Influence of a Low-Carbohydrate and Rich in Omega-3 Fatty Acids, Ascorbic Acid, Antioxidants, and Fiber Diet on Clinical Outcomes in Patients with Chronic Gingivitis

Abstract

INTRODUCTION Periodontitis is a chronic inflammatory disease in response to biofilm, causing dysregulated host inflammatory/immune response.[1] Various risk factors modify the host response, which can cause disease development and its further progression. These factors can be environmental (stress, bacterial load, and socioeconomic status [SES]), lifestyle (smoking, nutrition, and physical activity), and genetic. These risk factors can act alone or in consortium to modify the host response to microbial insult, resulting in reduced resolution of inflammation. Nutrition is an important aspect in any chronic disease regulation. Studies have shown micronutritional approaches, whereby systemically healthy volunteers are placed on a primitive diet to support the role of nutrition in periodontal inflammation.[23] Chronic, nonresolving inflammation is destructive in nature and the impact of nutrition on such chronic diseases such as periodontitis can be attributed to oxidative stress. In health, a balance exists between oxidants and antioxidants; however, as inflammation sets in, excess production of oxidants and /or depletion of antioxidants leads to oxidative stress, which causes local tissue damage as seen in periodontitis. This imbalance causes direct tissue damage by altering molecules, such as proteins, lipids, and DNA, production of proinflammatory molecules or indirectly via alteration in periodontal microbiota. The increase in oxidative stress can be regulated by complex systems of antioxidants and their supplementations can reduce the tissue damage. European workshop (2011) has suggested dietary recommendations for increasing the levels of diet-containing fruits, fibers, fish oils, vegetables and for reducing the levels of refined sugars as an adjunct to periodontal preventive/treatment.[4] A diet low in carbohydrates is beneficial, as suggested by a Swiss study on 10 adults placed in a stone age environment for four weeks. In this study, diet (low simple sugar, high antioxidant micronutrients, fish oils, and fibers) showed a significant decrease in gingival bleeding and probing depths.[3] Kim et al.[5] showed in vitro promotion of apoptosis and inhibition of periodontal ligament cells proliferation due to high levels of glucose. Studies on dietary supplementation with omega-3 fatty acids as an adjunctive to periodontal therapy showed a reduction in clinical parameters.[67] This indicates the essential role of omega-3 fatty acids in the resolution of inflammation. The benefits of the intake of vitamin C in periodontitis have shown a positive impact both clinically and in in vitro studies.[8] Nishada et al.[9] suggested that dietary intake of vitamin C has a weak but statistically significant relation to periodontal disease. Vitamin C acts as an antioxidant and helps in reducing oxidative stress in inflammatory condition.[10] However, very few randomized controlled trials have been conducted to evaluate dietary effects on gingival health. The primary objective of this study was to determine the impact of a diet low in carbohydrate, rich in omega-3 fatty acids, ascorbic acid, antioxidants, and fibers on PI, GI, PD, CAL, and BOP. The secondary objective was to determine the dietary compliance of the patient with diet modification. MATERIALS AND METHODS ETHICAL APPROVAL This was a double-blind randomized intervention study approved by the institutional ethical committee (ref. No. HIDSAR/ethics/2019/138). This prospective study was conducted in the department of Periodontology at Haldia Institute of Dental Sciences and Research from March 2019 to February 2020. Written informed consent was taken from the patients. Inclusion criteria were: subjects aged >18 and <60 years, patients with gingivitis (GI >0.5 and ≤3), and consuming a diet based primarily on carbohydrates as described by Frienman et al.[11] Exclusion criteria were subjects with systemic diseases, pregnancy or lactating mother, history of smoking, intake of any antibiotics, anti-inflammatory drugs, vitamin supplementation within the past six months before the start of the study period, any condition requiring special diet intake (e.g., diabetes), intake of any medications such as oral contraceptive pills, and anticoagulants that might have a role in gingival inflammation. STUDY PARTICIPANTS Patients diagnosed with gingivitis visiting the Department of Periodontology were recruited in the study after written consent. In both the test and control groups, those with gingival index scores >0.5 and ≤3 were enrolled in this study with no evidence of clinical attachment loss. Overall, 27 patients were enrolled in the control group, of whom 14 were women and 13 men. This group comprised those with a mean age of 35.2 ± 7.2 years (range 19 to 58 years). The test group enrolled 27 subjects, comprising 16 women and 11 men. This group comprised those with a mean age of 36.1 ± 8.3 years (range 21 to 59 years) [Table 1].Table 1: Demographic data of both the groupsSAMPLE SIZE DETERMINATION The sample size was based on a pilot study, which evaluated the effect of an optimal diet on patients with gingivitis.[12] Taking this study into consideration, a pilot study with 10 subjects in each group was undertaken, with a power = 80% and alpha = 5%; 22 subjects in each group were selected, taking a 20% attrition rate; and a sample of 27 subjects in each group was selected. Randomization Patients were randomly allocated to control or test group by using stratified randomization based on age, and a study was carried out by a dentist not directly involved in the study (P.S.). The patients were unaware of the randomisation and group allocation. The data on diet collection were taken by a dentist who was not involved in clinical parameter measurement (S.S.). Web-based randomization was done for the allotment of subjects using Prism 4.0 software package (GraphPad, La Jolla, CA, USA). Blinding The dentist who collected the measurement of primary and secondary outcomes (S.N.) was blinded to the group identity of the patients allocated in the test or control group. No questions on diet were asked to the patients during the clinical examination. The clinical measurement was done at baseline followed by a one-week adaptation period and then parameters were checked on a weekly basis for the next four weeks. DIETARY INTERVENTIONS Dietary recommendations were based on studies involving gingival/periodontal inflammation for reproducibility of the results.[1213] Dietary recommendations in the test group included the following diet regimen: Patients were advised to reduce intake of carbohydrates. A low-carb diet <130g/day intake was suggested. Subjects were instructed to have very minimal intake of fructose, flour-containing food (maida), rice, sweetened meals, beverages, and potatoes. No limitation was considered in terms of fruits and vegetables (polysaccharides). Intake of omega-3 fatty acids (seeds such as two spoons of Chia seeds, flaxseeds, sea fish) was advised to the patients. They were also suggested to reduce intake of trans-fatty acids (such as hot chips, cakes, fried meals) and omega-6 fatty acids (oils such as safflower oil, sunflower oil, sesame oil) daily. Intake of a source of ascorbic acid (citrus fruits such as orange, amla, lemon) daily. Intake of antioxidants (such as green tea, coffee, fruits) daily. Intake of fiber (fruits and vegetables) daily. The dietary recommendations were instructed in local language (Bengali) to the patients verbally, and a leaflet with written instructions on diet was handed over. The patients were advised to maintain dietary activities in a diary and were instructed to bring it in at every subsequent appointment. After the first visit, patients were instructed to visit the hospital after one week for sharing their dietary experiences and any problems related to the diet. CLINICAL MEASUREMENTS All the clinical parameters were measured by a dentist masked to the intervention (S.N.). The clinical parameters assessed were GI (by Loe and Silness),[14] PI (by Silness and Loe),[15] BOP, and PD. All the measurements were taken by using a UNC 15 probe (Hufriedy). After initial recruitment, subjects were advised to maintain the same oral hygiene behavior throughout the study duration; a soft bristle toothbrush and toothpaste were distributed to all subjects, and they were instructed to not indulge in the use of interdental aids. Baseline measurements were taken in the first week and this week was considered as transition time for the patients to adapt the new dietary behavior in the test group. The patients were instructed to visit hospital on a weekly basis and GI, PI, and diet dairies were examined at each appointment. Patients in the control group were examined by similar protocol, except no dietary instructions were given to them. At the end of the four weeks, all the clinical parameters were again evaluated. All the patients were asked questions related to SES, as per the modified Kuppaswamy scale.[16] Primary clinical outcomes were bleeding on probing and probing depth. The secondary clinical outcomes were GI, clinical attachment loss, and PI. STATISTICAL ANALYSIS Statistical analyses were performed with statistical software (SPSS for Windows, Version 16.0, SPSS Inc., Chicago, IL). The descriptive analysis included mean and standard deviation. A mixed linear regression analysis was performed to test differences between both groups. RESULTS In total, 54 patients diagnosed as having gingivitis were enrolled in this study. Each group consisted of 27 patients who were randomly assigned in control or test group. A flow chart of the study procedure is presented in Figure 1. The baseline demographic details are presented in Table 1. Clinical parameters PI, GI, PD, CAL, BOP, and degree of compliance in relation to dietary recommendations are presented in Tables 2 and 3, respectively. In this study, the primary clinical outcome was BOP, which was significantly reduced from the baseline 53.88 ± 1.75 to 23.55 ± 1.79 after four weeks of follow-up (P < 0.05); the secondary outcome GI was significantly reduced from baseline 1.34 ± 0.03 to 0.80 ± 0.11 at four weeks (P < 0.05) in the test group as compared with the control group (P < 0.05) [Table 2]. Furthermore, plaque scores, PD, and CAL showed no significant changes compared with the control group (P > 0.05). All the subjects were diagnosed as having gingivitis, and any periodontitis case was excluded and referred for necessary periodontal therapy. After the completion of the study period, all the patients received oral prophylaxis.Figure 1: Study participants’ flowchartTable 2: Clinical parameters of test and control groupsTable 3: Dietary recommendations complianceInfluence of the degree of compliance on the clinical parameters was performed for PI, GI, and BOP [Table 4] by using regression analysis. A score of 0 was given for no compliance and 1 when consumption was 100%. Regression analysis showed a significant negative association (P < 0.05) of PI with omega-3 fatty acids, antioxidants, and reduced carbohydrates and a positive association with fibers and vitamin C intake. GI was significantly positively associated (P < 0.05) with fibers and omega-3 fatty acid consumption. BOP was significantly negatively associated (P < 0.05) with antioxidants and positively associated with omega-3 fatty acids and fibers. Modified Kuppaswamy scale was used to determine the SES and in both the groups subjects with upper middle (II) class were enrolled for uniformity in the study.Table 4: Regression analysis regarding clinical parameters and degree of complianceDISCUSSION In the current study, we hypothesized that changes in dietary recommendations can lead to an improvement in periodontal clinical parameters. However, the study does not neglect the importance of nonsurgical periodontal therapy (NSPT), but it focuses on the possible adjunct role of dietary modification in periodontal health. The rationale for such hypothesis is based on literature substantiating the possible link between nutrition, inflammation, and periodontitis; the role of nutrients in reducing oxidative stress and their homeostatic role in balancing reactive oxygen species and the antioxidant defense system.[17] The current study was a part of an ongoing study evaluating the effects of diet modification as an adjunct to NSPT on periodontal health. The role of diet in oral health has been explored since ancient times. In their study, Hunter et al. and Adler et al. explored the role of ancestors’ oral health in relation to diet and found an association between oral health and dietary intake.[1819] The results of the current study showed that a diet low in carbohydrate and high in antioxidants, ascorbic acid, antioxidants, and fibers can significantly reduce gingival inflammation, which might be of clinical significance. This result is similar to a study by Woelber et al., where they found a positive association of plaque scores in a changed dietary pattern.[12] Several studies have shown an association of high glycemic carbohydrate intake and caries.[2021] A recent study on athletes’ dietary pattern and its effect on oral microbiome suggested that the consumption of a ketogenic low-carbohydrate high-fat diet leads to a reduction in the quantity of Haemophilus, Neisseria, and Prevotella and an increase in the number of Streptococcus species.[22] Moreover, a consensus report on the interaction of lifestyle, systemic disease with caries and periodontal disease identified processed carbohydrate as a shared risk factor for dental caries and periodontitis.[23] A study on the influence of the amount of ingested sugars on the microbial profile in dental plaque and saliva suggested the possibility of marginal influence on a high-carbohydrate diet on microorganisms, causing tissue destruction. Also, some caries-causing bacteria were less prevalent in subjects with low sugar consumption.[24] Another study by Edlund et al. on the metabolome analysis of the oral microbiome in in vitro sugar metabolism suggested the possible role of sugar metabolism in the oral microbiome.[25] All these studies suggest the possible role of nutrients intake and microbial association in various systemic diseases and oral health. In the current study, patients were advised to take a low-carbohydrate diet to reduce the microbial load, thereby reducing periodontal inflammation. Woundenberg et al. used the adapted dietary inflammatory index to associate with carbohydrate intake and they concluded that a high total caloric intake leads to systemic proinflammatory effects.[26] Lula et al. suggested that high glycemic food consumption can increase gingival and periodontal inflammation (NHANES III data).[27] However, in the current study, regression analysis showed no significant association between GI, PI, BOP index, and low-carbohydrate intake. In their study on high-fiber, low-fat-diet consumption for eight weeks, Kondo et al. showed improved periodontal disease markers and metabolic profiles.[28] Keeping this in view, in the current study the patients were encouraged to increase fiber content in their diet and we got similar results as in bleeding on probing and GI was significantly associated with high fiber diet intake. Fatty acids such as omega-6 fatty acids have proinflammatory potential and can promote periodontal inflammation.[29] In contrast, omega-3 fatty acids lower the systemic inflammation; several studies have suggested that the supplementation of omega-3 fatty acids can reduce periodontal inflammation and cytokines level.[3031] The current study also showed a significant positive association between GI in relation to omega-3 fatty acids intake. Antioxidants exhibit strong defense action by acting on the free radicals, neutralizing the primary radicals, forming chelates with transition metals, and maintaining homeostasis. Application of antioxidants as an adjunct to periodontal therapy has favorable results in improving the clinical parameters, lowering levels of local and systemic ROS.[32] Antioxidants are present in various micro- and macronutrients. A cross-sectional study conducted in the Japanese elderly population on the frequency of fruit and vegetable intake and its effect on oral of showed a strong positive association between the frequency of diet consumption and of oral In an study, et al. advised patients to have an intake of a high amount of fruits and vitamin and they that nonsurgical with dietary modification was in in terms of A on the role of antioxidant in periodontal therapy concluded that the of antioxidants and its outcome on oxidative stress does not a pattern and significant changes on various factors such as the quantity of antioxidants, their of study and measurement This also that the of the effect of nutrition on periodontal outcomes on various and of its effect by a study the of A study assessed antioxidant status in chronic periodontitis by a dietary intervention at increasing the consumption of fruits, and and found that dietary can increase healthy dietary intake and periodontal status at six months of In the current study, no significant association was seen between clinical parameters and literature support that vitamin C supplementation periodontal inflammation; vitamin C taken as dietary or in acts as a potential antioxidant and oxidative Vitamin C has a effect with and subjects were encouraged in the current study to also take antioxidants in the of green tea, coffee, fruits, and ascorbic et al. suggested that consumption of improved plaque and GI in patients with gingivitis, and the compliance was was based on and an of was collected at follow-up results were in the current we found high compliance dietary changes in patients with gingivitis, and a significant positive association in PI was seen in relation to ascorbic et al. showed a reduction in levels of and factor after of in patients with Also, bleeding on probing was reduced and similar results were in the current disease is a complex chronic microbial host tissue response, and various risk factors a role in disease and et study on intervention in patients with periodontal disease suggested that nutrition influence oral This leads to a risk factor that that can lead to dental periodontal systemic diseases such as and disease. supplementation of and as an adjunct to NSPT in the of chronic periodontitis with 2 a significant decrease in the oxidative stress markers and clinical parameters such as PI and This study further into the use of in chronic periodontitis with systemic modification can be also done by a of dietary which can in the of the amount of In the current study, no such was given to the patients and the patients were encouraged to take of antioxidants, vitamin fibers, and omega-3 fatty acids as it is The objective of this study was also to their dietary compliance this of consumption. All these studies the potential role of diet in altering host bacterial response, thereby reducing and inflammation. The to reduce plaque reduction by various and also on the possible of a of or micronutrients, to periodontal inflammation due to of proinflammatory nutrients and the possibility of intervention with periodontal therapy as a The in the of periodontal health a diet that is in and The dietary recommendations in the current study were in with the food based on the Table and this was to all the the dietary instructions were given and was done on a weekly has food to such associated with food in the where fish and is a subjects with similar dietary and socioeconomic status were taken into Also, due to the results be to an A study might a on dietary compliance and the effect of diet on clinical parameters. Modified Kuppaswamy scale was used to determine the SES, and scores were subjects with an SES score between 16 and were taken in the study. were not considered in the study as randomization lead to the of in the test or control group, which might result in the sample AND The of the study was the of the role of diet in clinical outcomes in gingival inflammation. few studies in literature have examined a dietary of low carbohydrate, rich in omega-3 fatty acids, ascorbic acid, antioxidants, and fibers in In the current study, we also evaluated the dietary compliance which can further in diet modification that is to periodontal therapy. The of the study are diary and no diet for Also, the of the consumption frequency of was based on the The food not all the and the was to a diet rich in omega-3 fatty acids, ascorbic acid, antioxidants, and however, a quantity was not assigned for These can cause was to who were to a low-carbohydrate this might be attributed to the local food in the study In rice, and fish was the food of all the recruited and are a rich source of carbohydrate and reducing the quantity of diet consumption of carbohydrate was The of the study was four A study be results are to be and also a diet intake might an which is in reducing gingival inflammation. Another limitation was during the initial pilot study with sample size = after the first week of clinical parameters measurement and dietary two weeks were assigned for diet and then the patients were followed for four weeks. However, the period to follow-up and the adaptation period was reduced to a one-week The for as per was that subjects less to the study, as they not visit the hospital in these two weeks and found in time A pilot study was conducted for sample size of the study and to determine the in the study. The potential in this study was based on the literature and studies on nutrition and periodontal disease. The in the current study were such as age, physical or oral systemic health, and SES, health history of and were the The study was conducted after the of participants’ such as age, SES, oral and health. Moreover, such as the amount of vegetables and fruits intake were to as a low-carbohydrate diet was the and dietary were the of diet-containing ascorbic acid, antioxidants, omega-3 fatty acids, and fibers. This was the potential limitation of this randomized and the possibility of factors that are or The current study showed that a dietary pattern with low carbohydrate, rich in omega-3 fatty acids, vitamin antioxidants, and fibers can significantly reduce gingival inflammation. Furthermore, having groups as supplementation are necessary for of impact on periodontal AND are no of ETHICAL AND

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