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ORIGINAL ARTICLE
Year : 2023 | Volume
: 22
| Issue : 4 | Page : 465-469
Effect of periostin in peri-implant sulcular fluid and gingival crevicular fluid: A comparative study
VC Santhosh1, Karishma2, Anas Abdul Khader3, Varun Ramachandra4, Rohit Singh5, B Kaushik Shetty6, Vaishnavi Kailash Nimbalkar7
1 Department of Periodontics, KMCT Dental College, Manassery, Mukkam, Calicut, Kerala, India
2 Department of Dentistry, AIIMS, Patna, Bihar, India
3 Department of Preventive Dentistry, College of Dentistry in ArRass, Qassim University, Kingdom of Saudi Arabia
4 Department of Oral and Maxillofacial Surgery, Manubhai Patel Dental College, Vadodara, Gujarat, India
5 Department of Prosthodontics Crown Bridge and Implantology, Patna Dental College and Hospital, Patna, Bihar, India
6 Department of Orthodontics and Dentofacial Orthopedics, Nitte (Deemed to be University), AB Shetty Memorial Institute of Dental Sciences (ABSMIDS), Mangalore, Karnataka, India
7 School of Dental Sciences, Krishna Vishwa Vidyapeeth, Karad, Maharashtra, India
Correspondence Address:
Karishma
Department of Dentistry, AIIMS, Patna, Bihar
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/aam.aam_171_22
Abstract
Background: Various similarities have been observed between gingival crevicular fluid (GCF) and peri-implant sulcular fluid (PISF). This has resulted in research that has evaluated similar biological fluid markers that are similar to those present within the gingival sulcus. These biomarkers have high sensitivity and are a reliable biological tool when compared to clinical and/or radiographic examination and aid in diagnosis as well as monitoring the progression of periodontal disease surrounding teeth as well as the implants. Aim: The study aimed to compare the effectiveness of periostin in peri-implant sulcular and gingival crevicular fluids. Materials and Methods: This experimental prospective in vitro analysis was done following clearance by the institutional ethical committee. A total of 100 patients were selected. They were categorized into two groups: (I) Group A patients had peri-implant disease (n = 50), whereas (II) Group B patients had periodontitis (n = 50). Clinical loss of attachment score was noted in six sites around natural teeth and four sites around the implants. Presterilized filter paper strips were inserted within the sulcus/pocket till pressure was felt for 60 s. Periostin concentration levels in GCF and PISF samples were measured by the enzyme-linked immunosorbent assay technique. Statistical analysis of data collected was performed using Shapiro–Wilk statistical tool for normally distributed numerical data. Results: Mean ± standard deviation concentration of periostin in gingival crevicular fluid from periodontitis cases was recorded as 20.15 ± 2.76 ng/30sn, whereas in PISF was 19.23 ± 1.89 ng/30sn. On statistical analysis, no statistically significant differences were seen after comparing the concentration of periostin in periodontitis as well as peri-implantitis groups (P > 0.05). Conclusion: The present study analyzed periostin levels in gingival crevicular fluid obtained from patients diagnosed with periodontitis and sulcular fluid obtained from the sulcus around implants. Early biological markers or indicators of inflammation should be studied to determine the prognosis of treatment apart from the clinical assessment for the patient's benefit.
Abstract in French Résumé
Contexte: Diverses similitudes ont été observées entre le fluide sulculaire gingival (GCF) et le fluide sulculaire péri-implantaire (PISF). Ce a abouti à des recherches qui ont évalué des marqueurs fluides biologiques similaires à ceux présents dans le sillon gingival. Ces les biomarqueurs ont une sensibilité élevée et sont un outil biologique fiable par rapport à l'examen clinique et/ou radiographique et aident à diagnostic ainsi que le suivi de la progression de la maladie parodontale entourant les dents ainsi que les implants. Objectif: L'étude visait à comparent l'efficacité de la périostine dans les fluides péri-implantaires sulculaires et gingivaux. Matériels et Méthodes: Ce test expérimental une analyse prospective in vitro a été effectuée après autorisation par le comité d'éthique de l'établissement. Au total, 100 patients ont été sélectionnés. Ils étaient classés en deux groupes: (I) les patients du groupe A avaient une maladie péri-implantaire (n = 50), alors que (II) les patients du groupe B avaient une parodontite (n = 50). Le score clinique de perte d'attache a été noté dans six sites autour des dents naturelles et quatre sites autour des implants. Bandes de papier filtre préstérilisées ont été insérés dans le sulcus/poche jusqu'à ce que la pression soit ressentie pendant 60 s. Les niveaux de concentration de périostine dans les échantillons GCF et PISF ont été mesurés par la technique de dosage immuno-enzymatique. L'analyse statistique des données recueillies a été effectuée à l'aide de la méthode statistique de Shapiro-Wilk. outil pour les données numériques distribuées normalement. Résultats: concentration moyenne ± écart-type de périostine dans le liquide gingival les cas de parodontite ont été enregistrés à 20,15 ± 2,76 ng/30sn, alors que dans le PISF, ils étaient de 19,23 ± 1,89 ng/30sn. Sur l'analyse statistique, pas statistiquement des différences significatives ont été observées après avoir comparé la concentration de périostine dans les groupes parodontite et péri-implantite (P > 0,05). Conclusion: La présente étude a analysé les niveaux de périostine dans le liquide créviculaire gingival obtenu chez des patients diagnostiqués avec une parodontite et fluide sulculaire obtenu à partir du sulcus autour des implants. Les marqueurs ou indicateurs biologiques précoces de l'inflammation doivent être étudiés pour déterminer le pronostic du traitement en dehors de l'évaluation clinique au bénéfice du patient.
Mots-clés: Créviculaire, liquide, gingival, péri-implantaire, parodontite, périostine, pronostic, sulculaire
Keywords: Crevicular, fluid, gingival, peri-implant, periodontitis, periostin, prognosis, sulcular
Introduction 
Dental implants are a good option for the replacement of missing teeth. Re-treatment may be required when there is the development of implant-associated diseases in surrounding peri-implant soft and hard tissues. These diseases include peri-implantitis as well as peri-implant mucositis. Peri-implant mucositis develops as a primary lesion that is identical to gingivitis due to clinical presentation. The clinical signs of peri-implant mucositis are pain, swelling, and erythema.[1] Peri-implant mucositis is a reversible condition that can be attained through oral health care and the treatment of periodontal disease.[2] Peri-implantitis is a clinical condition associated with inflammation of the surrounding peri-implant oral mucosa that involves the supporting alveolar bone. Hence, the clinical diagnosis of peri-implantitis is based on the clinical sign of bleeding after probing and also, on evaluating the loss of marginal alveolar bone by making use of radiographic analysis.[3]
When compared with a natural tooth, an implant is not supported by a periodontal ligament that aids in connecting the root surface of a tooth with the underlying alveolar bone. A healthy peri-implant associated with surrounding mucosa forms the supracrestal portion of a healthy implant. The peri-implant mucosa comprises connective tissue structures that have either a covering of keratinized or masticatory mucosa or that of nonkeratinized or lining mucosa. The surrounding tissue of an implant has an average thickness of 3–4 mm.
This peri-implant oral mucosa has weak adherence to the surface of an implant due to a thin (measuring 2 mm) junctional epithelial lining. Collagen fibers present within the supracrestal connective tissue portion are parallel with the surface of an implant that does not provide strong adhesion as with that of the gingiva.
On clinical examination, the healthy status of peri-implant supporting tissue is represented by an absence of inflammation in the surrounding soft tissues associated with an implant. Healthy implant-associated tissue is characterized by an absence of erythema or redness, bleeding following probing, tissue swelling, and/or the presence of suppuration or formation of pus.[4],[5],[6]
Peri-implant sulcus fluid is similar to gingival crevicular fluid as it reflects the inflammatory response. It has been stated that the exudate leaking from the peri-implant tissue into the peri-implant sulcus increases during the inflammatory process. Periostin is a cellular-based matrix proteinaceous product consisting of a total of 835 amino acids that weigh up to 90 kDa. This protein product has been included in the “fasciclin” family.[7],[8] Production of periostin can be induced by transforming growth factor-beta (TGF-β). This protein affects mechanical-based properties related to cross-linking of collagen as well as connective tissue. Apart from its interactions with extracellular matrix proteins, periostin undergoes interaction with the class of proteins known as the “integrins” that are cell membrane-associated proteins. TGF-β influences osteoblastic proliferation and their attachment through the production of periostin.[8] Periostin has an important role in the repair of wounds and the morphogenesis of the tooth.[9],[10]
Studies have reported that the concentration of periostin in the gingival crevicular fluid was found to decrease as the process of inflammation increases. A reduction in the level of periostin has been explained using two underlying mechanisms (a) the first mechanism is dependent on the responsiveness of bacterial microorganisms in an environment that causes modulation of expression of periostin and (b) the second underlying mechanism is associated with a reduction in the levels of periostin due to decrease in the population of periodontal ligament cells. These cells are the main synthesizing cells responsible for periostin production and also aid in the progression of periodontal disease.[11]
An increase in the level of gingival crevicular fluid has been seen as the first clinical sign of inflammation of the gingiva.[12] Stewart et al. have suggested that measuring levels of gingival crevicular fluid may serve as an objective clinical indicator of the degree of inflammation affecting periodontal tissues.[13]
The flow rate of production of peri-implant sulcular fluid (PISF) is observed to be identical with gingival crevicular fluid, there may be few volumetric differences existing as a result of various structures as well as vascular differences between peri-implant as well as gingival mucosal tissues.[14] Hence, it is important to confirm an association between the volume of PISF with clinical peri-implant parameters compared with the standard production of gingival crevicular fluid (GCF). Hence, there is a requirement of studying any inflammation-based biomarker to understand the underlying disease pathology in peri-implant tissues.
Hence, based on the evidence published in the scientific literature, this study was designed to comparatively evaluate the effects of periostin in peri-implant sulcular and gingival crevicular fluids.
Materials and Methods This experimental in vitro study was carried out after obtaining the institutional ethical committee clearance (EEC8/21/PDCH33). Written consent was obtained from all study participants before commencing the sampling procedure. The total sample size selected was 100, which were divided into two categories: (a) Group A: these patients were diagnosed with the peri-implant disease (n = 50) and (b) Group B: those with clinically assessed periodontal disease (n = 50). Both were confirmed using radiographic analysis and the use of William's periodontal probe.
Inclusion criteria for this study were: (a) patients who were above 18 years of age, (b) patients with no history of systemic medical diseases, (c) patients who had not been prescribed antibiotics and/or anti-inflammation-related agents within a period of the past 6 months, and (d) those patients who had received any dental treatment in a period of the past 6 months. Exclusion criteria for the study were: (a) patients who did not provide consent, (b) patients with any systemic diseases, and (c) Those on medications.
All the selected patients received oral prophylactic hygiene procedures 1 week before performing the sampling procedure.
Clinical oral examination
The gingival index (GI) and plaque index (PI) scores were measured at four different sites surrounding the implants as well as the natural teeth. Clinical loss of attachment score was also observed from six different sites surrounding natural teeth and from four different clinical sites surrounding the dental implants. For performing clinical measurements, calibrated metallic William's periodontal probe was used around natural teeth, whereas a nonmetallic or plastic probe was used to note down the clinical loss of attachment surrounding dental implants.
Collection of gingival crevicular fluid and peri-implant sulcular fluid samples and analysis
Collection of both gingival crevicular fluid and sulcular fluid samples was done after performing clinical assessments. The selection of periodontal pockets with the greatest depth was made by observing radiographs. Before performing a collection of fluid samples, isolation of selected tooth or diseased implant was performed by use of sterilized cotton rolls. The mucosa was then gently dried using an airstream. Following this, sterilized strips of filter paper were placed within a particular pocket till the point the patient felt some pressure. After 60 s, paper strips containing fluid were kept within a precalibrated Periotron 8000 instrument for the measurement of obtained gingival crevicular fluid and PISF volume. All obtained measurements were then recorded.
Collected sample strips were then stored at a temperature of − 80°C till analysis was performed. Periostin levels within gingival crevicular fluid and PISF samples were then measured according to manufacturer instructions using enzyme-linked immunosorbent assay method.
Statistical analysis
For performing the statistical evaluation of collected data, the normal distribution of numerical data was analyzed using the Shapiro–Wilk statistical test. Descriptive statistical analysis was done using mean ± standard deviation (SD). The statistical software used was SPSS version 22.0 (IBM, Chicago) for statistical analysis. A P < 0.05 was set as statistically significant.
Results and Observations A total of 100 samples were collected from 100 patients. In studying the gender distribution, 51 patients were male patients, whereas 49 patients were female. On analyzing the age distribution, participants were found to be aged between 3 and 72 years.
Statistical analysis revealed no statistical significance between both study groups when the comparison between PI and GI was made (P > 0.05) [Table 1] and [Graph 1]. The mean ± SD periostin concentrations in gingival crevicular fluid samples from periodontitis patients were found to be 20.15 ± 2.76 ng/30sn while in PISF was found to be 19.23 ± 1.89 ng/30sn. Furthermore, no statistically significant differences were obtained in making comparisons between periodontitis and peri-implantitis study groups while comparing the periostin concentrations between gingival crevicular fluid and PISF (P > 0.05) [Table 2].
Table 2: Comparisons between the concentration of periostin in both study groups Discussion Peri-implant-associated diseases are the most common complications that are seen to be associated with treatment related to the placement of dental implants.[15] These diseases bear similarities with periodontal disease due to their identical inflammatory pathways.[16] There are various clinical indices as well as inflammatory biomarkers that allow both clinical as well as biochemical follow-up of either of the diseases, for example, interleukin-1 beta (IL-1β).[17],[18]
Periostin is a matrixcellular protein molecule belonging to the “fasciclin” family. Periostin undergoes synthesis within fibrous connective tissues, for example, the periosteum as well as periodontal ligamental tissues. This protein has an important role in maintaining the integrity of tissues as well as their maturation and reparative process in healing wounds along with the integrity of tissues of the periodontal ligament. Hence, periostin may be utilized as a novel cellular biological marker.[19],[20],[21] Peri-implant crevicular fluid is an osmotically mediated inflammatory exudates; changes in the flow rate and profile occur according to the conditions of peri-implant tissues.[22]
Gündogar and Uzunkaya compared the levels of IL-1β and tumor necrosis factor α (TNF-α) levels in healthy and diseased areas. It was found that IL-1β and TNF-α among inflammatory cytokines in GCF/PISF were increased in periodontal and peri-implanter diseases.[23]
In the present study, no statistical difference was found in comparing the concentrations of periostin in gingival crevicular fluid with that of PISF. This is in accordance with the findings reported by Uzunkaya and Gundogar, who reported no statistically significant difference in similarly compared study groups.[24]
Balli et al., in a study conducted on patients suffering from gingivitis, chronic periodontitis as well as healthy controls, observed a statistical significance between the groups in PI, GI, and clinical loss of attachment.[25]
Padial-Molina et al. investigated the role of protein “periostin” over human periodontal cells under an inflammation-associated environment. The human periodontal ligament cells were subsequently treated using variable periostin concentrations. The study results demonstrated that “periostin” had a central role in preserving the integrity of periodontal tissues. This protein plays an important part in various cellular activities, for example, the proliferation of cells, migration of cells as well as activation of survival signaling pathways whenever they are exposed to inflammation-associated chemical mediators along with a variety of bacterial origin virulence-related factors.[26]
In contrast, Akman et al. (2018) reported no significant difference in relation to plaque and gingival indices and clinical attachment loss scores between healthy individuals and among patients who had an inflammatory condition of periodontium or those with implants.[27]
Similarly, Aral et al., in their comparative study on chronic and aggressive periodontitis observed that the patients with periodontitis, reported higher scores of PI and GI as well as loss of gingival attachment when compared with patients with normal periodontium; however, no statistically significant difference was observed between these studied groups.[28]
Shelke et al. evaluated and compared the levels of periostin in PISF in healthy peri-implant sites and sites with peri-implant mucositis and peri-implantitis with its clinical correlation. It was found that the periostin levels in PISF may prove to be a magnificent tool in the early and prompt diagnosis of peri-implant diseases.[29]
Bhardwaj and Prabhuji reported a positive as well as statistically significant correlation between volumes of gingival crevicular fluid and PISF. Clinical indices such as PI, bleeding index as well as GI showed highly positive as well as statistically significant correlations. Although a good correlation was observed between peri-implant-associated sulcus fluid and clinical parameters rather than gingival crevicular fluid (GCF).[21]
Conclusion Clinical measurement as well as quantification of host inflammatory response in peri-implant inflammatory tissues is an important tool in determining the prognosis and success for the placement of an implant. Various indices, alongside analyzing the depth of periodontal pocket with radiographic analysis, constitute convetionally utilized methods for the detection of peri-implant diseases. Although these can be easily applied, these clinical indices do not have the potential for the assessment of clinical onset as well as progression and destruction of periodontal as well as peri-implant tissues. Hence, considering the clinical placement of dental implants, it is very important to clinically detect any inflammation in its early stages to exclude early morbidity of implant that results in its failure. This causes a high financial burden on both patients as well as on the clinician.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References 
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