An oral health optimized diet can reduce gingival and periodontal inflammation in humans - a randomized controlled pilot study

Periodontal disease is a global burden affecting about 743 million people worldwide and is considered to be a primary cause of tooth loss at advanced age [1, 2]. Gingivitis is a prerequisite for the development of periodontal disease, and also correlates to long-term tooth loss [3]. A landmark study in 1965 by Löe and coworkers demonstrated the influence of dental plaque as an etiological factor for gingival inflammation by showing increased gingival inflammation when participants discontinued oral hygiene procedures [4]. However, Brecx et al. [5] showed that individuals reacted differently regarding their inflammatory response to plaque accumulation, with some individuals showing only a mild expression of gingival inflammation. A study by Baumgartner et al. [6] looking at participants during a stone-age experiment showed pronounced reductions of gingival and periodontal inflammation, even though oral hygiene was not performed at all. The authors concluded that the experimental gingivitis protocol is not applicable if the diet does not include refined carbohydrates. Thus, diet seems to have a profound impact on the gingival and periodontal inflammatory reaction. Examining the literature, several dietary recommendations for benefiting the health of periodontal tissues can be found, such as a reduction in carbohydrates, and an additional intake of Omega-3 fatty acids, vitamin C, vitamin D, antioxidants and fiber [7‐13].

Most importantly, the excessive intake of carbohydrates seems to promote dysbiosis and chronic inflammatory diseases [8, 14]. The clinical reduction of carbohydrate intake seems to reduce gingival inflammation [7]. In-vitro studies showed that high levels of glucose promote apoptosis and inhibit proliferation of periodontal ligament cells [15, 16].

Secondly, an imbalance between Omega-6 and Omega-3 fatty acids seems to foster inflammation. Reports indicate that the Omega-6 to Omega-3 ratio changed from 1:1 in a hunter-gatherer diet to 15:1 in a Western diet, accompanied by higher blood levels of several cytokines [10]. Interestingly, there is growing evidence that Omega-3 fatty acids lead to resolution of inflammatory processes [9]. The resolution of inflammation was also shown for periodontal tissues in vitro [17], while positive therapeutic effects were seen in two clinical studies in the field of periodontal therapy [18, 19].

Furthermore, the intake of vitamins C and D seem to play an important role in gingival and periodontal inflammation. Several studies showed the positive impact of vitamin D on periodontal tissues both in clinical and in-vitro studies [11, 20, 21]. Vitamin C has been described as an important vitamin for periodontal health, both in clinical and in-vitro studies for some time. The absence of vitamin C causes scurvy, which is accompanied by massive periodontal bone loss [22‐25].

Last but not least, the role of dietary antioxidants seems to be important for several processes regarding an adequate systemic reaction to oxidative stress. Both clinical and in-vitro studies showed positive effects on periodontal tissues [11, 12, 26‐28].

Despite these very promising findings, there is a substantial lack of dietary-interventional studies in controlled randomized settings [11]. Thus, the aim of this pilot study was to evaluate an oral health optimized diet low in carbohydrates, and rich in Omega 3-fatty acids, vitamins C and D, antioxidants and rich in fiber in a controlled, randomized study.

In total, 16 patients with gingivitis were recruited. In the experimental group, one participant dropped out of the study due to a lack of time for study participation.

The experimental group consisted of 10 participants with 6 women and 4 men. The mean age in this group was 34.4 ± 14.1 years, ranging from 23 to 70 years. The mean BMI was 24.53 ± 2.53 kg/m².

The control group consisted of 5 participants with 3 women and 2 men. The mean age in this group was 34.0 ± 16.5 years, ranging from 24 to 63 years. The mean BMI was 21.98 ± 3.24 kg/m².

Clinical data regarding PI, GI, PD, CAL, BOP and PISA are presented in Table 1. A flow chart of the procedures is presented in Fig. 1. In the experimental group, one patient suffered from mild periodontitis and one patient from moderate periodontitis [34]. In the control group, two patients suffered from mild periodontitis.

Regression analysis adjusted for age, gender and BMI revealed no significant differences between the groups regarding PI (p = 0.084), but significant differences regarding GI (p < 0.001), BOP (p = 0.012), and PISA (p < 0.001).

Table 2 presents the degree of compliance regarding dietary recommendations.

A regression analysis regarding the influence of the degree of compliance on the clinical parameters was performed for PI, GI, BOP, and PISA (Table 3). According to the regression analysis PI was significantly negatively associated with Omega-3 fatty acids and positively associated with fiber intake. GI was significantly negatively associated with Omega-3 fatty acid consumption and carbohydrate reduction. BOP und PISA were both significantly negatively associated with a reduction in carbohydrates.

Intraclass Correlation was 0.91, showing a high level of reproducibility. The computed power of the study was 100 %.

The results of this pilot study showed that an oral health optimized diet can significantly reduce gingival and periodontal inflammation in a clinically important range without any changes in oral hygiene performance. The results of this study are in accordance with those of Baumgartner et al. [6], questioning the positive association of plaque and gingival inflammation in a changed dietary environment. Although the overall effects of this diet were impressive, it is hard to determine in retrospect which dietary element had the most impact on clinical parameters, even though the regression analysis showed significant associations of clinical factors primarily to carbohydrate-reduction and Omega-3 fatty acid intake. The control group showed a trend of increasing plaque values although this was not significant. This result was expectedly due to the absence of interdental hygiene during the study in individuals who prior to this performed interdental hygiene. But also irrespectively to the control group, the experimental group experienced a significant decrease in inflammatory parameters with regard to the baseline values, which is comparable with the Baumgartner et al. study.

In total, the results support the assumptions that a modern, Western lifestyle, including lots of refined carbohydrates and a high Omega-6 to Omega-3 fatty acid ratio promotes inflammatory processes [8]. As long as no specific dietary component can be made out for this decrease in periodontal inflammation, results have to probably be considered to be a mixture of inhibition and increased resolution of the inflammatory processes.

Regarding the intake of high-glycemic carbohydrates which promotes higher blood glucose levels and insulinemia, the results of this study seem to be in line with the known relationship of periodontal disease and diabetes [35] and the recently investigated periodontitis-associated genes ANRIL, VAMP3, and GLT6D1 which in some way seem to be related to glucose metabolism or glycosylation [36‐38]. The association of carbohydrate consumption and gingivitis has been investigated in some earlier studies, also with impressive effects [7]. Looking into the literature there are several possible explanations for the inflammation triggering effect of carbohydrates. First of all, high glycemic index carbohydrates seem to directly promote inflammatory processes via NFkB-activation and oxidative stress [39, 40], and have been linked to higher C-reactive protein levels [41]. Secondly, high glycemic index carbohydrates may promote weight gain [42], with its associated inflammatory effects, based on an increase in adipokine secretion [43]. Looking at mean carbohydrate consumption in Germany, with more than 230 g per day or over 45 % of the total calorie intake [44], there may be associations with chronic inflammatory diseases in susceptible patients. Furthermore, the results are in line with Sidi & Ashley [45] who found a significant higher bleeding on probing in individuals on a high sugar diet compared to individuals on a low sugar diet, with no intergroup differences regarding the amount of plaque.

Regarding the effect of a decrease in the Omega-6 to Omega-3 fatty acid ratio, our results support the theory of resoleomics as stated by Serhan et al. [9], and the related periodontal studies [18, 19, 46]. Summarized, Serhan and colleagues discovered that the resolution of the inflammatory response is an active process based on metabolites of Omega-3 fatty acids, so called “specialized pro-resolving mediators” (SPM), rather than a passive event based on the elimination of the pro-inflammatory cytokines.

Looking at the intake of vitamins C and D and antioxidants, the results also support studies which have shown positive outcomes in this field. For a deeper discussion a reference should be made to Van der Velden et al. [11], where theoretical and clinical studies are described in detail.

The results raise several questions regarding the importance of dental plaque for the development of gingivitis/periodontitis and its impact on therapy. If dental examination reveals signs of an inflammation of the gingiva or the periodontium, representing a strongly host-mediated condition, a primary check of host-factors such as nutrition should be considered. The periodontist has the special opportunity – in contrast to that of other medical professions - to fairly easily get an impression about systemic inflammation, which could be a real contribution from periodontology in the prevention of other diseases related to chronic inflammation. This idea has been stated from by other authors as well [7, 47].

The primary limitations of this study can be seen in its small sample size, which is not a representative population, as well as with the rather uncontrolled intake of dietary components. However, to the best of the authors’ knowledge the study results are the currently only evidence beyond the Baumgartner et al. study in a randomized, controlled, interventional setting. Regarding the rather broad dietary recommendations, in the authors’ opinion it is very important to deliver a dietary protocol which is applicable to patients in daily practice. In other words, advising patients to implement this dietary pattern will show effects irrespective of whether they focus more on high glycemic index carbohydrate reduction, Omega-3 fatty acids, vitamin D, vitamin C, and/or antioxidants. Future studies should also include serum measurements of cytokines, cholesterol, HbA1c, vitamin D, etc. and also examine the oral microbiome. According to the exclusion criteria the study results are limited to patients with a mainly carbohydrate based diet. With regard to European epidemiological data, it can be assumed that this factor also applies to most individuals in the European population [48]. Furthermore, the assessment of dietary patterns using food diaries is not absolutely accurate. Thus, the presented data based on the food diaries can be seen as an indicator of compliance but not as a precise reflection of dietary patterns including quantitative values.

Within the limitations, the presented dietary pattern including a diet low in carbohydrates, but rich in Omega-3 fatty acids, vitamins C and D, antioxidants and fiber significantly reduced periodontal inflammation in humans.

GI, gingival index; PI, plaque index; PD, pocket probing depths; BOP, bleeding on probing; PISA, periodontal inflamed surface area; BMI, body mass index; ICC, intraclass correlation coefficient.