibadan in the rain forest belt of Western Nigeria. The high socio-economic group, often referred to in this report as the “optimal group” was drawn from the Yoruba families in the academic staff of the University of Ibadan. The inclusion of a family within the latter group involved rigorous tests. The family must be monogamous and both parents should be of Yoruba origin. In order to make the sample as comparable as possible to the low socio-economic community, all individuals in the high socio-economic group who had received professional dental care were excluded. Dietary habits
The diet of Osegere village community is based on a sedentary hoe agriculture and it is overwhelmingly carbohydrate in nature. The main staple food is cassava (Manihot utillissima) which has a crude protein content of 2.6 per cent. Usually, the cassava is grated, fermented and fried to produce gari before it is eaten and the processing reduces the crude protein content three-fold (OKE, 1966). Gari is often eaten with a
EPIDEMIOLOGY
OFPERIODONTALDISEASE INWESTERN NIGERIANS
1233
vegetable broth or soup of palm-oil. Analyses of the ascorbic acid contents of the common vegetables used as food in such Western Nigerian rural communities (OKE, 1967a) indicate that as much as 50-80 per cent of the vitamin is lost either by previous exposure to the sun in open markets or during the cooking process. Fresh fruits available in Osegere village are sold in the nearby city and rarely eaten by the villagers since the belief still prevails that fruits cause diarrhoea. Animal products are scarce and expensive. As in most cultures of the underdeveloped world, Osegere natives have not yet evolved an effective way of feeding the young child after weaning. Ogi is the postweaning diet in this village, and it consists mainly of the starch isolated by sieving milled corn (Zea muys) with a large volume of cold water. The globulins and most of the germ leach out during the processing of corn into ogi. The latter has a crude protein content of 6.9 per cent as against 11.8 per cent in the original cereal (OKE, 1967b). In this village, the protein-calorie malnutritional syndrome called kwashiorkor is highly prevalent, and child mortality in the first 5 yr of life is of the order of 46 per cent. The mortality rate within the first year of life is 20 per cent (EDOZIEN, personal observations). There is good evidence (WILLS and WATERLOW, 1958; BENGOA,JELLIFFEand PEREZ, 1959) that such high mortality figures especially in the 2-5 yr age group, indicate low nutritional status as well as poor health and socioeconomic standards. The dietary intake of the high socio-economic group was comparable to that of the middle and upper-middle classes in the technically developed parts of the world. The infant mortality in this group contrasted sharply with findings among their less privileged village counterparts and compared favourably with figures for the advanced countries. Methods All individuals examined were not informed previously about the survey. Every third house from a full list of all the houses in Osegere village was selected for sampling. All examinations were conducted by one of the authors (C.O.E.) under good natural light using Ash Number 5 mouth mirrors and Standard Ash dental probes with the patients seated on a portable dental chair. Oral hygiene status was assessed by the Simplified Oral Hygiene Index (OHI-S) of GREENEand VERMILLION(1964) which comprises the Debris Index (D&S) and Calculus Index (CI-S). Periodontal health was evaluated by the Periodontal Index (PI) of RUSSELL(1956). The brief visit of Dr. A. L. Russell to Nigeria while the survey was in progress afforded a unique opportunity for calibrating the examiner. In the survey, 402 Osegere village inhabitants and 539 members of the high socioeconomic group were examined. Table 1 shows the distribution of the study sample according to socio-economic status and age. For the high socio-economic group, it was not possible to include individuals over the age of 29 yr without running the risk of incorporating people whose early development was difficult to ascertain, and this might have occurred outside their present status. Findings in the males and females are pooled since preliminary analyses of the results indicated no marked differences between the sexes.
1234
C. 0.
ENWONWU AND J. C.
ED~ZIEN
TABLE1. NUMBER
OF PERSONSEXAMINED BY AGE GROUP AND %X210-ECONOMICSTATUS: WESTERN NIGERIA1965
Osegere village Age group 5-9 10-14 15-19 20-29 30-39 40-49 50 and over Total
Number examined 86 85 43 52 59 39
High socio-economic group
Mean age I.3 11.6 16.7 25.4 33.5 42.9 -
Number examined 110 186 218 25 539
Mean age 7.1 12.9 16.7 22.4 -
Biochemical studies
Blood samples were collected after an overnight fast from random sampling of the youngest age groups in both communities. Haemoglobin was estimated by the standard method of DACIE (1956). Total serum protein was measured spectrophotometrically by the biuret technique (WOLFSON et al., 1948). Electrophoretic separation of protein fractions was by the method of FLYNN and DE MAYO (1951), and the papers were scanned in the Chromoscan, an automatic reflectance scanner produced by Joyce, Loebl. & Co., Newcastle, England. Serum ascorbic acid was determined by the calorimetric method of ROE and KUETHER (1943). RESULTS Oral Hygiene Status and Periodontal Index Scores
Irrespective of age, most of the individuals examined in Osegere village showed massive accumulations of oral debris and calculus. Among the village children, mouths with teeth completely enveloped in deposits were seen occasionally. In some cases, the deposits extended into the vestibule of the mouth causing marked irritation of the adjoining soft tissues of the cheek. Table 2 shows the mean periodontal, debris, calculus and oral hygiene scores classified by age group for all persons examined in the two communities. For an easier visualization of the trends, the findings in Table 2 are represented in Fig. 1 and Fig. 2 for the high socio-economic and village groups respectively. In all age groups, CI-S was higher in the village than in the high socio-economic group. The mean calculus scores in the lowest age group were l-83 and 0.45 for the village and “optimal” groups respectively, and the difference was statistically significant at the 1 per cent level. In both communities, calculus level increased with age. The CI-S for the 20-29 yr age group in the “optimal” community was of the same order of magnitude as that for the youngest age group examined in the village. At all ages, OHI-S was lower in the high socio-economic group than in the village community. The most marked difference between the two communities was observed
NIGERIANS
EPIDEMIO~Y OP PERIODONTAL DISEASEIN WESTERN
1235
TABLE 2. MEAN PERIODONTAL,DEBRIS,CALCULUS,AND SOCIO-ECONOMIC
ORAL HYGIENE INDEX SCORES BY AGE STATUS FOR ALLPERSONS EXAMINED
AND
Mean index scores High socio-economic
Osegere village Age w
5-9 lo-14 15-19 20-29 30-39 40-49 50 and Over * t $ J
group
group
PI*
DI-St
CI-S:
OHI-S§
1.85 2.15 2.63 3.43 4.63 5.80 6.45
I.86 1.47 1.10 1.19 1.15 1.20 1.39
1.83 2.02 1.98 2.09 2.28 2.30 2.61
3.66 3.49 3.10 3.30 3.41 3.57 4.01
PI
DI-S
CI-S
OHI-S
0.50 1.36 1.44 1.93 -
1.15 1.30 1.24 0.84 -
0.45 1.54 1.63 1.76 -
1.60 2.85 2.87 2.61 -
Periodontal Index. Debris Index score. Calculus Index score. Oral Hygiene Index score.
Periodontal Calculus
7.0 1
m
Debris
index (PI) index
index
Oral hygiene
(Cl-S)
(DI-S) index
(OHI-S
6.0
)
i
5-9
IO-14
15-19
20-29
Age group
FIG. 1. Mean Periodontal,
Debris, Calculus, and Oral Hygiene Index scores by age group for the “optimal” community.
1236
C. 0. ENWONWU AND J. C. EDOZIEN Periodontol 70,
z
index
Cakulus index Debris Oral
(PI)
(CI-S)
Index
(M-S)
hygwne
index
(OHI-S)
5.0
2
40
D
.c ;
2
3.0
2.0
l-0
5-9
IO-14
15-19
20-29
30-39
40-49
501
Age group FIG. 2. Mean Periodontal,
Debris, Calculus and Oral Hygiene scores by age group for the Osegere village community.
in the youngest age group with the village children showing more than a two-fold increase in OHI-S over their high socio-economic group ethnic counterparts. In both communities, the PI scores showed consistent increase with age. A comparison of the two populations indicates that some degree of gingival pathology was detectable in the mouth of an average high socio-economic group child aged 5-9 yr (Table 2). At this age, with a PI score of 0.5, the change was essentially inflammatory with no clinical evidence of periodontal destruction. This was in sharp contrast to the condition in Osegere children who at the age of 5-9 yr, and with mean PI score of 1.85, showed well-established periodontal disease. By the mid-teens, most of the village children have approached the terminal stages of periodontal destruction with widespread alveolar bone resorption. In the “optimal” community, marked periodontal destruction was not evident until the second decade of life. Statistical analyses of jindings
For an assessment of the effects of dental calculus, oral debris and age on the periodontal status, correlation coefficients were calculated. In order to simplify the procedure, linear relationships between the dependent variable (PI), and the independent variables (CM, DI-S and Age) were assumed in the choice of computer program. Table 3 shows the simple linear correlation coefficients between the variables for the two communities. In the high socio-economic community, CI-S showed the strongest positive correlation with PI whilst in the village sample, age showed the
EPIDEMIOLOGY OF PERIODONTAL DISEASEIN WESTERN
NIGERIANS
1237
TABLE 3. SIMPLE LINEAR CORRELATION MATRICES FOR THREE SELECTED INDEPENDENTVARIABLES(AGE, DEBRIS,CALCULUS),WITHPERIODONTALINDEX SCOREASTHEDEPENDENTVARIABLE,FORTHEHIGH AND
L~WSOCIO-ECONOMIC
GROUPS: WESTERNNIGERIA 1965 Variable
4s Variable
B
A
l-00
-0.06 1.00
A
Age Debris Index score Calculus Index score
1.00
-
Calculus score
Debris score
-
B
-0.25 I.00
Periodontalscore
A
B
A
0.66 0.23 -
0.51 0.08 1.00
0.63 0.22 0.89
B
0.84 -0.16 0.56
A: High socio-economic group. B: Osegere village community.
strongest correlation with the dependent variable (PI). Since the village sample included much older age groups than the “optimal” community, linear correlation matrices were also calculated for the younger age groups in the former. As shown in Table 4, CI-S was stronger than age in its association with PI in the three youngest age groups examined in the village. In none of these age groups was the degree of correlation of
CM with PI as strong as in the “optimal” community. In Table 5, the mean periodontal scores are classified by age as well as CI-S. It is seen that within the same age group, persons with lower calculus scores tended to experience less severe periodontal disease than individuals with more deposits. In the 5-9 yr age group in the village sample, the PI score was l-20 when the CI-S was less than l-0. With increase in CI-S to l-l a9 and 2-3, the PI scores increased to 1.86 and 2 *08 respectively. A similar trend was observed in the “optimal” sample. There is also good evidence from Table 5 that in each age group, the same degree of calculus accumulation was associated with more periodontal damage in the village than in the “optimal” population. This was most evident in the 5-9 yr group where with a CI-S of TABLE ~.SI~LF LINEAR CORRELATION MATRICES FOR THREE SELECTED INDEPENDENT VARIABLES (AGE, DEBRIS,CALCULUS) WITHPERIODONTAL INDEX As THRDEPENDENT VARIABLEFORTHE FOUR YOUNGEST AGEGROUPS EXAMINEDIN OSEGERF.VILLAGE
Variable Age Variable Age Debris Index Calculus Index
1.00
A.O.B. 15/12-I
Debris Index
Calculus Index
Periodontal Index
5-9 10-14 15-19 20-29
5-9 lo-14 15-19 20-29
5-9 lo-14 15-19 20-29
0.05 -0.49 1.00
-0.35
0.25
O-13 -0.08 0.23
0.00
0.39
0.06 -0.05
0.08 0.11
0.33
0.24 -0*08-0.12
1.00
0.67
0.41
0.34 0.45 0.17
0.40 0.30
1238
C. 0. ENWONWUAND J. C.
EDOZIEN
TABLE 5. MEAN PERIODONTAL INDEX SCORES BY AGE AND CALCULUS HIGHSOCIO-ECONOMICCOMMUNITIES
Mean Periodontal (calculus
In::;
Index scores y
Number of persons
group)
2-3
Agegroup (yr) 5-9 10-14 15-19 20-29
SCORES FOR THE VILLAGE AND
A
B
A
B
A
B
0.44 0.54 0.70 +
1.20 + -
1.11 1.34 1.38 1.92
1.86 1.96 2.20 3.08
1.87 1.88 +
2.08 2.46 3.43 4.29
(Calculus I;dTF
10 1 -
10 126 155 22
61 51 28 34
group) 2-3 ___ A B
38 43 2
:: 15 18
A: High socioeconomic
group. B: Osegere Village group. + : Mean Periodontal Index scores not calculated for fewer than 10 cases.
less than 1.0, the village children showed a three-fold increase in PI score over their high socio-economic group counterparts. On the assumption that the observed changes in periodontal status were the direct effects of the independent variables, the results have been further analysed for the multiple correlation coefficients which indicate the simultaneous effects of these independent variables on the dependent variable. The relative importance of each of the independent variables as contributors to the total variance explained was calculated according to SNEDECOR (1956). Table 6 shows that the proportion of the variance in periodontal health explained by the simultaneous effects of the independent variables for individuals aged 5 to 29 yr was higher in the high socio-economic group (O-81) than in the village sample (0 - 30). As expected from the findings in Tables 3 and 4, calculus and age accounted for most of the explained variance in periodontal status. The findings in Table 6 also indicate that if the tested independent variables have a TABLE 6. EPFECXSONPERIODONTALSTATUSOFAGE,ORALDEBRISSCORESAND CALCULUS SCORES CONSIDERED SIMULTANEOUSLY FOR OSEGERE AND SOCIO-ECONOMICINDIWDUALS,AQED 5-29 YEARS
Item Coefficient of multiple correlation (R)* Multiple determination coefficient (R2) Of the explained variance, per cent due to the effects of (a) Age (b) Dental calculus (c) Oral debris
Osegere Village +0*55 0.30
39 46 15
HIGH
High socioeconomic group +0*90 0.81
36 51 13
l Multiple correlation coefficient was calculated on an IBM 1620 Computer at the University of Bristol, Bristol 8, England.
WJBTERNNIGERIANS
EPIDEMIOUX~YOFPERIODONTALDISEASEIN
1239
role in the aetiology of periodontal disease, there is still some residual variation in the observed periodontal status not accounted for, and this could be attributed to other unknown contributory factors. The low multiple determination coefficient in the village sample compared with the “optimal” sample would suggest that the unknown independent factors had more marked effects in the former than in the latter community. Biochemical results
The total serum proteins levels for the 5-9, and IO-14 yr age groups in the village sample were within the same range as those of their age counterparts in the high socio-economic community (Table 7) but differed in that the serum of the village population contained less albumin, and more globulin than the serum of the “optimal” population thus giving lower values for the albumin/globulin ratio. As also shown in Table 7, blood haemoglobin values were lower in the village community than in the high socio-economic group, although the values for the former group were within the range of acceptable values (ICNND, 1963). In Table 8, the serum ascorbic acid values recorded in the two communities have been interpreted using PEARSON'S (1962) guide for the correlation of serum vitamin C levels with dietary intake. In the high socio-economic group children, 85 per cent of the individuals studied had serum ascorbic acid levels above 0 *2 mg per 100 ml of serum which was equivalent to dietary intakes of ascorbic acid above 30 mg daily. None of the individuals in this well-fed group had a daily dietary intake of less than TABLE7.
COMPARISON
OF SERUM
PROTEIN AND BLOOD HAEMOGLOBM LEVELS IN ANDTHEHIGHSOCIO-ECONOMICINDIVIDUALS
High socio-economic
Osegere village
5-9 yr
Total serum protein km/lOOml) Albumin (gm/lOOml) Globulin (gm/lmml) Albumin/globulin ratio (per cent) Haemoglobin (g/lOOmU n : Number examined. 2’: Mean value. S: Standard error.
R
5-9 yr
lo-14 yr
?l=40 Item
n = 19 s
THE OSEGEREVILLAGE
1
group lo-14 yr
n = 15 s
2
s
R
n = 12 s
7.10
0.10
7.37
0.08
6.73
0.17
7.92
0.16
2.64
0.02
2.86
0.07
3.50
0.09
3.99
0.11
4.46
0.08
4.53
0.06
3.22
0.12
3.93
0.11
59.81 11.62
1.48 0.24
63.45 12.86
1.91 0.18
110.74 13.71
4.59 0.30
102.32 13.08
3.74 0.29
C. 0. EIWONWIJ
1240
AND J. C. EDOZIEN
TABLE8. INTERPRETATION OF SERUMASCORBIC ACID VALUES IN OSEOERE AND HIGH SOCIO-ECONOMIC COMMUNInES*
Intake (mg per day)
Osegere Village
Serum ascorbic acid level (mg per 100 ml)
n
% of total
96 61 63 2
43.2 21.5 28.4 0.9
70 * Guide to interpretation n: number of persons.
High socio-economic group n
% of total
9 42 9
15 70 15
-
of data was from PEARSON (1962).
10 mg. In contrast, 43 - 2 per cent of the village sample, with serum ascorbic acid levels less than 0.1 mg per 100 ml serum, had daily dietary intakes of less than 10 mg. Only 29 *3 per cent of the village sample had dietary intakes of ascorbic acid above 30 mg daily. DISCUSSION
More than half of the world’s population is still afflicted with hunger and malnutrition. In such sub-economic areas of the world, any conclusions on the pattern and distribution of diseases should take a proper ecologic approach which should recognize the role of the host as well as his environment. In this epidemiologic study of periodontal disease in the Yoruba tribe of Western Nigeria, we have by paying attention to the major indices of socio-economic status attempted to bring into focus three salient but closely related factors, namely, the local disease-producing agents, the host on whom the agents act, and the environment. The prevalence as well as the severity of periodontal disease was found to be high in the Yoruba populations studied. The unusually high PI score of 1.85 observed in the age range of 5-9 yr in Osegere village (Table 2) compares well with the score of l-6 reported by EMSLIE (1963) for Western Nigerian children aged 2-5 yr and with similar background as our low socio-economic group. Even the selected high socioeconomic class in this ethnic group had higher periodontal index scores than have been reported for similar age groups in the urban and rural communities of other subeconomic areas of the world (GREENE, 1960; ICNND, 1961; RUSSELL, 1963). Such geographic variations in the severity of periodontal disease should not, however, be regarded as absolute differences in view of the lack of intercalibrations of the various investigators. The severity of periodontal disease observed in this survey was closely related to the socio-economic status of the individuals. The highest PI score recorded for the well-fed, educated group was 1.93 in the age group 20-29 yr and this was within the range of PI scores observed in the village children aged 5-9 yr (Table 2). Similar
EPIDEMIOLOOY OFPERIOWNTALDISEASE IN WFSTERN NIGERIANS
1241
observations between periodontal health status and socio-economic status have been reported in India (MEHTAet al., 1956) and the United States of America (RUSSELLand AYERS,1960; MOBLEYand SMITH,1963). Such relationships between health status and general socio-economic development are often not straightforward but buried in a complex matrix of multiple causes and feed-back interactions. In this study as in many others (METHA er al., 1956; EMSLIE, 1963), it was easy to demonstrate the significance of poor oral hygiene in the pattern and distribution of periodontal disease. Nevertheless, findings in this survey suggest that Osegere children, in comparison with the “optimal” community, suffer more severe periodontal disease than can be attributed solely to poor oral hygiene. This necessitates consideration of other factors which might modify the disease process. Among these factors is the host tissue resistance which itself is modified by a number of factors including the nutritional status of the organism. Clinical appraisals, al though nonspecific, suggested deficiencies of numerous essential food nutrients in our village community as judged by growth retardation and the universal occurrence of glossitis, cheilosis of the lips and angular stomatitis. The serum albumin value which is a better index of protein nutriture than total serum protein level was much lower in the Osegere population than in the “optimal” community. The values of 2 *64 g. and 2 - 86 g. per 100 ml of serum for the 5-9 and 1O-14 yr age groups respectively lie within the lowest limit of the normal range for Nigerians and only slightly higher than the values reported in cases of the established protein malnutritional syndrome of kwashiorkor (EDOZIEN, 1960). It is not unlikely that a small drop of serum albumin carries an unusually high degree of importance, and therefore indicative of chronic, marginal malnutrition. This suggestion is supported by the observation of WATERLOW(1963) that low levels of serum albumin found in clinically manifest kwashiorkor represent a late event. Dietary and biochemical studies also indicated a deficiency of ascorbic acid in the village population. Ascorbic acid levels below 0.2 mg per 100 ml of serum indicate the probability of marked vitamin C deficiency (PEARSON,1962). Only 29 *3 per cent of the village sample as against 85 per cent of the high socio-economic group (Table S), with mean serum ascorbic acid level above 0.2 mg per cent, met the daily optimum recommended requirement of 30 mg (BR. MED. RES. COUNC., 1948). Almost half of the Osegere village sample (43.2 per cent) had serum ascorbic acid levels below 0.1 mg per cent, suggesting daily dietary intakes of less than 10 mg. This level of vitamin C intake, although believed to be adequate for the prevention of scurvy in healthy adults (UHL, 1958), is nevertheless less than the amount which has been reported to be closely associated with gingival pathology in the human (BERRYand SCHAEFER,1958). In addition to multiple malnutritional state, Osegere villagers were subject to parasitic infestations and other numerous endemic diseases. It is against this background of infection and malnutrition that we must view the outcome of super-imposed local factors known to be associated with causation of periodontal disease. The cells the periodontal tissues are not static, and in time must be replaced in varying degrees by the nutrients obtained from food. Numerous studies in laboratory animals have shown the deleterious effects on the periodontal tissues of deficiencies of vitamins
1242
C. 0. ENWONWUAND J. C.
EDOZIEN
(HELD, 1966) and proteins (CHAWLAand GLICKMAN,1951; GOLDMAN,1954). Experimental protein deficiency of shorter duration and lesser severity than the magnitude encountered in chronically malnourished populations in African villages has been shown to produce osteoporosis of the alveolar bone, with degeneration of the periodontal fibres (STAHL, 1966). In addition, there is good evidence from wound healing studies that deficiencies of dietary protein (KOBAKet al., 1947) or of specific essential amino acids (LOCALIO,MORGANand HINTON, 1948; WILLIAMSON and FROMM,1953) interfere with the immunologic response of the host and thereby delay connective tissue healing. The observations on Osegere community run counter to findings in other studies (RUSSELLet al., 1965) aimed at relating nutritional status to periodontal disease. The reasons for the difference are not immediately clear and may in part be due to differences in the severity of malnutrition in the communities involved. The findings of this study do not in any way indicate that nutritional factors per se initiated the observed trends in the periodontium. Certainly they did contribute to the severity of the lesions observed in the village population by decreasing defence and the healing capacity of the tissues. The principal structural protein of the periodontal tissue is collagen, and its integrity is essential for the normal functioning of the tissue. There is good presumptive evidence from the experiments of CARNEIRO and FAVA DE MORAE~ (1965) and CLAYCOMBand SUMMERS(1965) in laboratory animals that the human periodontium is characterized by a constant renewal of collagen and therefore sensitive to food deficiencies and metabolic disturbances. Acknowledgements-This study was undertaken while Drs. C. 0. ENWONWU and J. C. EDOZIEN were Rockefeller Foundation Research Fellow and Dean of Medicine respectively at the University of Ibadan, Nigeria. The authors express their gratitude to the University authority for the research facilities. Dr. C. 0. ENWON~IJ wishes to thank Professors A. I. DARLING and E. W. BRADFORD of Bristol University, and Professor A. L. RUSSELL of the University of Michigan for their help and encouragement during and after the studies. Thanks are due also to Miss V. D. ALLDRED for her excellent secretarial assistance.
R&m&-Une ttude tpidkmiologique a CtCentreprise dans le groupe Bthnique Yoruba dans 1’Ouest de Nigeria, en 1963. L’Btude a kt&entreprisc pour dCterminer le rapport entre l’Ctat griodontique et la condition socio&onomique et comprenait 941 personnes. Le groupe d’lge entre 5 et 19 ans comprenait 53 pour cent et respectivement 95 pour cent des communaut6s socio-tionomiques basses et hautes. L’index p&iodontique de Russell(PI) et l’index simplifie d’hygikne orale(OHI-S) comprenant les index de debris et calculeux, @I-S et CI-S) ont &t&enregistrb. L’Cvaluation de la condition nutritive des communaut& a CtCentreprise par l’btude diCtCtiquede l’alimentation et 1’6valuation biochimique de l’hkmoglobine du sang, les protCines du s&rum et le niveau de l’acide ascorbique dans le s&urn. Dans les deux communautks, le CI-S et l’Lge ktaient en corrblation Ctroite avec le PI. Dans tous les groupes d’Lge le meme niveau de CI-S etait associe avec un pointage plus 6levk du PI dans le groupe socio-&onomique has que dans l’autre groupe. Des multiples analyses des correlations indiquaient quelques variations r&duelles du PI, pas
EPIDEMIOUX~YOF PERIODONTALD~SEASEINWESTERNNIOERIANS
1243
expliquees par I’&, le CI-S et le DI-S et ceci &it plus evident dans le groupe socioeconomique bas. L’etude montre qu’en plus de I’hygiene orale, une grande attention devrait &e faite a la condition de l’individu et de son environment, quand on fait le plan des mesures prophylactiques pour les lesions p&iodontiques, surtout dans les populations ma1 nourries.
Zusammenfassung-In 1965 wurde an der Yoruba Volksgruppe in Westnigeria eine Zusammenfassung iiber Epidemien ausgearbeitet. Dieser Uberblick wurde unternommen, um die Beziehung von periodontalen Zustgnden auf den Status von 941 Personen festzustellen. In der Altersgruppe von 5 bis 19 Jahren kamen 53 Prozent aus den niedrigen und 95 Prozent aus den hohen sozialiikonomischen Gemeinschaftslassen. Russels Periodontaler Index (PI) und der Vereinfachte Orale Hygiene Index (OHI-S), die Zahn- und Zahnfleischsch%den registrieren, wurde xur Aufzeichnung verwendet (DI-S und CI-S). Beurteilung des Emiihrungszustandes in den Gemeinschaften wurden durch Studien fiber die Emghrung und biochemische Schiitzung des Bluthamoglobins, Serumproteins und der Ascorbinsiiumspiegel im Serum gemacht. In beiden Gemeinschaften waren CI-S und Alter in enger, wechselseitiger Beziehung mit PI. In allen Altersklassen war in der niedrigen, soxialbkonomischen Gruppe dieselbe Anzahl von CI-S-fallen mit einer hijheren Punktexahl von PI verbunden als in den hoheren sozialiikonornischen Gruppen. Eine verzweigte Wechselseitigkeitsanalyse deutet an, dass eine restliche Variation in PI weder auf Alter, CI-S oder DI-S zuriickgefiihrt werden kann, was bei der niedrigen soxialtikonomischen Klasse deutlicher zum Vorschein kam. Klinische, diatische und biochemische Studien lassen darauf schliessen, dass bei den niedrigen sozialiikonomischen Klassen bedeutender Mange1 an unentbehrlichen Lebensmittel herrscht. Der Uberblick xeigte, dass ausser Berticksichtigung von oraler Hygiene, entsprechende Aufmerksamkeit auf den Staat selbst und seine Umgebung bei Planung von prophylaktischen Massnahmen fiir periodontale Schlden, besonders bei untererniihren Vijlkem geschenkt werden sollte.
REFERENCES BENGOA,J. M., JELLIFFE,D. B. and PEREZ, C. 1959. Some indicators for a broad assessment of the magnitude of protein-calorie malnutrition in young children in population groups. Am. J. Clin. Nutr. 7, 714-720. BERRY, F. B. and SCHAEFER.A. 1958. Nutrition surveys in the Near and Far East. Report of the Interdepartmental Committee on Nutrition for National Defense. Am. J. Clin. Nutr. 6, 342-353. Barrrsrr MEDICAL R~EARCH COUNCIL. 1948. Vitamin C. requirement of human adults. Luncet 1, 853-858. CARNEIRO,J. and FAVA DE MORAES,F. 1965. Radioautographic visualization of collagen metabolism in the periodontal tissues of the mouse. Archs oral Biol. 10, 833-848. CHAWLA, T. N. and GLICKMAN,I. 1951. Protein deprivation and the periodontal structures of the albino rat. Oral Surg. 4, 578-602. CLAYCOMB,C. K. and SIJMMIXRS, G. W. 1965. Multi-peak incorporation of H3-proline into oral collagen, Archs oral Biol. 10,319-322. DACI~.,J. V. 1956. Practical Haematology, 2nd edn. p. 27, Churchill, London. EDOZIEN, J. C. 1960. The serum proteins in kwashiorkor, J. pediat. 57, 594-603. Er+rs~re,R. D. 1963. Cancrum oris. Dent. Pruct. 13,481-495. EMLIE, R. D. 1966. A dental health survey in the Republic of Sudan. Br. dent. J. 120,167-178. FLYNN, F. V. and DE MAYO, P. 1951. Microelectrophoresis of protein on fllter-paper. Lancer 2, 235-239. GALLETIT, R., BALDWIN,M. D. S. and DINA, I. A. 1956. The Nigerian Cocoa Farmers: The Patterns of Consumption wuf Living, p. 7. Oxford University Press, London. GOLDMAN,H. M. 1954. The effects of dietary protein deprivation and of age on the periodontal tissues of rat and spider monkey. J. Periodont. 25, 87-96.
1244 GREENE,
C. 0. ENWONWUAND
J.
C.
EDOZIEN
J. C. 1960. Periodontal disease in India. Report of an epidemiological study. J. dent. Res. 39, 302-312. GREENE, J. C. and VERMILLION, J. R. 1964. The simplified oral hygiene index. J. Am. dent. Ass. 68, 25-31. HELD, A. J. 1966. Periodontal diseases and general Pathology. ht. dent.J. 16, 260-269. ICNND. 1961. The West Indies. Nutrition Survey. A report by the Interdepartmental Committee on Nutrition for National Defense, N.I.H., Bethesda, Md. U.S.A. ICNND. 1963. Manual for Nutrition Surveys, 2nd edn, p. 235, Interdepartmental Committee on Nutrition for National Defense, N.I.H., Bethesda, Md. U.S.A. KOBAK, M. W., BENDI~T,E. P., WISSLER,R. W. and STEFFEE,C. H. 1947. The relation of protein deficiency to experimental wound healing. Surg., Gynec., Obstet. 85,751-756. LOCALIO,S. A., MORGAN,M. E. and HIN~~N J. W. 1948. The biological chemistry of wound healing. I. The effect of DL-methionine on the healing of wounds in protein-depleted animals. Surg., Gynec., Obstet. 86, 582-590. MEHTA, F. S., SANJANA,M. K., SHROFF,B. C. and DOCTOR,R. H. 1956. Prevalence of periodontal (parodontal) disease. 5. Epidemiology in Indian child population in relation to their socioeconomic status. Znt. dent. J. 6, 31-40. MOBLEY,E. L. and SM~XX,S. H. 1963. Some social and economic factors relating to periodontal disease in young Negroes. J. Am. dent. Ass. 66,486491. OKE, 0. L. 1966. Chemical studies on some Nigerian foodstuffs-“Gari”. Nature, Lond. 212, 10551056. OKE, 0. L. 1967a. The ascorbic acid content of Nigerian vegetables. J. Food Sci. 32, 85-86. OKE, 0. L. 1967b. Chemical studies on the Nigerian foodstuff “Ogi”. Food Technol. 21, 98-100. PEARSON,W. N. 1962. Biochemical appraisal of the vitamin nutritional status in man. J. Am. Med. Ass. 180,49-55. RAMFIORD,S. P. 1961. The periodontal status of boys 11-17 yr old in Bombay, India. J. Pertodont. 32,237-248. ROE, J. H. and KUETHER,C. A. 1943. The determination of ascorbic acid in whole blood and urine through the 3,4_dinitrophenylhydrazine derivative of dehydroascorbic acid. J. biol. Chem. 147, 399407. RUSSELL,A. L. 1956. A system of classification and scoring for prevalence surveys of periodontal disease. J. dent. Res. 35, 35&359. RUSSELL,A. L. and AYERS,P. 1960. Periodontal disease and socioeconomic status in Birmingham, Ala. Am. J. Publ. Hlth 50, 206-214. RUSSZLL,A. L. 1963. International Nutrition Surveys. A summary of preliminary dental findings. J. dent. Res. (Suppl.) 42, 233-247. RUSSELL, A. L., LEATHERWOOD,E. C., FRANK CONSOLAZIO,C., and VAN REEN, ROBERT. 1965. Periodontal disease and nutrition in South Vietnam. J. dent. Res. 44, 775-782. SHEIHAM,A. 1966. The prevalence and severity of periodontal disease in rural Nigerians. Dent. Pratt. 17, 51-55. SNEDECOR,G. W. 1956. Statistical Methods, p. 420, Iowa State College Press, Ames, Iowa. STAHL, S. S. 1966. Response of the periodontium to protein-calorie malnutrition. J. oral Med. 21, 146-151. UHL, E. 1958. Ascorbic acid requirements of adults: 30 mg or 75 mg? Am. J. Clin. Nutr. 6, 146-150. WATERLOW,J. C. 1963. The assessment of marginal protein malnutrition. Proct. Nutr. Sot. (Engl.) 22, 66-71. WILLIAMSON,M. B. and FROMM,H. J. 1953. Utilization of sulphur amino acids during healing of experimental wounds. Proc. Sot. exp. Biol. Med. 83, 329-333. WILLS, V. G. and WATERLOW,J. C. 1958. The death-rate in the age-group one to four years as an index of malnutrition. J. trop. Paediat. 3, 167-170. WOLFSON,W. Q., COHN, C., CALVARY,E. and ICHIBA,F. 1948. Studies in serum proteins. V. A rapid procedure for the estimation of total protein, true albumin, total globulin, alpha globulin, beta globulin and gamma globulin in 1-O ml of serum. Am. J. Clin. Path. 18, 723:730.WORLD HEALTHORGANIZA~ON(WHO). 1961. Periodontal Disease. Report of an Expert Committee on Dental Health, Technical Report Series No. 207. World Health Organization, Geneva.