Yoga - A Salubrious Routine to Prevent Periodontal Diseases:A Meta-analysis

Introduction

Yoga, a historical practice that was originated in the ancient times of India is one among the six astikas (hindu philosophical schools, Sankhya, Yoga, Nyaya, Vaisheshika, Mimamsa and Vedanta). The name Yoga, originated from a word in Sanskrit “yuj” which means “to unite”, to unite the body, brain and soul. Yoga is proved as most effective and valuable practice for man to treat many psychological and physical problems. According to many researches, yoga’s role in stress reduction is proved and it enhances perceptive skills.² Some psychological factors like anxiety, stress have effects directly on pathogenesis of illness and diseases. Moreover, stress is responsible for inflammatory destruction, and makes an individual much prone to several diseases, including periodontitis. Yoga leads to decreased levels of stress which helps an individual in reduction of anxiety and depression, and also aids in reduction of pain, inflammation and improves immune system.¹

The reason for deprived life quality, lower mental health, reduced work efficiency, greater suffering, and increased physician visits and personality disorders is stress. Stress has become a problem of community health concern and the practice of yoga promises to be an approach to combat it.³ A significant increase of T helper cells (CD8+), natural killer cells (NK) is noticed when an individual is under acute stress and returns to their normal values after a while.⁴ There was also an increase in plasma immunoglobulin levels (IgM, IgG) in the condition of stress. Several neuropeptides (substance P, somatostatin) gets released and affects the actions of immune system and the cytokines gets released.⁵

Many studies were conducted which clearly state that stress affects the periodontium. Periodontitis is a chronic inflammatory disease characterized by episodes of active destruction to pronounced inflammatory infiltration, attachment loss and alveolar bone loss.⁷ Some studies also state that stress affects the behavior of the individual thus affecting the health like neglecting oral hygiene, decreased intake of food, increased smoking and drinking alcohol which in turn affects the collagen synthesis, thus leading to periodontal diseases. Neglecting the maintenance of oral hygiene leads to accumulation of plaque on the teeth, oral mucous membranes, and other tissues present in the mouth, which mainly contains microorganisms that increases the periodontitis risk.⁸

An article stated that stress caused by any reason decreases the immune system action by activation of hypothalamus-pituitary-adrenal axis (HPA axis) by which ACTH (adreno cortico tropic hormone) gets released from anterior pituitary gland, which increases the cortisol secretion from adrenal cortex. Cortisol reduces the secretion of immunoglobulin A (Ig A) and immunoglobulin G (Ig G) and decreases the functioning of neutrophils, thus increasing the susceptibility to periodontal destruction.^6,9 Stress also directly stimulates the autonomous nervous system further stimulating the adrenal medulla secreting the epinephrine and nor epinephrine, which further leads to altered immune response and increased blood glucose, increasing the periodontal diseases risk as shown in Figure 1.

Periodontitis is an oral disease which is commonly found and can be seen in a severe form. Around 15-20 % of global population in the age group of 35-44 years are suffering from this disease, and it increases up to 70.1% in the population aged 65 years and above. It occurs in individuals who are exposed to high levels of stress, poor oral hygiene and suffering from systemic conditions like hypertension, diabetes mellitus.¹¹ The bacterial plaque, microbial by- products and host immune response are the factors that cause periodontitis.¹¹ The main characteristics of the disease includes loss of clinical attachment, periodontal pockets formation and apical migration of epithelial attachment called as gingival recession.¹¹ The periodontal destruction is mainly because of inflammatory destruction that is caused by pro inflammatory cytokines aggravated by the response of stress. Decreased inflammatory markers can be noticed in the individuals who are physically dynamic than the people practicing a sedentary life style. Pro inflammatory cytokines (Ex: IL-6, TNF-α) are responsible for the progression of periodontal disease. Physical exercise is linked to lower levels of IL-6 and proinflammatory cytokines when done regularly.¹³ As a result, yoga has a reversible impact on depression and stress-related periodontitis, and can also act as an adjunct after the periodontal therapy to recess the inflammation and pro inflammatory cytokines.13 Yoga increases the anti-inflammatory cytokines production like IL 6, suppressing the inflammatory action. IL – 6 acts as both pro inflammatory and anti-inflammatory cytokine.¹²

Yoga acts on body in several ways to decrease the stress, energizes immune system to act against pathogens and also stimulates vagus nerve to set body into resting state during stressful conditions. Yoga practice suppresses the HPA axis, leading to decreased production of cortisol, ultimately decreasing the stress. Decrease in stress leads to balanced inflammatory response by release of necessary cytokines. As the periodontitis is an inflammatory condition, it proves that yoga is helpful in maintaining a healthy periodontium. Other than the stress, it stimulates parasympathetic nerves conserving the energy by slowing heart rate, releases hormones that relax the body and brain. Autonomic nerves play a very important role in stress mechanism. Sympathetic nerves work while an individual is in stress and the recovery from stress is done by parasympathetic nervous sytem. Effects of yoga on body and periodontium are breifly summarized in Figure 2. It is proven that stress is reduced by practicing yoga, thus risk of diseases including periodontal diseases is reduced.¹⁰

Methodology

Protocol

Cochrane standards of systematic review was followed for designing the protocol of the analysis and the search criteria along with PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analysis Protocols) guideline.

Inclusion Criteria

Study type: Type of studies included were comparative descriptive studies, and case control studies, as they can answer the research question by comparison of periodontal condition between individuals that who do and who don’t practice yoga. This type of studies can clearly state influence of practicing yoga on periodontal disease, which helps reviewers for stating the conclusion from the selected studies.

Participants inclusion/exclusion criteria: Studies with participants who were systemically healthy and without stress were included. There were mainly two groups under inclusion criteria a) Systemically healthy participants who did yoga practice regularly b) Systemically healthy participants who didn’t practice yoga. The oral condition of the participant was not taken into consideration, during the selection of studies. All the studies had used any of these following clinical parameters for detecting the periodontal condition i.e plaque index, gingival index, debris index, calculus index, oral hygiene index, probing pocket depth, clinical attachment loss.

Method of search

A search was done for articles that were published on various databases Medline/Pubmed, Google scholar, LILACS, Cochrane, open grey and USC Upstate library. Terms used for searching the articles were yoga, chronic periodontitis, serum cortisol and stress.

Eligibility and data extraction

We have assessed all the search results that were displayed by using keywords and have excluded many articles by title, duplicate studies, reviews, abstract, study types, methods and selection of subjects in that particular study. We included only original research studies which clearly explained influence of yoga on periodontitis with specified results. The studies qualifying the criteria of inclusion were analyzed and then extraction of data was done. The data was extracted from the studies such as area of study, study participants size, criteria of inclusion of the study, clinical parameters measured in the participants, any treatment given if so, the follow up and final values and results of study and conclusion.

Risk of bias

The quality of studies included was tested by using the Cochrane risk of bias.

Statistical analysis

This meta-analysis was done to find out whether there was any influence on periodontal tissue health by practicing yoga or not. Both the groups, those who regularly practiced yoga and those who did not practice yoga were considered and certain clinical parameters like gingival index, plaque index, probing pocket depth and calculus index were recorded in various studies. Due to expected heterogenecity between the studies, model used was the Random Effects Model. Meta-analysis done for each clinical parameter measured in various included studies was presented by using Forest plots with means, standard deviation, sample sizes, mean differences.

Results

Records that were identified by searching databases were 591 and 32 were identified from other sources and 289 duplicate results were excluded. While assessing the titles of the articles, another 286 articles not qualifying the selection criteria were excluded. Total abstracts of 48 records were screened and 34 were excluded after reading the abstract. There were 14 full text articles that were suitable for consideration. Among them, nine records were excluded based on type of study and methods of selection and also the clinical parameters measured. After thorough assessment, five studies of similar type conducted in various areas of India were considered and were included for qualitative and quantitative synthesis. Figure 3 illustrates the model of complete search following the PRISMA guidelines and criteria of inclusion.

Characteristics of studies

The study selection was done by considering numerous factors such as method used for selection of study participants, study group, clinical parameters measured. There were five studies in total that were selected on the basis of criteria of inclusion and characteristics of each study is included in Table 1. All the studies included were comparative descriptive studies with one group of people practicing yoga regularly and another not practicing yoga. Certain studies included some additional groups which were not taken into consideration. Clinical parameters considered were gingival index, plaque index, oral hygiene index-simplified (OHI-S), clinical attachment loss, probing pocket depth. Although various other parameters were included in the studies, only the common parameters among any two studies were considered. Results of all the included studies showed significant lower values in the group that regularly practiced yoga.

Risk of bias assessment

Risk of bias was assessed for the selected studies using Cochrane risk of bias tool and the mean risk was high. Random sequence generation (Selection bias) was high with Kuldeep et al., 2017,¹⁴ Ananthalakshmi et al., 2020,²⁷ Katuri et al., 2020²⁸ and had a low rate of risk with Rajhans N et al., 2018²⁶, Archika et al., 2017.²⁵ Allocation concealment bias (Selection bias) assessment was done and was found to be high in all the selected studies. Reporting bias (selective reporting) was assessed and was found low for all the studies included. Participants blinding and personnel also called as performance bias was high for all the studies. So, the mean risk for three studies was high and remaining two studies were at medium. Overall mean risk for the studies was considered as high. The studies available on periodontitis and yoga were very limited. So, selection of the following studies for meta-analysis was necessary. Risks of bias assessment of the selected studies are mentioned in Table 2.

The Forest plots were made to address the heterogeneity of the involved studies. Random effect model was used for the quantitative analysis and was calculated at confidence intervals of 95%.

Forest plot was made for four studies25-28 which took plaque index as a clinical parameter for determining the periodontal condition between the control group and the group practicing yoga. It stated that plaque index was significantly reduced in the group practicing yoga with Z = 2.29 at p = 0.02* (significant). Forest plot prepared including the plaque index of the studies selected is mentioned as Figure 4.

Forest plot was made for three studies considering gingival index as the clinical parameter14,26,27 for determining the periodontal condition of the groups practicing yoga and control group. It stated that there was no difference in the gingival index score between both the groups with Z = 1.80 at p = 0.07 (Not significant). Here, based on gingival index, it cannot be clearly stated that yoga has any influence on periodontium. Forest plot was prepared for gingival index of the selected studies and manifested as Figure 5.

Forest plot was made including studies that considered clinical attachment level (CAL) as a clinical parameter for the determination of periodontal condition. It stated that there was difference noted in CAL scores between yoga and control group with Z=2.89 at p = 0.004 (significant). Forest plot was prepared including CAL of selected studies and is mentioned as Figure 6.

Forest plot was made considering pocket depth which was considered as clinical parameter in four studies^25-28 for the determination of periodontal condition. It stated that PPD was significantly reduced in the yoga group with Z = 2.53 at p = 0.01* (significant). According the acquired PPD values, it was clear that yoga had influence on periodontium. Forest plot of PPD of the studies selected is mentioned as Figure 7.

Discussion

In present conditions, according to some studies, around 20-50% of global population has periodontal diseases.²⁴ The diseases of periodontium are caused because of various etiological factors. The most ignored and uncontrollable etiology is stress, further leading to periodontal diseases and even worsens the pre-existing periodontitis. Because almost every individual has stress in their life and it is very common condition which cannot be prevented, yoga practice can resolve this condition. Yoga affects the body in such a way that is much beneficial for the physiologic functioning and even the psychological functioning, ultimately improving the life quality of an individual.^16-23 Yoga can abort both the modifiable and non- modifiable risk factors of periodontal disease, maintaining the periodontal health.¹⁵

Yoga originated in ancient India and is being practiced in many regions of the world. In this systematic review and meta-analysis, the studies were obtained from databases and only selected studies were included. All the studies were conducted in India but from various regions such as Haridwar,¹⁴ Ahmednagar,²⁵ Chennai,²⁷ Guntur²⁸ and the area was not specified in one study.²⁶ In every study, results were in the favour of the group regularly practicing yoga. It can be clearly noted that there was no influence of area over the obtained results, as the obtained results from all the studies were similar.

Although we found some other similar studies on yoga, stress and periodontium, we considered the clinical parameters measured, place where the study was done, transparency of study mentioned and the study method into consideration to minimize the bias, and to get accurate results. As there were very few studies on the effect of yoga on periodontium, we had selected the best among them with common methodology for the metaanalysis.

Meta-analysis was performed on the measured parameters and significant changes were noticed in plaque index between the people practicing yoga and people who doesn’t practice, as per the studies performed by Ananthalakshmi et al., 2020,²⁷ Katuri et al., 2020,²⁸ Rajhans N et al., 2018,²⁶ Archika et al., 2017.²⁵ The value of p was significant (p = 0.03) with a mean difference of -0.42. Significant reduction of the plaque scores was noticed in all the selected studies, which proves the decreased plaque content and the increased oral hygiene. In same manner, gingival index was analyzed in the studies conducted by Ananthalakshmi et al., 2020,²⁷ Rajhans N et al., 2018,²⁶ Kuldeep Singh et al., 2017.¹⁴ No significant difference was noticed in the values (p=0.07), with mean difference of -0.31. Reduction in scores of gingival index noticed in all selected studies showed the healthy gingival condition. CAL and PPD were calculated of participants in the studies conducted by Ananthalakshmi et al., 2020,²⁷ Katuri et al., 2020,²⁸ Rajhans N et al., 2018,²⁶ Archika et al., 2017.²⁵ Significant changes were noticed in CAL between both the groups (p = 0.004) and also the PPD values (p = 0.01), with a mean difference of the CAL as -1.03 and the PPD as -0.69. From these values, it was stated that yoga is effective in maintaining periodontal health.

There are some limitations of the selected studies. Ananthalakshmi et al.,²⁷ did not consider women for their study and the reason for that was not stated. It may be assumed that hormonal changes occur very frequently in women which is an etiological factor for periodontal tissues inflammation. Another limitation of their study was that the periodontal pathogens were not explored. Our meta-analysis too has a limitation as we ignored the age of the selected participants in their respective studies, which also acts as a factor for periodontal condition. Archika et al, 2017²⁵ conducted a study in which participant’s age was not considered for selection criteria, a random selection of participants was done (limitation of that particular study). No similarities in the participant’s age was noticed in any of the selected studies. Even Ananthalakshmi et al.,²⁷ considered the age 18-35 years as an inclusion criteria, whereas Kuldeep Singh et al, 2017¹⁴ included age of 25-55 years. Rajhans N et al, 2018²⁶ considered age of 35-44 years while Katuri et al, 2020²⁸ selected participants of age 35-60 years. Apart from that, the statistical analysis of all the selected studies were similar except the study by Katuri et al, 2020²⁸ as they analyzed mean of the sites having the PPD & CAL 5-8 mm and >8mm, rather than analyzing mean scores of PPD & CAL as the remaining studies. We had included these studies in spite of these limitations as the literature regarding this particular research question was so limited. There is a need for similar research studies to prove the effect of yoga on periodontitis.

Conclusion

Stress may lead to many disorders in the body because of hormonal imbalance, activating unnecessary cytokines and altered immune response and it is a major risk factor for periodontitis as periodontitis is an inflammatory disease that occurs due to inflammatory destruction of periodontium. There are many other factors other than stress like microbes, smoking etc. that causes or worsens periodontal conditions. By regular yoga practice, one can overcome periodontitis by affecting almost all the factors that causes periodontitis, thereby acquiring a healthy periodontium. Yoga has proven benefits over other systemic diseases apart from periodontitis. Numerous studies were conducted determining the effect of yoga on systemic diseases, but only few research studies were conducted specific to effect of yoga on periodontium. So we took a step to bring awareness among the people.

Conflicts of interest

None.