Narrative Review of Biomarkers in Patients with Peri-implantitis
Narrative Review of Biomarkers in Patients with Peri-implantitis
Keywords:
biomarkers, peri-implantitis, inflammatory diseaseAbstract
Background: Peri-implantitis is caused by the breakdown of homeostasis between the host's response to microbial pathogens. The aim of this study was to assess clinical studies by use of a systematic review on some mouth biomarkers except of interleukin, active metalloproteinase (MMP) and TNF-α in peri-implantitis patients. Materials and Methods: A regular and complete search was conducted through mesh keywords by search of the Science Direct, PubMed, Google Scholar database until August 6, 2024. Those articles that reported biomarkers other than interleukin, active metalloproteinase (MMP) and TNF-α were included in this review. The outcome was defined to be peri-implantitis. Two reviewers have searched and screened the articles completely independently of each other. For assessing the quality of the studies, risk of bias tool developed by Downes et al. were used. Results: In general, 41 articles were found for this review. Based on our findings, key markers include Neutrophil extracellular traps (NETs), proinflammatory cytokines, oxidative stress markers, salivary biomarkers, microRNAs, extracellular vesicles, proteomic and metabolomic changes, and microbial markers. Stress markers like cortisol also play a role. Risk of bias is low in most studies. Conclusion: Biomarkers found in this study suggest a complex cascade of events involved in pathophysiological pathway of peri-implantitis including the microbial colonization, immune activation, bone resorption, oxidative stress, vascular changes, stress responses, and epigenetic modifications
References
Turkmen M, Firatli E. The study of genetic predisposition on periodontitis and peri-implantitis. Nigerian Journal of Clinical Practice. 2022;25(11):1799-804.
https://doi.org/10.4103/njcp.njcp_19_22
PMid:36412285
Lumbikananda S, Srithanyarat SS, Mattheos N, Osathanon T. Oral Fluid Biomarkers for Peri-Implantitis: A Scoping Review. International Dental Journal. 2024;74(3):387-402.
https://doi.org/10.1016/j.identj.2023.11.005
PMid:38065782 PMCid:PMC11123564
Badea FC, Caraiane A, Balaban DP, Grigorian M, Bordeianu I. Interleukin-1β and interleukin-6 in peri-implant crevicular fluid and relationship with peri-implantitis . Arch Balk Med Union. 2017;52(1):15-21.
Farnoosh R, Navid T, Saba M. Peri-Implantitis Treatment Modalities: A Review. Journal of Craniomaxillofacial Research. 2024;10(4):136-45.
Pliavga V, Peceliunaite G, Daugela P, Leketas M, Gervickas A, Juodzbalys G. Peri-implantitis Diagnosis and Prognosis Using Biomarkers: A Systematic Literature Review. Int J Oral Maxillofac Implants. 2023;38(6):1095-105.
https://doi.org/10.11607/jomi.10353
PMid:38085740
Delucchi F, Canepa C, Canullo L, Pesce P, Isola G, Menini M. Biomarkers from Peri-Implant Crevicular Fluid (PICF) as Predictors of Peri-Implant Bone Loss: A Systematic Review. International Journal of Molecular Sciences. 2023;24(4):3202.
https://doi.org/10.3390/ijms24043202
PMid:36834613 PMCid:PMC9966862
Cafiero C, Spagnuolo G, Marenzi G, Martuscelli R, Colamaio M, Leuci S. Predictive Periodontitis: The Most Promising Salivary Biomarkers for Early Diagnosis of Periodontitis. J Clin Med. 2021;10(7):1488.
https://doi.org/10.3390/jcm10071488
PMid:33916672 PMCid:PMC8038382
Downes MJ, Brennan ML, Williams HC, Dean RS. Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open. 2016;6(12):e011458.
https://doi.org/10.1136/bmjopen-2016-011458
PMid:27932337 PMCid:PMC5168618
Ustaoğlu G, Yaman D, Avcı E. Oxidative stress and peri-implantitis: The role of oxidants and antioxidants. Journal of Oral Health and Oral Epidemiology. 2023;12(2):82-8.
https://doi.org/10.34172/johoe.2023.14
Al-Bakri SMR, Magan-Fernandez A, Galindo-Moreno P, O'Valle F, Martin-Morales N, Padial-Molina M, Mesa F. Detection and comparison of neutrophil extracellular traps in tissue samples of peri-implantitis, periodontitis, and healthy patients: A pilot study. Clinical Implant Dentistry and Related Research. 2024;26(3):631-41.
https://doi.org/10.1111/cid.13325
PMid:38556724
Al-Sowygh ZH, Aldamkh MK, Binmahfooz AM, Al-Aali KA, Akram Z, Qutub OA et al. Assessment of matrix metalloproteinase-8 and -9 levels in the peri-implant sulcular fluid among waterpipe (narghile) smokers and never-smokers with peri-implantitis. Inhalation Toxicology. 2018;30(2):72-7.
https://doi.org/10.1080/08958378.2018.1449273
PMid:29564945
Alasqah MN, Al-Shibani N, Al-Aali KA, Qutub OA, Abduljabbar T, Akram Z. Clinical indices and local levels of inflammatory biomarkers in per-implant health of obese and nonobese individuals. Clinical Implant Dentistry and Related Research. 2019;21(1):80-4.
https://doi.org/10.1111/cid.12700
PMid:30548778
Aldulaijan HA, Al-Zawawi AS, Shaheen MY, Ali D, Divakar DD, Basudan AM. Assessment of salivary alpha amylase and mucin-4 before and after non-surgical treatment of peri-implant mucositis. International Journal of Implant Dentistry. 2022;8(1):30.
https://doi.org/10.1186/s40729-022-00429-z
PMid:35834021 PMCid:PMC9283593
Algohar A, Alqerban A. Levels of procalcitonin in saliva and peri-implant crevicular fluid in patients with peri-implant diseases and health. Archives of Oral Biology. 2020;120:104931.
https://doi.org/10.1016/j.archoralbio.2020.104931
PMid:33113457
Alresayes S, Al-Askar M, Mokeem SA, Javed F, Vohra F, Abduljabbar T. Cortisol levels in the peri-implant sulcular fluid among patients with and without peri-implantitis. Journal of Periodontal Research. 2021;56(4):746-52.
https://doi.org/10.1111/jre.12873
PMid:33704787
Alsahhaf A, AlHamdan EM, Vohra F, Abduljabbar T, Chaudhry Z, Kuyunov I. Novel Biomarker Evaluation in Peri-Implant Crevicular Fluid as Disease Indicators for Peri-Implant Health. Journal of Biomaterials and Tissue Engineering. 2023;13(5):714-20.
https://doi.org/10.1166/jbt.2023.3293
Chaparro A, Atria P, Realini O, Monteiro LJ, Betancur D, Acuña-Gallardo S et al. Diagnostic potential of peri-implant crevicular fluid microRNA-21-3p and microRNA-150-5p and extracellular vesicles in peri-implant diseases. Journal of Periodontology. 2021;92(6):e11-e21.
https://doi.org/10.1002/JPER.20-0372
PMid:33185898
Chaparro A, Beltrán V, Betancur D, Sam Y-H, Moaven H, Tarjomani A et al. Molecular biomarkers in peri-implant health and disease: a cross-sectional pilot study. International Journal of Molecular Sciences. 2022;23(17):9802.
https://doi.org/10.3390/ijms23179802
PMid:36077204 PMCid:PMC9456434
Chaparro A, Sanz A, Wolnitzky A, Realini O, Bendek MJ, Betancur D et al. Lymphocyte B and Th17 chemotactic cytokine levels in peri-implant crevicular fluid of patients with healthy, peri-mucositis, and peri-implantitis implants. Journal of Oral Research. 2020:20-5.
Daubert DM, Pozhitkov AE, Safioti LM, Kotsakis GA. Association of Global DNA Methylation to Titanium and Peri-Implantitis: A Case-Control Study. JDR Clinical & Translational Research. 2019;4(3):284-91.
https://doi.org/10.1177/2380084418822831
PMid:30931716
de Mello-Neto JM, Teixeira MKS, Teixeira GS, Lourenço EJV, Telles DM, Lira-Junior R et al. Peri-implant treatment reduces the salivary levels of Colony stimulator factor-1 and S100A8/A9. Odontology. 2021;109(2):540-6.
https://doi.org/10.1007/s10266-020-00570-4
PMid:33185753
Dewan H, Robaian A, Divakar DD, Hegde SMR, Shankar SM, Poojary B. Levels of peri-implant sulcular fluid levels of soluble urokinase plasminogen activator receptor and TNF-α among cigarette smokers and non-smokers with peri-implantitis. Technology and Health Care. 2023;31:1-9.
https://doi.org/10.3233/THC-213123
PMid:35848046
Drafta S, Guita DM, Cristache CM, Beuran IA, Burlibasa M, Petre AE, Burlibasa L. Could Pro-Inflammatory Cytokines Levels IL-6, IL-8, TNFα, Total Antioxidant Status and Lactate Dehydrogenase Be Associated with Peri-Implant Bone Loss A Pilot Study. Applied Sciences. 2021;11(22):11012.
https://doi.org/10.3390/app112211012
Esberg A, Isehed C, Holmlund A, Lundberg P. Peri-implant crevicular fluid proteome before and after adjunctive enamel matrix derivative treatment of peri-implantitis. Journal of Clinical Periodontology. 2019;46(6):669-77.
https://doi.org/10.1111/jcpe.13108
PMid:30985016
Figueiredo LC, Bueno-Silva B, Nogueira CFP, Valadares LC, Garcia KMM, Filho GCdL et al. Levels of gene expression of immunological biomarkers in peri-implant and periodontal tissues. International Journal of Environmental Research and Public Health. 2020;17(23):9100.
https://doi.org/10.3390/ijerph17239100
PMid:33291232 PMCid:PMC7730812
Flores V, Venegas B, Donoso W, Ulloa C, Chaparro A, Sousa V, Beltrán V. Histological and Immunohistochemical Analysis of Peri-Implant Soft and Hard Tissues in Patients with Peri-Implantitis. International Journal of Environmental Research and Public Health. 2022;19(14):8388.
https://doi.org/10.3390/ijerph19148388
PMid:35886240 PMCid:PMC9321452
Gürlek Ö, Gümüş P, Nile CJ, Lappin DF, Buduneli N. Biomarkers and Bacteria Around Implants and Natural Teeth in the Same Individuals. Journal of Periodontology. 2017;88(8):752-61.
https://doi.org/10.1902/jop.2017.160751
PMid:28440740
Jansson L, Lundmark A, Modin C, Abadji D, Yucel‐Lindberg T. Intra‐individual cytokine profile in peri‐implantitis and periodontitis: A cross‐sectional study. Clinical Oral Implants Research. 2021;32(5):559-68.
https://doi.org/10.1111/clr.13725
PMid:33595852
Lira-Junior R, Teixeira MKS, Lourenco EJV, Telles DM, Figueredo CM, Bostrom EA. CSF-1 and IL-34 levels in peri-implant crevicular fluid and saliva from patients having peri-implant diseases. Clin Oral Investig. 2020;24(1):309-15.
https://doi.org/10.1007/s00784-019-02935-8
PMid:31102043
López-Jornet P, Hynninen JN, Parra-Perez F, Peres-Rubio C, Pons-Fuster E, Tvarijonaviciute A. The Role of Salivary Biomarkers in Monitoring Oral Health in Patients with Implants and Periodontitis. Applied Sciences. 2024;14(2):927.
https://doi.org/10.3390/app14020927
Marcello-Machado RM, Faot F, Schuster AJ, Bielemann AM, Nascimento GG, Del Bel Cury AA. Mapping of inflammatory biomarkers in the peri-implant crevicular fluid before and after the occlusal loading of narrow diameter implants. Clinical Oral Investigations. 2020;24(3):1311-20.
https://doi.org/10.1007/s00784-019-03010-y
PMid:31312971
-Marques Filho JS, Gobara Jr J, da Silva Salomao GV, Sumita LM, Shibli JA, Viana RG et al. Cytokine levels and human herpesviruses in saliva from clinical periodontal healthy subjects with peri‐implantitis: a case‐control study. Mediators of inflammation. 2018;2018(1):6020625.
https://doi.org/10.1155/2018/6020625
PMid:30158834 PMCid:PMC6109554
Menini M, Pesce P, Pera F, Baldi D, Pulliero A, Izzotti A. MicroRNAs in Peri-implant Crevicular Fluid Can Predict Peri-implant Bone Resorption: Clinical Trial with a 5-Year Follow-up. Int J Oral Maxillofac Implants. 2021;36(6):1148-57.
https://doi.org/10.11607/jomi.9040
PMid:34919614
Mousavi Jazi M, Sadeghi Pour Rodsari HR, Mirmiran F. Level of Oxidative Stress Markers in Peri-Implant Crevicular Fluid and Their Correlation with Clinical Parameters. J Dent (Tehran). 2015;12(5):340-6.
Pallos D, Sousa V, Feres M, Retamal-Valdes B, Chen T, Curtis M et al. Salivary microbial dysbiosis is associated with peri-implantitis: a case-control study in a Brazilian population. Frontiers in Cellular and Infection Microbiology. 2022;11:696432.
https://doi.org/10.3389/fcimb.2021.696432
PMid:35071026 PMCid:PMC8766799
Priyadharsini KS, Rajasekar A. Comparative Evaluation of C-Reactive Protein Levels among Peri-Implant Health and Disease Conditions. Journal of Long-Term Effects of Medical Implants. 2024;34(3):19-22.
https://doi.org/10.1615/JLongTermEffMedImplants.2023047435
PMid:38505889
Rakic M, Petkovic-Curcin A, Struillou X, Matic S, Stamatovic N, Vojvodic D. CD14 and TNFα single nucleotide polymorphisms are candidates for genetic biomarkers of peri-implantitis. Clinical oral investigations. 2015;19:791-801.
https://doi.org/10.1007/s00784-014-1313-3
PMid:25217276
Ramenzoni LL, Hofer D, Solderer A, Wiedemeier D, Attin T, Schmidlin PR. Origin of MMP-8 and Lactoferrin levels from gingival crevicular fluid, salivary glands and whole saliva. BMC Oral Health. 2021;21(1):385.
https://doi.org/10.1186/s12903-021-01743-5
PMid:34353321 PMCid:PMC8340507
Renvert S, Widén C, Persson GR. Cytokine expression in peri-implant crevicular fluid in relation to bacterial presence. Journal of Clinical Periodontology. 2015;42(7):697-702.
https://doi.org/10.1111/jcpe.12422
PMid:26085219
Saito Y, Nodai T, Munemasa T, Mukaibo T, Kondo Y, Masaki C, Hosokawa R. Diagnostic potential of endothelin-1 in peri-implant diseases: a cross-sectional study. International Journal of Implant Dentistry. 2024;10(1):32.
https://doi.org/10.1186/s40729-024-00551-0
PMid:38874661 PMCid:PMC11178717
Sanchez-Siles M, Lucas-Azorin J, Salazar-Sanchez N, Carbonell-Meseguer L, Camacho-Alonso F. Salivary Concentration of Oxidative Stress Biomarkers in a Group of Patients with Peri-Implantitis: A Transversal Study. Clin Implant Dent Relat Res. 2016;18(5):1015-22.
https://doi.org/10.1111/cid.12367
PMid:26230313
Sharma M, Singh AP, Kumar B, Girdhar P, Brar AS, Mittal P. Evaluation of C-Reactive Proteins Levels in Peri-Implantitis Patients. Journal of Pharmacy and Bioallied Sciences. 2024:10.4103/jpbs.jpbs_428_24.
https://doi.org/10.4103/jpbs.jpbs_428_24
PMid:39346192 PMCid:PMC11426756
Shelke AU, Dhadse PV. Assessment and comparison of Periostin levels in peri-implant sulcular fluid as a biomarker in healthy peri-implant sites and sites with periimplant mucositis and peri-implantitis. Eur J Mol Clin Med. 2020;7(2):2009-16.
Song Z, Weigl P, Wang B. Correlations of inflammatory cytokines, oxidative stress markers, and matrix metalloproteinases in gingival crevicular fluid with peri-implantitis. European Journal of Inflammation. 2019;17:2058739219845542.
https://doi.org/10.1177/2058739219845542
Soysal F, Unsal B, Isler SC, Akca G, Bakirarar B, Ozcan M. Evaluation of salivary stress markers and inflammatory cytokine levels in peri-implantitis patients. Clin Oral Investig. 2024;28(5):290.
https://doi.org/10.1007/s00784-024-05692-5
PMid:38691206 PMCid:PMC11062951
Teixeira MKS, Lira-Junior R, Lourenco EJV, Telles DM, Bostrom EA, Figueredo CM, Bostanci N. The modulation of the TREM-1/PGLYRP1/MMP-8 axis in peri-implant diseases. Clin Oral Investig. 2020;24(5):1837-44.
https://doi.org/10.1007/s00784-019-03047-z
PMid:31444693
Urvasizoglu G, Kilic A, Barlak N, Gundogdu M, Karatas OF. MiR-4484 Acts as a Potential Saliva Biomarker for Early Detection of Peri-implantitis. Int J Oral Maxillofac Implants. 2021;36(1):115-21.
https://doi.org/10.11607/jomi.8470
PMid:33600531
Urvasizoglu G, Kilic A, Capik O, Gundogdu M, Karatas OF. CXCL14 and miR-4484 serves as potential salivary biomarkers for early detection of peri-implantitis. Odontology. 2024 Jul;112(3):864-71.
https://doi.org/10.1007/s10266-023-00876-z
PMid:38087011
Wang HL, Garaicoa‐Pazmino C, Collins A, Ong HS, Chudri R, Giannobile WV. Protein biomarkers and microbial profiles in peri‐implantitis. Clinical oral implants research. 2016;27(9):1129-36.
https://doi.org/10.1111/clr.12708
PMid:26424287
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