Biomarkers for diagnosis of stage III, grade C with molar incisor pattern periodontitis in children and young adults: a systematic review and meta-analysis.
Aggressive
GCF
Interleukins
Juvenile
MMP
Molecular biomarkers
Periodontitis
Peripheral blood
Saliva
Serum
Stage III grade C
Journal
Clinical oral investigations
ISSN: 1436-3771
Titre abrégé: Clin Oral Investig
Pays: Germany
ID NLM: 9707115
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
received:
01
03
2023
accepted:
13
07
2023
medline:
11
9
2023
pubmed:
3
8
2023
entrez:
3
8
2023
Statut:
ppublish
Résumé
To explore the existing salivary, gingival crevicular fluid (GCF), blood, and serum biomarkers associated with grade C molar-incisor pattern (C/MIP) periodontitis in systemically healthy children and young adults. Cross-sectional, case-control, and cohort studies on stage III grade C periodontitis or former equivalent diagnosis with analysis of molecular biomarkers in saliva, GCF, blood, or serum were retrieved from six databases and screened based on the eligibility criteria. The risk of bias in included studies was evaluated. Meta-analysis was planned for biomarkers assessed using the same detection methods and sample type in at least two papers. Out of 5621 studies identified at initial screening, 28 papers were included in the qualitative analysis of which 2 were eligible for meta-analysis for IgG in serum samples. Eighty-seven biomarkers were assessed with the majority being higher in cases than in controls. Only the meta-analysis of total serum IgG with low heterogeneity value revealed a significant increase in its levels in C/MIPs compared to controls (standardised mean difference: 1.08; 95% CI: 0.76, 1.40). There is a paucity of data on biomarkers associated with molar-incisor pattern periodontitis. Although serum IgG levels are raised, other more specific biomarkers in saliva, GCF, and blood/serum may be promising but require further investigation.
Identifiants
pubmed: 37535199
doi: 10.1007/s00784-023-05169-x
pii: 10.1007/s00784-023-05169-x
pmc: PMC10492694
doi:
Substances chimiques
Biomarkers
0
Immunoglobulin G
0
Types de publication
Meta-Analysis
Systematic Review
Journal Article
Review
Langues
eng
Pagination
4929-4955Informations de copyright
© 2023. The Author(s).
Références
Wara-aswapati N, Howell TH, Needleman HL, Karimbux N (1999) Periodontitis in the child and adolescent. ASDC J Dent Child 66(167–74):154
pubmed: 10476354
Zhang L, Henson BS (2000) Camargo PM and Wong DT (2009) The clinical value of salivary biomarkers for periodontal disease. Periodontol 51:25–37. https://doi.org/10.1111/j.1600-0757.2009.00315.x
doi: 10.1111/j.1600-0757.2009.00315.x
Velsko IM, Harrison P, Chalmers N, Barb J, Huang H, Aukhil I, Shaddox L (2020) Grade C molar-incisor pattern periodontitis subgingival microbial profile before and after treatment. J Oral Microbiol 12:1814674. https://doi.org/10.1080/20002297.2020.1814674
doi: 10.1080/20002297.2020.1814674
pubmed: 33062199
pmcid: 7534306
Shaddox LM, Huang H, Lin T, Hou W, Harrison PL, Aukhil I, Walker CB, Klepac-Ceraj V, Paster BJ (2012) Microbiological characterization in children with aggressive periodontitis. J Dent Res 91:927–933. https://doi.org/10.1177/0022034512456039
doi: 10.1177/0022034512456039
pubmed: 22863892
pmcid: 3446830
Meusel DR, Ramacciato JC, Motta RH, Brito Júnior RB, Flório FM (2015) Impact of the severity of chronic periodontal disease on quality of life. J Oral Sci 57:87–94. https://doi.org/10.2334/josnusd.57.87
doi: 10.2334/josnusd.57.87
pubmed: 26062856
Allin N, Cruz-Almeida Y, Velsko I, Vovk A, Hovemcamp N, Harrison P, Huang H, Aukhil I, Wallet SM, Shaddox LM (2016) Inflammatory response influences treatment of localized aggressive periodontitis. J Dent Res 95:635–641. https://doi.org/10.1177/0022034516631973
doi: 10.1177/0022034516631973
pubmed: 26917438
pmcid: 4924542
Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, Greenwell H, Herrera D, Kao RT, Kebschull M, Kinane DF, Kirkwood KL, Kocher T, Kornman KS, Kumar PS, Loos BG, Machtei E, Meng H, Mombelli A, Needleman I, Offenbacher S, Seymour GJ, Teles R, Tonetti MS (2018) Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 45(Suppl 20):S162-s170. https://doi.org/10.1111/jcpe.12946
doi: 10.1111/jcpe.12946
pubmed: 29926490
Yoshida A, Bouziane A, Erraji S, Lakhdar L, Rhissassi M, Miyazaki H, Ansai T, Iwasaki M, Ennibi O (2021) Etiology of aggressive periodontitis in individuals of African descent. Jpn Dent Sci Rev 57:20–26. https://doi.org/10.1016/j.jdsr.2020.12.001
doi: 10.1016/j.jdsr.2020.12.001
pubmed: 33737991
pmcid: 7946349
Albandar JM (2000) (2014) Aggressive periodontitis: case definition and diagnostic criteria. Periodontol 65:13–26. https://doi.org/10.1111/prd.12014
doi: 10.1111/prd.12014
Miller K, Treloar T, Guelmann M, Rody WJ, Jr. and Shaddox LM (2018) Clinical characteristics of localized aggressive periodontitis in primary dentition. J Clin Pediatr Dent 42:95–102. https://doi.org/10.17796/1053-4628-42.2.3
Llanos AH, Silva CGB, Ichimura KT, Rebeis ES, Giudicissi M, Romano MM, Saraiva L (2018) Impact of aggressive periodontitis and chronic periodontitis on oral health-related quality of life. Braz Oral Res 32:e006. https://doi.org/10.1590/1807-3107bor-2018.vol32.0006
doi: 10.1590/1807-3107bor-2018.vol32.0006
pubmed: 29451591
Prakasam A, Elavarasu SS, Natarajan RK (2012) Antibiotics in the management of aggressive periodontitis. J Pharm Bioallied Sci 4:S252–S255. https://doi.org/10.4103/0975-7406.100226
doi: 10.4103/0975-7406.100226
pubmed: 23066264
pmcid: 3467876
Saygun I, Nizam N, Keskiner I, Bal V, Kubar A, Açıkel C, Serdar M, Slots J (2011) Salivary infectious agents and periodontal disease status. J Periodontal Res 46:235–239. https://doi.org/10.1111/j.1600-0765.2010.01335.x
doi: 10.1111/j.1600-0765.2010.01335.x
pubmed: 21261620
Mishra S, Gazala MP, Rahman W (2022) Clinical and diagnostic significance of blood leukocyte ratios in young patients with stage III grade C periodontitis. Acta Odontol Scand 80:161–168. https://doi.org/10.1080/00016357.2021.1969035
doi: 10.1080/00016357.2021.1969035
pubmed: 34436974
Patil PB, Patil BR (2011) Saliva: a diagnostic biomarker of periodontal diseases. J Indian Soc Periodontol 15:310–317. https://doi.org/10.4103/0972-124x.92560
doi: 10.4103/0972-124x.92560
pubmed: 22368352
pmcid: 3283925
Arias-Bujanda N, Regueira-Iglesias A, Balsa-Castro C, Nibali L, Donos N, Tomás I (2020) Accuracy of single molecular biomarkers in saliva for the diagnosis of periodontitis: a systematic review and meta-analysis. J Clin Periodontol 47:2–18. https://doi.org/10.1111/jcpe.13202
doi: 10.1111/jcpe.13202
pubmed: 31560804
Fatima T, Khurshid Z, Rehman A, Imran E, Srivastava KC, Shrivastava D (2021) Gingival crevicular fluid (GCF): a diagnostic tool for the detection of periodontal Health and diseases. Molecules 26. https://doi.org/10.3390/molecules26051208
Giannobile WV, Beikler T, Kinney JS, Ramseier CA (2000) Morelli T and Wong DT (2009) Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 50:52–64. https://doi.org/10.1111/j.1600-0757.2008.00288.x
doi: 10.1111/j.1600-0757.2008.00288.x
Subbarao KC, Nattuthurai GS, Sundararajan SK, Sujith I, Joseph J, Syedshah YP (2019) Gingival crevicular fluid: an overview. J Pharm Bioallied Sci 11:S135-s139. https://doi.org/10.4103/jpbs.Jpbs_56_19
doi: 10.4103/jpbs.Jpbs_56_19
pubmed: 31198325
pmcid: 6555362
de Lima CL, Acevedo AC, Grisi DC, Taba M Jr, Guerra E, De Luca CG (2016) Host-derived salivary biomarkers in diagnosing periodontal disease: systematic review and meta-analysis. J Clin Periodontol 43:492–502. https://doi.org/10.1111/jcpe.12538
doi: 10.1111/jcpe.12538
pubmed: 26926312
Schenkein HA, Koertge TE, Brooks CN, Sabatini R, Purkall DE, Tew JG (2010) IL-17 in sera from patients with aggressive periodontitis. J Dent Res 89:943–947. https://doi.org/10.1177/0022034510369297
doi: 10.1177/0022034510369297
pubmed: 20400718
pmcid: 3144093
Stefaniuk P, Szymczyk A, Podhorecka M (2020) The neutrophil to lymphocyte and lymphocyte to monocyte ratios as new prognostic factors in hematological malignancies - a narrative review. Cancer Manag Res 12:2961–2977. https://doi.org/10.2147/cmar.S245928
doi: 10.2147/cmar.S245928
pubmed: 32425606
pmcid: 7196794
Wang H, Luo Z, Lei L, Sun Z, Zhou M, Dan H, Zeng X, Chen Q (2013) Interaction between oral lichen planus and chronic periodontitis with Th17-associated cytokines in serum. Inflammation 36:696–704. https://doi.org/10.1007/s10753-013-9594-2
doi: 10.1007/s10753-013-9594-2
pubmed: 23338155
Andreu R, Santos-Del-Riego S and Payri F (2021) Serum inflammatory and prooxidant marker levels in different periodontal disease stages. Healthcare (Basel) 9. https://doi.org/10.3390/healthcare9081070
Machado V, Botelho J, Escalda C, Hussain SB, Luthra S, Mascarenhas P, Orlandi M, Mendes JJ, D’Aiuto F (2021) Serum C-reactive protein and periodontitis: a systematic review and meta-analysis. Front Immunol 12:706432. https://doi.org/10.3389/fimmu.2021.706432
doi: 10.3389/fimmu.2021.706432
pubmed: 34394107
pmcid: 8355591
Bramer WM, Giustini D, de Jonge GB, Holland L, Bekhuis T (2016) De-duplication of database search results for systematic reviews in EndNote. J Med Libr Assoc 104:240–243. https://doi.org/10.3163/1536-5050.104.3.014
doi: 10.3163/1536-5050.104.3.014
pubmed: 27366130
pmcid: 4915647
Shaddox LM, Wiedey J, Calderon NL, Magnusson I, Bimstein E, Bidwell JA, Zapert EF, Aukhil I, Wallet SM (2011) Local inflammatory markers and systemic endotoxin in aggressive periodontitis. J Dent Res 90:1140–1144. https://doi.org/10.1177/0022034511413928
doi: 10.1177/0022034511413928
pubmed: 21730256
pmcid: 3169885
Albandar JM, DeNardin AM, Adesanya MR, Diehl SR, Winn DM (2001) Associations between serum antibody levels to periodontal pathogens and early-onset periodontitis. J Periodontol 72:1463–1469. https://doi.org/10.1902/jop.2001.72.11.1463
doi: 10.1902/jop.2001.72.11.1463
pubmed: 11759856
Ebert MHaPCaTFaDD (2019) dmetar: companion R package for the guide ‘doing meta-analysis in R’. http://dmetar.protectlab.org/ . Accessed Acces Date
Balduzzi S, Rücker G, Schwarzer G (2019) How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health 22:153–160. https://doi.org/10.1136/ebmental-2019-300117
doi: 10.1136/ebmental-2019-300117
pubmed: 31563865
Viechtbauer W (2005) Bias and efficiency of meta-analytic variance estimators in the random-effects model. J Educ Behav Stat 30:261–293. https://doi.org/10.3102/10769986030003261
doi: 10.3102/10769986030003261
Acquier AB, De Couto Pita AK, Busch L, Sanchez GA (2017) Parameters of oxidative stress in saliva from patients with aggressive and chronic periodontitis. Redox Rep:Commun Free Radic Res 22:119–126. https://doi.org/10.1080/13510002.2016.1198104
doi: 10.1080/13510002.2016.1198104
Acquier AB, Pita AKDC, Busch L, Sanchez GA (2015) Comparison of salivary levels of mucin and amylase and their relation with clinical parameters obtained from patients with aggressive and chronic periodontal disease. J Appl Oral Sci: revista FOB 23:288–294. https://doi.org/10.1590/1678-775720140458
doi: 10.1590/1678-775720140458
pubmed: 26221923
pmcid: 4510663
Akalin FA, Bulut S, Yavuzyilmaz E (1993) Beta 2-microglobulin levels in serum and saliva of patients with juvenile periodontitis. J Nihon Univ Sch Dent 35:230–234. https://doi.org/10.2334/josnusd1959.35.230
doi: 10.2334/josnusd1959.35.230
pubmed: 8158282
Fine DH, Furgang D, McKiernan M, Rubin M (2013) Can salivary activity predict periodontal breakdown in A. actinomycetemcomitans infected adolescents? Arch Oral Biol 58:611–620. https://doi.org/10.1016/j.archoralbio.2012.10.009
doi: 10.1016/j.archoralbio.2012.10.009
pubmed: 23219180
Lehner T, Wilton JM, Ivanyi L, Manson JD (1974) Immunological aspects of juvenile periodontitis (periodontosis). J Periodontal Res 9:261–272
doi: 10.1111/j.1600-0765.1974.tb00681.x
pubmed: 4281821
Albandar JM, Kingman A, Lamster IB (1998) Crevicular fluid level of beta-glucuronidase in relation to clinical periodontal parameters and putative periodontal pathogens in early-onset periodontitis. J Clin Periodontol 25:630–639
doi: 10.1111/j.1600-051X.1998.tb02499.x
pubmed: 9722267
Alfant B, Shaddox LM, Tobler J, Magnusson I, Aukhil I, Walker C (2008) Matrix metalloproteinase levels in children with aggressive periodontitis. J Periodontol 79:819–826. https://doi.org/10.1902/jop.2008.070513
doi: 10.1902/jop.2008.070513
pubmed: 18454660
Bartova J, Krejsa O, Sirova M, Tlaskalova H, Prochazkova J, Duskova J (1995) Local antibodies and cytokine responses in crevicular fluid of patients with juvenile periodontitis. Adv Exp Med Biol 371B:1109–1112
pubmed: 7502763
Branco-de-Almeida LS, Cruz-Almeida Y, Gonzalez-Marrero Y, Kudsi R, de Oliveira ICV, Dolia B, Huang H, Aukhil I, Harrison P, Shaddox LM (2021) Treatment of localized aggressive periodontitis alters local host immunoinflammatory profiles: a long-term evaluation. J Clin Periodontol 48:237–248. https://doi.org/10.1111/jcpe.13404
doi: 10.1111/jcpe.13404
pubmed: 33205510
Friedman SA, Mandel ID, Herrera MS (1983) Lysozyme and lactoferrin quantitation in the crevicular fluid. J Periodontol 54:347–350
doi: 10.1902/jop.1983.54.6.347
pubmed: 6348246
Goncalves PF, Huang H, McAninley S, Alfant B, Harrison P, Aukhil I, Walker C, Shaddox LM (2013) Periodontal treatment reduces matrix metalloproteinase levels in localized aggressive periodontitis. J Periodontol 84:1801–1808. https://doi.org/10.1902/jop.2013.130002
doi: 10.1902/jop.2013.130002
pubmed: 23537121
pmcid: 4418528
Monteiro MF, Casati MZ, Sallum EA, Silverio KG, Nociti-Jr FH, Casarin RCV (2022) The familial trend of the local inflammatory response in periodontal disease. Oral Dis 28:202–209. https://doi.org/10.1111/odi.13738
doi: 10.1111/odi.13738
pubmed: 33252790
Celenligil H, Ebersole JL (1998) Analysis of serum antibody responses to periodontopathogens in early-onset periodontitis patients from different geographical locations. J Clin Periodontol 25:994–1002
doi: 10.1111/j.1600-051X.1998.tb02404.x
pubmed: 9869349
Sandholm L, Saxen L (1983) Concentrations of serum protease inhibitors and immunoglobulins in juvenile periodontitis. J Periodontal Res 18:527–533
doi: 10.1111/j.1600-0765.1983.tb00389.x
pubmed: 6196474
Sjodin B, Arnrup K, Matsson L, Wranne L, Carlsson J, Hanstrom L (1995) Periodontal and systemic findings in children with marginal bone loss in the primary dentition. J Clin Periodontol 22:214–224
doi: 10.1111/j.1600-051X.1995.tb00137.x
pubmed: 7790527
Kalash D, Vovk A, Huang H, Aukhil I, Wallet SM, Shaddox LM (2015) Influence of periodontal therapy on systemic lipopolysaccharides in children with localized aggressive periodontitis. Pediatr Dent 37:35–40
pubmed: 26531074
pmcid: 4634009
Zafiropoulos GG, Eldanassouri N, Flores-de-Jacoby L, Havemann K (1987) Determination of the ELP (elastase-like proteinase) plasma levels in patients with rapidly advancing and with juvenile periodontitis. Deutsche zahnarztliche Zeitschrift 42:1056–1060
pubmed: 3502646
Albandar JM, DeNardin AM, Adesanya MR, Winn DM, Diehl SR (2002) Associations of serum concentrations of IgG, IgA, IgM and interleukin-1beta with early-onset periodontitis classification and race. J Clin Periodontol 29:421–426
doi: 10.1034/j.1600-051X.2002.290506.x
pubmed: 12060424
Anil S, Remani P, Ankathil R, Vijayakumar T (1990) Circulating immune complexes in localised juvenile periodontitis. Singapore Dent J 15:17–19
pubmed: 2097723
Dibart S, Eftimiadi C, Socransky S, Taubman MA, Van Dyke TE (1998) Rapid evaluation of serum and gingival crevicular fluid immunoglobulin G subclass antibody levels in patients with early-onset periodontitis using checkerboard immunoblotting. Oral Microbiol Immunol 13:166–172
doi: 10.1111/j.1399-302X.1998.tb00728.x
pubmed: 10093531
Johnson RJ, Matthews JL, Stone MJ, Hurt WC, Newman JT (1980) Immunopathology of periodontal disease. I. Immunologic profiles in periodontitis and juvenile periodontitis. J Periodontol 51:705–712. https://doi.org/10.1902/jop.1980.51.12.705
doi: 10.1902/jop.1980.51.12.705
pubmed: 7009823
Schenck K, Porter SR, Tollefsen T, Johansen JR, Scully C (1989) Serum levels of antibodies against Actinobacillus actinomycetemcomitans in various forms of human periodontitis. Acta Odontol Scand 47:271–277
doi: 10.3109/00016358909007712
pubmed: 2589029
Spindler SJ, Thompson JJ, Yukna RA, Costales AD (1986) Juvenile periodontitis. I. Demonstration of local immunoglobulin synthesis. J Periodontol 57:300–304
doi: 10.1902/jop.1986.57.5.300
pubmed: 3457943
Unsal BT, Ozcan G, Balos K, Mevsim G (1996) Serum antibodies to Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in juvenile periodontitis and adult periodontitis (part I). J Marmara Univ Dent Fac 2:470–473
pubmed: 9569800
Kulshrestha D, Siddeshappa S, Biswas J (2013) Role of immunoglobulin G and A in periodontitis: a review. Jof Pure Appl Microbiol 70:673–676
Nibali L (2015) Aggressive periodontitis: microbes and host response, who to blame? Virulence 6:223–228. https://doi.org/10.4161/21505594.2014.986407
doi: 10.4161/21505594.2014.986407
pubmed: 25654663
pmcid: 4601283
Kantarci A, Oyaizu K, Van Dyke TE (2003) Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. J Periodontol 74:66–75. https://doi.org/10.1902/jop.2003.74.1.66
doi: 10.1902/jop.2003.74.1.66
pubmed: 12593599
Bhansali RS, Yeltiwar RK, Bhat K (2017) Evaluation of peripheral neutrophil functions in aggressive periodontitis patients and their family members in Indian population: an assessment of neutrophil chemotaxis, phagocytosis, and microbicidal activity. J Indian Soc Periodontol 21:449–455. https://doi.org/10.4103/jisp.jisp_107_17
doi: 10.4103/jisp.jisp_107_17
pubmed: 29551862
pmcid: 5846240
Meng H, Xu L, Li Q (2000) Han J and Zhao Y (2007) Determinants of host susceptibility in aggressive periodontitis. Periodontol 43:133–159. https://doi.org/10.1111/j.1600-0757.2006.00204.x
doi: 10.1111/j.1600-0757.2006.00204.x
Kornman KS (2008) Mapping the pathogenesis of periodontitis: a new look. J Periodontol 79:1560–1568. https://doi.org/10.1902/jop.2008.080213
doi: 10.1902/jop.2008.080213
pubmed: 18673011
Niklaus Lang PMB, Cullinan M, Jeffcoat M, Mombelli A, Murakami S, Page R, Papapanou P, Tonetti M, Van Dyke T (1999) Consensus report: aggressive periodontitis. Ann Periodontol 4:53
doi: 10.1902/annals.1999.4.1.53
Mani A, James R, Mani S (2018) Etiology and pathogenesis of aggressive periodontitis: a mini review. Galore Int J Health Sci Res 3(2):4–8
Lertpimonchai A, Rattanasiri S, Arj-Ong Vallibhakara S, Attia J, Thakkinstian A (2017) The association between oral hygiene and periodontitis: a systematic review and meta-analysis. Int Dent J 67:332–343. https://doi.org/10.1111/idj.12317
doi: 10.1111/idj.12317
pubmed: 28646499
Ji S, Choi Y (2015) Point-of-care diagnosis of periodontitis using saliva: technically feasible but still a challenge. Front Cell Infect Microbiol 5:65. https://doi.org/10.3389/fcimb.2015.00065
doi: 10.3389/fcimb.2015.00065
pubmed: 26389079
pmcid: 4558535
Trombelli L, Scapoli C, Tatakis DN, Minenna L (2006) Modulation of clinical expression of plaque-induced gingivitis: response in aggressive periodontitis subjects. J Clin Periodontol 33:79–85. https://doi.org/10.1111/j.1600-051X.2005.00873.x
doi: 10.1111/j.1600-051X.2005.00873.x
pubmed: 16441729
Bhuyan R, Bhuyan SK, Mohanty JN, Das S, Juliana N and Juliana IF (2022) Periodontitis and its inflammatory changes linked to various systemic diseases: a review of its underlying mechanisms. Biomedicines 10. https://doi.org/10.3390/biomedicines10102659
Cafiero C, Spagnuolo G, Marenzi G, Martuscelli R, Colamaio M and Leuci S (2021) Predictive periodontitis: the most promising salivary biomarkers for early diagnosis of periodontitis. J Clin Med 10. https://doi.org/10.3390/jcm10071488
Gupta S, Chhina S, Arora SA (2018) A systematic review of biomarkers of gingival crevicular fluid: their predictive role in diagnosis of periodontal disease status. J Oral Biol Craniofac Res 8:98–104. https://doi.org/10.1016/j.jobcr.2018.02.002
doi: 10.1016/j.jobcr.2018.02.002
pubmed: 29892530
pmcid: 5993463
Gupta M, Chaturvedi R, Jain A (2013) Role of monocyte chemoattractant protein-1 (MCP-1) as an immune-diagnostic biomarker in the pathogenesis of chronic periodontal disease. Cytokine 61:892–897. https://doi.org/10.1016/j.cyto.2012.12.012
doi: 10.1016/j.cyto.2012.12.012
pubmed: 23375122
Syed S, Kankara VR, Pathakota KR, Krishnan P, Mishra A (2020) Evaluation of deoxypyridinoline levels in gingival crevicular fluid and serum as alveolar bone loss biomarker in patients with periodontitis. J Indian Soc Periodontol 24:322–328. https://doi.org/10.4103/jisp.jisp_256_19
doi: 10.4103/jisp.jisp_256_19
pubmed: 32831504
pmcid: 7418550
Almășan O, Leucuța DC and Hedeșiu M (2022) Blood cell count inflammatory markers as prognostic indicators of periodontitis: a systematic review and meta-analysis. J Pers Med 12. https://doi.org/10.3390/jpm12060992
Akram Z, Rahim ZH, Taiyeb-Ali TB, Shahdan MS, Baharuddin NA, Vaithilingam RD, Safii SH (2017) Resistin as potential biomarker for chronic periodontitis: a systematic review and meta-analysis. Arch Oral Biol 73:311–320. https://doi.org/10.1016/j.archoralbio.2016.08.016
doi: 10.1016/j.archoralbio.2016.08.016
pubmed: 27567495
Pradeep AR, Manjunath RG, Kathariya R (2010) Progressive periodontal disease has a simultaneous incremental elevation of gingival crevicular fluid and serum CRP levels. J Investig Clin Dent 1:133–138. https://doi.org/10.1111/j.2041-1626.2010.00022.x
doi: 10.1111/j.2041-1626.2010.00022.x
pubmed: 25427270
Türer ÇC, Balli U, Güven B, Çetinkaya B, Keleş G (2016) Visfatin levels in gingival crevicular fluid and serum before and after non-surgical treatment for periodontal diseases. J Oral Sci 58:491–499. https://doi.org/10.2334/josnusd.16-0116
doi: 10.2334/josnusd.16-0116
pubmed: 28025432
Thorat M, Pradeep AR, Garg G (2010) Correlation of levels of oncostatin M cytokine in crevicular fluid and serum in periodontal disease. Int J Oral Sci 2:198–207. https://doi.org/10.4248/ijos10077
doi: 10.4248/ijos10077
pubmed: 21404969
pmcid: 3499000
Aldahlawi S, Youssef AR, Shahabuddin S (2018) Evaluation of chemokine CXCL10 in human gingival crevicular fluid, saliva, and serum as periodontitis biomarker. J Inflamm Res 11:389–396. https://doi.org/10.2147/jir.S177188
doi: 10.2147/jir.S177188
pubmed: 30464571
pmcid: 6216963
Tabeta K, Hosojima M, Nakajima M, Miyauchi S, Miyazawa H, Takahashi N, Matsuda Y, Sugita N, Komatsu Y, Sato K, Ishikawa T, Akiishi K, Yamazaki K, Kato K, Saito A, Yoshie H (2018) Increased serum PCSK9, a potential biomarker to screen for periodontitis, and decreased total bilirubin associated with probing depth in a Japanese community survey. J Periodontal Res 53:446–456. https://doi.org/10.1111/jre.12533
doi: 10.1111/jre.12533
pubmed: 29516504
Konopka T, Król K, Kopeć W, Gerber H (2007) Total antioxidant status and 8-hydroxy-2’-deoxyguanosine levels in gingival and peripheral blood of periodontitis patients. Arch Immunol Ther Exp (Warsz) 55:417–422. https://doi.org/10.1007/s00005-007-0047-1
doi: 10.1007/s00005-007-0047-1
pubmed: 18060366
Botelho J, Machado V, Hussain SB, Zehra SA, Proença L, Orlandi M, Mendes JJ, D’Aiuto F (2021) Periodontitis and circulating blood cell profiles: a systematic review and meta-analysis. Exp Hematol 93:1–13. https://doi.org/10.1016/j.exphem.2020.10.001
doi: 10.1016/j.exphem.2020.10.001
pubmed: 33068648
Celenligil H, Kansu E, Eratalay K (1990) Juvenile and rapidly progressive periodontitis. Peripheral blood lymphocyte subpopulations. J Clin Periodontol 17:207–210
doi: 10.1111/j.1600-051X.1990.tb00014.x
pubmed: 1693384
Tavakoli TT, Gholami F, Huang H, Gonçalves PF, Villasante-Tezanos A, Aukhil I, de Oliveira RCG, Hovencamp N, Wallet S, Ioannidou E, Shaddox LM (2022) Gender differences in immunological response of African-American juveniles with grade C molar incisor pattern periodontitis. J Periodontol 93:392–402. https://doi.org/10.1002/jper.21-0143
doi: 10.1002/jper.21-0143
pubmed: 34173226