Contemporary Clinical Dentistry
   
  Home | About us | Editorial board | Search
Ahead of print | Current Issue | Archives | Advertise
Instructions | Online submission| Contact us | Subscribe |

 

Login  | Users Online: 806  Print this pageEmail this pageSmall font sizeDefault font sizeIncrease font size 



 
 Table of Contents  
REVIEW ARTICLE
Year : 2020  |  Volume : 11  |  Issue : 1  |  Page : 3-9  

Meta-analysis of risk association between interleukin-17a gene polymorphism and chronic periodontitis


1 Department of Periodontics, JKKN Dental College, Namakkal, Tamil Nadu, India
2 Department of Periodontics, Saveetha Dental College, Chennai, Tamil Nadu, India
3 Department of Periodontics, JKKNDCH, Thiruchengodu, Tamil Nadu, India
4 Department of Oral Medicine Andradiology, KSR Institute of Dental Science and Research, Thiruchengodu, Tamil Nadu, India

Date of Submission10-Dec-2019
Date of Decision28-Feb-2020
Date of Acceptance17-Apr-2020
Date of Web Publication13-Jul-2020

Correspondence Address:
Dr. P K Sasikumar
Department of Periodontics, JKKN Dental College and Hospital, Namakkal - 638 183, Tamil Nadu
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ccd.ccd_448_19

Rights and Permissions
   Abstract 


The association of genetic polymorphisms with periodontitis has been studied extensively. The interleukin-7 (IL-17) is a group of cytokines, which comprises six different molecules (IL-17A, B, C, D, E, and F). Among this, IL-17A is the most commonly understood cytokine, and its polymorphism plays a critical role in inflammatory diseases and periodontal inflammation. The present study was aimed at pooling the data available for meta-analysis and to evaluate whether IL-17A (rs2275913) polymorphism is associated with the susceptibility of chronic periodontitis.

Keywords: Chronic periodontitis, ethnicity, interleukin-17A gene, interleukin-17A polymorphism


How to cite this article:
Sasikumar P K, Varghese SS, Kumaran T, Devi SS. Meta-analysis of risk association between interleukin-17a gene polymorphism and chronic periodontitis. Contemp Clin Dent 2020;11:3-9

How to cite this URL:
Sasikumar P K, Varghese SS, Kumaran T, Devi SS. Meta-analysis of risk association between interleukin-17a gene polymorphism and chronic periodontitis. Contemp Clin Dent [serial online] 2020 [cited 2020 Sep 29];11:3-9. Available from: http://www.contempclindent.org/text.asp?2020/11/1/3/289517




   Introduction Top


Periodontitis is a multifactorial disease that affects the supporting structures of teeth, resulting in partial or complete loss of teeth.[1] The microbial organisms present in the plaque and calculus are the most common etiological factors for the initiation of periodontal disease (PD) in particular sites.[2] Other factors such as environmental, anatomical factors, systemic diseases, and genetic background also play a vital role in PDs.[3] The genetic factors that are associated with periodontitis may alter the immunoregulatory mechanism which could modify the pathogenesis of periodontitis.

The association of genetic polymorphisms with periodontitis has been studied extensively.[4],[5],[6],[7] The interleukin-17 (IL-17) is a group of cytokine which comprises six different molecules (IL-17A, B, C, D, E, and F).[8],[9],[10] Among these, IL-17A and F are the most commonly understood cytokine, which plays a critical role in periodontal inflammation. These types of cytokines are released from CD4 + T-helper cells and involved in the central role of inflammation and autoimmune diseases.[11] IL-17A is an initiator of the inflammatory process that induces the fibroblast, macrophages, endothelial, and epithelial cells to produce the proinflammatory mediators.[12] T-cells produce IL-17 that activates many signaling events of innate cytokines such as tumor necrosis factor α and IL-1 β, and thus, it is considered as an important bridging molecule between the adaptive and innate immunity.[13] IL-17 also induces the expression of receptor activator of nuclear factor kappa-B ligand on osteoblasts and stimulates the differentiation and activation of osteoclasts, which can influence the bone resorption mediated by this cells.[14],[15],[16],[17] Many studies have demonstrated the presence of IL-17 in periodontal tissues, gingival crevicular fluid, saliva, and plasma of patients with PD.[18],[19],[20]

The two variations of gene polymorphism (rs227S913 and rs763780) from IL-17 family have been found to be commonly involved in systemic and PDs.[21],[22],[23],[24] The IL-17 polymorphism is also associated with inflammatory diseases such as rheumatoid arthritis, periodontitis, and inflammatory bowel diseases.[25] The individual studies have evaluated and showed the association between IL-17A and F gene polymorphism and the risk of periodontitis. In contrast to this, few studies were evaluated in patients with aggressive and chronic periodontitis based on the population distribution, smoking, nonsmoking status and stated that there was no significant association between the polymorphism (rs2275913 and rs763780) in IL-17A and F genes both in chronic/aggressive periodontitis patients.[26]

Nevertheless, the association of these genetic variations had influenced the molecular expression of IL-17 in PDs. Similarly, the IL-17A polymorphism was highly associated with chronic and aggressive periodontitis when compared with IL-17F polymorphism.[27] The variability of results between different studies of IL-17A polymorphism and periodontitis could be the reason which led to the search for a new literature of IL-17A polymorphism in chronic periodontitis. Therefore, the present study is aimed at pooling the data available for meta-analysis and to evaluate whether IL-17A (rs2275913) polymorphism is associated with the susceptibility of chronic periodontitis.


   Eligibility Criteria Top


Articles evaluating the association of IL-17A polymorphism with chronic periodontitis were included in this meta-analysis based on the recommended Preferred Reporting Items for Systemic Reviews and Meta-analysis Statement.[27] (1) The inclusion criteria were selected in the concept of P-Patient, problem or population, I-Intervention, C-Comparison, control, O-Outcome (PICO). (2) Articles compared the IL-17A polymorphism with or without chronic periodontitis. (3) Studies included were either case control or cohort design. (4) The articles included were based on population studies. (5) Diagnosis of the chronic periodontitis was confirmed through the clinical features and radiographic finding. (6) Studies also include IL-17A genotypic and allelic evaluation in chronic periodontitis. The exclusion criteria are as follows: (1) nonhuman studies, abstract only, reviews or letters, and mechanism studies; (2) family-based design or sibling pair studies; (3) studies with a lack of information; and (4) unpublished articles.


   Literature Search Top


The primary studies that would have met the inclusion criteria were included in this meta-analysis. This sensitive research has been done to retrieve the association between rs2275913 polymorphism in the IL-17A gene with chronic periodontitis articles by trained informed specialists. It gives the unbiased selection of studies based on the search results. We have included the sources which contain the appropriate database and electronic sources such as index journals and conferences to identify published reports. In addition to database searching, we evaluated the reports of eligible studies such as checking references in existing reviews, citation searching, and hand searching. We have also included free-text terms in the title and abstract and any suitable subject indexing in MeSH or EMTREE. The following keywords are used: IL-17A, or IL-17A, IL-17A, polymorphism genetic variation or rs2275913 polymorphism, or-197A/G polymorphism and periodontitis or PDs or chronic periodontitis [Figure 1]. There was a language restriction in the search strategy included in this meta-analysis which published before February 2019.
Figure 1: Selection process of the included publications

Click here to view



   Data Collection Top


Two investigators were involved in this initial appraisal phase and done the review process independently. The rigorous data collection was done at the protocol stage using the structured data collection. The synthesis and the interpretation data were collected with numerical and structured from six literatures. The articles were selected based on a standard protocol, and the data were collected from the published literatures if they met the following criteria: Original data, study assessed the association of IL-17A rs2275913 and the susceptibility to PDs, comparison between patients with chronic periodontitis and controls. The rs2275913 polymorphism was evaluated with genomic and allelic type frequencies according to the Hardy–Weinberg Equilibrium (HWE). We have collected the data for this analysis based on authors, publication data, country, ethnicity, and sample size, as shown in [Table 1]. The quality of each study included in this analysis was assessed by using the periodontal genetic association studies proposed by Nibali (<10 score was excluded).[28]
Table 1: Characteristic of studies included in the quantitative meta-analysis

Click here to view



   Risk of Bias Assessment Top


Before the start of study each and everyone involved in this assessment has been trained to use of the proper method of assessment tools. Two authors independently assessed and allotted six literatures for the final assessment with discussion. We have used ROBIS assessment tool to assess the bias for different statistical results found within the study.[29] The assessment of articles in phase 1 was based on ROBIS, and then, we have matched target questions with meta-analysis review questions (diagnostic test). When the risk of bias assessment details was compared with guideline documents, the whole analysis got the result of “partial match” among the literatures. In the second phase of assessment, we evaluated the bias by using four domains of ROBIS and identified the stage in which the bias was introduced in the review process (whether in study eligibility criteria, Identification of studies, data collection and finding). Finally, we found the answer of “probably yes” through the signaling questions. This depicted that our overall review had low levels of bias during the evaluation. We have made a transparent discussion among the authors completing assessments independently.

Statistical analysis

The statistical analysis of the data was calculated with the roman version 5.3 and STATA, version 11.0 (Stata Corp., Collage Station, TX, USA) the crude odds ratios (ORs) with 95% confidence intervals (CIs) were used to measure the strength of the association between IL-17A rs2275913 and chronic periodontitis. The significance of the pooled OR was measured by using of I2-test, and P < 0.05 was statistically significant. The pooled ORs of IL-17A rs2275913 polymorphism and risk of chronic periodontitis with smokers were evaluated for the codominant model (GA vs. GG and AA vs. GG), the dominant model (GA + AA vs. GG), and recessive model (GA + GG vs. AA) and also assessed for the allelic contrast (A vs. G). The forest plot graph was shown to assess the overall association between the IL-17A rs2275913 polymorphism and risk for chronic periodontitis. The heterogeneity of the studies had been calculated by using Cochrane's Q test and I2 assessment (defined as the ratio of overall variation that existed among study variants). In this study, P < 0.10 and I2 value higher than 50% considered as significant heterogeneity. The random-effect model was used when there is a presence of significant heterogeneity if not present the fixed effect model was selected. Beggers and Eggers, mean regression analysis was applied for publication bias when the P < 0.10.


   Results Top


Study characteristics

In this current meta-analysis, a total of six articles were analyzed. This quantitative analysis included 1172 cases (633 patients diagnosed with chronic periodontitis and 539 patients were controls). Two articles have evaluated both forms of periodontitis.

Chronic periodontitis and aggressive periodontitis and four articles have evaluated the chronic periodontitis with IL-17A polymorphism. Among them, three articles have been analyzed in smokers and non-smokers; none of the studies have stratified the patients by gender. Three articles were composed and studied in a mixed population more specifically in the Brazilian populations. The retrieved articles composed for this meta-analysis were in agreement with HWE.[30] The results showed no significant association between the mutant allele with the risk of chronic periodontitis, as shown in [Figure 1]. The random-effects statistical model was used for the OR calculation due to the high heterogeneity (I2 = 86%, df = 5 [P > 0.00001], overall effect Z = 1.07 [P = 0.28]). In mixed population and smoking status, there was a nonsignificant association between the rs2275913 polymorphism in IL-17A and chronic periodontitis in mutant allelic evaluation (P = 0.60). The IL-17A polymorphism and periodontitis in all allelic and genotypic evaluations, as well as in a stratified analysis by population and smoking status are shown in [Table 2] and [Table 3].
Table 2: Meta-analysis of association between interleukin-17A rs2275913 polymorphism and chronic periodontitis (allelic and genotypic comparisons)

Click here to view
Table 3: Association of interleukin-17A polymorphism and chronic periodontitis (allele and genotype frequency)

Click here to view


However, the overall disparity between the groups for the AA versus GG and GA + AA versus GG genotypes as well as that of the GA + GG versus AA were not associated with the risk of periodontitis (P > 0.05). [Figure 2] showed the forest plot of the risk of chronic periodontitis related to IL-17A 2275913 polymorphism. The fixed effect statistical model was used for the OR calculation. Our pooled evidence showed that none of the IL-17A rs2275913 comparison was associated with the risk of periodontitis and codominant, dominant, and recessive models (P > 0.05).
Figure 2: Forest plot of comparison of mutant allele versus wild type allele in rs2275913 polymorphism and chronic periodontitis

Click here to view


Heterogeneity and sensitivity analysis

There were significant heterogeneities in the information of IL-17A rs 2275913 variations. Because of major heterogeneity across studies, individual studies included in this metaanalysis were omitted consecutively to find out the change of pooled ORs qualitatively. The finding indicated that no individual study influenced the overall OR values for rs2275913 variation [Table 4]. The Beggs and Egger test was done to assess the publication bias. The funnel plot validating results also presented and showed in [Figure 3] with no asymmetry.
Table 4: Association of interleukin-17A polymorphism and chronic periodontitis by using codominant, dominant, and recessive models

Click here to view
Figure 3: A funnel plot for publication bias in allelic evaluation in rs2275913 polymorphism and chronic periodontitis

Click here to view



   Discussion Top


The meta-analysis was carried out to find the association of IL-17A polymorphism with chronic periodontitis. In this analysis, we have retrieved six studies (case-control) which included IL-17A polymorphism with chronic periodontitis in different populations. When considering the forest plot analysis, evaluation of rs 2275913 polymorphism in the IL-17A gene and chronic periodontitis showed no significant association between mutant allele with the risk of chronic periodontitis, as shown in [Figure 1] (OR 1.40, 95% CI 0.76, 2.59, P = 2.59). When compared with the previous meta-analysis, cumulative results showed that the possible association for three studies found and the remaining three studies showed no significant association, as given in [Figure 1]. However, there was some differences in the forest plot graph that consists of no significant association, even though increased P value (P = 0.28) when compared with the previous studies (P = 0.21). Distribution in the forest plot graph showed that two studies are significantly associated with IL-17A polymorphism with chronic periodontitis (CP) on the right side of the graph and three studies had a borderline association and only one study with no association on the left side of the graph.

In this analysis, there was substantial heterogeneity (86%) in the forest plot graph. Because two or more subgroups of studies presented in the data of Saraiva et al.[31] and Borilova et al.,[32] which have a different true effect. Our study also used a random-effects model, and there was no exact way to handle studies with small numbers when assuming random effects. I2 value was also depended on the strength of evidence for heterogeneity. The power of the test depends on the six studies included, the total information available, and the distribution of weights among the different studies. We have shown that the value of the study increases with the total information available rather than the number of studies. The data used in our study were unadjusted which generally recognized as the high potential of bias due to confounding factors. It also included the unadjusted OR from six studies without considering heterogeneity due to covariate adjustment. Even though the risk of bias involving in some individual studies, the results altogether showed no association of IL-17A polymorphism with the risk of chronic periodontitis (I2 = 86%, df = 5 (P > 0.00001), overall effect Z = 1.07 (P = 0.28) [Figure 2].

IL-17A rs 2275913 G/A polymorphism were analyzed by using codominant, dominant, and recessive models. When considering the allelic variants, A versus G showed no significant association with P value of 0.6249. In genotypic variations, GA versus GG consists of a protective factor against CP and all other genetic models (AA vs. GG, GA + AA vs. GG, AA vs. GA + GG) had causative factors against CP, as shown in [Table 4]. The study was done by Saraiva et al. also demonstrated the similar findings of increased frequency of A allele polymorphism in the IL-17A gene in the Brazilian population.[31] Zacarias et al. have shown that rs 2275913 AA genotype and A allele were associated with susceptibility to CP in a Brazilian population.[33] In contrast to our findings, Corrêa et al. indicated that rs2275913 AA genotype and A allele were a protective factor against CP in the Brazilian population.[34]

Considering the ethnicity of subjects, there was an important variable that differs between different ethnic groups. The mixed population of current meta-analysis with allelic (A vs. G, P = 0.58, OR = 0.852, CI = 0.435–1.783) and genotypes (AA vs. GG, GA vs. GG) variation found to be no differences (P = 0.78, OR = 0.653, CI = 0.198–1.192 and P = 0.75, OR = 1.581, CI = 0.905–2.932, respectively) [Table 2] when compared with previous meta-analysis.[25] The Brazilian population has been described, with a high degree of admixture from Amerindians, African, and or European ancestors.[31] Hence, only a few studies were included in this meta-analysis with pooled OR calculation showed limitation, although the results were accurate by the use of fixed-effect model. The highlight of this analysis was the evaluation of heterogeneity and sensitive analysis across the studies and found no individual study has an influence on the overall OR values for rs2275913 variation.

When dealing with methodological/experimental bias, some differences in the periodontal examinations, diagnosis, and severity of diseases were completely not available in the literature. The association of chronic periodontitis and smoking seems to be an important confounding variable, and consequently, the inclusion of smoking and nonsmoking participants can be an additional source of variation. Considering primary studies, three studies included individuals with mixed smoking status, and remaining, three studies selected nonsmoking individuals.[32],[35],[36],[37],[38] The rs2275913 polymorphism in IL-17A with smoking factors evidenced that nonsignificant association with CP when considering of allelic (A vs. G, P = 73 OR = 0.84 CI = 0.48-1.895) and genotypic variations (GA vs. GG, AA vs. GG, P = 0.84, OR = 0.895, CI = 0.198-5.015 and P = 0.89, OR = 1.09, CI = 0.315–4.983, respectively) [Table 2]. These results were supported and agreed with the previous study done by Souto et al. which showed a negative correlation between cigarettes smoked per day and IL-17A level in gingival sample tissues from the smokers of CP.[39]

There are several limitations of the current meta-analysis which includes first, limited number of studies which could be the reason for no significant association found in the pooled OR calculations. Second, the study information in this literature was based on unadjusted analysis and thus we were unable to determine the risk of PDs when considering environmental elements, age, family background, lifestyle or additional risk factors that could be have possible effects on pooled results. Third, the small numbers that were evaluated in the chronic form of periodontitis in this meta-analysis leads to the improper publication bias for rs2275913 polymorphism. Fourth, for the subgroup analysis of ethnicity, the number of each subgroup was very small, and there was not enough statistical power to explore the real association. Fifth, this meta-analysis has done by using the data in published literature, but some important data could be present in the unpublished studies being unable to be included. Sixth, we have not done the protocol registration at the NHIS webpage based on the Cochrane review before the start of the review process.

The results obtained from this study showed no association of IL-17A polymorphism with CP susceptibility. This meta-analysis with six articles in 633 patients diagnosed with CP, 539 control patients; totally, 1172 participants showed a no significant association between the rs 2275913 polymorphism in the IL-17 A with the risk of CP. The results also showed no significance in mixed population and smokers of chronic periodontitis based on allelic evaluation as well as in genomic comparisons. Further studies should assess the association of IL-17A polymorphism in larger samples with different populations by using precise genetic analysis for future perfectives.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Nares S. The genetic relationship to periodontal disease. Periodontol 2000 2003;32:36-49.  Back to cited text no. 1
    
2.
Nishihara T, Koseki T. Microbial etiology of periodontitis. Periodontol 2000 2004;36:14-26.  Back to cited text no. 2
    
3.
Darveau RP. Periodontitis: A polymicrobial disruption of host homeostasis. Nature Rev Microbiol 2010;8:481-90.  Back to cited text no. 3
    
4.
Deng JS, Qin P, Li XX, Du YH. Association between interleukin-1β C (3953/4) T polymorphism and chronic periodontitis: Evidence from a meta-analysis. Hum Immunol 2013;74:371-8.  Back to cited text no. 4
    
5.
Silva FR, Vasconcelos AC, França LF, Nascimento ML, Rodrigues LS, Lenardo D, et al. Relationship between -889 C/T polymorphism in interleukin- 1A gene and chronic periodontitis: Evidence from a meta-analysis with new published findings. Med Oral Patol Oral Cir Bucal 2017;22:e7-14.  Back to cited text no. 5
    
6.
Trevilatto PC, de Souza Pardo AP, Scarel-Caminaga RM, de Brito RB Jr., Alvim-Pereira F, Alvim-Pereira CC, et al. Association of IL1 gene polymorphisms with chronic periodontitis in Brazilians. Arch Oral Biol 2011;56:54-62.  Back to cited text no. 6
    
7.
Kornman KS, Crane A, Wang HY, di Giovine FS, Newman MG, Pirk FW, et al. The interleukin-1 genotype as a severity factor in adult periodontal diseases. J Clin Periodontol 1997;24:72-7.  Back to cited text no. 7
    
8.
Carvalho CN, do Carmo RF, Duarte AL, Carvalho AA, Leão JC, Gueiros LA. IL-17A and IL-17F polymorphisms in rheumatoid arthritis and Sjögren's syndrome. Clin Oral Investig 2016;20:495-502.  Back to cited text no. 8
    
9.
Senhaji N, Serrano A, Badre W, Serbati N, Karkouri M, Zaid Y, et al. Association of inflammatory cytokine gene polymorphisms with inflammatory bowel disease in a Moroccan cohort. Genes Immun 2016;17:60-5.  Back to cited text no. 9
    
10.
Benedetti G, Miossec P. Interleukin 17 contributes to the chronicity of inflammatory diseases such as rheumatoid arthritis. Eur J Immunol 2014;44:339-47.  Back to cited text no. 10
    
11.
Witowski J, Książek K, Jörres A. Interleukin-17: A mediator of inflammatory responses. Cell Mol Life Sci 2004;61:567-79.  Back to cited text no. 11
    
12.
Dong. TH17 cells in development: An updated view of their molecular identity and genetic programming, Nature Reviews Immunology 2008;8:337-48.  Back to cited text no. 12
    
13.
Beklen A, Ainola M, Hukkanen M, Gürgan C, Sorsa T, Konttinen YT. MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis. J Dent Res 2007;86:347-51.  Back to cited text no. 13
    
14.
Allam JP, Duan Y, Heinemann F, Winter J, Götz W, Deschner J, et al. IL-23-producing CD68(+) macrophage-like cells predominate within an IL-17-polarized infiltrate in chronic periodontitis lesions. J Clin Periodontol 2011;38:879-86.  Back to cited text no. 14
    
15.
Moutsopoulos NM, Kling HM, Angelov N, Jin W, Palmer RJ, Nares S, et al. Porphyromonas gingivalis promotes Th17 inducing pathway in chronic periodontitis. J Autoimmun 2012;39:294-303.  Back to cited text no. 15
    
16.
Ajung YJ, Choi YJ, An SJ, Lee HR, Jun HK, Choi BK. Tannerella forshythia GroEl induces inflammatory bone resorption and synergizes with interleukin-17. Mol Oral Microbiol 2017;32:301-13.  Back to cited text no. 16
    
17.
Yu JJ, Ruddy MJ, Wong GC, Sfintescu C, Baker PJ, Smith JB, et al. An essential role for IL-17 in preventing pathogen-initiated bone destruction: Recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 2007;109:3794-802.  Back to cited text no. 17
    
18.
Oda T, Yoshie H, Yamazaki K. Porphyromonas gingivalis antigen preferentially stimulates T cells to express IL-17 but not receptor activator of NF-kappaB ligand In vitro. Oral Microbiol Immunol 2003;18:30-6.  Back to cited text no. 18
    
19.
Vernal R, Dutzan N, Chaparro A, Puente J, Valenzuela MA, Gamonal J. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. J Clin Periodontol 2005;32:383-9.  Back to cited text no. 19
    
20.
Buduneli N, Buduneli E, Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. J Periodontol 2009;80:1274-80.  Back to cited text no. 20
    
21.
Wang L, Jiang Y, Zhang Y, Wang Y, Huang S, Wang Z, et al. Association analysis of IL-17A and IL-17F polymorphisms in Chinese han women with breast cancer. PLoS One 2012;7:e34400.  Back to cited text no. 21
    
22.
Shibata T, Tahara T, Hirata I, Arisawa T. Genetic polymorphism of interleukin-17A and -17F genes in gastric carcinogenesis. Hum Immunol 2009;70:547-51.  Back to cited text no. 22
    
23.
Arisawa T, Tahara T, Shibata T, Nagasaka M, Nakamura M, Kamiya Y, et al. The influence of polymorphisms of interleukin-17 A and interleukin-17 F genes on the susceptibility to ulcerative colitis. J Clin Immunol 2008;28:44-9.  Back to cited text no. 23
    
24.
Kadkhodazadeh M, Baghani Z, Ebadian AR, Youssefi N, Mehdizadeh AR, Azimi N. IL-17 gene polymorphism is associated with chronic periodontitis and peri-implantitis in Iranian patients: A cross-sectional study. Immunol Invest 2013;42:156-63.  Back to cited text no. 24
    
25.
Eskandari-Nasab E, Moghadampour M, Tahmasebi A. Meta-analysis of risk association between interleukin-17A and F gene polymorphisms and inflammatory diseases. J Interferon Cytokine Res 2017;37:165-74.  Back to cited text no. 25
    
26.
da Silva FR, Pessoa LD, Vasconcelos AC, de Aquino Lima W, Alves EH, Vasconcelos DF. Polymorphisms in interleukins 17A and 17F genes and periodontitis: Results from a meta-analysis. Mol Biol Rep 2017;44:443-53.  Back to cited text no. 26
    
27.
Moher D, Liberati A, Tetzlaff J, Altman DG, Grp P. Preferred reporting items for systematic reviews and metaanalyses: The PRISMA statement. Ann Intern Med 2009;89:873-80.  Back to cited text no. 27
    
28.
Nibali L. Suggested guidelines for systematic reviews of periodontal genetic association studies. J Clin Periodontol 2013;40:753-6.  Back to cited text no. 28
    
29.
Whiting P, Savović J, Higgins JP, Caldwell DM, Reeves BC, Shea B, et al. ROBIS: A new tool to assess risk of bias in systematic reviews was develop. J Clin Epidemiol 2015;69:225-34.  Back to cited text no. 29
    
30.
Munafò MR, Flint J. Meta-analysis of genetic association studies. Trends Genet 2004;20:439-44.  Back to cited text no. 30
    
31.
Saraiva AM, Alves e Silva MR, Correia-Silva JF, Costa JE, Collob KJ, Dutra WO, et al. Evaluation of IL17A expression and of IL17A, IL17F and IL23R gene polymorphisms in Brazilian individuals with periodontitis. Hum Immunol 2013;74:207-14.  Back to cited text no. 31
    
32.
Borilova L, Inhartova P, Kastovsky J, Lucanova S, Bartova J, Poskerova H, Vokurka J, et al. Interleukin-17A gene variability in patients with type 1 diabetes mellitus and chronic periodontitis: Its correlation with IL-17 levels and the occurrence of periodontopathic bacteria. Mediators Inflamm 2016;2016:2979846.  Back to cited text no. 32
    
33.
Zacarias JM, Sippert EÂ, Tsuneto PY, Visentainer JE, Silva CO, Sell AM. The influence of interleukin 17A and IL17F polymorphisms on chronic periodontitis disease in Brazilian patients. Mediators Inflamm 2015;2015:147056.  Back to cited text no. 33
    
34.
Corrêa JD, Madeira MF, Resende RG, Correia-Silva JF, Gomez RS, Souza DG, et al. Association between polymorphisms in interleukin-17A and -17F genes and chronic periodontal disease. Mediators Inflamm 2012;1-9 pages:846052.  Back to cited text no. 34
    
35.
Chaudhari HL, Warad S, Ashok N, Baroudi K, Tarakji B. Association of Interleukin-17 polymorphism (-197G/A) in chronic and localized aggressive periodontitis. Braz Oral Res 2016;30:1-7.  Back to cited text no. 35
    
36.
Jain N, Joseph R, Balan S, Arun R, Banerjee M. Association of interleukin-4 and interleukin-17F polymorphisms in periodontitis in Dravidian ethnicity. Indian J Hum Genet 2013;19:58-64.  Back to cited text no. 36
[PUBMED]  [Full text]  
37.
Erdemir E, Hendek M, Kocakap D, Ozkan S. Interleukin (IL)-17F (H161R) and IL-23R (R381Q) gene polymorphisms in Turkish population with periodontitis. J Res Med Dent Sci 2015;3:104-8.  Back to cited text no. 37
    
38.
Vahabi S, Nazemisalman B. Interleukin-2,16, and17gene- polymorphismsinIranian patients with chronic periodontitis. J Invest Clin Dent 2018;1-6 pages:e12319.  Back to cited text no. 38
    
39.
Lampiasi N, Montana G. Corrigendum to “An In vitro inflammation model to study the Nrf2 and NF-κB crosstalk in presence of ferulic acid as modulator” doi: 10.1016/j.imbio. 2017.10.046 [Immunobiology (2018) Vol 223; 349-355]. Immunobiology 2018;223:598.  Back to cited text no. 39
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
   Eligibility Criteria
   Literature Search
   Data Collection
    Risk of Bias Ass...
   Results
   Discussion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed548    
    Printed34    
    Emailed0    
    PDF Downloaded56    
    Comments [Add]    

Recommend this journal