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Article

Membrane Fluidity and Oxidative Stress in Patients with Periodontitis

by
Erandis Dheni Torres-Sánchez
1,
Joel Salazar-Flores
1,
Juan Ramón Gómez-Sandoval
2 and
Sarah M. Lomeli-Martinez
1,2,3,4,*
1
Department of Medical and Life Sciences, Centro Universitario de la Ciénega, University of Guadalajara, Ocotlán 47810, Jalisco, Mexico
2
Periodontics Specialty Program, Department of Integrated Dentistry Clinics, Centro Universitario de Ciencias de la Salud, University of Guadalajara, Guadalajara 44340, Jalisco, Mexico
3
Institute of Research in Dentistry, Department of Integral Dental Clinics, Centro Universitario de Ciencias de la Salud, University of Guadalajara, Guadalajara 44340, Jalisco, Mexico
4
Department of Wellbeing and Sustainable Development, Centro Universitario del Norte, Universidad de Guadalajara, Colotlán 46200, Jalisco, Mexico
*
Author to whom correspondence should be addressed.
Appl. Sci. 2023, 13(7), 4546; https://doi.org/10.3390/app13074546
Submission received: 7 March 2023 / Revised: 1 April 2023 / Accepted: 2 April 2023 / Published: 3 April 2023
(This article belongs to the Section Applied Dentistry and Oral Sciences)
Versions Notes

Abstract

:
Periodontitis leads to the destruction of dental tissue through polymicrobial interactions, inflammation, and increased oxidative stress. The aim of this study was to measure the levels of nitrates (NO3−), malondialdehyde (MDA), and membranal fluidity (MF) in the gingival tissue of subjects with or without periodontitis. A total of 120 participants from the Dentistry School of the University of Guadalajara were investigated. The study was approved by the ethics committee of our institution, with the registration number of CI-01221. The clinical parameters measured were probing depth (PD), clinical attachment level (CAL), and bleeding on probing (BoP). NO3− was measured using the Greiss reaction, while MDA was determined colorimetrically with the FR12 Kit (Oxford Biomedical Research). Membrane fluidity (MF) was measured using the quotient Ie/Im according to the method of Ortiz and collaborators. The Student t-test, Spearman correlation, and chi-square are used to calculate the results. The results showed higher levels of PD, CAL, and BoP in patients. There was a positive correlation between MF and PD. Moreover, MDA was positively correlated with PD and CAL. Increases in PD resulted in higher levels of NO3−, MDA, and MF. Similarly, increases in CAL resulted in higher levels of MDA and MF in patients. We conclude that PD and CAL facilitated the progression of periodontitis through increases in MDA and MF.

1. Introduction

Periodontitis, an inflammatory disease that results in the destruction of tooth support structures, is initiated and propagated through the complex interaction between a heterogenous polymicrobial dysbiosis in a dental biofilm structure and the immune response of the host [1,2,3,4]. During periodontitis, cytokines and chemokines, which are released in response to the bacteria in the dental biofilm, play a fundamental role in the inflammatory process, and some of them recruit polymorphonuclear leukocytes [2,4,5]. Cells of the innate immune system such as neutrophils and macrophages increase the production of reactive oxygen species (ROS) during phagocytosis through “respiratory burst” [2,5]. The reactive oxygen species (ROS) include the levels of superoxide anion (O2−), hydroxyl (OH−), and hydrogen peroxide (H2O2), all of which generate an imbalance in the antioxidant response, thereby triggering a cytotoxic effect responsible for tissue damage [1,2,6]. The activation of inflammatory cytokines stimulates the production of nitric oxide (NO), and its interaction with O2− releases the peroxinitrite radical (ONOO−). This chemical reaction releases NO3−, nitrites (NO2−), and OH−. Previous studies have shown that high concentrations of NO and NO3− were associated with the development of severe periodontitis [7,8]. Recent data indicate that periodontal damage disrupts the oxidative/antioxidant equilibrium [9,10,11,12], affecting the increase in lipoperoxide levels [9,11]. Veljovic and collaborators (2022) report high levels of MDA in patients with gingival inflammation [10]; this increase is also reported in the clinical trial by Moussa (2022), which included patients with stage II periodontitis [12]. Peroxidation stimulates a greater activity of lipoxygenases (type 5), which are responsible for oxidizing membrane phospholipids. This leads to a rearrangement of the periodontal membrane. This phenomenon decreases the thickness of the membrane, and generates changes in membrane fluidity and permeability, leading to tissue damage which may result in apoptosis [9,13]. It has been suggested that excess ROS indirectly promote the degeneration of hard tissue through osteoclastogenesis, as well as the destruction of soft tissue, thereby favoring the progression of periodontitis [1,6]. Previous studies have reported changes in some parameters of oxidative stress in saliva [14,15,16], serum [14], and gingival crevicular fluid [17]. Several studies are looking at biomarkers of oxidative stress in order to find a periodontal diagnostic [7,18,19,20]. However, the published data in this area are not conclusive, due to a high degree of heterogeneity in the methodology and results, in addition to the absence of MF evaluations in the gingival tissue of patients with periodontitis [7,14,15,16,19,21,22]. The objective of this study was to determine the levels of NO3−, MDA, and MF in the gingival tissues of patients with periodontitis, in relation to the corresponding levels in healthy subjects. This is the first trial to evaluate membrane fluidity levels in periodontal patients.

2. Materials and Methods

Ethical approval and informed consent: This study was conducted in line with the Declaration of Helsinki, and it was approved by the Ethics Committee in Research at the University of Guadalajara (registration number, CI-01221). Each of the participants signed an informed consent letter in which anonymity and confidentiality of the information provided were guaranteed.
Study subjects: The research was designed as a cross-sectional and observational study on 120 patients from the Periodontal Specialty Clinic of the Faculty of Dentistry of the University of Guadalajara, who were recruited from February 2019 to February 2021. The sample size was calculated using the finite population ratio formula for subjects with and without periodontitis; an α value of 0.05 and β value of 0.10 are used, with a frequency of exposure of 0.67 cases [23] and a frequency of 0.35 for controls [24]. A value of 37 patients with periodontitis was found in the result; however, 60 participants per group were recruited, and each case was matched with a control. The inclusion criteria covered patients with clinical characteristics of periodontitis, and periodontally healthy controls. Patients with systemic diseases, pregnant women, smokers, alcohol users, addicted individuals, and those who used antibiotics and/or hormonal or non-hormonal anti-inflammatory drugs 3 months prior to tissue collection were excluded from the study.
Periodontal clinical parameters: Each of the participants underwent a clinical periodontal evaluation consisting of measurement of six sites per tooth with a 15 mm long and 0.5 mm diameter Hu Friedy periodontal probe (Universidad de Carolina del Norte, UNC-15 Hu Friedy). The clinical parameters considered for each patient were: probing depth (PD) [3,16], clinical attachment level (CAL) [3,16], and bleeding on probing (BoP) [3,16]. All patients with periodontitis were diagnosed in line with the clinical sections of the classification of periodontal diseases [3]. The diagnosis of periodontitis was made by a calibrated specialist of the Clinic of the Specialty of Periodontics of the University of Guadalajara. Periodontally healthy patients did not develop gingival inflammation.
Study groups: The group of patients with periodontitis comprised 60 participants who presented at least 40% of periodontal sites with BoP, with a PD ≥ 3 mm, CAL ≥ 2 mm, and interdental alveolar bone loss ≥ 2 mm. The group of participants without periodontitis was made up of 60 subjects with clinically healthy gum, sites with PD ≤ 2 mm or CAL ≤ 2 mm, with X-rays which did not show any signs of bone loss.
Gingival tissue collection: Samples were collected from patients with periodontitis during the surgical phase of periodontal treatment. For the group of participants without periodontitis, tissue was obtained during cosmetic surgery or crown-lengthening procedures. All tissues obtained were immersed in SHE medium [250 mM sucrose, 25 mM HEPES (pH 7.5), and 1 mM EGTA] until completely homogenized at a temperature of 5 °C. Subsequently, the homogenates were centrifuged (Sorvall ST4 Plus Centrifuge, Thermo Scientific, Waltham, MA, USA) at 3500 rpm for 10 min [25], and the supernatant was evaluated for levels of NO3−, MDA, and MF.
Quantification of NO3− were measured in the tissue homogenate according to the method of Tenorio (2005), with slight modifications. Zinc sulfate was added to the tissue homogenate at a concentration of 0.09 M, followed by centrifugation at 10,000 rpm at 4 °C for 10 min. Then, 100 µL vanadium chloride was added to the supernatant at a concentration of 0.05 M. The reaction was started by addition of the enzyme nitrate reductase which catalyzed the conversion of NO3− to NO2−; and the Griess reaction quantified the total of NO3− in a reaction with 2% sulfanilamide and 0.1% of N-(1-naphthyl) ethylenediamine dihydrochloride. The concentration of NO3− was quantified in a spectrophotometer (Benchmark Plus microplate ®, Bio-Rad; Hercules, CA, USA) at 540 nm [26].
Quantification of lipoperoxide was evaluated through determination of MDA levels in line with the method of Esterbauer and Cheeseman (1990) using the colorimetric technique of Oxford Biomedical Research Inc. (FR12, Oxford, MI, USA). The assay was performed by adding 200 µL of supernatant from tissue homogenate to 455 µL of N-methyl-2-phenylindole in acetonitrile. This was followed by addition of 105 µL of methanesulfonic acid. The mixture was incubated for 60 min, after which it was centrifuged at 12,000 rpm for 10 min. The absorbance of the supernatant was read at 586 nm, and the MDA levels were calculated from a standard calibration curve of 1,1,3,3-tetramethoxypropane in Tris-HCl [27].
Determination of MF was determined using the method of Ortiz et al. (2008), with slight modifications. In this procedure, the fluorescent molecule 1, 3 dipyrylpropane (DiPP) was added to the supernatant from tissue homogenate. The DiPP was diluted to a concentration of 10 mM in Tris-HCl buffer, pH 7.8. The basal fluorescence (Im) of the mixture of tissue and DiPP at 30 °C was read in a spectrofluorometer (Perkin Elmer, LS50B; Buckinghamshire, UK) at intensities of 379 nm and 480 nm (monomer and excimer, respectively). Thereafter, the mixture was incubated for 5 h at 30 °C in complete darkness, during which DiPP was incorporated into the tissue membrane. Then, the fluorescence value (Ie) was re-measured under the same intensity conditions. From the results obtained, the MF ratio was calculated for each of the samples as a quotient, i.e., Ie/Im [28].
Statistical analysis was performed with the SPSS (IBM Corp. Released 2017. IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY, USA). Descriptive data are expressed as mean ± standard deviation (SD). The differences in the means of PD, CAL, BoP, and oxidative stress (NO3−, MDA, and Ie/Im) in subjects with and without periodontitis were compared with Student’s t-test since the data showed a normal distribution using the Kolmogorov test (p > 0.05). On the other hand, the correlation of oxidative stress values with PD, CAL, and BoP was sought in subjects with periodontitis using Spearman’s correlation; these data did not comply with a normal distribution.
Subsequently, PD and CAL values were pooled (Group 1 had values <5 mm, and Group 2 had values >5 mm) to compare differences between BoP means and oxidative stress levels. This comparison was carried out using the Mann–Whitney’s U-test, since the pooled data had no normal distribution that was verified using the Shapiro–Wilk test (p < 0.05). Chi-square (χ2) test was used to determine the association between oxidative stress quantitative data and PD and CAL (groups 1 and 2). For all tests, statistical significance was assumed at p < 0.05.

3. Results

The frequency distribution of the gender of the participants with and without periodontitis revealed that females were higher in number in both groups, with values of 51.66% and 61.66%, respectively. The mean age of the patients with periodontitis was 44.31 ± 10.17 years, while the mean age of the healthy subjects was 34.85 ± 14.26 years. There was no significant difference in age between the two groups (p > 0.05; Table 1).
As shown in Table 1, there were statistically significant differences in the values of the clinical parameters (PD, CAL, and BoP) between patients with periodontitis and healthy participants (p < 0.05 *). Moreover, the levels of oxidative stress markers (NO3− and Ie/Im) were increased in subjects with periodontitis, when compared to subjects without periodontitis. However, despite the increase, there were no statistically significant changes in the levels of the above markers, or in the MDA levels (p > 0.05; Table 1).
Table 2 shows the correlation of the clinical parameters with the markers of oxidative stress in patients with periodontitis. The results showed a weak positive correlation between Ie/Im and PD (r = 0.268; p = 0.037 *). Moreover, the MDA level was weakly positively correlated with PD and CAL (r = 0.294; p = 0.022 *; r = 0.446; p < 0.00 *). There were no correlations between the other variables in Table 2.
The outcomes in patients with periodontitis were re-classified on the basis of PD and CAL: Group 1 had depth ≤5 mm, while Group 2 had depth >5 mm. Mann–Whitney’s U-test was used to compare the BoP and oxidative stress values for both groups, as shown in Table 3.
A comparison of Group 1 and 2 showed no significant difference in the BoP of patients with periodontitis (p > 0.05). However, when the PD rose, there were significant increases in the levels of NO3−, MDA, and Ie/Im (p < 0.05 *; Table 3). Similarly, the classification of CAL showed increases in the levels of MDA and Ie/Im when the two groups were compared (p < 0.05 *; Table 3).
Furthermore, the oxidative stress markers (NO3−, MDA, and Ie/Im) of the patients with periodontitis were categorized at low and high levels to determine their association with PD and CAL, via a chi-square test (Table 4). In a previous study, NO3− levels were categorized as low for values ≤ 4.18 nmol/mL, and as high for values > 4.19 umol/mL [29]. Moreover, MDA levels were rated low for values ≤ 2.3 umol/mL, and high for values > 2.4 umol/mL [30]. Regarding MF, Ie/Im ratios ≤ 0.44 were considered low, while Ie/Im ratios > 0.44 were considered high [30]. The classifications of the depth of PD and CAL in Group 1 and 2 were handled as indicated previously. In Table 4, a comparison of the two categories indicated no associations between the observed and expected frequencies.

4. Discussion

In recent years, many studies have highlighted the role of oxidative stress as an underlying factor in the pathogenesis of a wide range of chronic inflammatory diseases such as cancer [31], diabetes mellitus [32], rheumatoid arthritis, atherosclerosis [33], and periodontitis [34]. Periodontitis is highly prevalent in patients with type 2 diabetes, rheumatoid arthritis, and atherosclerosis. The literature is consistent with reports on the association of the above-mentioned diseases with more severe periodontitis and decreased antioxidant capacity both locally and systemically, resulting in a sustained redox imbalance that enhances disease progression [1,2,6,35]. Oxidative stress in periodontitis exerts an important antimicrobial effect and counteracts the growth of invasive pathogenic micro-organisms of the crevicular groove. However, excess ROS may be considered as a “double-edged sword” because, on the one hand, it promotes a cytotoxic environment for host cells, while on the other hand, it is crucial for gene regulation and cell signaling [35].

4.1. Nitrate Levels

In the oral cavity, the homeostasis of nitrogen metabolites (NO, NO3−, and NO2−) is mediated by a balance between the inflammatory processes and activity of nitrate reductase in oral anaerobic bacteria [7,8,36,37]. Several studies have demonstrated that, in patients with periodontal disease, there is an increased production of NO, an important mediator of inflammation [7,38,39]. Similarly, increases in the levels of NO3− and NO2− have been reported in the saliva and tissues of periodontitis patients [8]. This is consistent with the increased level of NO3− seen in this study. In particular, periodontitis patients with high values of PD had high concentrations of NO3−. In a previous study, it was suggested that the release of NO3− may be a defensive strategy used by the host to combat the inflammatory process [8]. In addition, the high generation of nitrosative stress has been associated with bone loss [21,39,40]. This may explain the increase in PD seen in Table 3. On the other hand, although Table 1 shows an increase in NO3− in the group of patients with periodontitis, no significant differences were shown when compared with the group of healthy subjects. This response may be due to the high reactivity of reductase enzymes in the bacteria of the oral cavity. The bacterial reductase enzymes convert NO3− to NO2− which is subsequently reduced to NO or ammonium ion, depending on the pathway [36,37]. Previous studies reported that bacteria such as Haemophilus, N. flavescens, Actinomyces, F. nucleatum, P. melaninogenica, V. parvula, and P. intermedia have reductase enzyme activities. Indeed, V. parvula, P. melaninogenica, and P. intermedia are associated with periodontal disease [36,41]. Similarly, a study found no significant differences in NO3− between patients with periodontitis and those in control group, due to the enhanced conversion of NO3− to NO2− during the inflammatory process, a characteristic feature of periodontal disease [39].

4.2. Lipoperoxide Levels

The oxidation of membrane lipids, mainly polyunsaturated fatty acids, releases lipid peroxides, mainly MDA. This oxidation process affects MF (Ie/Im), tissue integrity, and cellular functionality [1,2,9,10,13,42,43,44]. In this study, there were no significant differences in MDA between periodontitis patients and those with healthy gums. A similar result was reported earlier by Wei et al. (2010). These authors have suggested the use of more specific lipid peroxidation products such as 4-hydroxynonenal, acrolein, and isoprotane, instead of MDA, which, in addition to being a product of lipid peroxidation, is also released when ROS attack gangliosides and deoxyribose [45]. Our MDA results in the patients with periodontitis, relative to healthy subjects, are also similar to those obtained in some previous studies which have suggested that periodontitis itself does not increase lipid peroxidation (MDA) [46,47,48]. However, most studies have reported significant increases in MDA in patients with periodontitis, when compared to the healthy control group [10,14,19,49].
On the other hand, in the present study, in patients with periodontitis, there were increases in the concentration of MDA for those subjects who had a depth greater than 5 mm for PD and CAL (group 2), in contrast to those who had a depth less than 5 mm (group 1). These results are consistent with the positive correlation of MDA with PD and CAL (Table 3), although the association was classified as moderate-to-weak (r < 0.5). These data are in agreement with previous literature reports, which indicate that increased lipoperoxidation exacerbates the inflammation and deterioration of the cells and tissues of patients with periodontitis [9,10,44,50]. Thus, a higher level of MDA corresponds to a greater progression of inflammation of periodontal tissue. The increase in lipoperoxidation initiates a series of chain reactions that exacerbates membrane lipid damage in cells and tissues [7].

4.3. Membrane Fluidity

To our knowledge, no studies have been reported on the evaluation of MF (Ie/Im) in an oral pathology such as periodontitis, although the membrane represents tissue stability, protection, and cellular functionality. The membrane structure depends on phospholipids, cholesterol, and lipid rafts that affect its fluidity. Thus, an increase in lipoperoxidation may modify the functionality of these fatty acids which function as support for the structural integrity of the membrane. Changes in MF alter tissue homeostasis, leading to pathological processes [51,52]. An analysis of MF (Ie/Im) in relation to the PD level revealed a moderate-to-weak positive correlation in patients with periodontitis (r < 0.5; Table 2). This result and the reported MDA levels showed similar correlations with PD (Table 2). This similarity was repeated for the MF (Ie/Im) and MDA values when Group 2 (PD/CAL > 5 mm) was compared with group 1 (PD/CAL ≤ 5 mm), as shown in Table 3. These results indicate that the degree of lipid peroxidation influences the MF response of patients with periodontitis. In a previous study, there were higher salivary levels of 8-hydroxyguanosine, a marker of oxidative stress in patients with chronic periodontitis, especially when CAL had a depth greater than 3 mm [50]. On the other hand, the integrity of the connective and epithelium tissues depends on several factors, including the physico-chemical characteristics of intracellular lipids grouped in membrane-lining granules that act as important barriers to the permeability of xenobiotics and pathogens [53,54]. An analysis of the lipid characteristics in the tissues of 45 patients with oral reactive hyperplasia revealed elevated levels of arachidonic acid, a polyunsaturated fatty acid [55]. This finding is relevant in our work for three reasons, the first being that arachidonic acid is highly vulnerable to oxidation, a deleterious process which affects the fluidity and integrity of the membrane [10,52]. Secondly, arachidonic acid is a precursor in the synthesis of prostaglandins (PG-2) and leukotrienes (Tx-2) which induce increased inflammation and tissue damage. Thirdly, with increased inflammation, there are increases in the induction of the enzymatic activities of phospholipases A2 (PLA-2) and lipooxygenase (type 5), which play important roles in increasing MF [9,13,52,55]. Unfortunately, there are no previous studies in the literature on MF in gingival tissue in patients with periodontitis. However, based on the similarity seen in the results of MF (Ie/Im) and MDA (Table 2 and Table 3), and with the study by Mesgarzadeh et al. (2017), it can be reasonably inferred that MDA levels affected the MF of the patients studied. However, to explain its relationship with PD and CAL, there is a need to study the proportion of polyunsaturated fatty acids in the gingival tissue, quantify the levels of PG and Tx as indices of tissue inflammation, and measure the enzyme activities of PLA-2 and lipoxygenase (type 5) in relation to MF (Ie/Im).
The increases in ROS and proinflammatory cytokines may be responsible, directly and indirectly, for the destruction of connective tissue and bone resorption through a decoupling mediated by the receptor activator for nuclear factor k B ligand (RANKL)/osteoprotegin. In this process, the balance between bone formation and bone resorption is broken, favoring bone loss, a major characteristic feature of periodontitis [56,57,58,59]. Some recently introduced compounds have a significant influence on the oral environment. The use of paraprobiotics [60], probiotics [61,62], and postbiotics [63] can modify the clinical and microbiological parameters in periodontal patients. Probiotics have been considered the future strategy for achieving a balance in the oral microbiome in the presence of periodontitis, limiting the excessive growth of certain micro-organisms and modulating the inflammatory response to prevent bone loss and control the progression of this pathology [63]. However, the mechanisms underlying the use of probiotics in the prevention or control of periodontitis are still not fully elucidated. Therefore, these products that can modify oral parameters should be considered in future clinical trials, also considering their effect on nitrate levels, lipoperoxide levels, and membrane Fluidity. Another alternative to periodontal treatment may be by antioxidants [2]. Previous results with therapeutics such as lycopene [64,65], vitamin E [65], curcumin, and resveratrol [66] have been linked to low levels of oxidative stress, the attenuation of inflammation, regulation of bone resorption, and reduction of damage to hard and soft tissues [64,65,66,67].
Among the limitations of this work is the lack of published information on the membrane fluidity in gingival tissue to contrast our results. In addition to not classifying periodontitis in the various stages of the disease, this can help us determine the extent of the damaged tissue.

5. Conclusions

Our findings suggest that elevated NO3− concentrations in patients with periodontitis are linked to high PD values. Furthermore, the generation of high nitrosative stress has been associated with bone loss; therefore, high oxidative stress in patients with periodontitis is associated with higher PD and CAL and the increased severity of the disease. In this study, it was found that MDA concentrations affects MF, and a correlation between the elevated levels of MDA with PD and CAL was identified. The observed increases in NO3, MDA, and MF levels cause a breakdown in the balance between bone formation and resorption, leading to bone loss and an increase in PD and CAL, and therefore the progression of periodontitis. It is important to perform clinical studies to find the risk biomarkers for patients with periodontitis and thus look for alternatives such as antioxidants, which, together with conventional techniques, contribute to the prevention and treatment of periodontitis.

Author Contributions

Conceptualization, S.M.L.-M. and E.D.T.-S.; methodology, S.M.L.-M. and J.S.-F.; software, J.S.-F.; validation, E.D.T.-S. and J.R.G.-S.; formal analysis, S.M.L.-M.; investigation, E.D.T.-S. and J.R.G.-S.; resources, S.M.L.-M.; writing—original draft preparation, E.D.T.-S.; writing—review and editing, S.M.L.-M.; visualization, J.S.-F. and J.R.G.-S.; supervision, S.M.L.-M.; project administration, S.M.L.-M.; funding acquisition, S.M.L.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee in Research at the University of Guadalajara (registration number, CI-01221, date of approval: 6 March 2021).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

All data of this study are available upon request by contact with the corresponding author.

Acknowledgments

We express thanks to the Laboratory of Human Immunodeficiencies and Retroviruses, Division of Neurosciences, CIBO, IMSS, Mexico for allowing us to carry out part of the experimentation.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Liu, C.; Mo, L.; Niu, Y.; Li, X.; Zhou, X.; Xu, X. The Role of Reactive Oxygen Species and Autophagy in Periodontitis and Their Potential Linkage. Front. Physiol. 2017, 8, 439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Wang, Y.; Andrukhov, O.; Rausch-Fan, X. Oxidative Stress and antioxidant system in Periodontitis. Front. Physiol. 2017, 8, 910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Tonetti, M.S.; Greenwell, H.; Kornman, K.S. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J. Periodontol. 2018, 89, S159–S172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Van Dyke, T.E.; Bartold, P.M.; Reynolds, E.C. The Nexus Between Periodontal Inflammation and Dysbiosis. Front. Immunol. 2020, 11, 511. [Google Scholar] [CrossRef] [PubMed]
  5. Kurita-Ochiai, T.; Jia, R.; Cai, Y.; Yamaguchi, Y.; Yamamoto, M. Periodontal disease induced atherosclerosis and oxidative stress. Antioxidants 2015, 4, 577–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Kanzaki, H.; Wada, S.; Narimiya, T.; Yamaguchi, Y.; Katsumata, Y.; Itohiya, K.; Fukaya, S.; Miyamoto, Y.; Nakamura, Y. Pathways that regulate ROS scavenging enzymes, and their role in defense against tissue destruction in periodontitis. Front. Physiol. 2017, 8, 108–115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Chen, M.; Cai, W.; Zhao, S.; Shi, L.; Chen, Y.; Li, X.; Sun, X.; Mao, Y.; He, B.; Hou, Y.; et al. Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: A systematic review and meta-analysis. J. Clin. Periodontol. 2019, 46, 608–622. [Google Scholar] [CrossRef]
  8. Sánchez, G.A.; Miozza, V.A.; Delgado, A.; Busch, L. Total salivary nitrates and nitrites in oral health and periodontal disease. Nitric Oxide 2014, 36, 31–35. [Google Scholar] [CrossRef]
  9. Kovačević, V.; Daković, D.; Stevanović, I. Oxidative / anti-oxidative effects of colloidal silver ions and chlorhexidine in saliva and gingival fluid of periodontal patients. Vojnosanit. Pregl. 2022, 79, 441–447. [Google Scholar] [CrossRef]
  10. Veljovic, T.; Djuric, M.; Mirnic, J.; Gusic, I.; Maletin, A.; Ramic, B.; Brkic, S. Lipid Peroxidation Levels in Saliva and Plasma of Patients Suffering from Periodontitis. J. Clin. Med. 2022, 11, 3617. [Google Scholar] [CrossRef]
  11. Fernández-Bravo, S.E. Antioxidants in Dentistry: Oxidative Stress and Periodontal Diseases. In Lipid Oxidation in Food and Biological Systems: A Physical Chemistry Perspective; Springer International Publishing: Cham, Switzerland, 2022; pp. 341–359. [Google Scholar] [CrossRef]
  12. Moussa, S. Evaluating the impact of vitamin E supplementation as an adjunct to periodontal therapy on lipid peroxidation in stage II periodontitis patients: A randomized controlled trial. Egypt. Dent. J. 2022, 68, 481–488. [Google Scholar] [CrossRef]
  13. Gaschler, M.M.; Stockwell, B.R. Lipid peroxidation in cell death. Biochem. Biophys. Res. Commun. 2017, 482, 419–425. [Google Scholar] [CrossRef] [PubMed]
  14. Ahmadi-Motamayel, F.; Goodarzi, M.T.; Jamshidi, Z.; Kebriaei, R. Evaluation of Salivary and Serum Antioxidant and Oxidative Stress Statuses in Patients with Chronic Periodontitis: A Case-Control Study. Front. Physiol. 2017, 8, 189. [Google Scholar] [CrossRef] [Green Version]
  15. Almerich-Silla, J.M.; Montiel-Company, J.M.; Pastor, S.; Serrano, F.; Puig-Silla, M.; Dasí, F. Oxidative Stress Parameters in Saliva and Its Association with Periodontal Disease and Types of Bacteria. Dis. Markers 2015, 2015, 653537. [Google Scholar] [CrossRef] [Green Version]
  16. Zamora-Perez, A.L.; Ortíz-García, Y.M.; Lazalde-Ramos, B.P.; Guerrero-Velázquez, C.; Gómez-Meda, B.C.; Ramírez-Aguilar, M.A.; Zúñiga-González, G.M. Increased micronuclei and nuclear abnormalities in buccal mucosa and oxidative damage in saliva from patients with chronic and aggressive periodontal diseases. J. Periodontal Res. 2015, 50, 28–36. [Google Scholar] [CrossRef]
  17. Ghallab, N.A.; Hamdy, E.; Shaker, O.G. Malondialdehyde, superoxide dismutase and melatonin levels in GCF of aggressive and chronic periodontitis patients. Aust. Dent. J. 2016, 61, 53–61. [Google Scholar] [CrossRef] [Green Version]
  18. Senouci, S.; Ait Yahia, D.; Bouziane, D.; Mehadj, M.; Malaisse, W.J. The diagnostic role of salivary biomarkers of oxidative stress and inflammatory status and their relationship in periodontitis stage III and grade C. Biologia 2021, 76, 1617–1625. [Google Scholar] [CrossRef]
  19. Cherian, D.A.; Peter, T.; Narayanan, A.; Madhavan, S.S.; Achammada, S.; Vynat, G.P. Malondialdehyde as a marker of oxidative stress in periodontitis patients. J. Pharm. Bioallied Sci. 2019, 11, S297–S300. [Google Scholar] [CrossRef] [PubMed]
  20. Maciejczyk, M.; Bielas, M.; Zalewska, A.; Gerreth, K. Salivary biomarkers of oxidative stress and inflammation in stroke patients: From basic research to clinical practice. Oxidative Med. Cell. Longev. 2021, 2021, 5545330. [Google Scholar] [CrossRef]
  21. D’Aiuto, F.; Nibali, L.; Parkar, M.; Patel, K.; Suvan, J.; Donos, N. Oxidative stress, systemic inflammation, and severe periodontitis. J. Dent. Res. 2010, 89, 1241–1246. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Acquier, A.B.; De Couto, P.A.K.; Busch, L.; Sanchez, G.A. Parameters of oxidative stress in saliva from patients with aggressive and chronic periodontitis. Redox Rep. 2017, 22, 119–126. [Google Scholar] [CrossRef] [Green Version]
  23. Herane, M.A.; Godoy, C.; Herane, P. Enfermedad periodontal y embarazo: Revisión de la literatura. Rev. Med. Clin. Condes 2014, 25, 936–943. Available online: https://www.elsevier.es/es-revista-revista-medica-clinica-las-condes-202-articulo-enfermedad-periodontal-embarazo-revision-literatura-S0716864014706418 (accessed on 2 January 2023).
  24. Rojo, N.R.; Flores, A.; Arcos, M. Prevalencia, severidad y extensión de periodontitis crónica. Rev. Odontol. Mex. 2011, 15, 31–39. Available online: https://www.scielo.org.mx/pdf/rom/v15n1/v15n1a6.pdf (accessed on 2 January 2023).
  25. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Fractionation of cells. In Molecular Biology of the Cell, 4th ed.; Garland Science: New York, NY, USA, 2002. Available online: https://www.ncbi.nlm.nih.gov/books/NBK26936/ (accessed on 2 January 2023).
  26. Tenorio, L.F.A.; del Valle, M.L.; Pastelín, H.G. Validación de un método analítico espectrofotométrico para la cuantificación de metabolitos estables de óxido nítrico en fluidos biológicos. Rev. Mex. Cienc. Farm. 2005, 36, 31–41. Available online: https://www.redalyc.org/articulo.oa?id=57936106 (accessed on 1 February 2023).
  27. Esterbauer, H.; Cheeseman, K.H. Determination of aldehydic lipid peroxidation products malonaldehyde and 4-hydroxynonenal. Methods Enzymol. 1990, 186, 407–421. [Google Scholar] [CrossRef] [PubMed]
  28. Ortiz, G.G.; Pacheco-Moisés, F.; El Hafidi, M.; Jiménez-Delgado, A.; Macías-Islas, M.A.; Corral, S.A.R.; de la Rosa, A.C.; Sánchez-González, V.J.; Arias-Merino, E.D.; Velázquez-Brizuela, I.E. Detection of membrane fluidity in submitochondrial particles of platelets and erythrocyte membranes from Mexican patients with Alzheimer disease by intramolecular excimer formation of 1,3 dipyrenylpropane. Dis. Markers 2008, 24, 151–156. [Google Scholar] [CrossRef] [Green Version]
  29. Soto-Brambila, A.P.; Ortiz, G.G.; Briones-Torres, A.L.; Rivero-Moragrega, P.; Cortés-Romero, C.; Pacheco-Moisés, F.P. Marcadores de estrés oxidativo en pacientes con esclerosis múltiple durante un brote y su remisión. Acta Bioquim. Clin. Latinoam. 2019, 53, 167–173. Available online: https://www.redalyc.org/articulo.oa?id=53560335004 (accessed on 2 January 2023).
  30. Jiménez-Delgado, A.; Ortiz, G.G.; Delgado-Lara, D.L.; González-Usigli, H.A.; González-Ortiz, L.J.; Cid-Hernández, M.; Pacheco-Moisés, F.P. Effect of melatonin administration on mitochondrial activity and oxidative stress markers in patients with Parkinson’s disease. Oxidative Med. Cell. Longev. 2021, 2021, 5577541. [Google Scholar] [CrossRef]
  31. Buczko, P.; Zalewska, A.; Szarmach, I. Saliva and oxidative stress in oral cavity and in some systemic disorders. J. Physiol. Pharmacol. 2015, 66, 3–9. [Google Scholar]
  32. Allen, E.M.; Matthews, J.B.; O’Halloran, D.J.; Griffiths, H.R.; Chapple, I.L. Oxidative and inflammatory status in type 2 diabetes patients with periodontitis. J. Clin. Periodontol. 2011, 38, 894–901. [Google Scholar] [CrossRef] [PubMed]
  33. Cheng, Z.; Meade, J.; Mankia, K.; Emery, P.; Devine, D.A. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Pract. Res. Clin. Rheumatol. 2017, 31, 19–30. [Google Scholar] [CrossRef] [PubMed]
  34. Carcuac, O.; Berglundh, T. Composition of human periimplantitis and periodontitis lesions. J. Dent. Res. 2014, 93, 1083–1088. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Wang, G.P. Defining functional signatures of dysbiosis in periodontitis progression. Genome Med. 2015, 7, 40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Pignatelli, P.; Fabietti, G.; Ricci, A.; Piattelli, A.; Curia, M.C. How periodontal disease and presence of nitric oxide reducing oral bacteria can affect blood pressure. Int. J. Mol. Sci. 2020, 21, 7538. [Google Scholar] [CrossRef]
  37. Rosier, B.T.; Takahashi, N.; Zaura, E.; Krom, B.P.; MartÍnez-Espinosa, R.M.; van Breda, S.G.; Mira, A. The importance of nitrate reduction for oral health. J. Dent. Res. 2022, 101, 887–897. [Google Scholar] [CrossRef] [PubMed]
  38. Riccia, D.N.; Bizzini, F.; Perilli, M.G.; Polimeni, A.; Trinchieri, V.; Amicosante, G.; Cifone, M.G. Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis. 2007, 13, 376–385. [Google Scholar] [CrossRef]
  39. Ali, O.T.; Akalin, F.A.; Sahbazoglu, K.B.; Yamalik, N.; Kilinc, K.; Karabulut, E.; Tözüm, T.F. Nitrite and nitrate levels of gingival crevicular fluid and saliva in subjects with gingivitis and chronic periodontitis. J. Oral Maxillofac. Res. 2014, 5, e5. [Google Scholar] [CrossRef] [Green Version]
  40. Thomas, M.V.; Puleo, D.A. Infection, inflammation, and bone regeneration: A paradoxical relationship. J. Dent. Res. 2011, 90, 1052–1061. [Google Scholar] [CrossRef]
  41. Scotti, E.; Boué, S.; Sasso, G.L.; Zanetti, F.; Belcastro, V.; Poussin, C.; Sierro, N.; Battey, J.; Gimalac, A.; Ivanov, N.V.; et al. Exploring the microbiome in health and disease: Implications for toxicology. Toxicol. Res. Appl. 2017, 1, 1–37. [Google Scholar] [CrossRef]
  42. Kumar, J.; Teoh, S.L.; Das, S.; Mahakknaukrauh, P. Oxidative stress in oral diseases: Understanding its relation with other systemic diseases. Front. Physiol. 2017, 8, 693. [Google Scholar] [CrossRef] [PubMed]
  43. Panjamurthy, K.; Manoharan, S.; Ramachandran, C.R. Lipid peroxidation and antioxidant status in patients with periodontitis. Cell. Mol. Biol. Lett. 2005, 10, 255–264. [Google Scholar]
  44. Tsai, C.C.; Chen, H.S.; Chen, S.L.; Ho, Y.P.; Ho, K.Y.; Wu, Y.M.; Hung, C.C. Lipid peroxidation: A possible role in the induction and progression of chronic periodontitis. J. Periodontal Res. 2005, 40, 378–384. [Google Scholar] [CrossRef] [PubMed]
  45. Wei, D.; Zhang, X.L.; Wang, Y.Z.; Yang, C.X.; Chen, G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust. Dent. J. 2010, 55, 70–78. [Google Scholar] [CrossRef]
  46. Shee, F.; Pralhad, S.; Natarajan, S.; Manaktala, N.; Arun, S.; Marathe, A. Cellular and biochemical changes in different categories of periodontitis: A patient-based study. J. Int. Soc. Prev. Community Dent. 2020, 10, 341–349. [Google Scholar] [CrossRef]
  47. Baltacıoğlu, E.; Yuva, P.; Aydin, G.; Alver, A.; Kahraman, C.; Karabulut, E.; Akalın, F.A. Lipid peroxidation levels and total oxidant/antioxidant status in serum and saliva from patients with chronic and aggressive periodontitis. Oxidative stress index: A new biomarker for periodontal disease? J. Periodontol. 2014, 85, 1432–1441. [Google Scholar] [CrossRef] [PubMed]
  48. Akalιn, F.A.; Baltacιoğlu, E.; Alver, A.; Karabulut, E. Lipid peroxidation levels and total oxidant status in serum, saliva and gingival crevicular fluid in patients with chronic periodontitis. J. Clin. Periodontol. 2007, 34, 558–565. [Google Scholar] [CrossRef] [PubMed]
  49. Sánchez-Villamil, J.P.; Pino-Vélez, C.; Trejos-Suárez, J.; Cardona, N.; España, A.L.; Alfonso, P.A. Salivary markers of oxidative stress and periodontal pathogens in patients with periodontitis from Santander, Colombia. Biomedica 2020, 40, 113–124. [Google Scholar] [CrossRef] [PubMed]
  50. Sezer, U.; Çiçek, Y.; Çanakçi, C.F. Increased salivary levels of 8-hydroxydeoxyguanosine may be a marker for disease activity for periodontitis. Dis. Markers 2012, 32, 165–172. [Google Scholar] [CrossRef]
  51. García, J.J.; López-Pingarrón, L.; Almeida-Souza, P.; Tres, A.; Escudero, P.; García-Gil, F.A.; Bernal-Pérez, M. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: A review. J. Pineal Res. 2014, 56, 225–237. [Google Scholar] [CrossRef] [PubMed]
  52. Varela-López, A.; Quiles, J.L.; Cordero, M.; Giampieri, F.; Bullón, P. Oxidative stress and dietary fat type in relation to periodontal disease. Antioxidants 2015, 4, 322–344. [Google Scholar] [CrossRef] [Green Version]
  53. Chede, L.S.; Wagner, B.A.; Buettner, G.R.; Donovan, M.D. Electron Spin Resonance Evaluation of Buccal Membrane Fluidity Alterations by Sodium Caprylate and L-Menthol. Int. J. Mol. Sci. 2021, 22, 10708. [Google Scholar] [CrossRef] [PubMed]
  54. Harris, D.; Robinson, J.R. Drug delivery via the mucous membranes of the oral cavity. J. Pharm. Sci. 1992, 81, 1–10. [Google Scholar] [CrossRef] [PubMed]
  55. Mesgarzadeh, A.H.; Akbarzadeh, A.; Rasipour, A.; Rasipour, T.; Mehdizadeh, A.; Shaaker, M. Secretory phospholipase-A2 and fatty acid composition in oral reactive lesions: A cross-sectional study. Cancer Cell Int. 2017, 17, 50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Martu, M.A.; Surlin, P.; Lazar, L.; Maftei, G.A.; Luchian, I.; Gheorghe, D.N.; Rezus, E.; Toma, V.; Foia, L.G. Evaluation of oxidative stress before and after using laser and photoactivation therapy as adjuvant of non-surgical periodontal treatment in patients with rheumatoid arthritis. Antioxidants 2021, 10, 226. [Google Scholar] [CrossRef] [PubMed]
  57. Lee, N.K.; Choi, Y.G.; Baik, J.Y.; Han, S.Y.; Jeong, D.-W.; Bae, Y.S.; Kim, N.; Lee, S.Y. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 2005, 106, 852–859. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Graves, D. Cytokines that promote periodontal tissue destruction. J. Periodontol. 2008, 79, 1585–1591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Cochran, D.L. Inflammation and bone loss in periodontal disease. J. Periodontol. 2008, 79, 1569–1576. [Google Scholar] [CrossRef] [PubMed]
  60. Butera, A.; Gallo, S.; Maiorani, C.; Preda, C.; Chiesa, A.; Esposito, F.; Pascadopoli, M.; Scribante, A. Management of Gingival Bleeding in Periodontal Patients with Domiciliary Use of Toothpastes Containing Hyaluronic Acid, Lactoferrin, or Paraprobiotics: A Randomized Controlled Clinical Trial. Appl. Sci. 2021, 11, 8586. [Google Scholar] [CrossRef]
  61. Vale, G.C.; Mayer, M.P.A. Effect of probiotic Lactobacillus rhamnosus by-products on gingival epithelial cells challenged with Porphyromonas gingivalis. Arch. Oral Biol. 2021, 128, 105174. [Google Scholar] [CrossRef] [PubMed]
  62. Bueno, M.R.; Ishikawa, K.H.; Almeida-Santos, G.; Ando-Suguimoto, E.S.; Shimabukuro, N.; Kawamoto, D.; Mayer, M.P.A. Lactobacilli Attenuate the Effect of Aggregatibacter actinomycetemcomitans Infection in Gingival Epithelial Cells. Front. Microbiol. 2022, 13, 846192. [Google Scholar] [CrossRef]
  63. Butera, A.; Gallo, S.; Pascadopoli, M.; Taccardi, D.; Scribante, A. Home Oral Care of Periodontal Patients Using Antimicrobial Gel with Postbiotics, Lactoferrin, and Aloe Barbadensis Leaf Juice Powder vs. Conventional Chlorhexidine Gel: A Split-Mouth Randomized Clinical Trial. Antibiotics 2022, 11, 118. [Google Scholar] [CrossRef] [PubMed]
  64. Chandra, R.V.; Srinivas, G.; Reddy, A.A.; Reddy, B.H.; Reddy, C.; Nagarajan, S.; Naveen, A. Locally delivered antioxidant gel as an adjunct to nonsurgical therapy improves measures of oxidative stress and periodontal disease. J. Periodontal Implant. Sci. 2013, 43, 121–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Muniz, F.W.; Nogueira, S.B.; Mendes, F.L.; Rosing, C.K.; Moreira, M.M.; de Andrade, G.M.; Carvalho, R.D.S. The impact of antioxidant agents complimentary to periodontal therapy on oxidative stress and periodontal outcomes: A systematic review. Arch. Oral Biol. 2015, 60, 1203–1214. [Google Scholar] [CrossRef] [PubMed]
  66. Nguyen, C.; Savouret, J.-F.; Widerak, M.; Corvol, M.-T.; Rannou, F. Resveratrol, Potential Therapeutic Interest in Joint Disorders: A Critical Narrative Review. Nutrients 2017, 9, 45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Kanzaki, H.; Shinohara, F.; Kajiya, M.; Kodama, T. The Keap1/Nrf2 Protein Axis Plays a Role in Osteoclast Differentiation by Regulating Intracellular Reactive Oxygen Species Signaling. J. Biol. Chem. 2013, 288, 23009–23020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Table
Table 1. Clinical parameters and markers of oxidative stress in the 2 groups.
Table 1. Clinical parameters and markers of oxidative stress in the 2 groups.
ParameterPeriodontitis Patients
(Mean ± SD; n = 60)		Participants without Periodontitis (Mean ± SD; n = 60)p
Age (years)34.85 ± 14.2644.56 ± 10.170.220
PD (mm)1.68 ± 0.365.40 ± 0.23<0.001 *
CAL (mm)0 5.15 ± 0.29<0.001 *
BoP (%)0 46.87 ± 11.54<0.001 *
NO3− (umole/mL)7.75 ± 2.089.06 ± 2.480.225
MDA (umole/mL)4.00 ± 0.883.94 ± 0.790.664
Ie/Im (arbitrary)0.44 ± 0.240.46 ± 0.230.666
* Values with p < 0.05.
Table
Table 2. Spearman correlation between clinical parameters and markers of oxidative stress.
Table 2. Spearman correlation between clinical parameters and markers of oxidative stress.
Periodontitis Patientsrp
Variable 1Variable 2
NO3−PD0.0340.792
NO3−CAL0.0150.905
NO3−BoP0.0110.939
MDAPD0.2940.022 *
MDACAL0.4460.000 *
MDABoP0.1820.162
Ie/ImPD0.2680.037 *
Ie/ImCAL0.0560.051
Ie/ImBoP0.2290.078
* Values with p < 0.05; r indicates the Pearson correlation coefficient.
Table
Table 3. Depth classification of PD and CAL in patients with periodontitis.
Table 3. Depth classification of PD and CAL in patients with periodontitis.
ParameterPDp
Group 1
(Mean ± SD; n = 19)		Group 2
(Mean ± SD; n = 41)
BoP (%)41.33 ± 17.646.32 ± 12.80.131
NO3− (umol/mL)11.07 ± 1.9613.95 ± 1.460.044 *
MDA (umol/mL)4.11 ± 0.628.79 ± 0.790.012 *
Ie/Im (arbitrary)0.50 ± 0.190.61 ± 0.090.049 *
ParametersCALp
Group 1
(Mean ± SD; n = 13)		Group 2
(Mean ± SD; n = 47)
BoP (%)39.12 ± 10.148.25 ± 8.30.110
NO3− (umole/mL)8.32 ± 2.919.26 ± 1.110.477
MDA (umole/mL)3.79 ± 0.764.48 ± 0.640.004 *
Ie/Im (arbitrary)0.33 ± 0.020.52 ± 0.080.001 *
The values in this table are only for patients with periodontitis; * Values with p < 0.05.
Table
Table 4. Association of markers of oxidative stress with PD and CAL in patients with periodontitis.
Table 4. Association of markers of oxidative stress with PD and CAL in patients with periodontitis.
Oxidative Stress ParameternPDχ2 Test (Degree of Freedom) Value, pYates Correction
(Degree of Freedom) Value, p		Fisher’s Exact Test (Degree of Freedom) Value, p
Group 1Group 2
NO3−Low 60520-(1) 0.003, 0.955-
High629
MDALow 60623(1) 1.0254, 0.311--
High1021
Ie/ImLow 60106(1) 0.064, 0.800--
High737
Oxidative Stress ParameternCALχ2 test (Degree of Freedom) Value, pYates Correction
(Degree of Freedom) Value, p		Fisher’s Exact Test (Degree of Freedom) Value, p
Group 1Group 2
NO3−Low 60714(1) 2.59, 0.107--
High633
MDALow 60527-(1) 0.81, 0.367-
High820
Ie/ImLow 6016--(1) 0.254, 0.614
High1241
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Torres-Sánchez, E.D.; Salazar-Flores, J.; Gómez-Sandoval, J.R.; Lomeli-Martinez, S.M. Membrane Fluidity and Oxidative Stress in Patients with Periodontitis. Appl. Sci. 2023, 13, 4546. https://doi.org/10.3390/app13074546

AMA Style

Torres-Sánchez ED, Salazar-Flores J, Gómez-Sandoval JR, Lomeli-Martinez SM. Membrane Fluidity and Oxidative Stress in Patients with Periodontitis. Applied Sciences. 2023; 13(7):4546. https://doi.org/10.3390/app13074546

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Torres-Sánchez, Erandis Dheni, Joel Salazar-Flores, Juan Ramón Gómez-Sandoval, and Sarah M. Lomeli-Martinez. 2023. "Membrane Fluidity and Oxidative Stress in Patients with Periodontitis" Applied Sciences 13, no. 7: 4546. https://doi.org/10.3390/app13074546

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