Diagnostic Accuracy of Oral Fluids Biomarker Profile to Determine the Current and Future Status of Periodontal and Peri-Implant Diseases
Abstract
:1. Introduction
2. Diagnosis of Periodontal Diseases
3. Limitations of Traditional Methods for Diagnosis
4. Need for Alternative Methods with Diagnostic and Prognostic Potential, Such as Use of Biomarkers
5. Sources of Biomarkers of Periodontal Disease in the Oral Cavity
6. Potential Biomarkers of Periodontal Diseases
6.1. IL1β
6.2. IL6
6.3. MMP8
6.4. Single vs Combination of Biomarkers
7. Detection Methods for Biomarkers in Periodontal Diseases
8. Periodontal Point-of-Care Test Kits
8.1. Microbiological Test Kits
8.2. Biochemical Test Kits
8.3. Genetic Test Kits
9. Clinical Implications and Challenges
10. Conclusions and Future Direction
Author Contributions
Funding
Conflicts of Interest
References
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Authors | Aim(s) | Study Groups | Oral Fluids Examined * | Biomarkers, Assays † | Clinical Criteria ¶ | Results |
---|---|---|---|---|---|---|
Ma et al., 2000 [105] | Investigate the correlation between GI, MMP8, and MMP13 level in PISF and amount of peri-implant bone loss | 13 patients having implants with different levels of bone resorption | PISF | MMP8 by time-resolved immunofluorometric assay and MMP13 by quantitative immunoblot | Peri-implant vertical bone loss was divided into: <1 mm, 1–3 mm, and >3mm Gingival inflammation recorded on scale from 0–3 | Both biomarkers potentially reflect osteolytic process but not GI |
Yamazaki-Kubota et al., 2010 [110] | Investigate the level of MMP2, MMP8, and subgingival bacteria in children with Down’s syndrome | Children with DS (n = 15) Healthy controls (n = 14) | GCF | MMP2 and MMP8 (ELISA) | OHI, PPD, and BOP | Both collagenolytic enzymes were significantly higher in GCF of children with DS than controls even with low oral hygiene index score and absence of BOP. |
Rai et al., 2010 [111] | Investigate the level of MMP8 and MMP9 in healthy periodontium and periodontitis | Periodontitis patients (n = 10) Healthy controls (n = 10) | GCF | Both MMPs measured by ELISA | At least 7 teeth with PPD >6 mm Having at least 12 posterior teeth | Significantly higher level of MMP8 and MMP9 in periodontitis vs healthy controls |
Leppilahti et al., 2011 [112] | Assessing the ability of PoC MMP8- mouth rinse, measured by three assays, TIMP1, and elastase activity to distinguish subjects with different periodontal conditions. Comparing assaying methods for MMP8 | Randomly selected patients with periodontitis (n = 214) | Mouth rinse samples | MMP8 assayed by IFMA, DentoELISA and commercial ELISA. TIMP1 and elastase measured by ELISA | BOP, PPD ≥4 mm, and PIBI | MMP-8/TIMP-1 combination showed higher diagnostic accuracy DentoELISA showed higher sensitivity and specificity in detecting MMP8 |
Kraft-Neumärker et al., 2012 [113] | Full-mouth analysis to investigate the correlation between clinical parameters and level of MMP8 | Females with periodontitis (n = 9) | GCF | MMP8 assayed by ELISA | GI, PI, BOP, and PPD (>30% of sites affected) | Increased PPD was associated with increased level of MMP8 |
Ebersole et al., 2013 [114] | Investigating the level of selected biomarkers in periodontal health and periodontal disease | Healthy (n = 30) Periodontitis (n = 50) | Saliva | IL1β, IL6, TNFα, and IFNα assayed by human Luminex® multiplex assays MMP8, PGE2, and albumin assayed by ELISA | Healthy: BOP <10% of sites, PPD ≤6 mm in <2% of sites, CAL >2 mm in <1% of sites Periodontitis: PPD ≥5 mm, CAL ≥3 mm, BOP ≥2 in at least 5 sites | Salivary MMP8, IL1β, and IL6 showed the highest diagnostic potential |
Leppilahti et al., 2014 [115] | Assess the accuracy of different biomarkers in diagnosing periodontitis Comparing two methods for assaying MMP8 | Healthy (n = 20 sites) Gingivitis (n = 19 sites) Periodontitis (n = 19 sites) | GCF | MPO, TIMP1 MMP13, and MMP14. Assayed by ELISA MMP8 Assayed by ELISA and IFMA | Healthy: PPD <3 mm, no CAL, no inflammation Gingivitis: BOP with no loss of attachment Periodontitis: PPD ≥5 mm, CAL ≥3 mm, >50% bone loss in radiograph | MPO and MMP8 can highly discriminate periodontitis. IFMA is more accurate than ELISA for assaying MMP8 |
Liu and Hwang, 2016 [116] | Assessment of the effect of smoking cessation on periodontal tissue over 12 months | Male smokers joined smoking cessation clinic (n = 122) | GCF, Saliva | MMP8, MMP9, and IL1β measured by ELISA, nicotine and cotinine assayed by chromatography-tandem mass spectrometry | PI, GI Patients exhibiting sites >5.5 mm were excluded | The level of MMP8 did not change significantly within the monitoring period between smokers, quit-smokers, oscillators and nonsmokers |
Ramseier et al., 2016 [89] | Assessment of biomarkers in PISF 10 years after implant placement | Implants (n = 504), adjacent teeth (n = 493) | GCF, PISF | MMP8, IL1β, MMP3, MMP1, and MMP1/TIMP1 measured by ELISA | PI, mGI, BOP, PPD, and CAL | Increased level of MMP8 was detected in 90% of sites with progressive inflammation around tooth/implant |
Gul et al., 2016 [117] | To assess combined biomarkers compared with single biomarker for predicting the outcome of treatment | Periodontitis patients (n = 30) | GCF | Active MMP8, elastase, cathepsin G, trypsin like enzyme and sialidase measured by colorimetric assay | Full mouth PI, BOP, PPD and CAL | Combined active enzyme profiling could provide significant prediction of outcome of treatment. |
Kumar et al., 2017 [118] | Evaluate the response of peri-implant connective tissue to titanium and zirconia abutments | Candidates for implant placement (n = 12) | PISF | MMP8 assayed by ELISA | GI, PI, and PPD measured by thermoplastic periodontal sensor probe | Titanium abutment induced higher expression of MMP8 at early stages than zirconia |
Gul et al., 2017 [119] | Assess the ability of a novel combination of biomarkers to predict treatment outcome of patients with chronic periodontitis | Periodontitis patients (n = 77) | GCF and plaque | Active MMP8, elastase and sialidase measured by colorimetric assay, Pg, Tf and Td level determined by qPCR. | Full mouth PI, BOP, PPD and CAL | The ‘‘fingerprint’’ of GCF enzymes and bacteria offers a way to predict the outcome of non-surgical periodontal treatment on a site-specific basis. |
Mauramo et al., 2018 [98] | Assessment of association between MMP8 level in oral fluids and periodontitis | Periodontitis patients (n = 258) | GCF, Saliva | MMP8 assayed by IFMA | DMFT, BOP, PPD, CAL | MMP8 in saliva and GCF was significantly associated with severity of periodontitis and PPD |
Borges et al., 2019 [120] | Investigate attachment loss at sites with progressive periodontal disease following SRP | Periodontitis stage II grade B (n = 18) Healthy controls (n = 9) | Saliva, GCF | IL-10, MMP8, VEGF, RANKL, OPG and TGF-β1 by Multiplex Cytokine Profiling Assay MMP8 level measured by ELISA | PPD, BOP, and relative CAL | Attachment loss continued in some sites even after SRP. Action of MMP8 seems to be modulated by IL-10 |
Hong et al., 2020 [107] | Comparing efficiency and accuracy of different biomarkers in diagnosing gingivitis | Healthy (n = 15) Gingivitis (n = 85) | Saliva and GCF | MMP8, MMP9, cystatin C, MPO, PAF, cathepsin B, lactoferrin, and ICTP ELISA | Gingivitis defined by BOP ≥10% | MMP8 and MPO were significantly and positively correlated with BOP. MMP8 was the most effective in diagnosis of gingivitis |
Karteva and Manchorova-Veleva, 2020 [121] | Assessing the accuracy of active (a)MMP8 in diagnosis of asymptomatic apical periodontitis (AAP) | AAP (n = 31) Control (n = 31) | GCF | aMMP8 by ELISA | CBCT used to confirm the presence of the lesion | Statistically significant increase in aMMP8 level collected from teeth with AAP compared to healthy controls |
Liu et al., 2020 [122] | Application of the combined use of baseline salivary biomarkers and clinical parameters in predicting the outcome of scaling and root planning | Advance periodontitis (n = 40) | Saliva | MMP8 and IL1β by ELISA, Pg, Aa, Pi and Tf by PCR. | PPD, BOP, and CAL | The combination of baseline salivary biomarkers and clinical parameters better predicted SRP outcomes than each alone |
Author, Year | Aim(s) | Study Groups | Oral Fluid Examined | PoC/Chairside Test | Clinical Criteria ¶ | Results |
---|---|---|---|---|---|---|
Mäntylä et al., 2006 [101] | Evaluate the efficacy of MMP8- specific chair-side dip-stick test in longitudinal monitoring of periodontal status of smoker and non-smoker periodontitis patients | Periodontitis patients (n = 16) | GCF | MMP8 assayed by chair-side dipstick test | Have at least 20 teeth, BOP, PPD ≥4 mm at 5 or more sites, PI, and CAL | Persistent elevation of MMP8 in GCF may indicate sites at risk and poor response to conventional nonsurgical periodontal treatment |
Sorsa et al., 2010 [81] | Comparing four methods to detect MMP8 in GCF | Periodontally healthy (n = 2), gingivitis (n = 2), moderate-severe periodontitis (n = 6) | GCF | IFMA, MMP-8 specific chair-side dip-stick test, Dento-Analyzer, and Amersham ELISA kit | PPD, AL | IFMA and Dento-Analyzer yielded comparable results, followed by chair-side dip-stick test, while Amersham ELISA results were not in line with other assays |
Nwhator et al., 2014 [97] | Investigate the clinical correlates of aMMP8-immunotest with BOP, oral hygiene, and PPD | Periodontitis and healthy (n = 86), Final analysis included 76 patients | Mouth rinse samples | aMMP8 measured by Lateral flow mouth rinse test (PerioMarker®) | BOP, debris index and calculus index scores, and BPE, PPD was charted when BPE score> 3 | aMMP8 showed high sensitivity for at least two sites with BOP and two sites with periodontal pockets |
Izadi Borujeni et al., 2015 [95] | To evaluate the sensitivity and specificity of aMMP8 PoC immunotest in detecting periodontitis | Untreated generalized periodontitis (n=30 equally distributed between moderate and severe cases) Healthy controls (n = 30) | Mouth rinse samples | aMMP8 measured by Lateral flow mouth rinse test (PerioMarker®) | Moderate periodontitis: PPD ≥3.5mm, CAL =3–4 mm at >30% of sites or ≥5 mm at <30% of sites Severe periodontitis: PPD ≥3.5 mm, CAL ≥5 mm at >30% of sites Healthy: PPD ≤3 mm, CAL ≤2 mm at <30% of sites | aMMP8 positively correlated with generalized periodontitis with diagnostic sensitivity = 87% and specificity = 60% |
Heikkinen et al., 2016 [41] | Investigate the ability of PoC aMMP8-mouthrinse to identify adolescents with oral inflammatory burden | Adolescent subjects (n = 47) | Mouth rinse samples | aMMP8 measured by Lateral flow mouth rinse test | Full-mouth clinical parameters, including BOP, PI, PPD ≥4mm, and caries sites | aMMP-8 chairside test effectively differentiated adolescents with early initial signs of periodontitis. However, caries was less efficiently detected |
Ritzer et al., 2017 [106] | Determine the efficiency of sensory chewing gums as 24/7 detector to differentiate between patients with peri-implant disease and healthy subjects | Peri-implantitis or mucositis group and healthy volunteers | PISF, Unstimulated saliva | aMMP-8 levels were assayed by DentoELISA, Dento-Analyzer, and peptide sensor (PCL ID #1c) | N/A | Level of MMP8 was significantly higher in patients with peri-implant diseases as compared to healthy controls |
Heikkinen et al., 2017 [96] | Determination of genetic background for initial periodontitis and caries by PoC aMMP8 immunotest | Adolescent subjects (n = 47) | Oral fluid samples | aMMP8 measured by Lateral flow mouth rinse test (PerioSafe®) | BOP ≥20% of sites, PPD, PI, and caries status | Genetic polymorphisms of MMP3 and VDR significantly associated with aMMP8 level |
Räisänen et al., 2018 [109] | Investigate the effectiveness of aMMP8 PoC immunotest in determining cost-effective treatment(s) | Adolescents (n = 47) Adults (n = 70) | Mouth rinse samples | aMMP8 measured by Lateral flow mouth rinse test | Treatment need defined by CPITN scores | Results from aMMP8 PoC immunotest were consistent with CPITN codes for treatment needs |
Grigoriadis et al., 2019 [145] | Using aMMP8 PoC immunotest for screening prediabetes and diabetes state in periodontal patients | Healthy (n = 21) Periodontitis: Stage I/II, grade A-C (n = 48) | Mouth rinse samples Capillary blood | aMMP8 assayed by Lateral flow mouth rinse immunoassay test and digital reader ORALyzer® Blood sugar by HbA1c test | PPD and BOP were measured | HbA1c and aMMP8 PoC test can provide dentists with opportunity to diagnose prediabetic and diabetic patients |
Räisänen et al., 2019 [146] | Comparing the effectiveness of aMMP8 PoC mouthwash vs BOP in detection pre-/subclinical periodontitis in adolescents | 47 adolescents (30 male and 17 female) | Mouth rinse samples | aMMP8 Lateral flow immunoassay test (PerioSafe®) | BOP (20% of sites), PPD≥ 4mm, PI, bitewing radiographs for premolars and molars | aMMP8 was twice higher in terms of sensitivity and more accurate than BOP in detecting early stages than BOP |
Schmalz et al., 2019 [147] | Investigate the association of aMMP8 with severity of periodontitis, periodontal bacteria, and blood parameters | Periodontitis patients (n = 188): Mild (n = 50) Moderate (n = 111) Severe (n = 27) | Mouth rinse samples, blood | aMMP8 measured by Lateral flow immunoassay test (Periomarker®) | Based on PPD and CAL, severity of periodontitis was divided into mild, moderate, and severe | aMMP8 was positively associated with severity of periodontitis and anaerobes highly involved in periodontal destruction |
Rautava et al., 2020 [123] | Compare the accuracy of aMMP8 PoC immunotest in subjects with and without Crohn’s disease (CD) | Controls (n = 47) CD (n = 41) | Mouth rinse samples | Lateral flow mouth rinse test (PerioSafe®) | Oral mucosal examination for CD-related lesions Caries prevalence by DMFS Gingivitis defined by BOP ≥15% of sites with no CAL or PPD Periodontitis defined by: PPD ≥4 mm, CAL ≥2 mm with or without BOP | Discrimination accuracy of aMMP8 PoC immunotest reduced and diagnosis of periodontitis was compromised with CD patients |
Sorsa et al., 2020 [40] | Assessing the usefulness of aMMP8 point of care (PoC) mouthwash in the interpretation of the “Staging” and “Grading” of the new classification system for periodontal disease | Healthy (n = 31) Periodontitis (n = 119) | Mouth rinse samples | Lateral flow mouth rinse test (PerioSafe®) and ORALyzer® | Healthy: BOP <10% of sites Periodontitis: Defined according to the new classification system 2018 | aMMP8 PoC mouthwash can be integrated for staging and grading of periodontitis |
Sorsa et al., 2020 [148] | Investigate the effectiveness of aMMP8 PoC mouthwash in diagnosing peri-implantitis | Healthy subjects (n = 20) Peri-implantitis (n = 20) | Mouth rinse samples | aMMP8 Lateral flow immunoassay test (ImplantSafe®) | Peri-implantitis, diagnosed clinically and radiographically | aMMP8 PoC test correctly diagnosed all healthy and Peri-implantitis cases |
Lähteenmäki et al., 2020 [149] | Assessing the accuracy aMMP-8 PISF POC test (ImplantSafe) as compared to other biomarkers of peri-implantitis. Evaluating the value of aMMP-8 lateral-flow PoC technologies in non-invasively monitoring periodontal treatment outcomes | Patients with peri-implantitis (n = 26) Healthy control (n = 26) Periodontitis patients (n = 15) | PISF, mouth rinse samples | aMMP8 Lateral flow immunoassay test (ImplantSafe®), (PerioSafe®) | Peri-implantitis, diagnosed by presence of PPD ≥4mm, BOP, radiographic bone loss ≥2 mm, PI, FI, mobility index Self-reported oral health (SROH)-questionnaires | aMMP8 PoC test discriminated health from peri-implantitis with higher accuracy than BOP, PMN-elastase, MMP9, TIMP1, and myeloperoxidase SROH can be used as adjunctive diagnostic method but not as alternative for oral fluid biomarkers |
Assay | Commercial Kit | Sample | Target? |
---|---|---|---|
Microbial test kit | PerioScan | Subgingival plaque | Utilizes the BANA test for bacterial trypsin-like proteases |
IAI Pado test | Subgingival plaque | Aa, Pg, Tf, and Td | |
Evalusite test | Subgingival plaque, GCF | Aa, Pi, and Pg | |
TOPAS | Subgingival plaque, GCF | Toxins derived from anaerobic metabolism and measures GCF protein level | |
Omnigene® diagnosctics | Saliva | Pg, Pi, Aa, Fn, Tf, Td, Ec, and Cr | |
Biochemical test | Prognostik | GCF | Serine proteinases and elastase |
Pocketwatch | GCF | Detects aspartate aminotransferase through colorimetric detection | |
Periogard | GCF | Detects the presence of aspartate aminotransferase | |
Periocheck | GCF | Detects presence of neutral proteinases (collagenase) | |
Progno-Stik | GCF | Elastase | |
PerioMarker® | GCF | Activated MMP8 | |
Dip Stick | GCF | MMP8 | |
Perio 2000 | GCF, Subgingival plaque | Sulfides in periodontal pockets | |
PerioSafe® | GCF, Mouth rinse | Activated MMP8 | |
ImplantSafe® | GCF, PISF | Activated MMP8 | |
ORALyzer® | GCF, Mouth rinse, Saliva | Activated MMP8 | |
Integrated microfluidic platform for oral diagnostics | Saliva | MMP8 | |
Oral Fluid NanoSensor test | Saliva | IL-1 and IL-8 | |
Electronic taste chip | Saliva | C reactive protien | |
Genetic test kits | GenoType®PST® | Saliva | Interleukin (IL-1α and IL-1β) genes polymorphism |
MyperioID | Saliva | Genetic variation/polymorphism within the IL-1 gene |
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Gul, S.S.; Abdulkareem, A.A.; Sha, A.M.; Rawlinson, A. Diagnostic Accuracy of Oral Fluids Biomarker Profile to Determine the Current and Future Status of Periodontal and Peri-Implant Diseases. Diagnostics 2020, 10, 838. https://doi.org/10.3390/diagnostics10100838
Gul SS, Abdulkareem AA, Sha AM, Rawlinson A. Diagnostic Accuracy of Oral Fluids Biomarker Profile to Determine the Current and Future Status of Periodontal and Peri-Implant Diseases. Diagnostics. 2020; 10(10):838. https://doi.org/10.3390/diagnostics10100838
Chicago/Turabian StyleGul, Sarhang S., Ali A. Abdulkareem, Aram M. Sha, and Andrew Rawlinson. 2020. "Diagnostic Accuracy of Oral Fluids Biomarker Profile to Determine the Current and Future Status of Periodontal and Peri-Implant Diseases" Diagnostics 10, no. 10: 838. https://doi.org/10.3390/diagnostics10100838
APA StyleGul, S. S., Abdulkareem, A. A., Sha, A. M., & Rawlinson, A. (2020). Diagnostic Accuracy of Oral Fluids Biomarker Profile to Determine the Current and Future Status of Periodontal and Peri-Implant Diseases. Diagnostics, 10(10), 838. https://doi.org/10.3390/diagnostics10100838