Meta-Analysis of Assessment of Total Oxidative Stress and Total Antioxidant Capacity in Patients with Periodontitis

Mohideen, Khadijah; Chandrasekaran, Krithika; Veeraraghavan, Harsha; Faizee, Shahul Hameed; Dhungel, Safal; Ghosh, Snehashish

doi:https://doi.org/10.1155/2023/9949047

Disease Markers

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Abstract Introduction Materials and Methods Results Discussion Conclusions Abbreviations Data Availability Additional Points Conflicts of Interest Authors’ Contributions References Copyright Related Articles

Review Article | Open Access

Volume 2023 | Article ID 9949047 | https://doi.org/10.1155/2023/9949047

Meta-Analysis of Assessment of Total Oxidative Stress and Total Antioxidant Capacity in Patients with Periodontitis

Khadijah Mohideen,¹Krithika Chandrasekaran,²Harsha Veeraraghavan,³Shahul Hameed Faizee,⁴Safal Dhungel,⁵and Snehashish Ghosh⁶

Academic Editor: Gaetano Isola

Received13 Aug 2023

Revised29 Sept 2023

Accepted05 Oct 2023

Published30 Oct 2023

Abstract

Background. Periodontitis is intricately linked to oxidative stress-antioxidant (redox) imbalance. The antioxidant system scavenges the oxygen free radicals in biological fluids in patients with periodontitis. However, little is still known about the free radicals mediated oxidative stress and reductive ability of the antioxidant system. Thus, the present meta-analysis aims to quantitatively review the literature that assessed the oxidative stress marker total oxidative stress (TOS) and total antioxidant capacity (TAC) in various biological fluids of patients with periodontitis. Methodology. Electronic databases were searched for studies that assessed TOS and TAC levels in various biological samples of patients with periodontitis. Results. From the 1,812 articles identified, 1,754 were excluded based on title and abstract screening due to irrelevance to the topic of interest. A full-text assessment of the remaining 58 articles led to the selection of 42 articles that satisfied the inclusion criteria. Of these, only 24 studies had consistent data for quantitative analysis. The periodontitis group displayed significantly elevated TOS levels () in serum, gingival crevicular fluid (GCF), and saliva samples in the studies evaluated. In contrast, the periodontitis group exhibited significantly attenuated TAC levels () compared to healthy controls in plasma, serum, and GCF samples of the studies evaluated, which was insignificant in salivary samples (). At the same time, the periodontitis group displayed insignificantly elevated TAC levels after periodontal therapy (). Conclusions. The present meta-analysis showed significantly higher TOS and lower TAC in periodontitis, reflecting the elevated oxidative stress level than the control group. Clinical Relevance. Scientific rationale for the study: The imbalance between oxidants and antioxidants (oxidative stress (OS)) plays a critical role in the onset and progression of periodontitis; the assessment of the relationship between OS-related biomarkers in regional samples and systemic samples of patients with periodontitis helps us to evaluate the periodontal disease progression. The OS biomarker levels can be used to assess periodontal disease and therapeutic efficacy.

1. Introduction

Reactive oxygen species or free radicals are anions with one unpaired electron in the outer shell. The complex effect of enzymatic and nonenzymatic antioxidants scavenge or neutralize the free radical activity [1]. Indeed, when the antioxidant reserve system is exhausted by the excessive accumulation of free radicals, there is no scavenging of reactive oxygen species (ROS) nor their neutralization. The resultant disruption of the antioxidant barrier is directly responsible for oxidative stress (OS)/nitrosative stress-mediated modifications of biological components [2]. OS plays a primary role in the etiopathogenesis of many systemic diseases, such as diabetes and cardiovascular diseases, as well as a possible risk factor for chronic renal failure, rheumatoid arthritis, and neurodegenerative diseases [3]. Chronic inflammatory disease, like periodontitis, is also intricately associated with oxidative-reductive imbalance. Many studies have shown that OS is directly responsible for the progressive degradation of extracellular matrix components of the periodontal attachment apparatus [4]. Recent literature indicates that redox disturbances are intensified in periodontitis patients with comorbidities. Therefore, the present meta-analysis aims to assess the literature that evaluated the total oxidative and antioxidative capacity of various biological fluids in patients with periodontitis.

2. Materials and Methods

2.1. Registration of the Protocol

PRISMA guidelines have been strictly followed for study selection. The meta-analysis protocol was recorded in the PROSPERO database (CRD42021281819).

2.2. Question of Observation

Is there any significant difference in the total oxidative stress (TOS) and total antioxidant capacity (TAC) levels of biological fluid samples between patients with periodontitis and the healthy control group?

Based on the research question, the following components were formulated:(i)Patient population: patients with periodontitis(ii)Exposure or marker of evaluation: mean and standard deviation value of TOS and TAC values(iii)Comparison: between patients with periodontitis and healthy control group(iv)Outcome: assessment of TOS and TAC in various biological fluid samples of patients with Periodontitis(v)Study: collect the literature of cross-sectional and case-controlled studies that evaluated the status of TOS and TAC in Periodontitis and control from 2000 to 2023.

2.3. Literature Search

Electronic databases, including PubMed, ScienceDirect, Cochrane, Wiley Online Library, and Cross Reference, were searched for published articles addressing the TOS and TAC in patients with periodontitis and the control group between 2000 and 2023. The keywords were employed: “periodontal disease,” “total oxidative stress,” “oxidative stress,” and “total antioxidant capacity.”

2.4. Screening for Selection

Articles discussing oxidative stress and TAC in periodontitis were collected and screened for relevance based on the titles and abstracts.

2.5. Inclusion Criteria

Studies discussed the TOS and TAC in patients with periodontitis and the healthy control group;(i)Both the case and control groups consisted of individuals who were in good systemic health, refraining from the use of antibiotics, anti-inflammatories, or any other medications. Moreover, they had not undergone any periodontal treatments within the past 3 months.(ii)The inclusion of studies examining systemic diseases in relation to periodontitis was contingent on the presence of two distinct evaluation groups: one for systemically healthy controls and another for the periodontitis-afflicted group.(iii)Studies investigating the correlation between periodontitis and smoking were considered only if they incorporated nonsmokers in both the periodontitis group and the control group as separate evaluation groups.(iv)Studies examining the impact of therapy on periodontitis were included only when they provided baseline values for both the periodontitis group and the control group.

Studies involving various biological fluid samples and expressed the assessed TOS and TAC values in mean, standard deviation, along with probability value:(i)Papers provided consistent data to allow comparison of patient and control groups with other relevant studies.

2.6. Exclusion Criteria

Articles with the unmatched title and objectives:(i)Studies that were duplicates, when they involved the same subjects and by the same authors.(ii)Observational studies exclusively focusing on pregnant women or children.(iii)The studies examined the therapeutic effect but did not include an evaluation of the control group.(iv)Studies included patients with systemic diseases or smokers but did not incorporate separate evaluation groups for systemically healthy individuals or nonsmokers in the periodontitis and control groups.(v)Being literature, critical, or systematic reviews.(vi)Studies used other markers of oxidative stress and antioxidant capacity for evaluation.(vii)The articles provided incompatible data for the comparison between control and periodontitis groups with other studies.(viii)The studies expressed the results in Graphical representation without the accurate value display.(ix)Studies discussed the TOS and TAC values in other oral chronic inflammatory diseases.

2.7. Full-Text Retrieval and Evaluation

Two authors screened the titles and objectives of the collected studies and excluded the presentations at higher risk of bias from the quantitative synthesis based on predefined criteria. Two authors have independently evaluated the full text of each included study. Two authors have collected data for the factors considered in the meta-analysis. After considering all the particulars, the authors have selected the articles for eligibility criteria. The authors resolved disagreements by consensus. Finally, all the authors participated in manuscript preparation.

2.8. Data Segregation

The extracted information from the full text of selected articles as the author, year of publication, sample size, TOS and TAC measurements in Periodontitis, and control group expressed as the mean with standard deviation along with specific measurement units and assessment methods.

2.9. Statistical Analysis

The meta-analysis was performed by deriving the forest plot using the standard mean difference method using comprehensive meta-analysis software version 3 (Biostat Inc. Englewood, NJ, USA). The standardized mean difference values of TOS and TAC in periodontitis were evaluated at a 95% confidence interval (CI). Due to significant heterogeneity, a random-effects model was chosen for the analysis. The studies that expressed the TOS and TAC levels in similar units in each sample were only selected for the meta-analysis.

3. Results

PubMed search yielded 783 papers, ScienceDirect search yielded 369 papers, Wiley Online Library yielded 265 papers, Cochrane search yielded 390 papers, and Cross-reference search yielded five papers. After search refinement, 1,754 articles were excluded due to unmatched titles and abstracts, including four duplicated data reports and one animal study. After the extraction of these articles, 58 articles had titles relevant to the present work. The full text was retrieved for the screened articles. Papers not meeting the selection criteria (n = 16) were excluded. Finally, 42 articles with matched objectives were selected for the systematic review. Only 24 articles had data compatible with the meta-analysis (Figure 1).

Newcastle–Ottawa scale of included studies in the meta-analysis was displayed in Table 1 [5–46]. Collected TOS and TAC assessment data, criteria for periodontitis diagnosis, and other relevant findings from included articles in various biological fluid samples were tabulated in Tables 2 and 3, respectively [47–52]. The different methodologies utilized for assessing TOS and TAC values were also displayed in Tables 2 and 3 [53–61]. The pre and posttreatment mean values of TAC in different biological fluid samples in patients with periodontitis data from the included studies are presented in Table 4. The analysis of TOS levels after therapeutic intervention could not be performed due to the scarcity of published studies.

Selection—Case definition, case selection, control definition, and selection.

Comparability—Consideration of matching known and potential confounding factors.

Exposure—Securing patient records, interviewer blindness to groups, similarity ascertainment between groups, and nonresponse rate.

Each criterion was awarded with one star. The overall score was determined by summing the awarded stars. Studies receiving scores in the range of 6–9 were categorized as high-quality, those scoring between 3 and 5 were classified as fair-quality, and studies with scores ranging from 0 to 2 were deemed to be of poor quality. Importantly, it’s worth noting that all the studies analyzed received scores exceeding 6, indicating a minimal risk of bias.

The periodontitis group displayed significantly elevated TOS levels () in serum, gingival crevicular fluid (GCF), and saliva samples in the studies evaluated. In contrast, the periodontitis group exhibited significantly attenuated TAC levels () compared to healthy controls in serum, plasma, and GCF samples of the studies evaluated, which was insignificant in salivary samples (). At the same time, the periodontitis group displayed insignificantly elevated TAC levels after periodontal therapy ().

The GCF samples showed an overall standard mean difference TOS value of 1.011 µmol H₂O₂ equivalent (Eq)/l with 95% CI (0.262–1.760) (Figure 2). The salivary samples displayed an overall standard mean difference TOS value of 1.784 µmol H₂O₂ Eq/l with 95% CI (1.003–2.565) (Figure 3). The serum samples depicted an overall standard mean difference TOS value of 0.694 µmol H₂O₂ Eq/l with 95% CI (0.092–1.297) (Figure 4).

The GCF samples showed an overall mean difference TAC value of −2.004 mmol Trolox equivalent (TEq)/l with 95% CI (−3.490 to −0.517) (Figure 5). The salivary samples displayed an overall standard mean difference TAC value of −0.709 mmol TEq/l with 95% CI (−2.481 to 1.063) (Figure 6). The serum samples showed an overall standard mean difference TAC value of −2.049 mmol TEq/l with 95% CI (−3.018 to −1.079) (Figure 7). The plasma samples showed an overall standard mean difference TAC value of −0.959 µmol TEq/l with 95% CI (−1.504 to −0.415) (Figure 8). The overall standard mean difference TAC value pre and posttherapy is 0.666 µmol TEq/l with 95% CI (−0.196 to 1.528) (Figure 9).

The meta-analysis of the TOS assessment presented high heterogeneity, reflected by the I² values 87.256, 85.382, and 83.513 in Figure 2–4, respectively. The meta-analysis of the TAC assessment presented high heterogeneity, reflected by the I² values 95.494, 98.970, 94.749, 82.757, and 88.617 in Figure 5, Figure 6, Figure 7, Figure 8, and Figure 9, respectively. The different methodologies utilized to measure TOS and TAC values could cause high heterogeneity.

3.1. Publication Bias

Studies included in this assessment of TOS in periodontitis meta-analysis showed Egger’s regression intercept values 9.162, −6.856, 3.689 with two-tailed p-values 0.45, 0.45, and 0.701 in saliva, GCF, and serum samples, respectively, indicating a low risk of publication bias of included studies in meta-analysis. Studies included in this assessment of TAC in periodontitis meta-analysis showed Egger’s regression intercept values −12.79, 1.895, −23.06 with two-tailed p-values 0.48, 0.67, and 0.07 in GCF, plasma, and saliva samples, respectively, denoting a lower risk of publication bias of included studies in meta-analysis. Studies included in this assessment of serum TAC in periodontitis meta-analysis showed Kendall’s S statistic (P–Q) value of −20.0 with two-tailed p-values of 0.051 (Begg and Mazumdar’s test for rank correlation), denoting a moderate risk of publication bias of included studies in the salivary assessment of TAC meta-analysis. The studies included the posttherapy TAC assessment in periodontitis meta-analysis showed Eggers regression intercept value of −2.67 with a two-tailed p-value of 0.73, indicating a low risk of publication bias of included studies in meta-analysis.

4. Discussion

Despite the increasing knowledge of the etiopathogenesis of inflammatory periodontal diseases, there are no definitive indicators for objectivizing the diagnosis, determining the disease’s severity, and evaluating treatment results. Hence, the present meta-analysis assessed the literature evaluated the oxidative stress markers such as TOS and TAC levels in the blood, GCF, and both stimulated and nonstimulated saliva in patients with periodontitis to find the validity of these markers in determining the diagnosis and prognosis of periodontitis as well as the treatment effects. In the present meta-analysis, Out of 10 studies of TOS assessment in serum, GCF, and saliva involving 260 patients in the study group and 212 in the control group, seven studies proved a significantly higher TOS in patients with periodontitis [9, 16, 19, 26–28, 42]. They also reported a strong correlation of TOS with the clinical parameters of periodontitis [12, 16]. This fact is unsurprising since the stimulated saliva secreted by the parotid gland is the primary source of free radicals (ROS) [62, 63]. However, Zhang et al. [64] showed no difference in the salivary TOS levels between periodontitis and healthy controls. Further, they found that a high bacterial load did not depict any correlation with salivary TOS values [64]. Toczewska et al. [65] found a weak correlation of TOS values with clinical periodontal parameters. These differences might be due to the selection criteria of patients in different studies. Since other factors related to subjects such as age, smoking, gender, and nutrition would yield distinct effects on the alteration of OS parameters; thus, it is essential to consider these factors when considering this parameter as a potential marker of periodontitis. Therefore, patient selection could be a crucial parameter influencing salivary levels of TOS.

The present meta-analysis of the evaluated studies displayed significantly elevated TOS levels () in GCF, saliva, and serum samples of the periodontitis group with the overall standardized mean difference value of 1.011, 1.784, and 0.694 µmol H₂O₂ Eq/l, respectively.

Out of 39 studies of TAC assessment in plasma, serum, GCF, and saliva, involving 1,418 patients in the study group and 1,340 in the control group, except 11 studies, the remaining 31 studies proved a significant decrease in the TAC in patients with periodontitis when compared to the clinically healthy periodontium [5, 6, 8, 14, 21–24, 27, 38, 39]. Chapple et al. [8] reported that GCF/salivary TAC values were significantly higher in patients with periodontitis than in the control group. The authors attributed that the initial increase in antioxidant response in periodontitis is due to local reactive or adaptive response to a first phase increase of oxidative burst (OS) occurring with periodontal inflammation. The adaptive antioxidant defense might decrease over time as ROS production becomes chronic. The excess utilization of antioxidants to neutralize the exaggerated ROS activity during periodontal inflammation results in the depletion of TAC levels in participants with periodontitis. The facts mentioned above might account for the different results reported in the various studies evaluating TAC levels in patients with periodontitis. Wei et al. [16] and Baltacıoğlu et al. [26] found significant correlations between salivary/serum TOS levels and clinical parameters of periodontitis (plaque index, gingival index, probing depth, and clinical attachment level). Baser et al. [33] and Zhang et al. [64] studies depicted plasma and salivary TAC values correlated with clinical periodontal parameters. Zhang et al. [64] further found that a high bacterial load did not exhibit any correlation with salivary TAC levels. Their study carried out a multifactorial analysis, and they depicted that out of many factors, the diagnosis of periodontitis was significantly related to TAC salivary values only regardless of other variables such as age, gender, smoking habits, or presence of periodontal pathogens in saliva. They also found a significant inverse relationship between salivary TAC and the clinical attachment level of periodontitis [64]. Toczewska et al. [65] research found a significant reduction of GCF total antioxidant activity in periodontal pockets compared to other gingival regions, and the extent of this reduction did not correlate with the different stages of periodontitis and weakly correlated with clinical periodontal parameters. Becerik et al. [66] stated that a significant decrease in the GCF antioxidant capacity (ferric reducing antioxidant power) in patients with periodontitis also displayed an inverse correlation with the clinical parameters of periodontitis, such as the clinical attachment level and pocket depth. Some previous studies demonstrated that reduced salivary TAC values correlated with increased inflammatory burden in periodontitis [11, 67, 68]. The three included studies of the present meta-analysis showed that periodontal therapy significantly improved salivary and serum TAC values in patients with periodontitis. It is also suggested that shifting the salivary/GCF redox balance in favor of the oxidative reactions (↓TAC, ↑TOS) predisposes to oxidative damage to proteins, lipids, and DNA in the periodontal tissue, which leads to progressive degradation of the periodontal attachment apparatus [4, 69]. Su et al. [13] and Panjamurthy et al. [70] reported higher serum, GCF, and salivary TAC values in periodontitis participants. However, some studies also showed that salivary TAC increases or remains at the same level in periodontitis patients compared to healthy controls [6, 32, 71]. Another study reported that neither gingivitis nor smoking habits influence salivary TAC values [72]. The variations in the results of TAC between different studies could be due to different analytical methods utilized in assessing TAC values.

The present meta-analysis of the evaluated studies exhibited significantly attenuated TAC levels () in the periodontitis group compared to healthy controls in GCF, serum, and plasma samples, which was insignificant in salivary samples (). The overall mean difference of TAC value in GCF, salivary, serum, and plasma samples were −2.004, −0.709, −2.049, and −0.959 µmol TEq/l.

At the same time, the periodontitis group displayed insignificantly () elevated TAC levels after periodontal therapy. The overall standard mean difference TAC value upon comparison of pre and posttherapy was 0.666 µmol TEq/l.

Although high heterogeneity was detected among included studies of the present meta-analysis, our results still indicate that periodontitis has statistically correlated with some local OS biomarkers, and oxidative stress played a critical role in the pathological process of periodontitis. Thus, TOS and TAC may be helpful and practical biomarkers for evaluating oxidative injury in periodontal tissues.

5. Conclusions

In conclusion, the present meta-analysis supports the rationale that there is a direct link between periodontitis and OS-related biomarkers in the local site. The imbalance of ROS and antioxidant systems may contribute to functional and structural remodeling that favors the occurrence of periodontitis. Furthermore, these two measurements can potentially evaluate the interaction between periodontal and systemic status and the effectiveness of periodontal treatment. Considering the above facts, it may be speculated that oxidative stress is an essential factor in periodontitis. Studying the antioxidant defense mechanisms may be regarded as a valuable biomarker that will help better understand the underlying pathology of tissue damage and novel therapeutic interventional strategies. Therefore, it is necessary to conduct further research on a larger number of patients with periodontitis to understand the oxidative stress and antioxidant status imbalance reported in patients with periodontitis.

Abbreviations

TOS:	Total oxidative stress
TAC:	Total anti-oxidant capacity
OS:	Oxidative stress
NS:	Nitrative stress
CI:	Confidence interval
GCF:	Gingival crevicular fluid
ROS:	Reactive oxygen species
PI:	Plaque index
GI:	Gingival index
PPD:	Periodontal probing depth
PD:	Probing depth
BOP:	Bleeding on probing
CAL:	Clinical attachment level
LB:	Loss of bone
FRAP:	Ferric reducing antioxidant power
ABTS:	2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonate)
Eq:	Equivalent
TEq:	Trolox equivalent
CC:	Case–control
CS:	Cross-sectional
PS:	Prospective study
LS:	Longitudinal study
RCT:	Randomized controlled trial.

Data Availability

Data analyzed in this study were a reanalysis of existing data, which are openly available at locations cited in the reference section.

Additional Points

Limitations. The chronic exposure of the oral cavity to many environmental factors destabilizes the local redox homeostasis. It reduces the diagnostic usefulness of redox biomarkers in periodontal diseases. Furthermore, due to a lack of redox salivary/GCF biomarkers reference values for assessment, it is difficult to compare the values obtained from different studies. In addition, the resultant differences might be due to the different patient selection criteria in reported studies. The attributed factors such as age, gender, smoking, and nutrition status would yield distinct effects on the alteration of OS parameters; thus, it is essential to consider these factors when considering OS as a potential marker of periodontitis.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

All the authors have equally contributed and been included in the present study.

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