Effect of Subgingival Instrumentation on Neutrophil Elastase and C-Reactive Protein in Grade B and C Periodontitis: Exploratory Analysis of a Prospective Cohort Study
Abstract
:1. Introduction
2. Material and Methods
2.1. Clinical Examination
2.2. Reclassification
2.3. Blood Samples
2.4. Anti-Infective Therapy
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AgP | aggressive periodontitis |
BD | most apical extension of bone loss |
BMI | body mass index |
BOP | bleeding on probing |
BP | grade B periodontitis |
CEJ | cemento-enamel junction |
ChP | chronic periodontitis |
COPD | chronic obstructive pulmonary disease |
CP | grade C periodontitis |
CRP | C-reactive protein |
CVD | cardiovascular disease |
GBI | gingival bleeding index |
IL | interleukin |
LBP | lipopolysaccharide-binding protein |
MANOVA | repeated measures analysis of variance |
NE | neutrophil elastase |
PAL-V | vertical probing attachment loss |
PCR | plaque control record |
PISA | periodontal inflamed surface area |
PMN | polymorphonuclear leukocytes |
PPD | probing pocket depth |
RAL-V | vertical relative attachment level |
SI | subgingival instrumentation |
References
- Armitage, G.C. Development of a classification system for periodontal diseases and conditions. Ann. Periodontol. 1999, 4, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Tonetti, M.S.; Greenwell, H.; Kornman, K.S. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J. Clin. Periodontol. 2018, 45 (Suppl. 20), S149–S161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilson, W.; Taubert, K.A.; Gewitz, M.; Lockhart, P.B.; Baddour, L.M.; Levison, M.; Durack, D.T. Prevention of infective endocarditis: Guidelines from the American Heart Association: A guideline from the American Heart Association Rheumatic Fever, Endocarditis and Kawasaki Disease Committee, Council on Cardiovascular Disease in the Young, and the Council on Clinical Cardiology, Council on Cardiovascular Surgery and Anesthesia, and the Quality of Care and Outcomes Research Interdisciplinary Working Group. J. Am. Dent. Assoc. 2007, 138, 739–745, 747–760. [Google Scholar] [PubMed] [Green Version]
- Wohlfeil, M.; Scharf, S.; Siegelin, Y.; Schacher, B.; Oremek, G.M.; Sauer-Eppel, H.; Eickholz, P. Increased systemic elastase and C-reactive protein in aggressive periodontitis (CLOI-D-00160R2). Clin. Oral Investig. 2012, 16, 1199–1207. [Google Scholar] [CrossRef] [PubMed]
- Eickholz, P.; Siegelin, Y.; Scharf, S.; Schacher, B.; Oremek, G.M.; Sauer-Eppel, H.; Schubert, R.; Wohlfeil, M. Non-surgical periodontal therapy decreases serum elastase levels in aggressive but not in chronic periodontitis. J. Clin. Periodontol. 2013, 40, 327–333. [Google Scholar] [CrossRef] [PubMed]
- Ramich, T.; Asendorf, A.; Nickles, K.; Oremek, G.M.; Schubert, R.; Nibali, L.; Wohlfeil, M.; Eickholz, P. Inflammatory serum markers up to 5 years after comprehensive periodontal therapy of aggressive and chronic periodontitis. Clin. Oral Investig. 2018, 22, 3079–3089. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eickholz, P.; Schroder, M.; Asendorf, A.; Schacher, B.; Oremek, G.M.; Kaiser, F.; Wohlfeil, M.; Nibali, L. Effect of nonsurgical periodontal therapy on haematological parameters in grades B and C periodontitis: An exploratory analysis. Clin. Oral Investig. 2020, 24, 4291–4299. [Google Scholar] [CrossRef]
- Covington, L.L.; Breault, L.G.; Hokett, S.D. The application of Periodontal Screening and Recording (PSR) in a military population. J. Contemp. Dent. Pract. 2003, 4, 36–51. [Google Scholar]
- Krankenkassen, B.Z. (Ed.) Richtlinien des Bundesausschusses der Zahnärzte und Krankenkassen für eine Ausreichende, Zweckmäßige und Wirtschaftliche Vertragszahnärztliche Versorgung (Behandlungsrichtlinien); Bundesanzeiger: Köln, Germany, 2006. [Google Scholar]
- Pretzl, B.; Salzer, S.; Ehmke, B.; Schlagenhauf, U.; Dannewitz, B.; Dommisch, H.; Eickholz, P.; Jockel-Schneider, Y. Administration of systemic antibiotics during non-surgical periodontal therapy-a consensus report. Clin. Oral Investig. 2019, 23, 3073–3085. [Google Scholar] [CrossRef]
- Lang, N.P.; Tonetti, M.S. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev. Dent. 2003, 1, 7–16. [Google Scholar]
- Ainamo, J.; Bay, I. Problems and proposals for recording gingivitis and plaque. Int. Dent. J. 1975, 25, 229–235. [Google Scholar]
- O’Leary, T.J.; Drake, R.B.; Naylor, J.E. The plaque control record. J. Periodontol. 1972, 43, 38. [Google Scholar] [CrossRef]
- Sanz, M.; Herrera, D.; Kebschull, M.; Chapple, I.; Jepsen, S.; Beglundh, T.; Sculean, A.; Tonetti, M.S.; EFP Workshop Participants and Methodological Consultants. Treatment of stage I-III periodontitis-The EFP S3 level clinical practice guideline. J. Clin. Periodontol. 2020, 47 (Suppl. 22), 4–60. [Google Scholar] [CrossRef]
- Quirynen, M.; Bollen, C.M.; Vandekerckhove, B.N.; Dekeyser, C.; Papaioannou, W.; Eyssen, H. Full- vs. partial-mouth disinfection in the treatment of periodontal infections: Short-term clinical and microbiological observations. J. Dent. Res. 1995, 74, 1459–1467. [Google Scholar] [CrossRef]
- Harks, I.; Koch, R.; Eickholz, P.; Hoffmann, T.; Kim, T.S.; Kocher, T.; Meyle, J.; Kaner, D.; Schlagenhauf, U.; Doering, S.; et al. Is progression of periodontitis relevantly influenced by systemic antibiotics? A clinical randomized trial. J. Clin. Periodontol. 2015, 42, 832–842. [Google Scholar] [CrossRef]
- Griffiths, G.S.; Ayob, R.; Guerrero, A.; Nibali, L.; Suvan, J.; Moles, D.R.; Tonetti, M.S. Amoxicillin and metronidazole as an adjunctive treatment in generalized aggressive periodontitis at initial therapy or re-treatment: A randomized controlled clinical trial. J. Clin. Periodontol. 2011, 38, 43–49. [Google Scholar] [CrossRef]
- Feres, M.; Soares, G.M.; Mendes, J.A.; Silva, M.P.; Faveri, M.; Teles, R.; Socransky, S.S.; Figueiredo, L.C. Metronidazole alone or with amoxicillin as adjuncts to non-surgical treatment of chronic periodontitis: A 1-year double-blinded, placebo-controlled, randomized clinical trial. J. Clin. Periodontol. 2012, 39, 1149–1158. [Google Scholar] [CrossRef]
- Nesse, W.; Abbas, F.; van der Ploeg, I.; Spijkervet, F.K.; Dijkstra, P.U.; Vissink, A. Periodontal inflamed surface area: Quantifying inflammatory burden. J. Clin. Periodontol. 2008, 35, 668–673. [Google Scholar] [CrossRef] [Green Version]
- Loos, B.G. Systemic markers of inflammation in periodontitis. J. Periodontol. 2005, 76, 2106–2115. [Google Scholar] [CrossRef]
- Tonetti, M.S.; D’Aiuto, F.; Nibali, L.; Donald, A.; Storry, C.; Parkar, M.; Suvan, J.; Hingorani, A.D.; Vallance, P.; Deanfield, J. Treatment of periodontitis and endothelial function. N. Engl. J. Med. 2007, 356, 911–920. [Google Scholar] [CrossRef] [Green Version]
- D’Aiuto, F.; Nibali, L.; Parkar, M.; Suvan, J.; Tonetti, M.S. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J. Dent. Res. 2005, 84, 269–273. [Google Scholar] [CrossRef]
- D’Aiuto, F.; Parkar, M.; Andreou, G.; Suvan, J.; Brett, P.M.; Ready, D.; Tonetti, M.S. Periodontitis and systemic inflammation: Control of the local infection is associated with a reduction in serum inflammatory markers. J. Dent. Res. 2004, 83, 156–160. [Google Scholar] [CrossRef]
- Paraskevas, S.; Huizinga, J.D.; Loos, B.G. A systematic review and meta-analyses on C-reactive protein in relation to periodontitis. J. Clin. Periodontol. 2008, 35, 277–290. [Google Scholar] [CrossRef]
- Guerrero, A.; Griffiths, G.S.; Nibali, L.; Suvan, J.; Moles, D.R.; Laurell, L.; Tonetti, M.S. Adjunctive benefits of systemic amoxicillin and metronidazole in non-surgical treatment of generalized aggressive periodontitis: A randomized placebo-controlled clinical trial. J. Clin. Periodontol. 2005, 32, 1096–1107. [Google Scholar] [CrossRef]
- Kim, T.S.; Schenk, A.; Lungeanu, D.; Reitmeir, P.; Eickholz, P. Nonsurgical and surgical periodontal therapy in single-rooted teeth. Clin. Oral Investig. 2007, 11, 391–399. [Google Scholar] [CrossRef] [Green Version]
- Cionca, N.; Giannopoulou, C.; Ugolotti, G.; Mombelli, A. Amoxicillin and metronidazole as an adjunct to full-mouth scaling and root planing of chronic periodontitis. J. Periodontol. 2009, 80, 364–371. [Google Scholar] [CrossRef]
Parameters Mean ± Standard Deviation | Periodontitis Grade B (n = 8) | Periodontitis Grade C (n = 46) | Grade B/C p |
---|---|---|---|
Age (years) | 61.0 ± 6.7 | 40.5 ± 11.5 | <0.001 |
Remaining teeth (n) | 26.6 ± 3.2 | 27.4 ± 2.9 | 0.492 |
Pack years | 6.8 ± 11.6 | 8.4 ± 15.0 | 0.665 |
Body mass index (kg/m2) | 24.4 ± 2.8 | 26.2 ± 4.7 | 0.324 |
Parameters Mean ± Standard Deviation | Periodontitis Grade B (n = 8) | Periodontitis Grade C (n = 46) | Grade B/C p | |
---|---|---|---|---|
Gingival Bleeding Index (%) | Baseline | 15.0 ± 7.9 | 13.4 ± 10.8 | 0.526 |
6 weeks | 6.3 ± 5.3 a | 3.7 ± 4.7 b | 0.113 | |
12 weeks | 6.4 ± 6.5 a | 5.9 ± 4.8 b,c | 0.981 | |
Plaque Control Record (%) | Baseline | 40.1 ± 26.2 | 35.8 ± 14.1 | 0.856 |
6 weeks | 22.0 ± 14.5 a | 31.5 ± 18.6 a | 0.169 | |
12 weeks | 32.8 ± 11.7 | 28.2 ± 16.8 a | 0.233 | |
Bleeding on probing (%) | Baseline | 49.4 ± 15.9 | 52.0 ± 13.7 | 0.575 |
12 weeks | 20.3 ± 7.6 a | 26.7 ± 10.4 b | 0.092 | |
Probing pocket depth (PPD) (mm) | Baseline | 3.4 ± 0.3 | 3.8 ± 0.7 | 0.242 |
12 weeks | 2.2 ± 0.3 a | 2.6 ± 0.4 b | 0.006 | |
PPD reduction (mm) | 1.2 ± 0.3 | 1.1 ± 0.5 | 0.342 | |
Attachment level (mm) (PAL-V) | Baseline | 4.3 ± 1.0 | 3.6 ± 1.8 | 0.093 |
(RAL-V) | Baseline | 11.1 ± 1.2 | 10.8 ± 1.5 | 0.715 |
(RAL-V) | 12 weeks | 10.6 ± 1.2 a | 10.4 ± 1.4 b | 0.715 |
Attachment gain (mm) (ΔRAL-V) | 0.4 ± 0.3 | 0.5 ± 0.4 | 0.789 | |
PISA (mm2) | Baseline | 1169 ± 201 | 1372 ± 543 | 0.273 |
12 weeks | 288 ± 112 a | 460 ± 303 b | 0.046 |
Parameters | Periodontitis Grade B (n = 8) | Periodontitis Grade C (n = 46) | Grade B/C p | |
---|---|---|---|---|
Neutrophil elastase (ng/mL) (NE) | Baseline | 8.75 (7/13.25) | 30.55 (12.4/37.2) | 0.008 |
1 day | 19.3 (14.5/25.1) b | 33.05 (21.8/40.1) a | 0.036 | |
6 weeks | 9.4 (8.01/17.55) | 32 (13.1/37.68) | 0.059 | |
12 weeks | 17.65 (10.75/34.65) | 28 (11.3/36.2) | 0.422 | |
Change baseline to 12 weeks | 3.75 (−0.14/0.05) | −1.15 (−4.2/1.4) | 0.051 | |
C-reactive protein (mg/dL) (CRP) | Baseline | 0.09 (0.08/0.13) | 0.17 (0.10/0.34) | 0.033 |
1 day | 0.75 (0.23/1.41) a | 0.54 (0.29/1.16) a | 0.990 | |
6 weeks | 0.15 (0.05/0.27) | 0.17 (0.11/0.34) | 0.336 | |
12 weeks | 0.14 (0.07/0.21) | 0.23 (0.10/0.34) | 0.278 | |
Change baseline to 12 weeks | 0.01 (−0.05/0.14) | 0 (−0.06/0.05) | 0.542 | |
CRP reduction ≥ 0.3 mg/dL (n/%) baseline to 12 weeks | 0 (0) | 4 (9) | 1.000 | |
CRP < 0.1 mg/dL (n) (%) | Baseline | 5 (63) | 8 (17) | 0.015 |
12 weeks | 3 (37) | 11 (24) | 0.413 | |
CRP 0.1 to 0.3 mg/dL (n) (%) | Baseline | 3 (37) | 26 (57) | 0.449 |
12 weeks | 4 (50) | 20 (43) | 1.000 | |
CRP > 0.3 mg/dL (n) (%) | Baseline | 0 (0) | 12 (26) | 0.176 |
12 weeks | 1 (13) | 15 (33) | 0.411 |
Degrees of Freedom | F-Ratio | p-Value | |
---|---|---|---|
Between subjects | |||
Grade C | 1 | 4.397 | 0.042 |
African origin | 1 | 2.589 | 0.115 |
Female | 1 | 0.464 | 0.499 |
Bleeding on probing (T0) | 1 | 1.669 | 0.203 |
Smoker | 1 | 1.359 | 0.250 |
Systemic antibiotics | 1 | 0.001 | 0.973 |
Number of teeth | 1 | 1.079 | 0.305 |
Body mass index (T0) | 1 | 2.716 | 0.107 |
PISA (T0) | 1 | 8.858 | 0.005 |
Error | 43 | ||
Within subjects | |||
NE | 3 | 3.406 | 0.020 |
NE × grade C | 3 | 3.533 | 0.017 |
NE × African origin | 3 | 0.666 | 0.574 |
NE × female | 3 | 0.107 | 0.956 |
NE × bleeding on probing (T0) | 3 | 0.481 | 0.696 |
NE × smoker | 3 | 3.091 | 0.029 |
NE × systemic antibiotics | 3 | 1.203 | 0.312 |
NE × number of teeth | 3 | 3.005 | 0.033 |
NE × body mass index | 3 | 0.524 | 0.666 |
NE × PISA (T0) | 3 | 5.218 | 0.002 |
Error | 129 |
Degrees of Freedom | F-Ratio | p-Value | |
---|---|---|---|
Between subjects | |||
Grade C | 1 | 0.254 | 0.617 |
African origin | 1 | 1.385 | 0.246 |
Female | 1 | 0.047 | 0.830 |
Bleeding on probing (T0) | 1 | 0.358 | 0.553 |
Smoker | 1 | 0.004 | 0.950 |
Systemic antibiotics | 1 | 1.284 | 0.263 |
Number of teeth | 1 | 0.178 | 0.675 |
Body mass index (T0) | 1 | 7.691 | 0.008 |
PISA (T0) | 1 | 1.129 | 0.294 |
Error | 44 | ||
Within subjects | |||
CRP | 3 | 0.539 | 0.657 |
CRP × grade C | 3 | 1.311 | 0.274 |
CRP × African origin | 3 | 0.581 | 0.628 |
CRP × female | 3 | 0.248 | 0.863 |
CRP × bleeding on probing (T0) | 3 | 0.818 | 0.486 |
CRP × smoker | 3 | 0.294 | 0.829 |
CRP × systemic antibiotics | 3 | 2.238 | 0.087 |
CRP × number of teeth | 3 | 0.243 | 0.866 |
CRP × body mass index | 3 | 0.467 | 0.706 |
CRP × PISA (T0) | 3 | 3.539 | 0.017 |
Error | 132 |
Parameters | Periodontitis Grade B (n = 8) | Periodontitis Grade C (n = 46) | Grade B/C p | |
---|---|---|---|---|
Leukocyte count (nL−1) | Baseline | 5.86 (3.95/7.62) | 6.37 (5.12/7.47) | 0.559 |
1 day | 5.05 (4.51/6.66) | 6.34 (4.98/7.34) | 0.330 | |
6 weeks | 5.01 (4.56/5.79) | 6.02 (4.9/7.49) b | 0.189 | |
12 weeks | 4.92 (4.29/5.30) | 5.97 (4.85/7.5) | 0.056 | |
LPS binding protein (µg/mL) (LBP) | Baseline | 22.2 (15.3/27.9) | 30.4 (22.3/45) a | 0.108 |
1 day | 40.4 (25.5/49.7) | 44.3 (31.7/57.6) | 0.488 | |
6 weeks | 32 (20.5/43.1) | 26.6 (19.5/42.9) a | 0.961 | |
12 weeks | 34 (18/44) | 24.7 (19.2/36.8) a | 0.618 | |
Interleukin 6 (pg/mL) (IL-6) | Baseline | 1.55 (1.25/2.5) b | 1.5 (0.9/2) a | 0.510 |
1 day | 2.95 (2.25/3.65) | 2.8 (2/5.1) | 0.855 | |
6 weeks | 1.25 (1/3) b | 1.25 (0.8/1.7) a,c | 0.626 | |
12 weeks | 1.2 (0.85/2.55) a | 1.5 (1.1/2.2) a,d | 0.502 | |
Interleukin 8 (pg/mL) (IL-8) | Baseline | 21.5 (17/29) | 17 (11/25) | 0.223 |
1 day | 27 (24/35.5) | 20.5 (13/29) | 0.125 | |
6 weeks | 36 (20/58.5) | 17 (13/28) | 0.108 | |
12 weeks | 24.5 (19.5/29) | 22.5 (15/37) c | 0.884 |
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Eickholz, P.; Asendorf, A.; Schröder, M.; Schacher, B.; Oremek, G.M.; Schubert, R.; Wohlfeil, M.; Zuhr, O. Effect of Subgingival Instrumentation on Neutrophil Elastase and C-Reactive Protein in Grade B and C Periodontitis: Exploratory Analysis of a Prospective Cohort Study. J. Clin. Med. 2022, 11, 3189. https://doi.org/10.3390/jcm11113189
Eickholz P, Asendorf A, Schröder M, Schacher B, Oremek GM, Schubert R, Wohlfeil M, Zuhr O. Effect of Subgingival Instrumentation on Neutrophil Elastase and C-Reactive Protein in Grade B and C Periodontitis: Exploratory Analysis of a Prospective Cohort Study. Journal of Clinical Medicine. 2022; 11(11):3189. https://doi.org/10.3390/jcm11113189
Chicago/Turabian StyleEickholz, Peter, Anne Asendorf, Mario Schröder, Beate Schacher, Gerhard M. Oremek, Ralf Schubert, Martin Wohlfeil, and Otto Zuhr. 2022. "Effect of Subgingival Instrumentation on Neutrophil Elastase and C-Reactive Protein in Grade B and C Periodontitis: Exploratory Analysis of a Prospective Cohort Study" Journal of Clinical Medicine 11, no. 11: 3189. https://doi.org/10.3390/jcm11113189