Periodontology 2000, Vol. 58, 2012, 93111 Printed in Singapore.

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2012 John Wiley & Sons A/S

PERIODONTOLOGY 2000

Nutrition, dietary guidelines and optimal periodontal health

E L I Z A B E T H K. K A Y E

Nutrients derived from the diet perform as antioxidants, co-enzymes in energy production and metabolic processes, and components of tissue structures that keep the bodys systems functioning properly and maintain good overall health, including oral health. Nutrients that are thought to be especially important for maintaining the periodontium have been the focus of epidemiological studies for many years. For example, folate, vitamin A and vitamin C ensure proper development and repair of mucosal and connective tissues; protein, calcium and phosphorus are incorporated into the structures of collagen, teeth and bone; omega fatty acids and vitamin D help to regulate immune function (22, 47). Epidemiological studies have not consistently found signicant associations between periodontal disease incidence or prevalence and the intake levels of these and other nutrients (66). However, it is important to consider the range of nutrient intakes or biomarkers in any given study population and how they relate to recommended levels when evaluating the evidence. This information is often lacking in studies of nutritional associations in periodontal research. There are a number of reasons why baseline levels of nutrient intake or biomarkers of nutrient availability inuence the likelihood of detecting an association. Relationships between nutritional status and disease outcomes are usually non-linear and typically exhibit a threshold effect (14). When two or more groups dened by nutritional status are contrasted, there is a much lower chance of nding signicant differences in disease if all groups are adequately nourished. Blood levels of some nutrients (e.g. calcium) are under negative feedback loop regulation by hormones, and associations with disease are more likely to be detected at extreme levels. Finally, associations between a single nutrient and disease may be dependent on the adequacy of a second or even

multiple nutrients, as seen in the inter-relationships of calcium, vitamin D and protein with respect to bone mineral density (15). One of the goals of nutritional research in general, and nutritional epidemiology in particular, is to be able to formulate population dietary guidelines and recommended intake levels that will promote overall health, not just address nutritional deciencies. As more research on nutrition and multiple disease outcomes is performed, including on periodontal disease, the cumulative knowledge is used to revise denitions of an optimal diet. The recommendations for vitamin D are an example of this process. The recommended dietary intake (RDA) for vitamin D in adults was previously 400 IU day or less, a level originally based on the amount of cod liver oil needed to prevent rickets (59). However, it is now known that vitamin D status is associated with a large number of health outcomes, including cancer, cardiovascular disease, inammatory diseases, motor function and the occurrence of falls. Current intake recommendations, up to 1000 IU day, take this multidisciplinary research into account (48). There has also been an upward shift in the serum vitamin D level that is considered optimal (48). In order to evaluate and revise recommended dietary intakes, it is necessary that intake ranges in a study population are well described. This review of studies of nutrition and periodontal disease aims to move beyond the question of whether or not significant associations exist, and examine the research needed to address the questions below. How did the intake or biomarker ranges in the study population inuence nature of the association, or lack of one, that was reported? Can we conclude that current recommended dietary intakes are sufcient to avoid increased risk of periodontal disease onset and progression?

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If not, do higher doses in the form of dietary supplements confer a benet? A number of methodological issues in terms of the study design, collection and analysis of dietary data also affect the interpretation of study results and the ability to reach conclusions about dietary recommendations. These issues will be briey discussed rst, with reference to more thorough reviews.

ease events. Not all intervention studies use random allocation of treatment or have a control group. Randomized controlled trial The investigator randomly assigns treatment or control status to participants who are then followed to measure disease events. Strength: successful randomization ensures that the treatment and control groups are comparable except for the exposure being studied. Limitations: many of the limitations of cohort studies also apply to intervention studies; in addition, participants may not be representative of the general population; harmful exposures cannot be studied using intervention studies. Although it has often been noted that more cohort and experimental studies are needed (51), crosssectional studies still outnumber cohort and interventional studies in the literature on nutrition and periodontal disease.

Study design
Design strategies for clinical and epidemiological studies can be classied as observational or experimental (intervention). The observational study category includes ecological, cross-sectional, case control and cohort (prospective) studies and case reports. Heaton & Dietrich (25) provides an in-depth review of each designs strengths and weaknesses elsewhere in this volume. The most common study designs that have been used in studies of nutrition and periodontal disease fall into one of the categories described briey below. Major strengths and limitations are noted.

Methods to assess dietary intake and nutritional status

Research into diet and periodontal disease requires valid and reliable means to measure and describe dietary intake. The optimal nutritional assessment tool for a specic research question depends on many factors, including whether one wishes to estimate recent diet or habitual diet, total diet vs. a few key nutrients or intake vs. nutrient availability, plus the motivational level of the participants and the expense. However, gathering and interpreting information about an individuals food intake is fraught with difculties. Diet is a complex, ever-changing mixture of nutrients, non-nutritive compounds and contaminants that can have signicant benecial or harmful effects on health. Furthermore, the reporting of food intake by study participants is susceptible to memory errors and bias, and all dietary intake tools rely to some degree on memory and cooperation for accurate information. Nutrient intake and biological availability are not necessarily equivalent, as a persons age, medical conditions, meal composition and other factors can affect the bodys ability to absorb and utilize nutrients. Several tools for assessing dietary intake and nutritional status exist for use in clinical and epidemiological studies. Each has unique assumptions, strengths and limitations. Dietary assessment and analysis methods and nutritional biochemical markers have been extensively described (21, 42, 49, 76).

Observational studies
Cross-sectional Exposure and disease outcome in individuals is assessed at single point in time. Strength: useful for generating hypotheses; generally less expensive than cohort and experimental studies Limitation: inability to establish the temporal sequence of exposure and disease events. Cohort The exposure status of individuals is known at study onset, and participants are followed over time to assess new cases of disease. Strengths: direct measurement of disease events establishes the temporal sequence of exposure and outcome; efcient for studying rare exposures; can study multiple diseases. Limitations: expensive; large losses to follow-up may affect validity.

Experimental studies
Intervention studies The investigator assigns treatment (exposure) to participants, who are then followed to measure dis-

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The primary strengths and limitations of those most commonly used in epidemiological studies of nutrition and periodontal disease are summarized below.

24 h recall
In this method, a trained interviewer elicits from the study participant a detailed list of all foods and beverages consumed within a 24 h period. As the data gathered refer to diet within the past day, little can be assumed about the long-term diet, and foods that are eaten infrequently but contribute signicant amounts of a nutrient (e.g. carotenes) are likely to be missed. The 24 h recall method imposes relatively little burden on the participant, making it easier to obtain a representative sample of the population, provides no opportunity for the participant to actively change his or her eating behavior, and the recall period is brief and recent enough that, with prompting, most people can easily remember what they ate. The principal use of 24 h recall in research is to describe mean nutrient intakes at the population level. The cross-sectional NHANES III and NHANES surveys since 1999 derive nutrient intake data by 24 h recall (1, 50, 53, 54).

Food diaries
The problem of memory encountered with a 24 h recall can be bypassed by having the participant prospectively write down details of each food and beverage as it is consumed. Accuracy is enhanced if all portions are weighed or measured. Like the 24 h recall method, the information only represents current diet. Typically, 37 days of recording are recommended, with both weekday and weekend days represented. Recording for periods longer than a week introduces participant burden, which may have the adverse effects of changing the very diet that one wishes to assess, and increasing errors of omission, but these problems can be alleviated by splitting the recording period into several short, non-consecutive intervals. Food diaries are often the reference method when validating food frequency questionnaires.

are often under-estimated relative to the other methods. Food lists are not comprehensive, fewer details are collected about the items on the list, the consumption frequency response grid is often collapsed into categories (e.g. 13 times month, 2+ times day), and items often combine several foods that have similar nutrient content but may not be eaten with equal frequency. Because of these limitations, it is recommended that rank values or percentiles of nutrient distributions be used rather than absolute values to dene intake level. The analysis of food group consumption frequency is also possible. FFQs are often self-administered, with minimal instruction time needed, and are formatted so the completed forms can be scanned electronically. These properties make them very useful in large-scale epidemiological studies. FFQs readily allow study of associations of disease with food groups in addition to nutrients. Pitiphat et al. (62) and Merchant et al. (44) derived intake data on types of alcoholic beverages and whole-grain foods, respectively, from FFQs that comprised more than 100 food items. Shortened FFQs can be developed that impose less of a burden on the participant if all that is desired is a measure of the intake of one specic food, such as green tea (36), or nutrients found in a limited number of foods, such as calcium and vitamin D (52). However, these shortened FFQs limit the ability to control for other nutrients that act as confounders of the dietdisease relationship.

Biomarkers
Assessment of dietary intake alone is not always the best indicator of a persons nutritional exposure. As noted above, all methods used to measure food intake have issues regarding memory or participant motivation that introduce error and bias. In addition, the amount of a nutrient that is actually available for use by the bodys tissues is inuenced by many factors other than intake, including endogenous production, variation in intestinal absorption, nutrientnutrient and nutrientmedication interactions, disease status, and smoking. To be a useful biomarker, the level of a nutrient or its metabolite in body uids and tissues must correlate moderately well with changes in dietary intake over a wide range of intakes. The ability to measure nutrient availability objectively is the main advantage of using a nutrient biomarker to predict intake, but not all nutrients have meaningful biomarkers (42). In summary, the 24 h recall and food record methods provide the best information about absolute intakes but only measure current diet. The FFQ is

Food frequency questionnaires

A food frequency questionnaire consist of a list of commonly eaten foods and beverages, and a response grid for each item on which the respondent checks off their typical frequency of consumption, usually over a 6-month period or longer. Absolute nutrient intakes derived from food frequency questionnaires (FFQs)

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better structured to assess habitual diet, but this comes at the cost of reduced accuracy. The ability of a biomarker to reect recent or long-term dietary intake is nutrient-specic. Cohort and experimental studies can circumvent these weaknesses to some extent by using the tools in combination and at repeated intervals throughout the study.

potentially confound the results. This is important because higher intakes of certain nutrients and foods may be surrogate measures for a healthy lifestyle. The concordance of overall diet quality with other health habits, particularly smoking (63), is strong, and intakes of specic nutrients and foods such as omega 3 fatty acids and sh are correlated with physical activity, obesity and social status (31, 69).

Analysis of dietary intake data

Compliance with dietary recommendations
Information derived from FFQs, 24 h recall and food diaries can be converted into estimates of daily nutrient intakes by use of food composition tables, or into patterns of food group consumption. Estimates of nutrients and food groups can then be compared with dietary guidelines and recommended intakes to evaluate the adequacy of the diet. In the USA, several standards have been established for this purpose. The estimated average requirement (EAR) is the value that is estimated to meet the requirements of 50% of the population, and is used to estimate the prevalence of intakes that are likely to be inadequate (56). The data used to dene the EAR consider multiple health outcomes, not only nutritional deciencies. The recommended dietary allowance is the EAR plus two standard deviations, and represents the intake level that will meet the needs of 9798% of the population (56). Not all nutrients have an RDA because there may be a lack of studies or because the existing research is inconclusive. If an RDA is not dened, there may be an adequate intake value for the nutrient; this is the level that is believed to meet the needs of all the population (56). RDAs and adequate intake values are appropriate benchmarks against which an individuals nutrient intakes are evaluated. Other guidelines exist for evaluating diet on the basis of food groups. The US Dietary Guidelines for Americans and USDA Food Pyramid Guide provide recommendations for composition and number of servings per day from the grain, vegetable, fruit, milk and meat bean food groups (79). The healthy eating index is an index of overall diet quality that uses the food pyramid recommendations to score overall diet and ten dietary components (32).

Diet and periodontal health

Numerous reviews of associations between diet and periodontal disease have been published, including those by Schifferle (66) and van der Putten et al. (80), who focused on studies of intakes of selected vitamins and minerals in the elderly. These reviews concluded that, due to limitations in study design (mostly cross-sectional) and measurement of diet (recent intake only), there are no consistent associations between dietary intake or serum levels of vitamins B, C, D, calcium and magnesium and periodontal disease in non-institutionalized elderly people (80), and insufcient evidence to justify vitamin and mineral supplementation in adequately nourished individuals (66). The objective of the remainder of the present review is to evaluate studies of diet and periodontal disease from the perspective of how usual recommended nutrient intake and normal biomarker levels in the study population inuenced the nature of the association, or lack of one, that was reported, and whether this information is helpful in conrming or revising dietary recommendations. Not all studies of nutrition and periodontal disease provide this information. The ndings of studies that do are summarized in Tables 15.

Selected vitamins
Folate Adequate dietary intake levels of folic acid are required for synthesis of thymidylate, which is used in the manufacture of DNA, and for synthesis of the amino acid methionine. The EAR for folic acid is 320 lg day and the adequate intake value is 400 lg day (56). Normal serum folate levels, which reect only recent dietary intake (19), are 43317 nmol l (1.914 ng ml). Usual intakes blood levels. In a sub-group of NHANES 20002002 participants aged 60 years and older, the odds of periodontal disease were reduced

Adjustment for covariates

Most observational studies adjust estimates of periodontal disease risk for other characteristics that

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Table 1. Summary of studies of periodontal disease with respect to folate, vitamin C, vitamin A and vitamin E intake
Reference Study design Study population Periodontal disease gingivitis denition 10% of sites with CAL > 4 mm and 10% sites with PPD > 3 mm Mean CAL 1.5 mm Nutritional status assessment method Serum Nutrient Intake serum level* Range (ng ml) <11.2 11.215.9 16.021.4 >21.4 Range (mg day) 180 100179 6099 3059 029 Median (lmol l) 8.5 24.98 39.75 52.24 70.41 Trend Effect estimate

Yu et al. (84)

XS

NHANES 20012002, males and females, age 60 years, n = 844 NHANES III, males and females, age 20 years, n = 12,419 NHANES III, males and females, age 20 years, n = 11,895

Folate

OR 1.0 0.77 0.53** 0.53** OR 1.0 1.16** 1.21** 1.26** 1.30** OR (severe) 1.0 0.67 0.63** 0.47** 0.38** 0.71**

Nishida XS et al. (54)

24 h recall

Vitamin C

Chapple XS et al. (11)

Mild PD = CAL 3 mm + PPD 4 mm at 1 mesiobuccal site Severe PD = CAL 5 mm at 2 mesiobuccal sites + PPD 4 mm at 1 site

Serum

Vitamin C

Vitamin A

Median (lmol l) 1.33 1.68 1.92 2.20 2.69 Trend

OR (severe) 1.0 0.66 0.80 0.69 0.69 0.88 OR (severe) 1.0 1.03 0.93 0.87 0.83 0.87 OR (severe) 1.0 0.90 1.39 1.27 0.89 0.92

b-carotene Median (lmol l) 0.11 0.17 0.26 0.41 0.73 Trend Vitamin E Median (lmol l) 16.42 20.06 23.45 27.98 37.48 Trend

XS, cross-sectional; PD, periodontal disease; CAL, clinical attachment loss; PPD, probing pocket depth; OR, odds ratio. *Values in bold include recommended intake or normal optimal serum ranges. **P < 0.05 relative to the reference group. Trend refers to an increase or decrease in odds ratio with increasing nutrient level.

by approximately half among those with serum folate levels above the median (>16 ng ml) relative to those below the median (83). The odds were adjusted

for age, sex, race, education, body mass index, bleeding on probing, chronic diseases, vitamin B12 and homocysteine levels, smoking and alcohol. The

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Table 2. Summary of studies of periodontal disease with respect to calcium and vitamin D intake
Reference Study design Study population Periodontal disease gingivitis denition Mean CAL (mm) Nutritional status assessment method Serum Nutrient(s) Intake serum level* Effect estimate

Dietrich XS et al. (16)

NHANES III, male and female, age 20 years, n = 11,202

Vitamin D Range (nmol l) 40.2 40.453.7 53.967.9 68.185.4 85.6 (reference) Vitamin D Median (nmol l) 32.4 47.4 60.7 75.6 99.6 Trend Calcium Intake (mg day) 800 500799 2499 Intake (mg day) 1000 1000

b (M 50 years) 0.39** 0.23** 0.06 0.09 0.00 OR 1.0 0.98 0.90 0.88 0.80** 0.90** OR (M) 1.0 1.3** 1.3**

b (F 50 years) 0.26** 0.10 0.00 0.10 0.00

Dietrich XS et al. (17)

NHANES III, male and female, age 13 years, never smokers, n = 6700 NHANES III, male and female, age 20 years, n = 12,419

% mesio buccal sites per subject with BOP

Serum

Nishida XS et al. (53)

Mean CAL 1.5 mm

24 h recall

OR (W) 1.0 1.3** 1.5**

Krall (35)

FFQ PD pro PRO, VA Dental gression: 7 years Longitudinal number of Study, males only, mean age teeth with worsening 63 years, of ABL n = 550 from 20% to >20% since baseline Mean Periodontal PPD, CEJ maintenance AC patients with moderate to se- distance, BOP, vere PD, male furcation and involvement female, n = 51 (23 supplement users, 28 non-users)

Calcium

Mean number of teeth SE ABL progression 2.6 0.2 2.0 0.1**

Miley XS et al. (46)

FFQ and Calsupplement cium + questionnaire vitamin D

Use of supplement Yes (1.7 g 1049 IU) No (0.6 g 156 IU) Yes No Yes No Yes No

Mean (95% CI) Probing depth (mm) 2.18 (2.02.4) 2.33 (2.12.6) Attachment loss (mm) 1.80 (1.42.2) 2.01 (1.62.4) % bleeding sites 60 (5269) 66 (5874) CEJAC (mm) 1.71 (1.32.1) 2.04 (1.62.5)

XS, cross-sectional; PRO, prospective; PD, periodontal disease; CAL, clinical attachment loss; PPD, probing pocket depth; BOP, bleeding on probing; CEJAC, distance from cemento-enamel junction to alveolar crest; ABL, alveolar bone loss; FFQ, food frequency questionnaire; b, standardized regression coefcient from multiple linear regression; M, males; F, females; OR, odds ratio; 95% CI, 95% condence interval; SE, standard error. *Values in bold include recommended intake or normal optimal serum ranges. **P < 0.05 relative to the reference group. Values for calcium are in grams; those for vitamin D are in IU.

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Table 3. Summary of studies of periodontal disease with respect to omega fatty acid intake
Reference Study design Study population Periodontal disease gingivitis denition Nutritional status assessment method Nutrient Intake serum level Effect estimate

Naqvi XS et al. (50)

4 mm PPD 24 h recall NHANES and 3 mm and supple 19992004, ment ques CAL on any male and female, mid-facial or tionnaire mesial tooth age 20 years, n = 9182

Docosahexae Range (g day) noic acid 0 > 0 to < 0.04 0.04

OR 1.0 0.70** 0.77**

Eicosapentae Range (g day) noic acid 0 > 0 to < 0.01 0.01 Linolenic acid Range (g day) < 0.91 0.911.67 > 1.67

OR 1.0 0.77** 0.84 OR 1.0 1.06 0.79 Mean gingival index change 0.68 (reference) 0.31 )1.04** )0.07

n-3, n-6 Three Rosenstein RCT, Volunteers, Changes in supplement et al. (64) 12 males only, mean groups plus gingival weeks age 18 index, mean placebo 60 years, PPD with periodontal disease, n = 24

Placebo Fish oil (3 g n-3) Borage oil (3 g n-6) Fish + borage oil (1.5 g n-3 + 1.5 g n-6)

Mean PPD change Placebo 0.02 (reference) Fish oil (3 g n-3) )0.41 Borage oil (3 g n-6) )0.50** Fish + borage oil )0.17 (1.5 g n-3 + 1.5 g n-6)

XS, cross-sectional; RCT, randomized controlled trial; PPD, probing pocket depth; CAL, clinical attachment loss; n-3, omega 3 fatty acid; n-6, omega 6 fatty acid; OR, odds ratio. **P < 0.05 relative to the reference group.

upper limit of serum folate in the lowest quartile was 11.2 ng ml, which is well within the normal range (Table 1). Since 1998, our has been fortied with folate in the USA, which may explain why the serum levels were relatively high in all quartiles. A crosssectional study from Japan found inverse correlations between the percentage of sites with bleeding on probing and dietary folic acid intake, but no correlation between dietary folic acid intake and the community periodontal index (20). The authors reported a mean intake (SD) of 372 199 lg day, but there was no indication of how many participants had inadequate intakes. This study restricted participation to non-smokers with at least 20 teeth, which may have excluded individuals with severe chronic periodontitis from the study population. More studies that include younger age groups and measures of dietary intake are required to determine whether

increasing intake above the current RDA will reduce the risk of periodontal disease. Ascorbic acid (vitamin C) Ascorbic acid performs several key metabolic roles that make it important for maintaining the integrity of connective tissue. It is a co-factor for the hydroxylation of proline and lysine, two proteins used to manufacture collagen. Once hydroxylated, these proteins form cross-links in the collagen molecule that stabilize its structure. Vitamin C insufciency may affect immunocompetence. Ascorbic acid also acts as an intracellular antioxidant to protect DNA from oxidative damage. The role of ascorbic acid deciency in causing scurvy is well known, but it is not certain whether milder degrees of insufciency have clinically important effects on the periodontium. The EAR for vitamin C is 75 mg day (men) and

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Table 4. Summary of studies of food groups with respect to periodontal disease

Study population Health Professionals Follow-up Study, males only, age 4075 years, free of PD at start, n = 34,160 Self-report Have you had professionally diagnosed periodontal disease with bone loss? FFQ Whole grains RR 1.0 0.89 0.77** 0.81** 0.77** OR Median (servings day) 0.2 0.9 1.6 2.6 4.7 Milk Range (g day) 027.9 2889.9 90199.9 200 027.9 2889.9 90199.9 200 Lactic acid foods (e.g. yogurt) Range (g day) 0 0.127.9 2854.9 55 0 0.127.9 2854.9 55 1.0 1.07 0.98 0.78 0.80 % subjects with PPD 4 mm 21 19 19 20 CAL 5 mm 19.5 22 17 21 FFQ OR PPD 4 mm 1.0 0.59** 0.63 0.40** CAL 5 mm 1.0 0.71 0.63 0.50** Median (servings day) 0.3 0.8 1.3 1.9 3.4 Periodontal disease gingivitis denition Nutritional status assessment method Food Intake level* Effect estimate

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NHANES III, male and female, age 18 years, n = 13,665 CAL 3 mm + PPD 4 mm at 1 site 24 h recall Dairy foods The Hisayama (Japan) Study, male and female, age 4079 years, 10 teeth, n = 942 CAL 5 mm at 10% of sites; PPD 4 mm at 20% of sites

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Reference

Study design

Merchant et al. (44)

PRO, 12 years

Al-Zahrani (1)

XS

Shimizaki et al. (68)

XS

Dietary guidelines and periodontal health

XS, cross-sectional; PRO, prospective; PD, periodontal disease; CAL, clinical attachment loss; PPD, probing pocket depth; FFQ, food frequency questionnaire; RR, relative risk; OR, odds ratio. SD, standard deviation. *Values in bold include recommended intake or normal optimal serum ranges. **P < 0.05 relative to the reference group.

Daily milk Daily milk consumption Yes (252 ml/day) No (57 ml day)

Median (g day) OR 1.0 13.1 0.8 26.2 0.79 37.4 0.65** 53.6 0.68** 86.8

Intake level*

60 mg day (women). The corresponding RDAs are 90 mg day and 75 mg day (56). Plasma values reect recent intake. Normal plasma values are 23 114 lmol l. Values <23 lmol l but >11 lmol l are considered low, and values <11 lmol l are considered decient. Plasma levels reach a plateau at approximately 68107 lmol l when dietary intake exceeds 200 mg day (29). Usual intakes blood levels. Chapple et al. (11) analyzed serum levels of several vitamins in relation to periodontal disease prevalence in the NHANES III population survey. The median ascorbic acid value in the lowest quintile (8.5 lmol l) fell in the decient range, but median values in quintiles 25 were well within the normal range (24.98, 39.75, 52.24 and 70.41 lmol l, respectively). There was a signicant inverse trend between quintile of serum ascorbic acid and odds of both mild and severe periodontal disease (Table 1). Compared with the lowest serum quintile, individuals in quintile 5 had a 50% reduction in the odds of mild periodontal disease and a 62% reduction in the odds of severe periodontal disease. The odds ratios were adjusted for age, gender, race ethnicity, cigarette smoking, oral contraceptive and hormone replacement use, diabetes, povertyincome ratio, and education and NHANES III sampling design. Dietary ascorbic acid intake was examined in the same population (54). Individuals whose intake was below 30 mg day had 40% higher odds of periodontal disease than those whose intake was 180 mg or more. The odds of disease were also 2030% higher among those with intakes between 30 and 179 mg day, controlling for age, gender, smoking and gingival bleeding (Table 1). The study by Chapple et al (11). indicated that the highest risk of periodontal disease occurs when the serum vitamin C level approaches the decient range, and risk is lowest when serum levels reach a plateau. The dietary vitamin C data are consistent with the serum ndings, and suggest that ascorbic acid intake greater than the current RDA is associated with decreased periodontal disease risk. However, the value of supplementation with larger doses of ascorbic acid to prevent periodontal disease has not been demonstrated (66). Supplement studies trials. Studies by Leggott et al. (38) of the effects of short-term depletion and replacement of ascorbic acid on measures of periodontal disease showed no signicant effect of ascorbic acid supplements on pocket depth and attachment loss. Intake of vitamin C was reduced from 250 to 5 mg day for 32 days to create a state of

Mean number of PD events (SD) 9.6 6.1 10.3 7.3 PD event: change in CAL by FFQ 3 mm from baseline value PRO, 6 years Survey of older adults in Niigata City (Japan), male and female, age 70 years, n = 261 Yoshihara et al. (82)

Effect estimate

Periodontal disease gingivitis denition

Table 4. (Continued)

Study design

Tanaka et al. (71)

Reference

XS

Freshmen in Dietetic Courses Self-report Have you been diagnosed as having Study II (Japan), females periodontal disease by a only, age 1822 years, dentist? n = 3956

Study population

Diet history questionnaire (past month)

Nutritional status assessment method

Total soy

Food

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Study population Erie County (NY) study, male and female, age 25 74 years, n = 1371 <5 5 <10 10 <10 10 NHANES III, male and Mean CAL 1.5 mm female, age 20 years, n = 13,198 Alcohol-specic questionnaire: number of drinks day number of days month that alcohol was consumed in past 12 months Range (drinks week) <5 5 <10 10 <15 15 <20 20 FFQ: how often, on average, consumed beer (1 bottle or can), wine (118 ml glass) and liquor (1 drink or shot) in the past year; converted to g day Alcohol-specic questionnaire: frequency and volume of beer, wine and hard liquor; converted into centiliters (cl) ethanol Mean longitudinal change in ABL (ACapex distance as percentage of CEJapex distance) GB at >0.35% of sites; severe CAL > 4 mm; severe ABL 4 mm Alcohol-specic questionnaire: usual number of drinks week Range (drinks week) <5 5 OR GB 1.0 1.65** Severe CAL 1.0 1.36** GB 1.0 1.62** Severe CAL 1.0 1.44** OR 1.0 1.2** 1.0 1.4** 1.0 1.5** 1.0 1.7** Range (g day) RR 1.0 0 1.24** 0.14.9 1.18** 514.9 1.18** 1529.9 1.27** 30 Range (cl day) 01 1.012 2.013 3.014 4.015 >5 Mean SD 71.3 76.0 72.7 75.4 75.2 73.7 14.6 10.5 11.3 12.0 8.2 10.9 Periodontal disease gingivitis denition Nutritional status assessment method Intake level Effect estimate Health Professionals Follow-up Study, males only, age 40 75 years, n = 39,461, free of PD at start County of Stockholm Study, male and female, mean age 54.9 years, n = 477 Self-report Have you had professionally diagnosed periodontal disease with bone loss?

Table 5. Summary of studies of alcohol with respect to periodontal disease

Krall Kaye

Reference

Study design

Tezal et al. (74)

XS

Tezal et al. (75)

XS

Pitiphat et al. (62)

PRO, 8 years

Jansson (30)

PRO, 20 years

Dietary guidelines and periodontal health

XS, cross-sectional; PRO, prospective; GB, gingival bleeding; CAL, clinical attachment loss; BOP, bleeding on probing; ABL, alveolar bone loss; AC, alveolar crest; CEJ, cemento-enamel junction; OR, odds ratio; RR, relative risk; SD, standard deviation; M, males; F, females. **P < 0.05 relative to the reference group. 5 cl is equivalent to approximately 1.7 uid ounces.

Effect estimate

OR (M) CAL 3 mm 1.03 1.0 0.53 0.51** 0.34** %BOP 25 1.79** <1 16 (reference) 1.0 0.98 713 0.78 1420 0.81 21

depletion. Only gingival bleeding increased; mean pocket depth and attachment loss did not change in this initial period. When participants then took supplements of either 60 or 250 mg day for 56 days, bleeding returned to baseline levels but there was still no change in mean pocket depth or attachment loss. Vitamin A and carotenes a-carotene, b-carotene, lycopene, cryptoxanthin and lutein are the most common dietary forms of carotenes. All function as antioxidants. In addition, bcarotene is converted into the biologically active form of vitamin A, retinoic acid, which is essential for maintaining the integrity of mucosal tissues and for proper differentiation of cells, including those of the immune system (61). EARs and RDAs exist only for total vitamin A; the EAR is 625 lg retinol activity equivalents day; the RDA is 900 lg retinol activity equivalents day for men and 700 lg retinol activity equivalents day for women) (56). There is no specic recommendation for b-carotene, although the US Institute of Medicine states that 36 mg of b-carotene daily (equivalent to 277500 lg retinol activity equivalents) will maintain blood levels of b-carotene in the range associated with lower risks of chronic diseases (55). Adequate serum values are 0.7 3 lmol l for vitamin A and 0.181.58 lmol l for bcarotene. Vitamin A is stored in the liver and serum levels are closely regulated, so low and decient serum values signify depletion of the liver stores. Usual intakes blood levels. Serum levels of b-carotene and total vitamin A were inversely related to adjusted odds of severe periodontitis in NHANES III participants (11). Median total vitamin A values were all within the normal range (Table 1), but median b-carotene values in the two lowest quintiles were below normal (0.11 and 0.17, respectively). There were similar trends for mild periodontal disease and total vitamin A, carotene and lutein. In a study of older men with a diagnosis of low-threshold (mild) or high-threshold (severe) periodontal disease, periodontal disease was associated with low serum a- and b-carotene, but no data were given for the range of values within each quintile (40). More studies of periodontal disease, vitamin A and carotene intakes are needed. Vitamin E Vitamin E functions as an antioxidant and prevents propagation of damage to cell membranes by peroxyl radicals formed by the oxidation of lipids. The EAR for vitamin E is 12 IU, and RDAs are 15 IU for adult

OR (F)

1.19 1.0 1.05 0.85 0.82

Table 5. (Continued)

Study design

Reference

Kongstat et al. (34)

XS

Copenhagen City Heart Mean CAL 3 mm; %BOP 25 Alcohol-specic questionnaire: weekly intake of beer, wine, Study, male and spirits (1 drink = 12 g alcohol) female, age 20 95 years, n = 1521

Study population

Periodontal disease gingivitis denition

Nutritional status assessment method

Range (drinks week) <1 16 (reference) 713 1420 21

Intake level

1.02 1.0 1.10 0.86 1.24

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men and 12 IU for adult women (56). Normal serum value ranges from 12 to 46 lmol l. Usual intakes blood levels. To date, studies have not found signicant associations between serum vitamin E levels and periodontal status (11, 40). Chapple et al. (11) examined serum vitamin E by quintiles, and found no associations with either severe (Table 1) or mild disease. Median serum values in quintiles 15 were all within the normal range (16.42, 20.06, 23.45, 27.98 and 37.48 lmol l).

quintiles 1 and 5 differed signicantly (16). In a subset of the NHANES III population who never smoked, the odds of gingival bleeding at sites without attachment loss in quintile 5 (median 99.6 nmol l) were 20% lower compared with quintile 1 (median 32.4 nmol l), and, overall, the odds decreased 10% for each 30 nmol l increase in 25(OH)D (17). These two studies suggest that the denition of optimal serum level for vitamin D is appropriate for periodontal disease. Calcium Calcium performs a structural function as a component of the hydroxyapatite crystals of teeth and bone. This critical function has been clearly shown in systemic bone, with reductions in the rates of bone loss and osteoporotic fracture incidence in older persons as a result of providing calcium intake levels of at least 1000 mg daily in combination with vitamin D (18, 72). The adequate intake value for calcium is 1000 mg day for adults 1950 years old, and 1200 mg day for ages 51 and older (56). The hypothesis that adequate calcium intake reduces the risks of oral bone loss and periodontal disease dates back over 50 years. Early cross-sectional studies and supplementation trials suggested that increased calcium intake may reduce gingival bleeding, increase alveolar crest height and decrease probing depth and tooth mobility, but were hampered by lack of detail regarding methods used to assess these periodontal outcomes (26). In the past decade, further studies have examined this hypothesis. Usual intakes blood levels. An analysis of more than 12,000 adults from NHANES III suggested that low levels of dietary calcium intake are associated with a higher prevalence of periodontal disease (53). After controlling for age and smoking status, the odds of a higher than average periodontal attachment loss (1.5 mm) were 1.27 (men) and 1.54 (women) times greater among those whose calcium intake was below 800 mg day compared with thise whose calcium intake was 800 mg day (Table 2). A 7-year prospective study of 552 older men suggested that calcium intakes in the highest quartile (above approximately 1000 mg day) were associated with slower alveolar bone loss progression, independently of age, initial number of teeth, smoking status, vitamin D intake, caries status and clinical periodontal disease status, relative to lower intakes (35) (Table 2). However, as noted in the discussion of dietary assessment methodology,

Vitamin D and calcium

Vitamin D Vitamin D is an inclusive term for several forms of the hormone cholecalciferol. The best-known action of the biologically active form of this hormone, 1,25-dihydroxycholecalciferol [1,25(OH)2D3], is regulation of plasma calcium and phosphorus levels. Vitamin D also has a role in the immune system. Antigen-presenting cells, macrophages and lymphocytes express a nuclear receptor for vitamin D. In vitro, 1,25(OH)2D3 inhibits the production of pro-inammatory cytokines and T-lymphocyte proliferation, and also increases production of antiinammatory cytokines (81). Vitamin D can be manufactured by conversion of 7-dehydrocholesterol found in the skin into pre-vitamin D after exposure to the sun. In the absence of sun exposure, the RDA for vitamin D is 5 lg day (200 IU) for adults aged 1950 years, 10 lg (400 IU) for adults aged 5170 years, and 15 lg (600 IU) for those over 70 years old (56). Vitamin D status is best determined by the level of serum or plasma 25-hydroxyvitamin D [25(OH)D], which reects the total contribution from both dietary and endogenous sources. Although blood levels <10 nmol l indicate deciency, levels between 75 and 100 nmol l are now considered optimal. It is estimated that intakes of vitamin D of 17.525 lg (7001000 IU) are required to achieve blood 25(OH)D levels in the optimal range (48). Usual intakes blood levels. Two studies used NHANES III participants to examine the odds of periodontal disease in relation to quintiles of serum 25(OH)D values (16, 17). As seen in Table 2, the mean periodontal attachment loss in quintiles 1 and 2 (<40.2 and 40.453.7 nmol l, respectively) was signicantly higher than in quintile 5 (85.6 nmol l) among men aged 50 years and older. Among women,

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nutrient estimates derived from FFQ are only approximate. Supplement studies trials. Miley et al. (46) compared several measures of periodontal disease between patients who voluntarily used vitamin D and calcium supplements and those who did not (Table 2). All participants were periodontal maintenance patients with moderate to severe periodontal disease. The mean vitamin D intake among supplement users was 1048 IU, compared to only 156 IU among non-users. Mean calcium intakes in the two groups were 1769 and 642 mg, respectively. Although both mean vitamin D and mean calcium intakes in the supplement group were greater than recommendations, there were no signicant differences in probing pocket depth, bleeding on probing, furcation involvement, or the distance between the cemento-enamel junction and the gingival margin (57). In another study, supplements of calcium (1000 mg) in combination with vitamin D (800 IU) were shown to result in gain of alveolar bone height and bone mass over 3 years among post-menopausal women (13); however, there was no control group who did not receive supplements. To date, the results of human studies evaluating the effects of low dietary calcium intake on periodontal disease remain inconclusive (26).

exhibited less periodontal disease than persons not taking such drugs (44). Clinical trials of the effect of magnesium supplementation on periodontitis are lacking, but are not warranted until further cohort studies have been performed (45).

Macronutrients
Omega 3 (n-3) and omega 6 (n-6) polyunsaturated fatty acids These long-chain fatty acids are incorporated into structural lipids of the cell membranes and contribute to membrane integrity. They are the precursors of eicosanoids (prostaglandins, prostacyclins, thromboxane and leukotrienes), which act as modulators of immune function. Important eicosanoids include the n-3 fatty acids eicosapentaenoic acid, docosahexaenoic acid and a-linolenic acid, and the n-6 fatty acid c-linolenic acid. Eicosanoids derived from n-3 fatty acids compete with n-6-derived mediators but are less potent in their pro-inammatory actions. A second group of mediators known as resolvins, which possess anti-inammatory properties, are derived from eicosapentaenoic acid and docosahexaenoic acid (24). Thus, higher intakes and blood levels of n-3 polyunsaturated fatty acids are expected to attenuate the inammatory response. The American Heart Association states that 5001800 mg per day of combined docosahexaenoic acid and eicosapentaenoic acid will signicantly reduce the all-cause death rate (39). Usual intakes blood levels. Naqvi et al. (50) examined associations between periodontal disease prevalence (at least one tooth with a pocket depth 4 mm and attachment loss 3 mm) and intake tertiles of docosahexaenoic acid, eicosapentaenoic acid and linolenic acid in the 19992004 NHANES population. Intakes from diet alone and diet plus supplements were evaluated. Signicantly lower odds of periodontal disease (2330% lower) were observed for the middle docosahexaenoic acid and eicosapentaenoic acid tertiles, which encompassed >0 but <40 mg day docosahexaenoic acid, and >0 but <10 mg day eicosapentaenoic acid (Table 3). The results did not differ when supplemental omega fatty acids were added to the diet. These intake levels are considerably lower than recommended for prevention of heart disease. There was no association between linolenic acid and periodontal disease status. A 5-year prospective study from Japan reported a 49% higher risk of periodontal disease in the lowest vs. highest tertiles of docosahexaenoic acid (28). However, the ranges of intakes in each tertile were not provided.

Other minerals
Magnesium Magnesium is necessary for numerous enzymatic reactions that synthesize and activate nutrients, and plays important roles in stabilization of membranes and ion transport. Approximately two-thirds of the bodys magnesium is found in mineralized tissues. Reduced serum magnesium concentrations are associated with an enhanced inammatory response to bacterial challenge. Normal serum magnesium levels are 0.750.95 mmol l. Usual intakes blood levels. Among participants age 40 years and older, serum magnesium was signicantly positively correlated with the percentage of sites with probing pocket depth and clinical attachment loss 4 mm, but no data were provided for the range of serum magnesium values (44). The extent of periodontitis was inversely related to the quartile of the magnesium:calcium ratio, but this appears to be the only study to have used this ratio. Supplement studies trials. In the above study, subjects taking magnesium-containing medications

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Supplement studies trials. In a pilot placebo-controlled clinical trial, daily supplements of sh oil totaling 3 g eicosapentaenoic acid, 3 g c-linolenic acid (borage oil) or 1.5 g each of eicosapentaenoic acid and c-linolenic acid were given to men with mild to severe periodontitis (64). Although mean probing depth and gingival index tended to improve over the 12-week study in all three groups relative to the placebo group, the ndings were statistically signicant only in the group given borage supplements alone (Table 3). These ndings conict with an earlier pilot study of healthy subjects that suggested that 1.8 g n-3 polyunsaturated fatty acids reduced gingival inammation to a greater degree than did olive oil, which contains only 0.06 g of n-3, but had no effect on gingival bleeding (9). The study by Naqvi et al. suggests that a benecial effect on periodontal disease can be obtained from modest intakes of n-3 fatty acids, but other studies do not consistently support the notion that more benet is gained from large doses. More research is required to resolve these discrepancies. Fiber Dietary ber is a term used for plant-derived cellulose, polysaccharides and lignins that cannot be completely digested by humans. A low ber intake is associated with poor glycemic control (3), which independently increases the risk of periodontal disease (12). A higher intake of dietary ber may also be a surrogate marker for overall dietary quality. Recommended levels of ber intake are 14 g/1000 Kilocalories per day (79). Usual intakes blood levels. Petti et al. (60) performed a study of dietary ber intakes among teenage girls, some of whom had gingival bleeding at one or more sites and others with no bleeding. Intakes of several nutrients, including ber, were compared between the groups. Fiber intake frequency, but not absolute grams of ber, was signicantly associated with lower odds of gingival bleeding. No data on the prevalence of low intakes were provided.

associations between periodontal disease and food groups, although the interpretation of ndings still presents a challenge, as in most cases, high consumption of one food group necessarily displaces other food groups in the overall diet. Table 4 summarizes studies of periodontal disease and food groups. Grains Grains are good sources of ber, B vitamins and magnesium. The USDA Food Pyramid recommends six servings per day for adults, with at least three of those servings as whole grains (79). Usual intakes blood levels. Merchant et al. (44) reported that the risk of developing periodontal disease was highest among men who consumed fewer than 0.6 servings per day of whole grains, and the risk decreased with increasing whole-grain consumption (Table 4). This trend was also seen for quintiles of cereal ber intake. Yoshihara et al. (82) found an increased risk of periodontal disease with higher consumption of cereals, nuts and seeds, but this grouping also included rened sugars and confectionary products as well as whole grains. Dairy foods Dairy foods are good sources of not only calcium and vitamin D, but also other nutrients with important roles in bone health, such as phosphorus, magnesium and B vitamins. For a 2000 kilocalorie diet, three servings of dairy foods per day are recommended (79). Usual intakes blood levels. Al-Zaharani (1) observed a signicant inverse trend between daily servings of dairy foods and adjusted odds of periodontal disease in an analysis of NHANES III data. Participants whose dairy food consumption was in the 4th and 5th highest quintiles (median of 2.6 and 4.7 servings per day, respectively) had 20% and 22% lower odds of disease compared to those in the lowest quintile (Table 4). These odds ratios were adjusted for age, gender, race ethnicity, smoking, education, diabetes, poverty index, vitamin use, body mass index, physical activity, time since last dental visit, gingival bleeding and dental calculus, but not other nutrients or food groups. Shimizaki et al. (68) reported no signicant difference in the prevalence of generalized deep pockets (20% sites 4 mm) and severe attachment loss (10% sites 5 mm) among quartiles of milk intake (Table 4). The highest quartile included intakes 200 g milk (6.5 uid ounces or more). However, for persons consuming 55 g or more

Food groups
For the purpose of translating basic and clinical research ndings into public health policy and guidelines, it is important to identify the best combinations of foods or eating habits that provide a balance of benecial and detrimental nutrients. However, as nutrients with similar function tend to be found in similar foods, it is difcult to isolate the effects of single nutrients on disease. A few studies have examined

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of foods containing lactic acid (yogurt and lactic acid drinks), the odds of deep pockets and severe attachment loss were less than half those in persons who consumed none. Another study conducted in Japan found no association between progression of clinical attachment loss and daily consumption of milk (83). Daily milk drinkers consumed an average of 252 ml, or approximately one cup (Table 4). Taken together, these studies suggest that an intake of one cup of milk or dairy products is not sufcient to demonstrate an association with periodontal disease, but higher intake of two or more servings may be protective. More studies at higher intakes are required. Fruits and vegetables These foods are the primary sources of dietary ber, carotenes and water-soluble vitamins such as vitamin C and folate. The US Dietary Guidelines recommend four servings (two cups) per day of fruit and ve servings (2.5 cups) of vegetables. Of the vegetable servings, ten servings per week should comprise dark green and yellow vegetables (79). Usual intakes blood levels. Worsening of periodontal disease (change in clinical attachment loss 3 mm from baseline value) was inversely related to consumption (g kg body weight) of dark green and yellow vegetables in a cohort of 70-year-old men and women (82). No data on number of servings were provided.

stein and daidzein in a study of young women. The highest two quintiles of total soy intake were associated with 3235% reduction in the odds of periodontal disease (Table 4). Signicant reductions in the odds of periodontal disease, but of smaller magnitude, were also observed for total isoavones, genistein and daidzein. Alcohol Metabolism of ethanol produces acetaldehyde, which is toxic to tissues. In a rat model, chronic alcohol consumption increased gingival levels of tumor necrosis factor, polymorphonuclear leukocytes and alveolar bone loss relative to control animals (27). Alcoholics present with more extensive periodontal disease than non-alcoholics (2), but it is not clear how light and moderate drinking affects disease risk. Moderate drinking is dened as not more than two drinks per day for men and not more than one drink for women (79). One drink contains 13.7 g of ethanol, and is equivalent to 355 ml of beer, 148 ml of wine and 44 ml of liquor. Usual intakes blood levels. Studies of alcohol use and periodontal disease are shown in Table 5. Several of these studies suggest that moderate and heavy alcohol consumption increase the risk of clinical attachment loss, deep probing pockets and gingival bleeding (74, 75) or self-reported periodontal disease (62). However, Jansson et al. (30) reported that subjects with high alcohol consumption (>5 cl ethanol per day) did not develop more periodontal disease or gingivitis relative to non-drinkers, but they did have more surfaces with caries and apical lesions. Further conicting results were reported in the Copenhagen City Heart Study, in which alcohol consumption appeared to be protective; the odds of mean clinical attachment loss 3 mm was 0.34 among men who drank 35 or more drinks per week relative to those who drank less than one drink week (34). Probiotics Probiotics are living microorganisms that have benecial effects on human health. In the American diet, yogurt is a primary source of several of the Lactobacillus strains of bacteria that have these properties. Actions of probiotic bacteria that have a potentially benecial inuence on periodontal disease include secretion of antimicrobial substances (e.g. organic acids and hydrogen peroxide), competition with pathogenic strains for adhesion to the mucosa, modication of intra-oral pH, and reduction in the quantity of plaque (73). Probiotics administered in

Other constituents of food

There are many other compounds in foods that may affect human health but are not considered essential nutrients, may not have recommended intake levels, and, in some cases, potentially cause harm. Several of these constituents have been examined in relation to periodontal disease risk. Soy Soybeans are a unique source of isoavones (primarily genistein and daidzein) that resemble estrogen in their structure and biological activity. One effect of isoavones is to enhance cell-mediated immunity (65). In animal models, isoavones have been shown to affect adhesion molecules and decrease activities of the pro-inammatory cytokines tumor necrosis factor-a and interleukin-6, but their effect in humans is not clear (6). Tanaka et al. (71) examined the relationship between self-reported periodontal disease and intake levels of total soy products which are sources of the isoavones geni-

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tablet form reduce pathogenic bacteria levels (41, 67), and a liquid milk product containing a strain of Lactobacillus casei signicantly reduced activities of polymorphonuclear elastase, myeloperoxidase and matrix metalloproteinase-3 in an 8-week trial (70). However, no difference in papillary bleeding was found between subjects receiving the probiotic drink and those consuming their regular diet (70). Thus, the role of benecial bacteria in preventing the emergence of pathogenic species and to maintain or improve periodontal status remains unclear (73). Other polyphenols Polyphenols are a group of phytochemicals that include avonoids, isoavonoids, catechins and anthocyanidins. Chocolate and green tea are good sources of catechins. The number of cups of green tea per day was inversely related to mean pocket depth, clinical attachment loss and extent of bleeding on probing in a study of Japanese men (36). Cranberries, grapes and blueberries are rich sources of anti-inammatory and antibacterial polyphenols (7, 57). Complementary and alternative medicine supplements Various components of complementary and alternative medicine and herbal supplements possess antimicrobial, antioxidant or immunity-enhancing properties, including echinacea (5), garlic (23), ginger (77), ginseng (33) and combinations of plant extracts referred to as traditional Chinese and Japanese herbal medicines (8). Their effectiveness for treating periodontal disease infections has been studied to a limited degree. These components inhibit growth in vitro of a broad spectrum of species of periodontal pathogens (4, 10, 58, 78), but more research is required to determine the effects on clinical periodontal disease parameters. Environmental contaminants Persistent organic pollutants may alter the immune system and have been linked to several inammatory chronic diseases. Increased serum levels of organic pollutants were associated with higher odds of having at least one site with pocket depth 4 mm and clinical attachment loss 4 mm in the NHANES 1999 2002 survey (37). The strongest associations, with odds ratios in the range 25, were seen for organochlorine pesticides commonly found in the food supply.

Summary and directions for future research

It is a fact that a good diet is important for overall health. A considerable amount of research has contributed to the formulation of dietary intake recommendations and guidelines that take into account the effects of nutrients on multiple health and disease outcomes. These guidelines continue to evolve, and research on diet and periodontal disease can play a valuable part in determining whether recommendations need to be revised in order to cover periodontal disease. To date, there is insufcient evidence that current dietary intake recommendations and guidelines need to be changed in order to promote optimal periodontal health. However, the research is incomplete. In order to ll the gaps in our understanding, future research should: comprise more prospective, and, when appropriate, controlled intervention studies estimate absolute nutrient intakes, use accurate dietary assessment methods (diet records, 24 h recall), and, whenever possible, multiple tools to measure nutritional status provide detailed information about usual intake or biomarker ranges and the prevalence of the population with insufciency and deciency status expand the range of nutrients to include phytochemicals, probiotics and the herbs and spices found in complementary and alternative medicines expand the focus to overall diet and healthy eating patterns rather than trying to isolate individual nutrients determine whether recommendations differ for persons who already have periodontal disease compared to those without disease

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