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Relation between Ascorbic Acid Intake and Periodontal Disease in the United States
JABA
The possible association between deficiency of ascorbic acid and periodontal disease is scrutinized by the results of the data from the NHANES I survey.
Relation between ascorbic acid intake and periodontal disease in the United States
Am id I. Ismail, BDS, M PH Brian A. Burt, BDS, M PH, PhD Stephen A. Eklund, DDS, M H S A , DrPH
T
-H- he relation between levels of ascor bic acid (vitamin C) intake and periodon tal disease status has been of interest ever since the poor gingival condition of people with scurvy was observed long ago.1 Studies with guinea pigs2 8 and monkeys9'11 have shown an association between changes in the periodontal tis sues and ascorbic acid deficiency. Most of these studies, however, did not consider the possible effects of other nutritional deficiencies in the animals’ diet, nor the effect of bacteria in the initiation of ob served changes in the periodontal tissues. A recent nonblind experimental study9 with monkeys suggested that ascorbic acid deficiency may be an exacerbating agent rather than a primary causative agent of periodontal disease. A similar Ascorbic acid under polarized light. conclusion was also reached by Dreizen and others,11 and Glickman.12 The results of these animal studies cannot be easily applied to human studies A number of epidemiologic studies in trition and National Defense (ICNND), because of different requirements for as corbic acid in humans and animals, plus humans have examined the relation be which recorded the nutritional and oral health status of selected samples of the other physiologic differences. For exam tween ascorbic acid deficiency and ple, humans require less ascorbic acid periodontal disease status.1420 Russell,15 population in eight countries. The as than do rhesus monkeys. There are dif in 1963, summarized the results of the sessment of nutritional deficiencies was ferences in the oxidative catabolism of as studies conducted under the auspices of based on clinical examinations and on the Interdepartmental Committee for Nu biochemical tests of blood and urine in a corbic acid between the two species.13 JADA, Vol. 107, December 1983 ■ 927
A R T IC L E S
Among those who reported taking vitamin supplements, there is nothing to support any association between levels of ascorbic acid ingestion and periodontal health. small subsample. Serum levels of ascor bic acid were used in the ICNND studies to assess deficiency levels. Russell15 con cluded that age and oral hygiene contrib uted most to the variance in PI scores; an association between ascorbic acid defi ciency and increased PI scores could not be established. In the Ten-State Nutrition Survey,19 a “weak” correlation was re ported between ascorbic acid deficiency and the presence of periodontal disease. There are other reports in the literature, some of questionable study design and some apparently unethical by current standards,21 that conclude that there was a relation between ascorbic acid defi ciency and periodontal disease.21-22 The results of the previous studies, and other evidence,23'28 do not support the contention that routine ingestion of as corbic acid above recommended lev els— so-called “therapeutic” or “mega d o s e ” a m o u n ts — is b e n e fic ia l to periodontal health. Moreover, large doses of ascorbic acid might cause diarrhea29 and may interfere with specific drug ac tions.30,31 Despite the uncertainty about the dental benefits of ascorbic acid, large doses of vitamin C have been advocated as an adjunct in the treatment and preven tion of periodontal disease.32 34
Purpose of study This study investigates the association between the reported levels of dietary as corbic acid intake and the presence of periodontal disease in the representative
sample of the US population provided by the first National Health and Nutrition Examination Survey (NHANES I), 1971 to 1974. The NHANES I survey was a com prehensive survey of health and nutrition in more than 20,000 individuals, aged 1 to 74, in the continental United States. A de tailed description of the background, methods, and objectives of NHANES I has been reported in detail by Burt and others,35 and a summary version was de scribed in an earlier paper.36 Some dental information from this survey has been previously published.35'38 This report analyzes data collected from 8,609 dentulous persons, aged 25 to 74 years, who received a dental examina tion during NHANES I and with whom a 24-hour dietary recall interview was con ducted. The purpose of this analysis is to investigate the association between periodontal disease and reported dietary intake of ascorbic acid, and to determine whether a more-than-recommended daily intake of ascorbic acid was associated with better periodontal health.
Data sources Periodontal disease status (Periodontal Index, PI),39 and oral hygiene status (Sim plified Oral Hygiene Index, OHI-S),40 in addition to other oral and dental health assessments, were mea sured by ten trained dentists at 65 examination locations d uring the four years of the NHANES I survey. The dental examinations were con ducted in m obile vans that were used as exam ination centers. Diagnostic reliability was as sessed by repeated exam inations.35
Ascorbic acid intake was calculated from the foods reportedly consum ed by each in d iv id u a l in the survey d uring the preceding 24 hours. The 24-hour dietary recall interviews were conducted by interviewers trained in gather ing nutritional and dietary data. Food recalls excluded foods eaten on weekends as there were no interviews on Sundays and Mondays. It was recognized that weekend eating patterns m ay have differed from those d u rin g the week.41 In this report, the term “ dietary ascor bic acid” refers to ascorbic acid reportedly consumed in the 24-hour dietary recall, w ith out considering vitam in supplements. The dietary interview lasted approximately 20 minutes. Food portion models were used to assist the resp o n d e n ts in e s tim a tin g the am ount of food consumed. The models were those previously used in the Ten-State N utri tio n Survey.19 A com puter program ,42 also used in the Ten-State N utrition survey and based on a program developed originally at Tulane University, was used to calculate the total daily am ount of ascorbic acid and other nutrients consumed by each individual. Individuals were asked whether they were taking any vitam in supplem ent, but the quan tity and the brand names of ingested ascorbic acid supplem ents were not recorded. The vitam ins and m ineral supplements reportedly taken by the in d iv id uals in NHANES 1 were grouped by the N ational Center for Health Sta tistics into m u ltip le vitamins; m ultiple vita m ins w ith minerals; iron only; m ultiple vitam ins w ith iron; vitam ins E, A, and D; vitam in C; and calcium . A com plication in the analysis developed because the v ita m in supplem ents reported were not categorized into m utually exclusive groups in the N HANES I data. In our analysis, this problem was dealt w ith by defining three categories of users of vitam in supplements.
Table 1 ■ M ean Periodontal Index39 scores by dietary ascorbic acid adequacy levels and reported ingestion of vitam in supplem ents in the NHANES I population, 25 to 74 years of age. Type of vitamin supplements Vitamin C and multiple vitamin supplements Dietary ascorbic acid levels* 0-<26 26-<51 51-<76 76-C101 101-C126 126-<151 151-C176 176 + Total P-value*
n 217 177 178 142 123 107 131 639 1,714
Mean PI 1.2 1.1 1.0 1.1 0.9 0.9 0.9 1.0 1.0 >.50
No vitamin supplements n 1,030 815 680 497 381 429 335 1,698 5,865
‘ Percentages of NHANES I standard from dietary intake (without supplements), tlnclude vitamins A, D, E, and iron and calcium supplements. t ANOVA P-values testing the hypothesis that there is no difference among the mean PI scores.
928 ■ JADA, Vol. 107, December 1983
Mean PI 1.7 1.8 1.4 1.4 1.4 1.2 1.2 1.2 1.4 <.001
Other vitamins and mineral supplementst n 120 104 no 85 75 70 72 394 1,030
Mean PI 1.1 0.8 1.0 0.9 1.1 0.8 0.8 0.8 0.9 >.10
H x
,
!
,
’
A R T IC L E S
Table 2 ■ M ean Oral Hygiene Index-Simplified40 scores, mean age, and mean fam ily incom e group* by dietary ascorbic acid adequacy levels and reported ingestion of vitam in supplem ents in N HANES I population, 25 to 74 years of age. Type of vitamin supplements Vitamin C and multiple vitamin supplements Dietary ascorbic acid levels 0-<26 26-<51 51-<76 76-C101 101-<126 126-C151 151-C176 176+ Total P-valuei
Other vitamins and mineral supplementst
No vitamin supplements
Mean OHI-S
Mean family income group
Mean OHI-S
Mean family income group
Mean OHI-S
Mean family income group
1.1 0.9 0.8 1.0 0.7 0.9 0.9 0.9 0.9 >.1
17.5 18.0 18.0 18.0 18.4 18.0 18.5 18.2 18.1 <.01
1.6 1.5 1.3 1.4 1.3 1.2 1.1 1.1 1.3 <.001
17.0 17.3 17.7 17.8 17.5 18.2 18.0 18.1 17.7 <.001
1.1 0.8 0.7 1.1 1.0 1.0 0.6 0.7 0.8 <.001
17.7 18.0 17.6 17.7 18.3 18.6 18.7 18.5 18.2 <.001
‘ Total family income was divided into 12 groups in the NHANES I starting w ith group 11 ($1,000 per year or less) to group 22 ($25,000 per year or more), tlnclude vitamins A, D, E, and iron and calcium supplements. t ANOVA P-values testing the hypothesis that there is no difference among the means.
Table 3 ■ Spearman rank correlation coefficients of the relation between OHI-S scores, PI scores, dietary ascorbic acid levels, v itam in C supplements, gender, age, and education in the N HANES I sample._______ Variables
Ascorbic acid adequacy levels
Vitamin supplements*
-0.14 0.15 -0.00 0.07
-0.17 0.10 0.09
0.00
-0.33 -0.19 0.16
0.19 -0.11
0.16 -0.12
-0.37 0.66
OHI-S Income Gender Age Highest grade attended PI
OHI-S
‘ Vitam in supplements were divided into: 1 = no vitamin supple ments, 2 = vitamins A, D, and E, iron or calcium supplements, and 3 = vitamin C and/or multiple vitamins.
The first included those who reported taking vitam in C and m u ltip le v itam in supplements, the second were those who reported taking no vitam in supplements, and the third included those who reported taking vitam ins A, D, E, iron, and calcium supplements. Serum ascor bic acid levels w ould have been the preferred measure of ascorbic acid adequacy, but unfor tunately this measurement is unavailable in NHANES I data.
Definition of ascorbic acid adequacy The NHANES I standards43 for ascorbic acid w e re th e N a t io n a l R e s e a r c h C o u n c ilR e com m ended D ietary A llo w a nc e s (NRCRDA) for 1968.44 For the group aged 25 to 74 years, these standards recommended a daily intake of 55 and 60 mg of ascorbic acid daily for females and males, respectively. Adequacy values for dietary ascorbic acid were calculated by div idin g the reported daily dietary consum ption by the standard value. The distribution of the ascorbic acid adequacy values was divided into eight categories (0 to <26, 26 to < 51, 51 to <76, 76 to <101, 101 to <126, 126 to <151, 151 to 176, and 176+ %). The first category (less than 26% of the NRCRDA) is referred to as the lo w intake of ascorbic acid in one day, whereas the last category (176+ % of the NRC-RDA) is referred to as the h igh intake. The assum ption was made that
those who reported taking vita m in supple ments were receiving an adequate am ount of ascorbic acid regardless of its intake from dietary sources. G rouping of in d iv id uals into users of vitam in C and m u ltip le vitam ins, and other vitam ins users was done only for the purpose of comparison.
Statistical analysis Statistical analyses were conducted using the M ichigan Interactive Data Analysis System (MIDAS), supported by the Statistical Research Laboratory, and Organized Set of Integrated Routines in Statistics (OSIRIS IV), supported by the Institute of Social Research, University of M ichigan. Analysis of variance using sam ple weights was calculated to test for d if ference among means. Control for potential confounding variables (age, gender, race, in come, education, and oral hygiene status) was achieved by using a m u ltip le linear regression model.
Results Mean PI scores by ascorbic acid adequacy level and type of vitam in supplem ents are presented in Table 1. No significant differences were found among the mean PI scores of the dif ferent dietary adequacy levels for those who reported taking vitam in supplements, regard
less of whether these supplem ents were specif ically vitam in C or any other stated type (P > .5 and P > .1. respectively). For those w ho re ported taking no v ita m in supplem ents, the m ean PI scores are s ig n ific a n tly different among the different levels of adequacy (P < .0 01 ).
In the nonsupplem ent group, the significant differences in the m ean PI scores between those who reported low dietary ascorbic acid and those reporting h igh dietary ascorbic acid may suggest that ascorbic acid intake and periodontal health are associated. Further more, comparison of m ean PI scores between those w ho reported taking vita m in supp le ments and those w h o reported not taking vita m in s u p p le m e n ts at each ad eq uacy level (Table 1), may suggest that ingestion of vita m in C supplem ents is conducive to better periodontal health. The apparent differences in Table 1, h o w ever, are strongly confounded by differences between the v itam in supplem ent users and nonusers in income, age, gender, status of oral hygiene, and education (Tables 2, 3). Both those who reported taking vitam in supp le ments and those w h o reported higher intake of dietary (nonsupplem ental) ascorbic acid were from higher incom e fam ilies compared w ith those w ho reported taking no supplem ents and receiving lower dietary ascorbic acid. Because income levels are correlated w ith both total as corbic acid intake and status of oral hygiene (Table 3), the relation between ascorbic acid in ta k e a n d p e r io d o n t a l d is e a s e b e c o m e s complicated— even the weak association ob served in Table 1 m ay be the result of the m ulticollinearity45 am ong the variables just described. Looking only at the bivariate asso ciations between the PI and OHI-S scores and the reported ascorbic acid intake, w ithout tak ing the other confounding variables into ac count, m ay therefore lead to faulty conclu sions. A ccounting for the potentially confounding variables of age, gender, race, education, in come, and oral hygiene status was done by re gressing the PI scores on dietary ascorbic acid adequacy and the c o n fo u n d in g variables. (Sm oking could not be included in the regres sion analysis because sm oking history data
Ismail—Burt—Eklund : RELATION BETWEEN ASCORBIC ACID AND PERIODONTAL DISEASE ■ 929
A R T IC L E S
Dental practitioners are better advised to concentrate on plaque control rather than vitamin C supplements to prevent and control periodontal disease in their patients.
were taken only from a sm all subsample of ex am ined subjects.36) The regression procedure was carried out separately for those w ho re ported taking vitam in C supplements; those w ho reported taking no vitam in C supple ments; and those w ho reported taking other vitam ins and minerals. The results of the re gression analysis for those who reported taking vitam in supplem ents suggest that dietary as corbic acid adequacy levels do not explain any of the variance in the PI scores after controlling for age, gender, race, income, education, and oral hygiene status. Results of the regression analyses for the other adequacy levels are not p u b lish e d in the interest of space, b u t are available from the authors on request. For those w ho reported taking no vitam in supplem ents, a significant linear relation (P = .002) was fo un d between the PI scores and dietary ascorbic acid adequacy levels in the re gression m odel. But statistical significance does not necessarily mean clinical importance; the unstandardized and standardized regres sion coefficients showed that dietary ascorbic a cid adequacy, w h en com pared w ith oral hygiene status, is of m inor importance. Fur thermore, the reason the coefficient for ascor bic acid adequacy is statistically significant for the group taking no vitam in supplements but not for the group taking just vitam in C, even though the absolute values of the standardized coefficients in both were equal, is that the sam ple size for the first (n = 5,865) is about three times the sample size of the latter (n = 1,714). This points to the hazard of interpretation w hen using large samples in w h ich even trivial differences can be statistically significant. Moreover, because of the presence of a correla tio n between income, dietary ascorbic acid in take, and oral hygiene status, the effect of dietary intake of ascorbic acid alone cannot be derived from the regression model w ithout tak ing the other variables into account. Comparisons between the groups in Table 1 indicate that those w ho reported taking vita m in sup p le m e n ts h a d s ig n ific a n tly low er m ean PI scores than those who did not, regard less of dietary ascorbic acid adequacy level. This fin d in g , however, cannot be taken to suggest that vitam in supplements have some prim ary beneficial effect on periodontal health unless the possible effects of gender, race, in come, an d oral hygiene status differences are considered. W hen these factors were again taken into account through regression analysis at each level of dietary ascorbic acid adequacy level, the results showed that no significant re lation existed between the PI scores and the taking of vitam in supplements.
Discussion Although the results of cross-sectional studies like this one cannot lead to 930 ■ JADA, Vol. 107, December 1983
cause-and-effect conclusions, they can suggest some important associations be tween risk factors and disease. However, interpretation of the results derived from the NHANES I nutritional data should be made with caution because of the inher ent problems in this type of research. One problem in animal experiments and epidemiologic studies with humans is the definition of a deficiency. There is a lack of agreement among the expert bodies who set dietary intake standards on m inim um recommended daily intake level of ascorbic acid.43,44'46-49 For exam ple, the NHANES I standards43 for ascor bic acid are the same as the 1968 NRCRDA levels for the United States,44but are higher than the joint standards set by the Food and Agricultural Organization and the World Health Organization.48 In the United States, the 1974 NRC-RDA46 stan dards for ascorbic acid for adults were re duced by 25% from the 1968 standards,44 but the 1980 NRC-RDA standards were again similar to the 1968 NRC-RDA stan dards, except in the recommended allow ances for adult females that were altered to equal those for adult males.47 Although all these standards are based on an expert judgment of the minim um requirement of nutrients conducive to good health, the obvious uncertainties about the minim um requirement should be taken into account when comparisons are made between deficient and sufficient dietary ingestion of ascorbic acid and other nutrients. The m ethod used to estimate the dietary intake of the population in the NHANES I survey, the 24-hour dietary re call, is one of the most commonly used methods for measuring dietary intake pat terns. It requires less time to complete than other dietary assessment methods, is less expensive, and requires minimum cooperation from the interviewees. There are certain limitations, however, in the in terpretation and generalizability of the data collected through one-day dietary recall.50-52 For example, it is considered an invalid estimator of the nutrient intake of an individual because of the potential variation in quantity and quality of food intake from day to day—if the previous day had included a party, fast, or a marathon, food intake could obviously be atypical. For a group, however, it can be used to estimate the usual intake of a nu
trient with reasonable validity53'55 be cause the reported eating patterns aver age out over the group. Attempts to define the prevalence of a long-term deficiency of a specific nutrient from a one-day dietary recall should be made cau tiously.56 An additional problem associated with the 24-hour dietary recall as an estimate of long-term dietary patterns is the dayto-day variation in the daily consumption of a nutrient. Beaton56estimated the ratio of intraindividual variation (within an individual) to interindividual variation (between individuals) in the intake of most nutrients during six months to be in the range of 1.2 to 1.6. Hence, an under estimation of the long-term intake of any nutrient is apt to result from the use of the 24-hour dietary recall, increasing the possibility of false negative conclusions. Statistical correction for this problem has been suggested by Beaton and others,52 and Liu and others.57 Despite these limitations, there are still considerable benefits to be gained from analyzing data from a national survey like NHANES I. The value of a large represen tative sample can combine w ith the power of the regression techniques to produce v a lid associations. In this analysis, there was no clear difference in periodontal disease status between those who reported taking vitam in supple ments (of any kind) and those who did not. Among those who reported taking vitamin supplements, there is nothing to support any association between levels of ascorbic acid ingestion and periodontal health. In those who reported not taking vitamin supplements, low ascorbic acid intake was weakly and equivocally as sociated with periodontal disease. The strength of this association was much weaker than that found with oral hygiene status, age, race, and gender, and even this weak association may have resulted from the multicollinearity problem de scribed earlier. It can be concluded from this analysis, and within the limitation of the data, that there is no support for using more-thanrecommended intakes of ascorbic acid in the prevention or treatment of periodon tal diseases. This conclusion supports the recommendation of the Council on Dental Therapeutics of the American Dental As sociation.25 Once a practitioner is satis-
ARTICLES fied that a patient is receiving the RDA of ascorbic acid, either by supplement or through dietary sources like fruits and vegetables, then treatment and preven tion of periodontal disease can be most ef fectively concentrated on long-term con trol of plaque.
Summary Only a weak association between periodontal disease and ascorbic acid de ficiency has been shown in the analysis of nutritional and periodontal health data collected from a representative sample of the US population. Intake of ascorbic acid in amounts larger than those recom mended by the dietary standards does not seem to be associated with better periodontal health. The results of this study also suggest that dental practitio ners are better advised to concentrate on plaque control rather than vitamin C supplements to prevent and control periodontal disease in their patients.
___________________________ ja o & The authors thank Frances E. Thompson, research investigator, Program in Human Nutrition, School of Public Health, University of Michigan, for assistance in this study. The original data for tliis paper were supplied by the National Center for Health Statistics. Analysis was supported in part by the USPHS contract no. 233-79-2092. Results of analysis and conclusions reached are solely those of the authors. Dr. Ismail is a doctoral candidate, Program in Den tal Public Health, School of Public Health, University of Michigan, Ann Arbor, Mich 48109, and is on study leave from School of Dentistry, University of Baghdad, Iraq. Dr. Burt is professor, and Dr. Eklund is assistant professor, Program in Dental Public Health, School of Public Health, University of Michigan. Ad dress requests for reprints to Dr. Ismail. 1. Stewart, C.P., and Guthrie, D., eds. Lind’s treatise on scurvy. Edinburgh, University Press, 1953, p 114. 2 . Hojer, J.A. Studies in scurvy. Acta Paediatr Scand (Suppl) 3:1-278, 1924. 3. Hojer, A., and Westin, G. Jaws and teeth in scor butic guinea pigs. A histopathological study. Dent Cosmos 67(l):l-24, 1925. 4. Boyle, P.E.; Bessey, O.; and Wolbach, S.B. Ex perimental production of diffuse alveolar bone at rophy type of periodontal disease by diets deficient in ascorbic acid (vitamin C). JADA 24(11):1768-1777, 1937. 5. MacLean, D.L.; Sheppard, M.; and McHenry, E.W. Tissue changes in ascorbic acid deficient guinea pigs. Br J Exp Pathol 20(6):451-457, 1939. 6. Hunt, A.M., and Paynter, K.J. The effects of as corbic acid deficiency on the teeth and periodontal tissues of guinea pigs. J Dent Res 38(2):232-243,1959. 7. Schow, S.R. A serial study of ascorbic acid depletion in the guinea pig. JDent Res 45(4):1232,1966. 8 . Turesky, S.S., and Glickman, I. Histochemical evaluation of gingival healing in experimental ani mals on adequate and vitamin C deficient diets. J Dent Res 33(2):273-280, 1954. 9. Alvares, O., and others. The effect of subclinical ascorbate deficiency on periodontal health in nonhuman primates. J Periodorit Res 16(6):628-636, 1981. 10. Waerhaug, J. Effect of C-avitaminosis on the
supporting structures of the teeth. J Periodontol 29(2):87-97,1958. 11. Dreizen, S.; Levy, B.M.; andBernick, S. Studies on the biology of the periodontium of marmosets:VII. The effect of vitamin C deficiency on the marmoset periodontium. J Periodont Res 4(4):274-280,1969. 12. Glickman, I. Acute vitamin C deficiency and periodontal disease. I. The periodontal tissues of the guinea pig in acute vitamin C deficiency. J Dent Res 27(l):9-23, 1948. 13. Jukes, T.H. Further comments on the ascorbic acid requirement. Proc Natl Acad Sci USA 72(10) :4151-4152, 1975. 14. Burrill, D.Y. Relationship of blood plasma vitamin C level to gingival and periodontal disease. J Dent Res 21(4):353-363,1942. 15. Russell, A.L. International nutrition surveys: a summary of preliminary dental findings. J Dent Res 42(l):233-244, 1963. 16. Russell, A.L., and others. Periodontal disease and nutrition in South Vietnam. J Dent Res 44(4):775-782, 1965. 17. Enwonwu, C.O., and Edozien, J.C. Epidemiol ogy of periodontal disease in western Nigerians in re lation to socioeconomic status. Arch Oral Biol 15(12):1231-1244,1970. 18. Barros, L., and Witkop, C.J., Jr. Oral and genetic study of Chileans 1960-III. Periodontal disease and nutritional factors. Arch Oral Biol 8(2):195-206,1963. 19. Center for Disease Control. Ten State Nutrition Survey, 1968-1970. Department of Health, Education, and Welfare Pub no (HSM) 72-8131, Washington, DC, Government Printing Office, 1972, pp 87-93. 20. Shannon, I.L., and Gibson, W.A. Intravenous ascorbic acid loading in subjects classified as to periodontal status. J Dent Res 44(2):355-361,1965. 21. Hodges, R.E., and others. Clinical manifesta tions of ascorbic acid deficiency in man. Am J Clin Nutr 24(4}:432-443, 1971. 22. Pierce, H.B., and others. Ascorbic acid sup plementation. I. Response of gum tissue. Am J Clin Nutr 8(3}:353-362,1960. 23. Heifetz, S.B., and Suomi, J.D. The control of dental caries and periodontal disease; a fundamental approach. J Public Health Dent 33(l):2-6, 1973. 24. El-Ashiry, G. M.; Ringsdorf, W.M.; and Cheraskin, E. Local and systemic influences in periodontal disease: II. Effect of prophylaxis and natural versus synthetic vitamin C upon gingivitis. J Periodontol 35(3):250-259, 1964. 25. Council on Dental Therapeutics, American Dental Association. Accepted dental therapeutics, ed 39. Chicago, American Dental Association, 1982, pp 137-138, 339. 26. Shaw, J.H. Nutritional guidance in the preven tion of oral disease. Dent Clin North Am 16(4):733746,1972. 27. Shaw, J.H. The relation of nutrition to periodontal disease. J Dent Res 41(l):264-274, 1962. 28. Parfitt, G.J., and Apeirs, D.M. Role of nutrition in prevention and treatment of periodontal disease. J Canad Dent A 36(6):224-227,1970. 29. Goldsmith, G.A. Common cold: prevention and treatment with ascorbic acid not effective. JAMA 216(2):337, 1971. 30. Gilman, A.G.; Goodman, L.S.; and Gilman, A., eds. The pharmacological basis of therapeutics, ed 6. New York, MacMillan, 1980, pp 1579-1580. 31. Briggs, M.H.; Gracia-Webb, P.; and Davies, P. Urinary oxalate and vitamin C supplements. Lancet 2{7822):201, 1973. 32. Pauling, L. For the best of health—how much vitamin C do you need? Pa Dent J 43(3):53-56, 1976. 33. Cheraskin, E. The diet dilemma in dentistry. Am Soc Prevent Dent 4(3):25-32, 1974. 34. Ringsdorf, W.M., Jr., and Cheraskin, E. Diet and sulcus depth. NY State Dent J 30(l):3-8,1964. 35. Burt, B.A., and others. Diet and dental health; a study of relationships: United States 1971-1974. Na tional Center for Health Statistics, series 11, no. 225, Washington, DC, Government Printing Office, 1982, pp vii, 85. 36. Ismail, A.I.; Burt, B.A.;.and Eklund, S.E. Epidemiologic patterns of smoking and periodontal
disease in the United States. JADA 106(5):617-621, 1983. 37. National Center for Health Statistics. Basic data on dental examination findings of persons 1-74 years, United States 1971-1974. Series 1 1 , no. 214, Washing ton, DC, Government Printing Office, 1979. 38. National Center for Health Statistics. Decayed, missing, and filled teeth among persons 1-74 years, United States. Series 11, no. 223, Washington, DC, Government Printing Office, 1981. 39. Russell, A.L. A system of classification and scoring for prevalence surveys of periodontal disease. J Dent Res 35(3):350-359,1956. 40. Greene, J.C., and V erm illion, J.R. The simplified oral hygiene index. JADA 68(1):7-13,1964. 41. Youland, D.M., and Engle, A. Practices and problems in HANES. J Am Diet Assoc 68(l):22-25, 1976. 42. Tulane Dietant. Listing of dietant identifica tion data and food values per 100 gram edible portion. Computer printout. New Orleans. Nutrition Section, Biomedical Computing System, Tulane University, 1969. 43. National Center for Health Statistics. Caloric and selected nutrient values for persons 1-74 years of age, United States, 1971-1974, Series 11, no. 209, Washington, DC, Government Printing Office, 1979. 44. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1968, pp 31-33. 45. Neter, J., and Wasserman, W. Applied linear statistical model: regression, analysis of variance, and experimental designs. Homewood, 111, Richard D. Ir win, Inc, 1974, pp 251-254, 339-347. 46. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1974, pp 63-64. 47. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1980, pp 72-82. 48. World Health Organization. Requirements of ascorbic acid, vitamin D, vitamin B12, folate, and iron. WHO Tech Rep Series no. 452, Geneva, 1970, pp 25-31. 49. US Interdepartmental Committee on Nutrition for National Defense. Manual for nutrition surveys. Bethesda, National Institutes of Health, 1963, pp 257-258. 50. Garn, S.M.; Larkin, F.A.; and Cole, P.E. The problem with one-day dietary intakes. Ecol Food Nutr 5(4):245-247, 1976. 51. Hegsted, D.M. Problems in the use and in terpretation of the recommended dietary allowances. Ecol Food Nutr l{4):255-265,1972. 52. Beaton, G.H., and others. Sources of variance in the 24-hour dietary recall data: implications for nutri tion study design and interpretation. Am J Clin Nutr 32(12):2546-2559, 1979. 53. Young, C.M., and others. A comparison of dietary study methods. II. Dietary history vs sevenday record vs 24-hour recall. J Am Diet Assoc 28(3):218-221, 1952. 54. Gersovitz, M.; Madden, J.P.; and Wright, H.S. Validity of the 24-hr. dietary recall and seven day rec ord for group comparisons. J Am Diet Assoc 73(l):48-55,1978. 55. Madden, J.P.; Goodman, S.J.; and Smici KlasWright, H. Validity of the 24-hr. recall. J Am Diet Assoc 68(2):143-147,1976. 56. Beaton, G.H. What do we think we are estimat ing? In Beal, V.A., and Laus, M.J., eds. Proceedings of the symposium on dietary data, collection, analysis, and significance. Amherst, Mass, Agricultural Exper iment Station, College of Food and Natural Re sources, University of Massachusetts, Res Bulletin 675,1982, pp 36-49. 57. Liu, K., and others. Statistical methods to as sess and minimize the role of intra-individual varia bility in obscuring the relationship between dietary lipids and serum cholesterol. J Chronic Dis 31(6/ 7):399-418,1978.
Ismail-Burt-Eklund : RELATION BETWEEN ASCORBIC ACID AND PERIODONTAL DISEASE ■ 931
The possible association between deficiency of ascorbic acid and periodontal disease is scrutinized by the results of the data from the NHANES I survey.
Relation between ascorbic acid intake and periodontal disease in the United States
Am id I. Ismail, BDS, M PH Brian A. Burt, BDS, M PH, PhD Stephen A. Eklund, DDS, M H S A , DrPH
T
-H- he relation between levels of ascor bic acid (vitamin C) intake and periodon tal disease status has been of interest ever since the poor gingival condition of people with scurvy was observed long ago.1 Studies with guinea pigs2 8 and monkeys9'11 have shown an association between changes in the periodontal tis sues and ascorbic acid deficiency. Most of these studies, however, did not consider the possible effects of other nutritional deficiencies in the animals’ diet, nor the effect of bacteria in the initiation of ob served changes in the periodontal tissues. A recent nonblind experimental study9 with monkeys suggested that ascorbic acid deficiency may be an exacerbating agent rather than a primary causative agent of periodontal disease. A similar Ascorbic acid under polarized light. conclusion was also reached by Dreizen and others,11 and Glickman.12 The results of these animal studies cannot be easily applied to human studies A number of epidemiologic studies in trition and National Defense (ICNND), because of different requirements for as corbic acid in humans and animals, plus humans have examined the relation be which recorded the nutritional and oral health status of selected samples of the other physiologic differences. For exam tween ascorbic acid deficiency and ple, humans require less ascorbic acid periodontal disease status.1420 Russell,15 population in eight countries. The as than do rhesus monkeys. There are dif in 1963, summarized the results of the sessment of nutritional deficiencies was ferences in the oxidative catabolism of as studies conducted under the auspices of based on clinical examinations and on the Interdepartmental Committee for Nu biochemical tests of blood and urine in a corbic acid between the two species.13 JADA, Vol. 107, December 1983 ■ 927
A R T IC L E S
Among those who reported taking vitamin supplements, there is nothing to support any association between levels of ascorbic acid ingestion and periodontal health. small subsample. Serum levels of ascor bic acid were used in the ICNND studies to assess deficiency levels. Russell15 con cluded that age and oral hygiene contrib uted most to the variance in PI scores; an association between ascorbic acid defi ciency and increased PI scores could not be established. In the Ten-State Nutrition Survey,19 a “weak” correlation was re ported between ascorbic acid deficiency and the presence of periodontal disease. There are other reports in the literature, some of questionable study design and some apparently unethical by current standards,21 that conclude that there was a relation between ascorbic acid defi ciency and periodontal disease.21-22 The results of the previous studies, and other evidence,23'28 do not support the contention that routine ingestion of as corbic acid above recommended lev els— so-called “therapeutic” or “mega d o s e ” a m o u n ts — is b e n e fic ia l to periodontal health. Moreover, large doses of ascorbic acid might cause diarrhea29 and may interfere with specific drug ac tions.30,31 Despite the uncertainty about the dental benefits of ascorbic acid, large doses of vitamin C have been advocated as an adjunct in the treatment and preven tion of periodontal disease.32 34
Purpose of study This study investigates the association between the reported levels of dietary as corbic acid intake and the presence of periodontal disease in the representative
sample of the US population provided by the first National Health and Nutrition Examination Survey (NHANES I), 1971 to 1974. The NHANES I survey was a com prehensive survey of health and nutrition in more than 20,000 individuals, aged 1 to 74, in the continental United States. A de tailed description of the background, methods, and objectives of NHANES I has been reported in detail by Burt and others,35 and a summary version was de scribed in an earlier paper.36 Some dental information from this survey has been previously published.35'38 This report analyzes data collected from 8,609 dentulous persons, aged 25 to 74 years, who received a dental examina tion during NHANES I and with whom a 24-hour dietary recall interview was con ducted. The purpose of this analysis is to investigate the association between periodontal disease and reported dietary intake of ascorbic acid, and to determine whether a more-than-recommended daily intake of ascorbic acid was associated with better periodontal health.
Data sources Periodontal disease status (Periodontal Index, PI),39 and oral hygiene status (Sim plified Oral Hygiene Index, OHI-S),40 in addition to other oral and dental health assessments, were mea sured by ten trained dentists at 65 examination locations d uring the four years of the NHANES I survey. The dental examinations were con ducted in m obile vans that were used as exam ination centers. Diagnostic reliability was as sessed by repeated exam inations.35
Ascorbic acid intake was calculated from the foods reportedly consum ed by each in d iv id u a l in the survey d uring the preceding 24 hours. The 24-hour dietary recall interviews were conducted by interviewers trained in gather ing nutritional and dietary data. Food recalls excluded foods eaten on weekends as there were no interviews on Sundays and Mondays. It was recognized that weekend eating patterns m ay have differed from those d u rin g the week.41 In this report, the term “ dietary ascor bic acid” refers to ascorbic acid reportedly consumed in the 24-hour dietary recall, w ith out considering vitam in supplements. The dietary interview lasted approximately 20 minutes. Food portion models were used to assist the resp o n d e n ts in e s tim a tin g the am ount of food consumed. The models were those previously used in the Ten-State N utri tio n Survey.19 A com puter program ,42 also used in the Ten-State N utrition survey and based on a program developed originally at Tulane University, was used to calculate the total daily am ount of ascorbic acid and other nutrients consumed by each individual. Individuals were asked whether they were taking any vitam in supplem ent, but the quan tity and the brand names of ingested ascorbic acid supplem ents were not recorded. The vitam ins and m ineral supplements reportedly taken by the in d iv id uals in NHANES 1 were grouped by the N ational Center for Health Sta tistics into m u ltip le vitamins; m ultiple vita m ins w ith minerals; iron only; m ultiple vitam ins w ith iron; vitam ins E, A, and D; vitam in C; and calcium . A com plication in the analysis developed because the v ita m in supplem ents reported were not categorized into m utually exclusive groups in the N HANES I data. In our analysis, this problem was dealt w ith by defining three categories of users of vitam in supplements.
Table 1 ■ M ean Periodontal Index39 scores by dietary ascorbic acid adequacy levels and reported ingestion of vitam in supplem ents in the NHANES I population, 25 to 74 years of age. Type of vitamin supplements Vitamin C and multiple vitamin supplements Dietary ascorbic acid levels* 0-<26 26-<51 51-<76 76-C101 101-C126 126-<151 151-C176 176 + Total P-value*
n 217 177 178 142 123 107 131 639 1,714
Mean PI 1.2 1.1 1.0 1.1 0.9 0.9 0.9 1.0 1.0 >.50
No vitamin supplements n 1,030 815 680 497 381 429 335 1,698 5,865
‘ Percentages of NHANES I standard from dietary intake (without supplements), tlnclude vitamins A, D, E, and iron and calcium supplements. t ANOVA P-values testing the hypothesis that there is no difference among the mean PI scores.
928 ■ JADA, Vol. 107, December 1983
Mean PI 1.7 1.8 1.4 1.4 1.4 1.2 1.2 1.2 1.4 <.001
Other vitamins and mineral supplementst n 120 104 no 85 75 70 72 394 1,030
Mean PI 1.1 0.8 1.0 0.9 1.1 0.8 0.8 0.8 0.9 >.10
H x
,
!
,
’
A R T IC L E S
Table 2 ■ M ean Oral Hygiene Index-Simplified40 scores, mean age, and mean fam ily incom e group* by dietary ascorbic acid adequacy levels and reported ingestion of vitam in supplem ents in N HANES I population, 25 to 74 years of age. Type of vitamin supplements Vitamin C and multiple vitamin supplements Dietary ascorbic acid levels 0-<26 26-<51 51-<76 76-C101 101-<126 126-C151 151-C176 176+ Total P-valuei
Other vitamins and mineral supplementst
No vitamin supplements
Mean OHI-S
Mean family income group
Mean OHI-S
Mean family income group
Mean OHI-S
Mean family income group
1.1 0.9 0.8 1.0 0.7 0.9 0.9 0.9 0.9 >.1
17.5 18.0 18.0 18.0 18.4 18.0 18.5 18.2 18.1 <.01
1.6 1.5 1.3 1.4 1.3 1.2 1.1 1.1 1.3 <.001
17.0 17.3 17.7 17.8 17.5 18.2 18.0 18.1 17.7 <.001
1.1 0.8 0.7 1.1 1.0 1.0 0.6 0.7 0.8 <.001
17.7 18.0 17.6 17.7 18.3 18.6 18.7 18.5 18.2 <.001
‘ Total family income was divided into 12 groups in the NHANES I starting w ith group 11 ($1,000 per year or less) to group 22 ($25,000 per year or more), tlnclude vitamins A, D, E, and iron and calcium supplements. t ANOVA P-values testing the hypothesis that there is no difference among the means.
Table 3 ■ Spearman rank correlation coefficients of the relation between OHI-S scores, PI scores, dietary ascorbic acid levels, v itam in C supplements, gender, age, and education in the N HANES I sample._______ Variables
Ascorbic acid adequacy levels
Vitamin supplements*
-0.14 0.15 -0.00 0.07
-0.17 0.10 0.09
0.00
-0.33 -0.19 0.16
0.19 -0.11
0.16 -0.12
-0.37 0.66
OHI-S Income Gender Age Highest grade attended PI
OHI-S
‘ Vitam in supplements were divided into: 1 = no vitamin supple ments, 2 = vitamins A, D, and E, iron or calcium supplements, and 3 = vitamin C and/or multiple vitamins.
The first included those who reported taking vitam in C and m u ltip le v itam in supplements, the second were those who reported taking no vitam in supplements, and the third included those who reported taking vitam ins A, D, E, iron, and calcium supplements. Serum ascor bic acid levels w ould have been the preferred measure of ascorbic acid adequacy, but unfor tunately this measurement is unavailable in NHANES I data.
Definition of ascorbic acid adequacy The NHANES I standards43 for ascorbic acid w e re th e N a t io n a l R e s e a r c h C o u n c ilR e com m ended D ietary A llo w a nc e s (NRCRDA) for 1968.44 For the group aged 25 to 74 years, these standards recommended a daily intake of 55 and 60 mg of ascorbic acid daily for females and males, respectively. Adequacy values for dietary ascorbic acid were calculated by div idin g the reported daily dietary consum ption by the standard value. The distribution of the ascorbic acid adequacy values was divided into eight categories (0 to <26, 26 to < 51, 51 to <76, 76 to <101, 101 to <126, 126 to <151, 151 to 176, and 176+ %). The first category (less than 26% of the NRCRDA) is referred to as the lo w intake of ascorbic acid in one day, whereas the last category (176+ % of the NRC-RDA) is referred to as the h igh intake. The assum ption was made that
those who reported taking vita m in supple ments were receiving an adequate am ount of ascorbic acid regardless of its intake from dietary sources. G rouping of in d iv id uals into users of vitam in C and m u ltip le vitam ins, and other vitam ins users was done only for the purpose of comparison.
Statistical analysis Statistical analyses were conducted using the M ichigan Interactive Data Analysis System (MIDAS), supported by the Statistical Research Laboratory, and Organized Set of Integrated Routines in Statistics (OSIRIS IV), supported by the Institute of Social Research, University of M ichigan. Analysis of variance using sam ple weights was calculated to test for d if ference among means. Control for potential confounding variables (age, gender, race, in come, education, and oral hygiene status) was achieved by using a m u ltip le linear regression model.
Results Mean PI scores by ascorbic acid adequacy level and type of vitam in supplem ents are presented in Table 1. No significant differences were found among the mean PI scores of the dif ferent dietary adequacy levels for those who reported taking vitam in supplements, regard
less of whether these supplem ents were specif ically vitam in C or any other stated type (P > .5 and P > .1. respectively). For those w ho re ported taking no v ita m in supplem ents, the m ean PI scores are s ig n ific a n tly different among the different levels of adequacy (P < .0 01 ).
In the nonsupplem ent group, the significant differences in the m ean PI scores between those who reported low dietary ascorbic acid and those reporting h igh dietary ascorbic acid may suggest that ascorbic acid intake and periodontal health are associated. Further more, comparison of m ean PI scores between those w ho reported taking vita m in supp le ments and those w h o reported not taking vita m in s u p p le m e n ts at each ad eq uacy level (Table 1), may suggest that ingestion of vita m in C supplem ents is conducive to better periodontal health. The apparent differences in Table 1, h o w ever, are strongly confounded by differences between the v itam in supplem ent users and nonusers in income, age, gender, status of oral hygiene, and education (Tables 2, 3). Both those who reported taking vitam in supp le ments and those w h o reported higher intake of dietary (nonsupplem ental) ascorbic acid were from higher incom e fam ilies compared w ith those w ho reported taking no supplem ents and receiving lower dietary ascorbic acid. Because income levels are correlated w ith both total as corbic acid intake and status of oral hygiene (Table 3), the relation between ascorbic acid in ta k e a n d p e r io d o n t a l d is e a s e b e c o m e s complicated— even the weak association ob served in Table 1 m ay be the result of the m ulticollinearity45 am ong the variables just described. Looking only at the bivariate asso ciations between the PI and OHI-S scores and the reported ascorbic acid intake, w ithout tak ing the other confounding variables into ac count, m ay therefore lead to faulty conclu sions. A ccounting for the potentially confounding variables of age, gender, race, education, in come, and oral hygiene status was done by re gressing the PI scores on dietary ascorbic acid adequacy and the c o n fo u n d in g variables. (Sm oking could not be included in the regres sion analysis because sm oking history data
Ismail—Burt—Eklund : RELATION BETWEEN ASCORBIC ACID AND PERIODONTAL DISEASE ■ 929
A R T IC L E S
Dental practitioners are better advised to concentrate on plaque control rather than vitamin C supplements to prevent and control periodontal disease in their patients.
were taken only from a sm all subsample of ex am ined subjects.36) The regression procedure was carried out separately for those w ho re ported taking vitam in C supplements; those w ho reported taking no vitam in C supple ments; and those w ho reported taking other vitam ins and minerals. The results of the re gression analysis for those who reported taking vitam in supplem ents suggest that dietary as corbic acid adequacy levels do not explain any of the variance in the PI scores after controlling for age, gender, race, income, education, and oral hygiene status. Results of the regression analyses for the other adequacy levels are not p u b lish e d in the interest of space, b u t are available from the authors on request. For those w ho reported taking no vitam in supplem ents, a significant linear relation (P = .002) was fo un d between the PI scores and dietary ascorbic acid adequacy levels in the re gression m odel. But statistical significance does not necessarily mean clinical importance; the unstandardized and standardized regres sion coefficients showed that dietary ascorbic a cid adequacy, w h en com pared w ith oral hygiene status, is of m inor importance. Fur thermore, the reason the coefficient for ascor bic acid adequacy is statistically significant for the group taking no vitam in supplements but not for the group taking just vitam in C, even though the absolute values of the standardized coefficients in both were equal, is that the sam ple size for the first (n = 5,865) is about three times the sample size of the latter (n = 1,714). This points to the hazard of interpretation w hen using large samples in w h ich even trivial differences can be statistically significant. Moreover, because of the presence of a correla tio n between income, dietary ascorbic acid in take, and oral hygiene status, the effect of dietary intake of ascorbic acid alone cannot be derived from the regression model w ithout tak ing the other variables into account. Comparisons between the groups in Table 1 indicate that those w ho reported taking vita m in sup p le m e n ts h a d s ig n ific a n tly low er m ean PI scores than those who did not, regard less of dietary ascorbic acid adequacy level. This fin d in g , however, cannot be taken to suggest that vitam in supplements have some prim ary beneficial effect on periodontal health unless the possible effects of gender, race, in come, an d oral hygiene status differences are considered. W hen these factors were again taken into account through regression analysis at each level of dietary ascorbic acid adequacy level, the results showed that no significant re lation existed between the PI scores and the taking of vitam in supplements.
Discussion Although the results of cross-sectional studies like this one cannot lead to 930 ■ JADA, Vol. 107, December 1983
cause-and-effect conclusions, they can suggest some important associations be tween risk factors and disease. However, interpretation of the results derived from the NHANES I nutritional data should be made with caution because of the inher ent problems in this type of research. One problem in animal experiments and epidemiologic studies with humans is the definition of a deficiency. There is a lack of agreement among the expert bodies who set dietary intake standards on m inim um recommended daily intake level of ascorbic acid.43,44'46-49 For exam ple, the NHANES I standards43 for ascor bic acid are the same as the 1968 NRCRDA levels for the United States,44but are higher than the joint standards set by the Food and Agricultural Organization and the World Health Organization.48 In the United States, the 1974 NRC-RDA46 stan dards for ascorbic acid for adults were re duced by 25% from the 1968 standards,44 but the 1980 NRC-RDA standards were again similar to the 1968 NRC-RDA stan dards, except in the recommended allow ances for adult females that were altered to equal those for adult males.47 Although all these standards are based on an expert judgment of the minim um requirement of nutrients conducive to good health, the obvious uncertainties about the minim um requirement should be taken into account when comparisons are made between deficient and sufficient dietary ingestion of ascorbic acid and other nutrients. The m ethod used to estimate the dietary intake of the population in the NHANES I survey, the 24-hour dietary re call, is one of the most commonly used methods for measuring dietary intake pat terns. It requires less time to complete than other dietary assessment methods, is less expensive, and requires minimum cooperation from the interviewees. There are certain limitations, however, in the in terpretation and generalizability of the data collected through one-day dietary recall.50-52 For example, it is considered an invalid estimator of the nutrient intake of an individual because of the potential variation in quantity and quality of food intake from day to day—if the previous day had included a party, fast, or a marathon, food intake could obviously be atypical. For a group, however, it can be used to estimate the usual intake of a nu
trient with reasonable validity53'55 be cause the reported eating patterns aver age out over the group. Attempts to define the prevalence of a long-term deficiency of a specific nutrient from a one-day dietary recall should be made cau tiously.56 An additional problem associated with the 24-hour dietary recall as an estimate of long-term dietary patterns is the dayto-day variation in the daily consumption of a nutrient. Beaton56estimated the ratio of intraindividual variation (within an individual) to interindividual variation (between individuals) in the intake of most nutrients during six months to be in the range of 1.2 to 1.6. Hence, an under estimation of the long-term intake of any nutrient is apt to result from the use of the 24-hour dietary recall, increasing the possibility of false negative conclusions. Statistical correction for this problem has been suggested by Beaton and others,52 and Liu and others.57 Despite these limitations, there are still considerable benefits to be gained from analyzing data from a national survey like NHANES I. The value of a large represen tative sample can combine w ith the power of the regression techniques to produce v a lid associations. In this analysis, there was no clear difference in periodontal disease status between those who reported taking vitam in supple ments (of any kind) and those who did not. Among those who reported taking vitamin supplements, there is nothing to support any association between levels of ascorbic acid ingestion and periodontal health. In those who reported not taking vitamin supplements, low ascorbic acid intake was weakly and equivocally as sociated with periodontal disease. The strength of this association was much weaker than that found with oral hygiene status, age, race, and gender, and even this weak association may have resulted from the multicollinearity problem de scribed earlier. It can be concluded from this analysis, and within the limitation of the data, that there is no support for using more-thanrecommended intakes of ascorbic acid in the prevention or treatment of periodon tal diseases. This conclusion supports the recommendation of the Council on Dental Therapeutics of the American Dental As sociation.25 Once a practitioner is satis-
ARTICLES fied that a patient is receiving the RDA of ascorbic acid, either by supplement or through dietary sources like fruits and vegetables, then treatment and preven tion of periodontal disease can be most ef fectively concentrated on long-term con trol of plaque.
Summary Only a weak association between periodontal disease and ascorbic acid de ficiency has been shown in the analysis of nutritional and periodontal health data collected from a representative sample of the US population. Intake of ascorbic acid in amounts larger than those recom mended by the dietary standards does not seem to be associated with better periodontal health. The results of this study also suggest that dental practitio ners are better advised to concentrate on plaque control rather than vitamin C supplements to prevent and control periodontal disease in their patients.
___________________________ ja o & The authors thank Frances E. Thompson, research investigator, Program in Human Nutrition, School of Public Health, University of Michigan, for assistance in this study. The original data for tliis paper were supplied by the National Center for Health Statistics. Analysis was supported in part by the USPHS contract no. 233-79-2092. Results of analysis and conclusions reached are solely those of the authors. Dr. Ismail is a doctoral candidate, Program in Den tal Public Health, School of Public Health, University of Michigan, Ann Arbor, Mich 48109, and is on study leave from School of Dentistry, University of Baghdad, Iraq. Dr. Burt is professor, and Dr. Eklund is assistant professor, Program in Dental Public Health, School of Public Health, University of Michigan. Ad dress requests for reprints to Dr. Ismail. 1. Stewart, C.P., and Guthrie, D., eds. Lind’s treatise on scurvy. Edinburgh, University Press, 1953, p 114. 2 . Hojer, J.A. Studies in scurvy. Acta Paediatr Scand (Suppl) 3:1-278, 1924. 3. Hojer, A., and Westin, G. Jaws and teeth in scor butic guinea pigs. A histopathological study. Dent Cosmos 67(l):l-24, 1925. 4. Boyle, P.E.; Bessey, O.; and Wolbach, S.B. Ex perimental production of diffuse alveolar bone at rophy type of periodontal disease by diets deficient in ascorbic acid (vitamin C). JADA 24(11):1768-1777, 1937. 5. MacLean, D.L.; Sheppard, M.; and McHenry, E.W. Tissue changes in ascorbic acid deficient guinea pigs. Br J Exp Pathol 20(6):451-457, 1939. 6. Hunt, A.M., and Paynter, K.J. The effects of as corbic acid deficiency on the teeth and periodontal tissues of guinea pigs. J Dent Res 38(2):232-243,1959. 7. Schow, S.R. A serial study of ascorbic acid depletion in the guinea pig. JDent Res 45(4):1232,1966. 8 . Turesky, S.S., and Glickman, I. Histochemical evaluation of gingival healing in experimental ani mals on adequate and vitamin C deficient diets. J Dent Res 33(2):273-280, 1954. 9. Alvares, O., and others. The effect of subclinical ascorbate deficiency on periodontal health in nonhuman primates. J Periodorit Res 16(6):628-636, 1981. 10. Waerhaug, J. Effect of C-avitaminosis on the
supporting structures of the teeth. J Periodontol 29(2):87-97,1958. 11. Dreizen, S.; Levy, B.M.; andBernick, S. Studies on the biology of the periodontium of marmosets:VII. The effect of vitamin C deficiency on the marmoset periodontium. J Periodont Res 4(4):274-280,1969. 12. Glickman, I. Acute vitamin C deficiency and periodontal disease. I. The periodontal tissues of the guinea pig in acute vitamin C deficiency. J Dent Res 27(l):9-23, 1948. 13. Jukes, T.H. Further comments on the ascorbic acid requirement. Proc Natl Acad Sci USA 72(10) :4151-4152, 1975. 14. Burrill, D.Y. Relationship of blood plasma vitamin C level to gingival and periodontal disease. J Dent Res 21(4):353-363,1942. 15. Russell, A.L. International nutrition surveys: a summary of preliminary dental findings. J Dent Res 42(l):233-244, 1963. 16. Russell, A.L., and others. Periodontal disease and nutrition in South Vietnam. J Dent Res 44(4):775-782, 1965. 17. Enwonwu, C.O., and Edozien, J.C. Epidemiol ogy of periodontal disease in western Nigerians in re lation to socioeconomic status. Arch Oral Biol 15(12):1231-1244,1970. 18. Barros, L., and Witkop, C.J., Jr. Oral and genetic study of Chileans 1960-III. Periodontal disease and nutritional factors. Arch Oral Biol 8(2):195-206,1963. 19. Center for Disease Control. Ten State Nutrition Survey, 1968-1970. Department of Health, Education, and Welfare Pub no (HSM) 72-8131, Washington, DC, Government Printing Office, 1972, pp 87-93. 20. Shannon, I.L., and Gibson, W.A. Intravenous ascorbic acid loading in subjects classified as to periodontal status. J Dent Res 44(2):355-361,1965. 21. Hodges, R.E., and others. Clinical manifesta tions of ascorbic acid deficiency in man. Am J Clin Nutr 24(4}:432-443, 1971. 22. Pierce, H.B., and others. Ascorbic acid sup plementation. I. Response of gum tissue. Am J Clin Nutr 8(3}:353-362,1960. 23. Heifetz, S.B., and Suomi, J.D. The control of dental caries and periodontal disease; a fundamental approach. J Public Health Dent 33(l):2-6, 1973. 24. El-Ashiry, G. M.; Ringsdorf, W.M.; and Cheraskin, E. Local and systemic influences in periodontal disease: II. Effect of prophylaxis and natural versus synthetic vitamin C upon gingivitis. J Periodontol 35(3):250-259, 1964. 25. Council on Dental Therapeutics, American Dental Association. Accepted dental therapeutics, ed 39. Chicago, American Dental Association, 1982, pp 137-138, 339. 26. Shaw, J.H. Nutritional guidance in the preven tion of oral disease. Dent Clin North Am 16(4):733746,1972. 27. Shaw, J.H. The relation of nutrition to periodontal disease. J Dent Res 41(l):264-274, 1962. 28. Parfitt, G.J., and Apeirs, D.M. Role of nutrition in prevention and treatment of periodontal disease. J Canad Dent A 36(6):224-227,1970. 29. Goldsmith, G.A. Common cold: prevention and treatment with ascorbic acid not effective. JAMA 216(2):337, 1971. 30. Gilman, A.G.; Goodman, L.S.; and Gilman, A., eds. The pharmacological basis of therapeutics, ed 6. New York, MacMillan, 1980, pp 1579-1580. 31. Briggs, M.H.; Gracia-Webb, P.; and Davies, P. Urinary oxalate and vitamin C supplements. Lancet 2{7822):201, 1973. 32. Pauling, L. For the best of health—how much vitamin C do you need? Pa Dent J 43(3):53-56, 1976. 33. Cheraskin, E. The diet dilemma in dentistry. Am Soc Prevent Dent 4(3):25-32, 1974. 34. Ringsdorf, W.M., Jr., and Cheraskin, E. Diet and sulcus depth. NY State Dent J 30(l):3-8,1964. 35. Burt, B.A., and others. Diet and dental health; a study of relationships: United States 1971-1974. Na tional Center for Health Statistics, series 11, no. 225, Washington, DC, Government Printing Office, 1982, pp vii, 85. 36. Ismail, A.I.; Burt, B.A.;.and Eklund, S.E. Epidemiologic patterns of smoking and periodontal
disease in the United States. JADA 106(5):617-621, 1983. 37. National Center for Health Statistics. Basic data on dental examination findings of persons 1-74 years, United States 1971-1974. Series 1 1 , no. 214, Washing ton, DC, Government Printing Office, 1979. 38. National Center for Health Statistics. Decayed, missing, and filled teeth among persons 1-74 years, United States. Series 11, no. 223, Washington, DC, Government Printing Office, 1981. 39. Russell, A.L. A system of classification and scoring for prevalence surveys of periodontal disease. J Dent Res 35(3):350-359,1956. 40. Greene, J.C., and V erm illion, J.R. The simplified oral hygiene index. JADA 68(1):7-13,1964. 41. Youland, D.M., and Engle, A. Practices and problems in HANES. J Am Diet Assoc 68(l):22-25, 1976. 42. Tulane Dietant. Listing of dietant identifica tion data and food values per 100 gram edible portion. Computer printout. New Orleans. Nutrition Section, Biomedical Computing System, Tulane University, 1969. 43. National Center for Health Statistics. Caloric and selected nutrient values for persons 1-74 years of age, United States, 1971-1974, Series 11, no. 209, Washington, DC, Government Printing Office, 1979. 44. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1968, pp 31-33. 45. Neter, J., and Wasserman, W. Applied linear statistical model: regression, analysis of variance, and experimental designs. Homewood, 111, Richard D. Ir win, Inc, 1974, pp 251-254, 339-347. 46. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1974, pp 63-64. 47. National Academy of Sciences, National Re search Council. Recommended Dietary Allowances. Washington, National Academy of Sciences, 1980, pp 72-82. 48. World Health Organization. Requirements of ascorbic acid, vitamin D, vitamin B12, folate, and iron. WHO Tech Rep Series no. 452, Geneva, 1970, pp 25-31. 49. US Interdepartmental Committee on Nutrition for National Defense. Manual for nutrition surveys. Bethesda, National Institutes of Health, 1963, pp 257-258. 50. Garn, S.M.; Larkin, F.A.; and Cole, P.E. The problem with one-day dietary intakes. Ecol Food Nutr 5(4):245-247, 1976. 51. Hegsted, D.M. Problems in the use and in terpretation of the recommended dietary allowances. Ecol Food Nutr l{4):255-265,1972. 52. Beaton, G.H., and others. Sources of variance in the 24-hour dietary recall data: implications for nutri tion study design and interpretation. Am J Clin Nutr 32(12):2546-2559, 1979. 53. Young, C.M., and others. A comparison of dietary study methods. II. Dietary history vs sevenday record vs 24-hour recall. J Am Diet Assoc 28(3):218-221, 1952. 54. Gersovitz, M.; Madden, J.P.; and Wright, H.S. Validity of the 24-hr. dietary recall and seven day rec ord for group comparisons. J Am Diet Assoc 73(l):48-55,1978. 55. Madden, J.P.; Goodman, S.J.; and Smici KlasWright, H. Validity of the 24-hr. recall. J Am Diet Assoc 68(2):143-147,1976. 56. Beaton, G.H. What do we think we are estimat ing? In Beal, V.A., and Laus, M.J., eds. Proceedings of the symposium on dietary data, collection, analysis, and significance. Amherst, Mass, Agricultural Exper iment Station, College of Food and Natural Re sources, University of Massachusetts, Res Bulletin 675,1982, pp 36-49. 57. Liu, K., and others. Statistical methods to as sess and minimize the role of intra-individual varia bility in obscuring the relationship between dietary lipids and serum cholesterol. J Chronic Dis 31(6/ 7):399-418,1978.
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