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ORIGINAL ARTICLE
Year : 2022  |  Volume : 26  |  Issue : 1  |  Page : 37-43  

Evaluation of the reactive oxygen metabolite levels in plasma, gingival crevicular fluid, and saliva in generalized chronic periodontitis patients before and after nonsurgical periodontal therapy: A case–control and interventional study


1 Department of Periodontology, Adhiparasakthi Dental College and Hospital, Melmaruvathur, India
2 Department of Periodontology, Mahatma Gandhi Post Graduate Institute of Dental Sciences, Puducherry, India
3 Department of Periodontology, KSR Institute of Dental Science and Research, Tiruchengode, Tamil Nadu, India

Date of Submission16-Jul-2020
Date of Decision21-Mar-2021
Date of Acceptance20-Jun-2021
Date of Web Publication01-Jan-2022

Correspondence Address:
Jayakumar Manjeu
Department of Periodontology, Adhiparasakthi Dental College and Hospital, Melmaruvathur - 603 319, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jisp.jisp_519_20

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   Abstract 


Background: Reactive oxygen metabolites (ROMs) produced in periodontitis could contribute to excessive tissue damage. Thus, treatment of chronic periodontitis may decrease the ROM levels. The aim of this study is to evaluate the ROM levels in plasma, saliva, and gingival crevicular fluid (GCF) in generalized chronic periodontitis (GCP) patients before and after nonsurgical periodontal treatment. Materials and Methods: Two groups were included in this study. Group I consisted of 30 healthy controls (C) and Group II consisted of 30 subjects with GCP. Plaque index (PI), papillary bleeding index, Probing Depth (PD), and clinical attachment level were recorded. GCF, saliva, and plasma samples were collected from both groups. ROM levels were assessed. A baseline comparison was made between the two groups. Nonsurgical periodontal treatment was carried out for Group II subjects. Two months posttreatment, the clinical parameters and ROM levels in GCF, saliva, and plasma were reassessed in Group II, and the data were compared with their baseline values. Statistical analysis was done using SPSS 20 software and results were derived. Results: Two months posttreatment, Group II exhibited significant reduction in ROM levels in plasma, saliva, and GCF with significant decrease in PI, bleeding on probing, probing depth, and attachment loss. Conclusion: Thus, significant oxidative stress may occur in chronic periodontitis and nonsurgical periodontal therapy may be regarded as an effective treatment modality to treat the diseased periodontium, thereby preventing possible systemic diseases in future.

Keywords: Chronic periodontitis, nonsurgical periodontal therapy, oxidative stress, reactive oxygen metabolite


How to cite this article:
Manjeu J, Babu SP, Kala CN, Paul GT, Soorya KV, Gandhimadhi D. Evaluation of the reactive oxygen metabolite levels in plasma, gingival crevicular fluid, and saliva in generalized chronic periodontitis patients before and after nonsurgical periodontal therapy: A case–control and interventional study. J Indian Soc Periodontol 2022;26:37-43

How to cite this URL:
Manjeu J, Babu SP, Kala CN, Paul GT, Soorya KV, Gandhimadhi D. Evaluation of the reactive oxygen metabolite levels in plasma, gingival crevicular fluid, and saliva in generalized chronic periodontitis patients before and after nonsurgical periodontal therapy: A case–control and interventional study. J Indian Soc Periodontol [serial online] 2022 [cited 2022 Jan 19];26:37-43. Available from: https://www.jisponline.com/text.asp?2022/26/1/37/334322




   Introduction Top


Chronic periodontitis is an inflammatory condition characterized by the destruction of the supporting structures of the teeth. This progressive destruction of the periodontal ligament and the alveolar bone leads to clinically detectable attachment loss and periodontal pocket formation. Local factors such as the plaque and calculus deposited on tooth surface usually cause this inflammatory condition.[1] Even though the Gram-negative bacteria primarily initiate the tissue destruction, majority of the tissue damage occurs due to the inappropriate host response to these microorganisms and their products. When stimulated by periodontal pathogens, the host cells (e.g., polymorphonuclear neutrophils [PMNs] and macrophages) release reactive oxygen species (ROS) as a part of immune reaction. Excessive production of these molecules further worsens the inflammatory condition. As the condition progresses, the ROS enter the blood stream from the oral environment.[2] This in turn could subject the individual to oxidative stress and contribute to various systemic diseases. The family of reactive species includes superoxide radical, hydrogen peroxide, and hydroxyl radical. The member, hydrogen peroxide, is not a radical and hence termed as “reactive oxygen metabolite” (ROM).[3]

The purpose of this study is to evaluate the ROM levels in gingival crevicular fluid (GCF), saliva, and plasma in generalized chronic periodontitis (GCP) patients before and after nonsurgical periodontal therapy (scaling and root planing).


   Materials and Methods Top


The present study was conducted in a total of 60 subjects, randomly selected from age group of 30–60 years, irrespective of their gender. Subjects were selected from those attending the department of periodontology for their routine treatment needs. Research and ethical committee clearance was obtained before the start of the study. Medical and dental history was obtained. Patients were divided into two groups based on their clinical parameters. Group I consisted of 30 healthy controls (C) with no evidence of interproximal attachment loss, probing depth ≤3 mm at all sites on all teeth, bleeding on probing in <10% of sites of entire dentition, with no gingival enlargement, erythema, or tooth mobility. Group II consisted of 30 systemically healthy individuals with GCP. The selection criteria included patients with a minimal complement of twenty teeth, of which at least 30% of teeth exhibited probing depth ≥4 mm. Furthermore, the patients should not have received any periodontal therapy for the past 6 months prior to the period of study. Pregnant and lactating women, smokers, and patients who were on antioxidant (AO) supplements or anti-inflammatory medications or antibiotics were excluded from the study. Considering the severity, extent, complexity, and rate of disease progression, the periodontitis patients were classified under Stage III generalized periodontitis with Grade A category. This is in accordance with the 2017 new classification scheme for periodontal and peri-implant diseases put forth by the world workshop[4] [Figure 1]. The subjects were informed about the proceedings of the study, and informed written consent was obtained from each.
Figure 1: Orthopantomogram of a Periodontitis patient (Stage III, Grade A Generalized periodontitis

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Two blinded examiners who did not involve in treating the patients recorded the clinical observations to prevent bias. The baseline data for both groups were recorded by the first examiner. The clinical parameters recorded at the baseline included the plaque index (PI), papillary bleeding index (PBI), probing depth (PD), and clinical attachment level (CAL). A mouth mirror and a dental explorer were employed for assessing the PI. The four gingival areas of the tooth, the distofacial, facial, mesiofacial, and lingual surfaces were examined.[5] PBI was recorded by inserting a periodontal probe into the gingival sulcus and the intensity of bleeding was scored.[6] PD and CAL were measured using UNC-15 probe at all six sites (mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual, and distolingual) per tooth, and the mean value was obtained.[7],[8]

The teeth were isolated and about 1 μl of GCF was collected using extracrevicular method with the help of volumetric, microcapillary pipettes. These were transferred to microcentrifuge tubes containing 100 μl of phosphate-buffered saline (PBS). PBS, being isotonic, increases the volume of GCF obtained without affecting the contents.[9] The samples were centrifuged to obtain the supernatant which was stored at -70°C until the assay. GCF collection using micropipettes has its own advantages and disadvantages. Although this method provides undiluted sample of native GCF whose volume can be accurately evaluated, a very long collection period is involved. The collection of sample is strenuous owing to the viscous nature of fluid that makes aspiration difficult. Furthermore, collecting GCF from healthy sulcus is a difficult task. Holding the microcapillary tube for lengthy periods at the sulcus entrance may sometimes cause gingival trauma unknowingly. Longer collection period is likely to influence the protein concentration of the collected sample. Careful isolation is essential to avoid contamination with saliva and blood. Sometimes, the tube may become clogged with debris. Sample retrieval from the microcapillary pipettes is also laborious.[10]

About 2 ml of unstimulated saliva was collected. Participants were made to sit comfortably in an upright position and tilt their heads down slightly to pool saliva in the mouth. They were made to gently spit the saliva into the graduated test tubes offered to them. The saliva samples were then centrifuged and the supernatant thus obtained was stored at -80°C until the assay.[11]

About 3 ml of venous blood was drawn from vein in the antecubital fossa of each patient with a syringe and transferred to a sterile test tube coated with ethylenediaminetetraacetic acid. The samples were centrifuged at ×3000 g for 5 min to obtain the supernatant which was stored at -80°C until the test procedure.[12]

Group I subjects (healthy controls) did not receive any kind of periodontal treatment after sample collection and baseline clinical examination, whereas the Group II (GCP cases) received nonsurgical periodontal therapy (scaling and root planing). The therapy was performed quadrant wise (1-h session per quadrant) within 2 weeks. Under local anesthesia, full mouth scaling and root planing was done using ultrasonic scaler and Gracey Curettes (Hu-Friedy, Chicago, IL, USA) by another periodontist who did not engage in data collection. Oral hygiene instructions were delivered. No antibiotics were prescribed after the treatment. The patients were reevaluated for clinical parameters 2 months after the completion of phase I therapy. Postprocedural data were recorded by the blinded second examiner. Plasma, GCF, and saliva samples were again collected from Group II and analyzed for ROM levels. This is a case–control and interventional study.

The test performed was based on Fenton's reaction in which iron catalyzed hydroperoxides breakdown into alkoxyl (RO+) and peroxyl (ROO++) radicals and then reacts with a chromogen to form a colored compound, the absorbance of which is detected photometrically.[13] The intensity of the color correlates directly with the quantity of free radicals, which in turn will reflect the oxidative status of the sample. This is in accordance with the Beer Lambert's law. About 20-μl of the biological sample was treated with 1 ml of acetate buffer (pH 4.8) and 20 μl chromogenic substrate (N-N-dimethyl-p-phenylenediamine) was added. The mixture was immediately incubated for 5 min at 37°C. The absorbance was recorded at 505 nm by an ultraviolet-visible spectrophotometer. The ROM levels were measured in Carratelli units (CARR U). It had been previously established that 1 CARR U corresponds to 0.08 mg/dl hydrogen peroxide.[14] Thus, the ROM levels in GCF, saliva, and plasma were obtained.

SPSS stands for Statistical Product and Service Solutions. It is a software used for statistical analysis, currently developed and owned by IBM corporation, USA. Mean and Standard deviation values were calculated. Student t-test was used to compare the mean of two groups. Paired t-test was used to compare the means between two related groups of the sample. Analysis of variance (ANOVA) was employed when multiple groups were compared. P < 0.001 was considered to be of high statistical significance, whereas P > 0.05 was considered to be statistically nonsignificant.


   Results Top


In Group I subjects (controls), the mean PI value was 0.14 ± 0.26, mean PBI value was 0.24 ± 0.14, mean PD value was 2.69 ± 0.35 mm, and mean CAL was 2.69 ± 0.35 mm. Furthermore, in Group I subjects, the mean ROM values of plasma, saliva, and GCF were 358.57 ± 61.28 CARR U, 350.55 ± 49.14 CARR U, and 352.98 ± 54.09 CARR U, respectively. In Group II (GCP cases), the mean PI value was 4.31 ± 0.75, mean PBI value was 3.49 ± 0.51, mean PD value was 5.51 ± 0.90 mm, and mean CAL was 6.26 ± 1.01 mm. Furthermore, the mean ROM values of plasma, saliva, and GCF in Group II subjects were 1142.86 ± 394.14 CARR U, 1038.42 ± 373.02 CARR U, and 1060.66 ± 462.99 CARR U, respectively. The above data are represented in [Figure 2] and [Figure 3].
Figure 2: Comparison of baseline values of clinical parameters studied between cases (generalized chronic periodontitis) and control groups. Plaque index; papillary bleeding index; probing depth; clinical attachment level. PI – Plaque index; PBI – Papillary bleeding index; PD – Probing depth; CAL – Clinical attachment level

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Figure 3: Comparison of baseline values of ROM levels studied between cases (generalized chronic periodontitis) and control groups. Reactive oxygen metabolite; gingival crevicular fluid. ROM – Reactive oxygen metabolite ; GCF – Gingival crevicular fluid

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When the pretreatment scores among the two groups were compared using t-test, a statistically significant difference (P < 0.001) was found for PI, PBI, PD, and CAL as shown in [Table 1]. When the preprocedural scores of ROM levels in plasma, saliva, and GCF were compared using t-test among the two groups, a statistically highly significant difference (P < 0.001) was found as shown [Table 1]. The Group II cases GCP exhibited high ROM values when compared with Group I (controls). Two months after nonsurgical periodontal therapy, the mean PI value was 1.58 ± 0.41, mean PBI value was 1.45 ± 0.37, mean PD value was 2.52 ± 0.66 mm, and mean CAL was 3.35 ± 0.81 mm in Group II [Figure 4]. The mean ROM values of plasma, saliva, and GCF were 501.44 ± 166.87 CARR U, 442.14 ± 122.35 CARR U, and 465.40 ± 148.99 CARR U, respectively, in Group II [Figure 5].
Figure 4: Comparison of baseline and post 2 months values of clinical parameters studied in cases (generalized chronic periodontitis). Plaque index; papillary bleeding index; probing depth; clinical attachment level. PI – Plaque index; PBI – Papillary bleeding index; PD – Probing depth; CAL – Clinical attachment level

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Figure 5: Comparison of baseline and post 2 months values of ROM levels studied in cases (generalized chronic periodontitis). Reactive oxygen metabolite; gingival crevicular fluid. ROM – Reactive oxygen metabolite ; GCF – Gingival crevicular fluid

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Table 1: Comparison of baseline values of the parameters studied between generalized chronic periodontitis and control group

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When the pretreatment scores and posttreatment scores after 2 months were compared in Group II using paired t-test, a highly statistically significant difference (P < 0.001) was found for PI, PBI, PD, CAL, and ROM levels [Table 2]. This significant reduction in values could reflect the reduction in inflammatory status after periodontal therapy.
Table 2: Comparison of baseline and 2 months posttreatment values of the parameters studied in generalized chronic periodontitis group

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When the mean percentage reduction of all the above parameters was compared among different age groups using ANOVA, there was no statistical significant difference observed (P > 0.05) [Figure 6] and [Table 3]. The mean percentage reduction of parameters studied between male and female showed that there was no statistically significant difference between male and female population gender wise (P > 0.05) [Figure 7] and [Table 4].
Figure 6: Comparison of mean percentage reduction of values of the parameters from pretreatment to posttreatment studied between different age groups in generalized chronic periodontitis group. Plaque index; papillary bleeding index; probing depth; clinical attachment level; reactive oxygen metabolite; gingival crevicular fluid. PI – Plaque index; PBI – Papillary bleeding index; PD – Probing depth; CAL – Clinical attachment level; ROM – Reactive oxygen metabolite ; GCF – Gingival crevicular fluid

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Figure 7: Comparison of mean percentage reduction of values of the parameters from pretreatment to posttreatment studied between male and female in generalized chronic periodontitis group. Plaque index; papillary bleeding index; probing depth; clinical attachment level; reactive oxygen metabolite; gingival crevicular fluid. PI – Plaque index; PBI – Papillary bleeding index; PD – Probing depth; CAL – Clinical attachment level; ROM – Reactive oxygen metabolite ; GCF – Gingival crevicular fluid

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Table 3: Comparison of mean percentage reduction of values of the parameters from pretreatment to posttreatment studied between different age groups in generalized chronic periodontitis group

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Table 4: Comparison of mean percentage reduction of values of the parameters from pretreatment to posttreatment studied between male and female in generalized chronic periodontitis group

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   Discussion Top


When the periodontium is exposed to bacterial toxins, the host cells release certain inflammatory cytokines. These cytokines, in turn, recruit the PMN's to the site of infection. The PMNs release ROS into the extracellular environment via oxidative burst catalyzed by NADPH oxidase.[15] The released ROS or ROM are not target specific and thus they damage the resident host tissue. At high concentrations, these molecules exhibit destructive effects on cellular components such as the proteins, lipids, and DNA. The superoxide anion, hydroxyl radical, and hydrogen peroxide are considered to be the three chief ROMs of physiological importance.[16] In our study, significantly higher PI, PBI, PD, and CAL were observed in Group II when compared to Group I at the baseline. Numerous studies have associated such altered clinical parameters in subjects with chronic periodontitis as compared to the healthy controls.[17],[18] Group II subjects presented with significantly higher levels of ROM in plasma, saliva, and GCF when compared with Group I. Oxidation-dependent changes occurring in collagen within the periodontal connective tissues could retard neutrophil transfer through the tissues and they produce ROS. A recent study reported that chronic periodontitis patients exhibited hyperactive neutrophil phenotypes, which, in turn, could influence plasma ROS.[19] ROM is considered to be a useful indicator of ROS in blood.[12] Furthermore, in our present study, the plasma ROM levels decreased from 1142.86 ± 394.14 CARR U (baseline) to 501.44 ± 166.87 CARR U (posttreatment) in Group II. The significant reduction (P < 0.001) of plasma ROM levels may be attributed to the resolution of periodontal inflammation post treatment. Animal studies provide evidences that periodontitis induces oxidative tissue damage in the aorta[20] and liver,[21] as serum ROS increases. Thus, periodontitis could result in injury to various organs by increasing the production of ROS in blood. Therefore, periodontal therapy may reduce the ROS/ROM levels in blood, thus reducing the chances of systemic diseases in future.

GCF is considered to be a serum transudate, originating from the underlying periodontal connective tissues. Hence, the connective tissue metabolites associated with alveolar bone resorption or remodeling may be carried by the GCF into the oral cavity. The metabolites released from the alveolar bone do not interact functionally with the other matrix components and their adequately small size allows them to pass through the connective tissue into the GCF.[22] Biochemical evaluation of inflamed gingival tissue suggested that the core proteins of gingival proteoglycans present in those inflamed tissues undergoes extensive breakdown, whereas the sulfated glycosaminoglycan chains remain relatively intact. This corresponds to the mechanisms of ROS degradation of proteoglycans.[23] When proteoglycan metabolites from GCF were compared with the parent macromolecule, reduction in the proportions of certain amino acids was observed. ROMs seem to alter the functional group of these amino acids as suggested by some studies.[24] Our study showed a significant reduction in ROM levels in GCF from 1060.66 ± 462.99 CARR U (baseline) to 465.40 ± 148.99 CARR U (posttreatment) in Group II. Our results are in harmony with the studies conducted by Sobaniec et al.,[25] Sheikhi et al.,[26] and Tsai et al.[27] Hendek et al.[28] concluded that peroxidation of lipid molecules occurs in GCF of diseased periodontium and initial periodontal therapy may prove fruitful. Our results are in accordance with their study.

We also observed that ROM levels in saliva decreased from 1038.41 ± 373.02 CARR U (baseline) to 442.14 ± 122.35 CARR U (posttreatment) in Group II subjects. To reduce the chances of temporal fluctuations in salivary redox homeostasis, the sample collection was done between 9.00 AM and 12.00 PM.[29] Several studies established positive correlation between the oxidative stress markers of saliva and periodontal disease severity. In our study, the elevated ROM levels in saliva of chronic periodontitis cases could be partially due to increased lipid peroxidation occurring against the bacteria and their toxins in the saliva itself and partially due to increased leakage of ROM into saliva from serum and GCF. When the equilibrium between ROS and AOs gets disturbed, inflammatory diseases of the oral cavity may occur.[2],[30] Thus, the increased salivary ROM levels detected in our study suggested an increase in the level of lipid peroxidation in oral environment in chronic periodontitis. The ROM levels dropped posttreatment due to reduction of inflammation and restoration of tissue integrity. Furthermore, nonsurgical phase is always considered as the initial phase when treating the diseased periodontium. Literature holds evidence that deeper pockets respond well to surgical phase when preceded by scaling and root planing.[31] The cases included in our study exhibited mean probing depth of about 5.51 ± 0.90 mm initially and were considered for nonsurgical therapy with regard to the above-mentioned fact. Nonsurgical periodontal therapy had resulted in the improvement of all clinical parameters after 2 months in Group II when compared with their baseline values. Similar results were observed in various studies.[30]

In the present study, statistically significant, strong, and positive correlations were observed between clinical parameters and ROM levels in plasma, saliva, and GCF. When the mean percentage reduction of parameters from baseline to 2 months postoperative was compared between males and females, there was no statistically significant difference (P > 0.05) observed. This might indicate that both sexes responded similarly to the treatment and gender does not impact the treatment results. Similarly, when the mean percentage reduction of parameters was compared between different age groups, no statistically significant difference was found (P > 0.05). More extensive studies would be needed to conclude the influence of gender and age on periodontal therapy outcomes. Furthermore, during the study period, diet, exercise, stress levels, and other genetic factors were presumed to be comparable between Group I and GROUP II. This may be another limitation of the study.


   Conclusion Top


Thus, the above study proves that periodontitis could elevate the ROM levels in the body and demonstrates the efficacy of nonsurgical periodontal therapy (scaling and root planing) in effectively eliminating the etiologic agent, thereby decreasing the deleterious effects of inflammation on the periodontium. This, in turn, improved the clinical parameters and decreased the ROM (oxidative stress marker) levels. As a result, the balance between the AOs and oxidants in the tissues would be restored which is not only essential for maintenance of a healthy periodontium but also to keep up good systemic health. Thus, besides eradicating bacterial plaque and diminishing periodontal inflammation effectively, nonsurgical periodontal therapy could also prevent the risk of future systemic diseases by bringing down the amount of local and circulating ROMs. As a result, various chronic diseases associated with oxidative stress may be prevented.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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