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ORIGINAL ARTICLE
Year : 2018  |  Volume : 22  |  Issue : 6  |  Page : 480-486  

Comparison of gingival crevicular fluid periostin levels in healthy, chronic periodontitis, and aggressive periodontitis


Department of Periodontics, Sri Ramakrishna Dental College and Hospital, Coimbatore, Tamil Nadu, India

Date of Submission17-Apr-2018
Date of Acceptance20-Jun-2018
Date of Web Publication1-Nov-2018

Correspondence Address:
Dr. Fazal Ilahi Jamesha
Department of Periodontics, Sri Ramakrishna Dental College and Hospital, SNR College Road, Coimbatore - 641 006, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jisp.jisp_266_18

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   Abstract 


Background: In both states of health and disease, the integrity of connective tissue along with regulation in formation of bones are well maintained by periostin (POSTN) which is a matricellular protein secreted by fibroblasts. The present study aimed to assess the gingival crevicular fluid (GCF) POSTN levels in patients with chronic periodontitis (CP) and aggressive periodontitis and to compare them with that of healthy controls. Materials and Methods: A total of 39 individuals were recruited and allocated into the healthy group, and two periodontitis groups (the chronic and the aggressive types) (13 in each group). The samples of GCF fluid were collected using microcapillary pipette. The POSTN levels were estimated using the enzyme-linked immunosorbent assay. Results: The mean levels of total POSTN in GCF fluid (in pg/μl) were 182.41, 79.87, and 49.28 for the healthy, CP, aggressive periodontitis groups, respectively. There was a statistically significant difference between the groups with P < 0.05. Furthermore, there were statistically significant differences when compared among the groups with P < 0.05. When all three groups were examined together, there were negative correlations between GCF POSTN levels and clinical parameters. Conclusion: The GCF POSTN levels reduced with an increase in the severity of the periodontitis. With the present study results, we could conclude that the GCF POSTN level can be considered as a dependable marker in periodontal disease diagnosis, disease activity, and healing.

Keywords: Aggressive periodontitis, chronic periodontitis, gingival crevicular fluid, healing, periostin


How to cite this article:
Jamesha FI, Maradi AP, Chithresan K, Janakiram S, Maddur PK, Rangaraju R. Comparison of gingival crevicular fluid periostin levels in healthy, chronic periodontitis, and aggressive periodontitis. J Indian Soc Periodontol 2018;22:480-6

How to cite this URL:
Jamesha FI, Maradi AP, Chithresan K, Janakiram S, Maddur PK, Rangaraju R. Comparison of gingival crevicular fluid periostin levels in healthy, chronic periodontitis, and aggressive periodontitis. J Indian Soc Periodontol [serial online] 2018 [cited 2018 Dec 19];22:480-6. Available from: http://www.jisponline.com/text.asp?2018/22/6/480/244562




   Introduction Top


The disparities in immunoinflammatory responses of the host are believed to be the cause of pathogenesis of periodontal diseases. The chronic periodontitis (CP) can be defined as “a disease of infectious origin causing inflammation within the periodontium, progressive loss of attachment, and alveolar bone.”[1] Aggressive periodontitis (AgP) includes a group of uncommon, often severe, swiftly advancing forms of periodontitis, frequently characterized by clinical manifestation at an early age and with the following characteristics– no related medical history, faster loss of attachment and destruction of bone, familial aggregation of cases.[2]

Periodontal disease results from a complex relationship between the immunoinflammatory events of host and subgingival biofilm. The events develop in the tissues of periodontium in response to the bacterial challenge. The consequence of the inflammatory changes is the destruction of the periodontal ligament fibers, with resultant clinical attachment loss (CAL), along with alveolar bone resorption.[3]

The inflammatory and immune processes that develop in the tissues of periodontium in response to the long-standing biofilm presence subgingivally are protective by intent, but significant damage to tissues also occurs. This host response is orchestrated by mediators such as cytokines, prostanoids, and matrix metalloproteinases.[4]

Periostin (POSTN) is found to be important in the regulation of formation of bone.[5] Biologically, the functions of POSTN also include the maintenance of the integrity of connective tissue in both states of health and disease.[6] It functions as a matricellular protein in activation of the cell, by attaching to their cell surface receptors, thus exerting its actions of biological nature.[7] POSTN, secreted by fibroblasts, is found to be present in various tissues, serum, saliva and also gingival crevicular fluid (GCF).

GCF contains a wide range of substances, such as proteins, cytokines, enzymes, cellular elements of bacterial origin, immunoinflammatory cells from periodontal tissues and peripheral blood. Since GCF collection is noninvasive and simple, it can be a tool to observe the periodontal disease pathogenesis. The periodontal disease activity is been detected, and patients at risk for diseases of periodontium are been distinguished through the components of GCF.[8] The levels of GCF POSTN have been found to be inversely related with the severity and progression of CP[9] and also in AgP.[10]

POSTN can act as a new biomarker in connection with the pathogenesis of CP and AgP. In the present study, the GCF POSTN level of patients diagnosed with CP and AgP were assessed and compared with that of healthy controls as the previous studies concentrated only on the comparison between its presence in serum, saliva and in gingivitis patients.[9],[10] We, the authors, believe that this is the first study to assess the POSTN levels in GCF exclusively of patients diagnosed with CP and AgP, and to correlate with clinical parameters.

The aim of the present study was to investigate GCF POSTN levels in patients with CP and AgP and to compare them with GCF POSTN of healthy individuals, and to find the correlation between the levels of POSTN in GCF and age, plaque index, modified Sulcular Bleeding Index (mSBI), CAL in the three groups.


   Materials and Methods Top


Study design

The sample size was calculated using the Sampling software (G. Power Version 3.1.9.2) with an alpha error of 5% and power of 95%, and it was found to be 12 in each group. One extra sample was collected in each group as a standby for avoiding any errors while processing, and hence, the total number of samples was 13 in each group. The study population was recruited from the Outpatient Department of Periodontics in a Dental College and Hospital of south India. Following the examination of the individuals clinically and radiographically, they were divided into three groups as follows: the healthy group, CP group, and AgP group (13 in each group). The protocol of the study was approved by the Institutional Review Board and Ethical Committee of the institution in which the study was conducted. The informed consent was signed by all individuals after describing the need for the study.

Inclusion criteria

GROUP-I-Healthy controls-subjects with periodontal probing depth <3 mm, no bleeding on probing and no evidence of bone loss radiographically; GROUP-II-generalized (or) localized mild, moderate, or severe CP patients (According to Armitage criteria); GROUP-III-localized (or) generalized AgP patients (According to Lang's criteria).

Exclusion criteria

The subjects who were pregnant, lactating mothers, current smoker or former smoker, underwent periodontal therapies during the past 6 months, with any drug intake during the past 3 months, with any systemic condition that could compromise POSTN levels such as diabetes mellitus, cancer, and ventricular hypertrophy were not included in the study.

Clinical examination

During clinical examination, the parameters assessed were as follows: Plaque Index using the criteria given by Silness and Loe (1964),[11] modified Sulcular Bleeding Index (mSBI) using the criteria given by Mombelli et al.,[12] conventional probing depth on each tooth from the margin of the gingiva to the bottom of the sulcus/pocket using William's periodontal probe at 6 specific sites per tooth (mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual, and distolingual surfaces),[13] Clinical Attachment Level (CAL) recorded from cementoenamel junction to the bottom of the gingival sulcus/periodontal pocket using William's periodontal probe at all the six sites as mentioned for probing depth.[14]

Collection of gingival crevicular fluid

Site selection

GCF from sites with the greatest CAL and demonstrating maximum bleeding score as assessed by the mSBI in patients with CP and AgP; and from the most convenient site in healthy individuals.

Method of collection

GCF samples were obtained using microcapillary pipettes.[15] The collection time was between 2 and 4 pm. The site was isolated by means of cotton/gauze. The plaque along with the supragingival calculus was removed with a universal curette to avoid contamination and blocking of the microcapillary pipette by plaque. The sulcular areas were gently air-dried. A color coded, calibrated (10 μl) volumetric microcapillary pipette [-Microcapillary pipettes, Drummond, Broomall, USATM] was placed at the entrance of the gingival sulcus. The GCF samples which were mixed with blood, exudate, or saliva were thrown away, and fresh samples were collected.

Storage

Each microcapillary pipette containing 2 μl GCF was wrapped in aluminum foil, placed inside separate sterile tubes and stored at −80°C in an ultra-low temperature freezer (Thermo Fisher Scientific India Pvt. Ltd, Mumbai, India), until further analysis of POSTN by ELISA procedure.

ELISA analysis for gingival crevicular fluid samples

The contents of the kit and the samples were brought to room temperature. For duplication, the samples were divided into two (1 μl each) and diluted to 2 μl. A 50 μl standard was added to the standard well. A 40 μl of diluted sample was added to sample wells and then 10 μl anti-POSTN antibody was added to sample wells, then 50 μl streptavidin- horseradish peroxidase was added to sample wells and standard wells but not added in the blank control well and thoroughly mixed. The plate was covered with a sealer and incubated for 60 min at 37°C. The sealer was removed, and the plate was washed 5 times with wash buffer. The wells were soaked with at least 0.35 ml wash buffer for 30 s to 1 min for each wash. The plate was blotted onto paper towels. A 50 μl substrate solution A was added to the individual wells, and then 50 μl substrate solution B was added to the individual wells. The plate shielded with a new sealer was incubated for 10 min at 37°C in the dark. A 50 μl stop solution was then added to the individual wells, and the blue color changed into yellow immediately. The optical density values of the individual wells were determined immediately using a microplate reader set to 450 nm within 30 min following the addition of the stop solution. The concentrations of POSTN were expressed as picograms per microliter (pg/μl).

Statistical analysis

A commercially available software (SPSS 16.0; SPSS Inc., Chicago, IL, USA) was used to perform the statistical analysis. The data were distributed normally, and it was investigated using Shapiro–Wilk test. Analysis of variance (ANOVA) – one-way, was used to compare the variables in the three groups and Tukey honestly significant difference was used for multiple comparisons. Comparisons of the level of POSTN in GCF, age, plaque index, mSBI, and CAL were analyzed and correlated using Pearson correlation in healthy, CP, AgP groups.


   Results Top


All GCF samples in three groups showed the presence of POSTN. The demographics, clinical parameters, and GCF POSTN levels are summarized in [Table 1] and ANOVA comparison in [Table 2].
Table 1: Demographic parameters of study population, clinical parameters, periostin levels in gingival crevicular fluid measured in the study population

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Table 2: Analysis of variance - comparison of age, plaque index, modified sulcular bleeding index score, clinical attachment level, gingival crevicular fluid periostin values between the groups

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The mean age in healthy, CP and AgP groups was statistically significant between the groups [Table 2]; P < 0.05]. When the mean age was compared among groups [Table 3], there was a statistically significant difference among healthy and CP groups (P < 0.05), among CP and AgP groups (P < 0.05) and there was no statistically significant difference when age was compared among healthy and AgP groups (P = 0.610).
Table 3: Tukey Honestly Significant Difference - Comparison of age, Plaque Index, modified Sulcular Bleeding Index score, clinical attachment level, and Gingival Crevicular Fluid Periostin values among the groups

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The clinical parameters that were examined such as mean Plaque Index scores, mSBI percentage, CAL were statistically significant between the groups [Table 2]; P < 0.05]. When these clinical parameters were compared among groups, there was a statistically significant difference among healthy and CP groups [Table 3]; P < 0.05], among healthy and AgP groups [Table 3]; P < 0.05] and not statistically significant among CP and AgP groups [Table 3]; P = 0.232, 0.827, and 0.582, respectively].

The mean levels of total POSTN in GCF were 182.41 pg/μl, 79.87 pg/μl and 49.28 pg/μl for the healthy, CP, AgP groups, respectively [Table 1]. There was a statistically significant difference between the groups [Table 2]; P < 0.05]. The mean levels of total POSTN in GCF were significantly lower in the CP and AgP groups than in the healthy controls. The amount of POSTN in GCF decreased by 56% in CP group and by 73% in AgP group when compared to the healthy group. There was also statistically significant difference among the groups [Table 3]; P < 0.05].

Correlation between gingival crevicular fluid periostin levels and clinical parameters

The Pearson correlation is shown in [Table 4]. When all clinical groups were observed together, there were negative correlations between POSTN levels in GCF and age, mSBI, plaque index, CAL, that is, the POSTN levels in GCF were inversely related to age, mSBI, plaque index, CAL. It was found that the negative correlation between the POSTN levels in GCF and age (r = −0.303; P = 0.061) was not statistically significant and the negative correlations between the POSTN levels in GCF and mSBI, plaque index, CAL (r = −0.788, r = −0.655, r = −0.691, respectively; P < 0.01) were statistically significant (two-tailed).
Table 4: Pearson correlation between the levels of Periostin in Gingival Crevicular Fluid and age, modified Sulcular Bleeding Index score, Plaque Index and clinical attachment level

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Furthermore, in the healthy group, negative correlations were found between the POSTN levels in GCF and age (r = −0.302; P = 0.317), and the POSTN levels in GCF and Plaque Index (r = −0.146; P = 0.635), but the correlations were not statistically significant. The correlations between the POSTN levels in GCF and mSBI and the POSTN levels in GCF and CAL were not found.

In CP group, negative correlations were found between the POSTN levels in GCF and mSBI (r = −0.204; P = 0.504), and the POSTN levels in GCF and Plaque Index (r = −0.373; P = 0.209), but the correlations were not statistically significant. The correlation between the POSTN levels in GCF and age (r = 0.333; P = 0.267) and the POSTN levels in GCF and CAL (r = 0.370; P = 0.214) were positive and not statistically significant.

In AgP group, a negative correlation was found between the POSTN levels in GCF and age (r = −0.280; P = 0.354) which was not statistically significant. However, the correlations between the POSTN levels in GCF and mSBI (r = 0.499; P = 0.082), the POSTN levels in GCF and Plaque Index (r = 0.228; P = 0.454), and the POSTN levels in GCF and CAL (r = 0.427; P = 0.145) were found to be positive and not statistically significant.


   Discussion Top


The present study consisted of three groups-healthy controls, patients with CP and AgP. The GCF was collected from all the individuals of the study groups and was analyzed by ELISA procedure for the presence and level of POSTN. The levels of POSTN in GCF were compared between and among the groups and were correlated with the clinical parameters recorded. POSTN is found to be important in the regulation of formation of bone.[5] Biologically, the functions of POSTN also include the maintenance of the integrity of connective tissue in both states of health and disease.[6] It functions as a matricellular protein in activation of the cell, by attaching to their cell surface receptors, thus exerting its actions of biological nature.[7] POSTN, secreted by fibroblasts, is found to be present in various tissues, serum, saliva, and also GCF. The levels of GCF POSTN have been found to be inversely related with the severity and progression of CP[9] and also in AgP.[10] POSTN can act as a novel biomarker for the periodontal disease activity and healing tissues. To the best of the knowledge of the authors, this is the first study to detect POSTN in exclusively GCF of healthy controls and patients with CP and AgP and to correlate with the clinical parameters.

The sample size calculated was 12 in each group. One extra sample was collected in each group as a standby for avoiding any errors while processing and hence the total number of samples was 13 in each group.

In the present study, the mean age in all the three groups was statistically significant between the groups. When it was compared among groups, there were statistically significant differences among healthy and CP groups, among CP and AgP groups and there was no statistically significant difference among healthy and AgP groups. Similarly, in Aral et al.'s study, the mean age was higher in the CP than in the AgP group which was statistically significant (P < 0.05).[10]

The mean plaque index scores were statistically significant between the groups. When the mean plaque index was compared among groups, there were statistically significant differences among healthy and CP groups, among healthy and AgP groups and there was no statistically significant difference among CP and AgP groups. In Aral et al.'s study, CP (1.66) and AgP (1.85) patients presented with higher mean plaque index scores than the nonperiodontitis (0.78) group (P < 0.001); though, no significant differences were found between CP and AgP groups (P > 0.05),[10] which was similar to the present study. In Balli et al.'s study, there was a significant difference (P < 0.016) in the mean plaque index score between the healthy (0.49) and CP (2.30) groups which are similar to the present study results.[9]

When the mSBI was compared among groups, there were statistically significant differences among healthy and CP groups, among healthy and AgP groups and there was no statistically significant difference among CP and AgP groups. Similar to the present study, no significant difference in full-mouth bleeding on probing score was observed between CP (55.35%) and AgP groups (58.99%) (P > 0.05) in Aral et al.'s study.[10]

When the mean CAL was compared among groups, there was a statistically significant difference among healthy and CP groups, among healthy and AgP groups and it was not statistically significant among CP and AgP groups. Similarly, in Aral et al.'s study, there was a statistically significant difference in the mean CAL value among healthy (0.18 mm) and CP (3.82) groups and among healthy and AgP (4.13) groups.[10]

Compared to healthy and CP groups, GCF POSTN levels in the AgP group were the lowest. Similarly, GCF POSTN levels in the CP group were lower than in the healthy group (P < 0.05). Similar to the present study findings, Aral et al. investigated GCF POSTN levels in CP and AgP patients and found that there was a significant decrease in GCF POSTN levels in CP (0.58 pg/30 s) and AgP (0.46 pg/30 s) groups when compared to non-periodontitis (0.72 pg/30 s) group.[10] In Balli et al.'s study, GCF POSTN levels were found to be higher in healthy controls (346.93 pg/μl) than in gingivitis (108.86 pg/μl) and CP patients (51.64 pg/μl) and they concluded that GCF POSTN levels were inversely related to the severity and progression of periodontitis,[9] which is in accordance with the present study.

The present study results, therefore, confirmed a negative correlation between GCF POSTN levels and diseases of the periodontium. The delay in tissue repair found in periodontal tissue inflammation may be explained by the reduced GCF POSTN levels seen in periodontitis groups, in this study. There were significant differences among all three groups in GCF POSTN levels, and it is reduced more in the periodontitis groups than in healthy groups, signifying POSTN's role in the disease activity in periodontal diseases. In a study conducted by Kumaresan et al., a statistically significant difference in GCF POSTN concentration was seen between healthy controls (6.54 ng/ml) and CP group (3.46 ng/ml) (P < 0.01).[16] Therefore, as anticipated, the grade of inflammation and damage to the tissues which affected the POSTN levels in GCF potently and inversely was observed in the present study. The role of this novel molecule taking part in maintaining normal function of periodontal tissue might be suggested by the decreased level of POSTN in GCF in the periodontitis groups.[9]

In Padial-Molina et al.'s study, it was found that the GCF POSTN levels (in pg/μl) elevated with time and a correlation was found with the healing process in periodontitis and healthy controls. The analysis revealed that levels of POSTN before the surgery (367.85) were statistically significantly lower than those at the 2nd day (1496.14) (P < 0.001) and at the 14th day (836.80) (P < 0.024). It is found in the Padial-Molina et al.'s study that GCF POSTN levels were lower in diseased condition than in healthy, similar to the present study and increased during healing after treatment.[17] The repair and regeneration of the tissues of periodontium are affected directly by the reduced levels of POSTN.[18],[19]

A negative correlation was found between all the examined clinical parameters and GCF POSTN value when compared in all groups [Table 4], in the present study. These results were similar to Aral et al.'s study, in which there was a negative correlation found between full-mouth bleeding on probing score and GCF POSTN value, plaque index score and GCF POSTN value and CAL and GCF POSTN value when compared in all groups (r = −0.580,−0.505 and − 0.581, respectively).[10]

In the present study, there was a negative correlation between Plaque Index and GCF POSTN value in healthy and CP groups, and there was a positive correlation between CAL and the levels of POSTN in GCF in CP and AgP groups [Table 4]. However, in Balli et al.'s[9] study, a negative correlation (r = −0.712) between CAL and the levels of POSTN in GCF was found in CP group. Baeza et al. also reported that, with disease severity, that is, with an increase in CAL, there was a decrease in GCF POSTN levels.[20]

The amount of POSTN in GCF decreased by 56% in CP group and by 73% in AgP group in comparison with the healthy group. In Balli et al.'s[9] study, the amount of POSTN in GCF decreased by 85% in CP group in comparison with the healthy group and in Aral et al.'s[10] study, the amount of POSTN in GCF decreased by 19% in CP group and by 36% in AgP group in comparison with the nonperiodontitis group.

Hence, by assessing the POSTN concentration in GCF of patients with the diseased condition and comparing with the healthy controls, early detection of the diseased states is easy and simple. The limitations of this study include smaller sample size and also not assessing the post-treatment POSTN levels since the levels of POSTN in GCF was found to be higher in healing tissues.[17] The patients during menstruation/hormonal variations were not considered which is also one of the limitations of the study. Further studies can be performed to detect the POSTN levels in GCF or tissues in CP and AgP patients after nonsurgical and surgical treatments. Further newer research on chairside POSTN detection kit will be of great help to make the procedure easier, simpler and time-saving. Hence, POSTN can be considered as a marker of periodontal inflammation, and the findings of the present study may bring up the proposal that averting the depletion of POSTN or increasing the levels of POSTN may be helpful in repairing the tissues at a faster rate and increasing attachment gain.


   Conclusion Top


From this study, the following conclusions were drawn:

  1. POSTN was present in each GCF sample of all the study groups, and its level was seen to be the highest in the healthy group, lower in the CP group and the lowest in the AgP group
  2. The mean levels of total POSTN in GCF reduced with an increase in disease severity
  3. The POSTN levels in GCF and inflammatory changes were inversely related.


By combining the results in the present study with those of studies conducted earlier, it might be concluded that the levels of POSTN in GCF could be contemplated as a dependable marker in periodontal disease diagnosis and its activity.

Acknowledgement

The authors would like to thank all patients and healthy controls who participated in the study and also to all friends who supported.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Preshaw PM, Taylor JJ. Periodontal pathogenesis. In: Newman MG, Takei HH, Carranza FA, editors. Clinical Periodontology. 11th ed. New Delhi: Elsevier; 2012. p. 263.  Back to cited text no. 3
    
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Aral CA, Köseoğlu S, Sağlam M, Pekbağrıyanık T, Savran L. Gingival crevicular fluid and salivary periostin levels in non-smoker subjects with chronic and aggressive periodontitis: Periostin levels in chronic and aggressive periodontitis. Inflammation 2016;39:986-93.  Back to cited text no. 10
    
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Baeza M, Garrido M, Hernández-Ríos P, Dezerega A, García-Sesnich J, Strauss F, et al. Diagnostic accuracy for apical and chronic periodontitis biomarkers in gingival crevicular fluid: An exploratory study. J Clin Periodontol 2016;43:34-45.  Back to cited text no. 20
    



 
 
    Tables

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



 

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