Is inflammatory potential of the diet related to oral and periodontal health?

Abstract Inflammation is among the risks of periodontal diseases. The relationship between the inflammatory load of the diet and inflammation has been shown in previous studies, but the relationship between periodontal diseases and the inflammatory load of the diet is not clear. In this study, it was aimed to examine the relationship between dietary inflammatory index (DII) and periodontal health. Board approved the protocol. Information about the study was given to the patients who met the criteria of the study and agreed to participate in the study. Oral health status was evaluated by measuring the Decayed, Missing, and Filled Teeth (DMFT). Periodontal health status was determined using the plaque index (PI) and gingival index (GI). Twenty‐four‐hour dietary record was taken for 1 day to calculate the inflammatory load gained from daily diet, and the DII score was used. The study group consisted of 138 participants. DMFT scores were found with median 4.0, and no statistically significant difference was observed between DII quartiles. 65.8% of the participants had absence or small amount of plaque accumulation, while 39.2% had moderate or dense amount of plaque accumulation according to the PI classification. While DII did not differ by PI classification, DII quartile between second and third found a difference according to the GI classification. The new definition of periodontal health has been proposed as the absence of clinically detectable inflammation. It seems that pro‐inflammatory properties of the diet and periodontal health are related. But future randomized controlled trials are needed.

the emergence of organic acids in high concentrations, and lead to demineralization of tooth enamel (Mahan & Raymond, 2016;Stanski & Palmer, 2015).If demineralization exceeds remineralization over time, cavitation of the enamel surface will occur, leading to decay (Kleinman & Greer, 2014).The type, form, and frequency of food and drink consumed have a direct effect on oral pH and microbial activity, which can increase tooth decay (Mahan & Raymond, 2016).
Studies have shown that the risk of dental caries is low if the per capita simple sugar intake is less than 15 kg per year (Moynihan, 2005).
In addition, a diet rich in refined carbohydrates and saturated fat can initiate inflammatory processes through the production of reactive oxygen species.Restricting refined carbohydrates and saturated fats can reduce the activation of pro-inflammatory pathways (Gondivkar et al., 2019).
Plaque formation is considered to be the main factor in the development of periodontal diseases.As a result of the increase in plaque volume, a suitable environment is created for the development of periodontopathogens.The increase in plaque volume is associated with high sucrose intake, and studies show that high sucrose intake is associated with an increased risk of gingivitis (Gondivkar et al., 2019).Another mechanism for the effect of excessive sugar consumption on periodontal diseases is associated with chronic inflammation.Sugary foods and beverages contribute to high glycemic load, which leads to inflammation, insulin resistance, and impaired beta-cell function.It has been suggested that these inflammatory changes resulting from the consumption of sugary foods and beverages may lead to an increase in the prevalence of periodontal diseases (Song et al., 2016).
Studies indicate that oxidative stress is an important part of the pathogenesis of periodontal diseases (Muniz et al., 2015).The progression of periodontal diseases seems to depend on the individual's immune response and oxidative sensitivity.Cytokines, which are responsible for the initiation and maintenance of the inflammatory and immune response, transmit all kinds of local and systemic inflammatory responses in the host (Nibali et al., 2012).They play an important role in many chronic inflammatory and systemic diseases, including periodontal diseases, rheumatoid arthritis, and diabetes (Okada & Murakami, 1998).Adipose tissue-derived cytokines and hormones are thought to have a key role in the formation of periodontal diseases (Saito & Shimazaki, 2007).Among these secreted cytokines, especially tumor necrosis factor-alpha (TNFα), interleukin (IL)-1 (β and α), and IL-6 are important for the development of periodontal disease (Okada & Murakami, 1998).Proinflammatory cytokines are known to play a role in the pathogenesis of periodontal disease; IL-1, IL17,TNFα,and prostaglandin E2,interferon (IFN)α, IFNβ, and transforming growth factorβ (Dinarello, 2000;Takashiba et al., 2003).Based on the relationship between inflammatory markers reported in the literature, the dietary inflammatory index (DII) was developed to measure the potential inflammatory effect of a person's diet, and a high DII score indicated a pro-inflammatory diet.It is well documented that this index correlates with serum C-reactive protein (CRP) level (Shivappa et al., 2014).In one study, it was shown that there is a relationship between dental hygiene, preventive dental care, dental health, and systemic inflammatory markers (Frisbee et al., 2010).Most of the studies have focused on a protective role of single nutrients to periodontal health or the deleterious effect of cariogenic dietary patterns.However, the pro-or anti-inflammatory effects of the whole diet on the enhance of caries and periodontal disease remain elusive.Therefore, this study was planned to evaluate the relationship between the dental health and the inflammatory index of the diet.

| Participants
Exclusion criteria included using drugs (antidepressants, metformin, etc.), having conditions affecting appetite, chronic or systemic diseases, psychiatric diseases, and/or receiving eating behavior therapy, pregnancy, or lactation.Non-Interventional Clinical Researches Ethics Board approved the protocol.Detailed information about the study was given to the participants who met the criteria of the study and agreed to participate in the study.

| Oral and dental examination
The determination of oral and dental health was carried out by a dentist.Oral health status was evaluated by measuring the Decayed, Missing, and Filled Teeth (DMFT).Periodontal health status was determined using the plaque index (PI) and gingival index (GI).

| Decayed, Missing, and Filled Teeth
DMFT index was determined by using the number of DMFT of the individuals.The DMFT index shows the number of caries per person in a permanent set of teeth.

| Plaque index
It evaluates the bacterial plaque and plaque thickness in contact with the marginal gingiva.This index is particularly suitable for examining the effect of bacterial plaque on gingivitis.Measurements are made by rubbing and pulling the periodontal probe on the tooth surface in the gingival pocket.The Silness and Löe PI was used to evaluate the amount of plaque on the teeth.Plaque evaluation on the surface (mesial, distal, labial, lingual) in four regions for each tooth was made by periodontal probe and visual inspection, and each surface was given a value between 0 and 3.
The personal PI score is calculated by dividing the total score by the number of tooth surfaces examined; the population PI can be calculated by dividing the total PI by the total number of people.
Calculated PI value was classified as absence of plaque, small, moderate, or dense amount of plaque accumulation.

| Gingival index
The Silness and Löe GI was used to assess the severity of gingival inflammation.As a result of clinical evaluation of gingival appearance and probing of the gingival sulcus on four gingival surfaces of all teeth (mesial, distal, labial, lingual), bleeding status was evaluated and a value between 0 and 3 will be given for each surface.
Evaluations were made with the force applied with the WHO periodontal probe not exceeding 20 g and by moving it in the gingival groove.According to this evaluation index, the health of the mucosa around the teeth is scored.The classification of the GI was recognized as the absence of inflammation, mild, moderate, or severe inflammation.

| The DII
Twenty-four-hour dietary records were taken for 1 day.These records were analyzed with the BEBIS program to determine the daily energy and 25 nutrients intake of the participant, including protein, carbohydrate, fiber, total fat, saturated fat, polyunsaturated fatty acids, monounsaturated fatty acids, omega-3 fatty acids, omega-6 fatty acids, cholesterol, vitamin A, β-Carotene, vitamin D, vitamin E, vitamin C, thiamin, riboflavin, niacin, vitamin B12, vitamin B6, folic acid, Fe, Mg, Se, and Zn.To calculate the inflammatory load gained from daily diet, DII score was used (Shivappa et al., 2014).

| RE SULTS
The study group consisted of 138 participants in total (47 female [36.2%] and 83 male [63.8%]).Mean age was 32.8 ± 7.9 years.DII values based on the percentiles for each of the 25 food parameters are shown in Table 1.The scores range from 0.73 to −2.60.
Oral and dental examination of the participants is given in Table 2. 65.8% of the participants had absence or small amount plaque accumulation, while 39.2% had moderate or dense amount of plaque accumulation according to the PI classification.According to the GI, majority of the participants had absence or mild inflammation (86.8%), whereas moderate or severe inflammation was found in 13.2% (Table 2).
DMFT scores were found with median 4.0, and no statistically significant difference was observed between DII quartiles.Median of PI and GI scores were found to be 0.96 and 0.70, respectively, and were not statistically different between DII quartiles.While DII did not differ by PI classification, DII quartile between second and third found a difference according to the GI classification (Table 3).
No statistically significant correlation was found between DII mean score and DMFT, PI, GI mean scores.

| DISCUSS ION
A relationship between the inflammatory properties of the diet and periodontal diseases could occur.Although the number of previous studies is small, results supporting that inflammatory diet may be associated with oral diseases have been reported (Machado et al., 2021).One study found that an anti-inflammatory diet was associated with less missing teeth (Kotsakis et al., 2018), and another study reported that an anti-inflammatory diet could reduce gingivitis (Woelber et al., 2019).In our study, we aimed to investigate the relationship between the DII of the diet and DMFT, GI, PI, and the main findings of our study were (i) no significant difference between DMFT and DII quartiles, (ii) DII did not differ by PI qualification, and (iii) significant difference between DII quartiles of second and third according to GI classification.
Dietary behaviors are suggested to be a risk factor for periodontal dise ases (Hujoel & Lingström, 2017).In a cross-sectional study, an inverse relation between dietary fiber intake and periodontal disease among US adults ≥30 years old has been reported (Nielsen et al., 2016).In addition, improvement of periodontal disease markers by treatment with high-fiber, low-fat diet for 8 weeks has been shown (Kondo et al., 2014).Furthermore, higher intakes of vitamins B 6 , B 12 , C, and E, and folate, iron, potassium, and magnesium were significantly associated with a lower risk of periodontal TA B L E 1 Quartiles of the dietary inflammatory index (DII).

DII n (%)
First quartile 34 (24.6)disease (Watson et al., 2022).But these studies focused on specific nutrients, and the relation between inflammatory properties of the whole diet and periodontal diseases still remains unclear.Two recent studies have investigated interactions between DII and periodontal diseases (Li et al., 2021;Machado et al., 2021).Machado reported (Woźniewicz et al., 2018).
The new definition of periodontal health has been proposed as the absence of clinically detectable inflammation (Chapple et al., 2018), and some studies investigated the relation between systemic burden and periodontitis (Li et al., 2021).Considering that an anti-inflammatory diet can improve systemic inflammation (Mukherjee et al., 2023), it can be said that dietary interventions are also important in the treatment of periodontal diseases.For instance, a diet rich in fiber, fruit, and vegetables and low in saturated fats and processed products lowers the production of proinflammatory cytokines that may stimulate the periodontal immune response (Giugliano et al., 2006).In addition, ameliorating effect of bilberry consumption on some markers of gingival inflammation has been reported by Widén et al. (2015).On the other hand, a stone age diet for 4 weeks has been shown to increase plaque levels, but to decrease bleeding on probing and probing depth (Baumgartner et al., 2009).
This study has some limitations.First of all, sample size is small.
Second, we used 24-h dietary recall to determine food consumption and to calculate DII, but this method may not reflect overall diet of the participants.Finally, this study has a cross-sectional design, and to evaluate the relation between anti-inflammatory diet and oral ad periodontal health, randomized controlled trials are needed.
In this study, we evaluated the relation between pro-inflammatory properties of diet and DMFT, GI, and PI.We used DII to determine pro-inflammatory properties of diet and found no significant relation between DII and DMFT, PI but found a significant relation between second and third quartiles of DII for GI.To sum up according to the results of our and other's studies investigating the relation between DII and periodontal health, it seems that pro-inflammatory properties of diet and periodontal health are related and so dietary strategies on the treatment of periodontal diseases should be considered.

O RCI D
Ziya Erokay Metin https://orcid.org/0000-0002-0685-8150 et al. (2021) demonstrated a relation between DII and periodontal probing depth, and Li et al. (2021) showed that consuming a proinflammatory diet is associated with periodontal disease.These studies used periodontal probing depth as periodontal disease marker.In our study, we used DMFT for evaluating oral health and GI and PI for evaluating periodontal health, and in the contrary, we found no relation between DII and DMFT, PI.But we have found a significant difference between DII quartiles of second and third according to GI classification.Benamghar et al. (1982) have based GI on signs of inflammation (and in a recent study, improvement of gingival and plaque indices has been shown by consumption of cranberry functional beverage.But in the same study, no effect of cranberry functional beverage on systemic inflammation has been Oral and dental examination. TA B L E 3 Oral and dental examination by quartiles of the dietary inflammatory index (DII).Values arise from ANOVA for continuous variables or chi-square tests for categorical variables.Bold indicates statistically significant values (p < .05).Means having the different letters (a, b) in the same rows are significantly different.Abbreviations: DMFT, Decayed, Missing, and Filled Teeth; GI, gingival index; PI, plaque index.