Table 1.
Observational studies analyzing oxidative stress in periodontitis.
| Study design | Sample size | Note | Sample type | Outcome | References |
|---|---|---|---|---|---|
| Cross-sectional study | 20 AgP patients 20 ChP patients 20 controls | – | Saliva | ↑ ROS, TBARS with AgP; TRAP ↓ with AgP compared to ChP | Acquier et al., 2017 |
| Case-control study (cross-sectional) | 55 ChP patients 55 healthy controls | – | Serum Saliva | ↓ TAC in serum and saliva; ↑ MDA increased in serum and saliva vs. controls | Ahmadi-Motamayel et al., 2017 |
| Prospective study | 33 PW with ChP 18 PW with gingivitis 21 PW controls 27 non-PW ChP 25 non-PW controls | Pregnancy | Serum GCF | ↓ TAC, SOD in PW vs. non-PW and in ChP group compared to controls; ↑ TAC, SOD in third trimester in PW with ChP vs. PW with ChP in the first trimester | Akalin et al., 2009 |
| Comparative study (cross-sectional) | 20 T2DM patients with periodontitis 20 T2DM patients PH 20 SH patients with periodontitis | T2DM | Plasma | ↓ plasma small molecule antioxidant capacity ↑ PC in T2DM with periodontitis vs. PH T2DM patients | Allen et al., 2011 |
| Cross-sectional study | 33 ChP patients 16 patients with gingivitis 37 healthy controls | – | Saliva | ↑ TAC, 8-OHdG, MDA and activity of SOD, GPx in ChP vs. controls | Almerich-Silla et al., 2015 |
| Observational study (cross-sectional) | 19 non-T2DM patients 24 T2DM patients with good metabolic control 27 T2DM patients with poor metabolic control T2DM | T2DM | Saliva | ↓ GPx, glutathione reductase in poor metabolic control T2DM patients; ↑ GSSG/GSH ratio in poor metabolic control T2DM | Arana et al., 2017 |
| Case-control study | 15 PH + normal weight 15 gingivitis + normal weight 15 ChP + normal weight 15 PH + obese 18 gingivitis + obese 15 ChP + obese | Obesity | GCF | ↑ MDA, PC and ↓ TAC in ChP + obese group | Atabay et al., 2017 |
| Cross-sectional study | 32 ChP post-menopausal women 31 ChP pre-menopausal 25 PH post-menopausal women 26 PH pre-menopausal women | Menopause | Serum GCF | ↓ TAC, SOD activity in post-menopausal women with ChP in serum and GCF | Baltacioglu et al., 2006 |
| Cross-sectional study | 35 AgP patients 33 ChP patients 30 PH controls | – | Serum Saliva | ↑ MDA, TOS, OSI in periodontitis groups; ↓ TAC in periodontitis groups vs. controls (except serum MDA) | Baltacioglu et al., 2014 |
| Cross-sectional study | 23 ChP patients 19 PH controls | – | Saliva | ↑ TBARS in ChP (men) ↓ TAC in ChP (women); trend toward ↓ DNA integrity in ChP | Banasová et al., 2015 |
| Cross-sectional study | 9 patients with periodontitis 9 healthy controls | – | Gingival tissue | ↑ activities of MPO, GPx, glutathione S-transferase in periodontitis group; ↑ TBARS and GSSG levels increased vs. controls | Borges et al., 2007 |
| Cross-sectional study | 20 ChP patients 20 healthy controls | – | Serum Saliva GCF | ↓ TAC in GCF and plasma in ChP vs. control; ↓ TAC in saliva in ChP vs. control | Brock et al., 2004 |
| Cross-sectional study | 32 ChP patients 32 PH control | – | Saliva Gingival tissue | ↑ 8-OHdG and mtDNA deletions in ChP group vs. control | Canakci et al., 2009 |
| Cross-sectional study | 30 ChP patients 30 PH control | – | Blood Gingival tissue | ↑ mtDNA deletion in ChP group vs. control | Canakci et al., 2006 |
| Cross-sectional study | 10 preeclampsia ChP 10 preeclampsia PH 10 normotensive ChP 10 normotensive PH | Preeclampsia | Serum Saliva GCF | ↓ TAC in ChP women with preeclampsia (GCF, serum, saliva); ↓ SOD and GPx activities decreased in ChP women with preeclampsia (GCF and serum); ↑ MDA in ChP preeclamptic women (GCF, serum) | Canakci et al., 2007 |
| Cross-sectional study | 31 pre-menopausal 31 peri-menopausal 31 post-menopausal ChP women | Menopause | GCF Gingival tissue | ↑ 8-OHdG in ChP post-menopausal women in GCF and gingival tissue | Chandra et al., 2017 |
| Cross-sectional study | 10 ChP patients 10 PH control | – | Plasma GCF | ↓ TAC in GCF and plasma in ChP vs. control; ↓ GSH and GSSG in GCF in ChP | Chapple et al., 2002 |
| Observational correlational study | 11,480 participants; 1,567 with mild periodontitis 609 with severe periodontitis | – | Serum | ↓ vitamin C, bilirubin and TAC (calculated) in mild or severe periodontitis | Chapple et al., 2007b |
| Cross-sectional study | 17 periodontitis patients 20 healthy controls | – | Saliva | ↓ TAC in periodontitis | Diab-Ladki et al., 2003 |
| Cross-sectional study | 12 SH and PH controls 15 SH and ChP patients 8 well-controlled T2DM patients with ChP 14 poor-controlled T2DM patients with ChP | T2DM | Gingival tissue | Peroxiredoxin 1 and GPX1 overexpressed in ChP; Peroxiredoxin 2 and SOD2 up-regulated especially in poor—controlled T2DM with ChP | Duarte et al., 2012 |
| Cross-sectional study | 20 ChP patients with RA 20 PH patients with RA 20 ChP patients SH 20 SH and PH controls | Rheumatoid arthritis | Serum GCF | ↑ TOS in GCF of ChP and RA ChP groups (no difference for TOS and OSI in serum) | Esen et al., 2012 |
| Cross-sectional study | 18 ChP patients with hyperlipidemia 18 PH patients with hyperlipidemia 19 ChP patients SH 19 PH SH controls | Hyperlipidemia | Serum | ↑ MDA and 8-OHdG in patients with ChP and hyperlipidemia | Fentoglu Ö et al., 2015 |
| Cross-sectional study | 24 ChP with depression 23 ChP without depression | Depression | Plasma | ↑ nitric oxide metabolites, lipid peroxides, AOPP and TRAP in ChP with depression | Gomes et al., 2017 |
| Cross-sectional study | 16 T1DM with periodontitis 25 T2DM with periodontitis 24 SH with periodontitis | T1DM T2DM | Saliva | ↓ GSH and ↓GSSG in the patients with T1DM | Gumus et al., 2009 |
| Case-control study | 115 P women (6 month postpartum follow-up) 72 non-P women | Pregnancy | Saliva | ↑ 8-OHdG in PW; ↓ GPx decreased in PW; ↓ TBARS postpartum vs. non-pregnant women | Gümüş et al., 2015 |
| Prospective study | 218 P women 459 P women with mild periodontitis 114 P women with moderate-severe periodontitis | Pregnancy | Serum | ↑ 8-isoprostane in PW with moderate-severe periodontitis | Hickman et al., 2011 |
| Prospective study | 50 ChP patients 50 healthy controls | – | Serum Saliva | ↓ SOD in saliva and serum; ↑ prostaglandin E2, D2, prostaglandin F2α and TXB2, 5- hydroxyeicosatetraenoic acid, F2-isoprostanes; ↑ prostacyclin I2 and 13- hydroxyoctadecadienoic acid, 9- hydroxyoctadecadienoic acid | Huang et al., 2014 |
| Cross-sectional Study | 55 patients with DS 74 patients with mental retardation 88 healthy controls | Down Syndrome Mental retardation | Whole blood | ↑ oxidative burst activity of blood (monocytes and granulocytes) in DS patients with decreased periodontal health | Khocht et al., 2014 |
| Cross-sectional study | 26 AgP patients 30 ChP patients 25 healthy controls | – | Gingival blood Peripheral blood | ↑ 8-OHdG in gingival blood of ChP and AgP patients; ↓ TAC in gingival blood of ChP patients; ↓ TAC in peripheral blood of both groups | Konopka et al., 2007 |
| Cross-sectional study | 1,258 old men | Old age | Serum | ↓ beta-cryptoxanthin and beta-carotene with decreased periodontal health of old men | Linden et al., 2009 |
| Cross-sectional study | 356 periodontitis patients 207 PH controls | – | Plasma | ↑ reactive oxygen metabolites and shorter leukocyte telomere length in ChP | Masi et al., 2011 |
| Cross-sectional Correlational study | 20 ChP patients 20 PH controls | – | Saliva | ↑ 8-OHdG, MDA in ChP; ↓ uric acid, GPx activities and TAC in ChP (correlation with bone loss markers) | Miricescu et al., 2014 |
| Cross-sectional study | 10 T2DM patients PH 8 SH controls | T2DM | Periodontal tissue | ↑ MDA, ↓ GSH in periodontal tissue of T2DM | Monea et al., 2014 |
| Cross-sectional study | 24 ChP patients with ACS 24 patients PH with ACS 24 ChP patients without ACS 24 controls PH without ACS | Acute coronary syndrome | Saliva | ↑ 8-OHdG, MDA, and PC in patients (correlation with periodontal and cardiovascular markers) | Nguyen et al., 2016 |
| Cross-sectional study | 25 ChP patients 25 healthy controls | – | Plasma Gingival tissue Erythrocytes | ↑ TBARS in ChP; ↑ SOD, CAT, GPx activities in ChP; ↓ vitamins E, C and GSH in ChP | Panjamurthy et al., 2005 |
| Cross-sectional study | 29 ChP patients 20 healthy controls | – | Saliva | ↑ 8-OHdG in ChP (correlation with P. gingivalis) | Sawamoto et al., 2005 |
| Cross-sectional cohort study | 46 severe periodontitis patients 37 moderate periodontitis patients 46 mild periodontitis and healthy | – | Saliva | ↑ PC increased in severe periodontitis; ↓ urate and FRAP in severe periodontitis | Sculley and Langley-Evans, 2003 |
| Cross-sectional study | 20 ChP patients with RA 20 PH patients with RA 20 ChP patients without RA 20 PH SH controls | Rheumatoid arthritis | Serum | ↑ OSI and prolidase in ChP patients with RA | Sezer et al., 2013 |
| Cross-sectional study | 20 ChP patients with PS 20 PH patients with PS 20 ChP patients with PsA 20 PH patients with PsA 20 ChP SH patients 20 PH SH controls | Psoriasis Psoriatic arthritis | Serum | ↑ OSI (irrespective of periodontitis) in patients groups; (PS and PsA showed no effect on clinical parameters in ChP patients) | Sezer et al., 2016 |
| Cross-sectional study | 4,717 participants | Diabetes mellitus Hypertension | Serum | Periodontitis with highest 8-isoprostane quartile associated with ↑ CRP | Singer et al., 2015 |
| Cross-sectional correlational study | 29 severe periodontitis 77 moderate periodontitis 96 mild periodontitis and healthy | Diabetes mellitus Hypertension | Serum | ↑ ROM in patients with worst periodontal status | Tamaki et al., 2014b |
| Cross-sectional study | 25 severe periodontitis 43 moderate periodontitis 92 mild periodontitis and healthy | Diabetes mellitus Hypertension | Saliva | Superoxide and hydroxyl radical scavenging activities associated with periodontitis | Tamaki et al., 2015 |
| Cross-sectional study | 39 patients with periodontitis | – | Saliva | ↓ antioxidant concentrations related to periodontal status | Tartaglia et al., 2017 |
| Cross-sectional study | 23 smokers with ChP 23 former smokers with ChP 19 non-smokers with ChP 20 PH non-smokers controls | Smoking | Serum Gingival tissue | ↑ MDA in serum and gingival tissue in smoking ChP patients groups; ↓ SOD, CAT and GPx in ChP groups | Tonguç et al., 2011 |
| Cross-sectional study | 82 children | – | Saliva | TBARS in correlation to periodontal status; TAC related to periodontal status and oral hygiene; AOPP related to caries in children | Tothova et al., 2013 |
| Cross-sectional study | 30 ChP patients with T2DM 30 ChP SH patients 30 PH patients with T2DM 30 PH SH controls | T2DM | Plasma Saliva Red blood cell lysate | ↑ MDA in ChP patients irrespective of T2DM | Trivedi et al., 2014 |
| Cross-sectional study | 100 ChP patients 50 healthy controls | – | Saliva | ↑ 8-OHdG and human neutrophil elastase/alpha1-proteinase inhibitor in ChP | Villa-Correa et al., 2015 |
| Cross-sectional study | 19 patients with periodontitis 8 healthy controls | - | GCF | ↑ GPx, lactoferrin, myeloperoxidase and IL-1beta in periodontal tissues (correlation with clinical periodontal markers) | Wei et al., 2004 |
| Cross-sectional study | 31 smokers 90 non-smokers | Smoking | Saliva | ↑ 8-epi-PGF(2alpha) with periodontal status and smoking; Smoking ↑ TXB(2) and PGF(2alphas) and ↓ 6-oxo-PGF(1alpha) | Wolfram et al., 2006 |
| Cross-sectional study | 58 ChP patients 42 AgP patients 60 healthy controls | – | Saliva Buccal mucosa | ↑ micronuclei and nuclear abnormalities, as well as 8-OHdG in both periodontitis groups | Zamora-Perez et al., 2015 |
| Cross-sectional study | 45 severe periodontitis patients 37 healthy controls | – | Saliva | ↓ TAC in periodontitis (TOS no difference) | Zhang et al., 2015 |
ChP, chronic periodontitis; AgP, aggressive periodontitis; SH, systematically healthy; PH, periodontal healthy; T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus; PS, psoriasis; PsA, psoriatic arthritis; DS, Down syndrome; PW, pregnant woman; RA, Rheumatoid arthritis; ACS, Acute coronary syndrome; GCF, gingival crevicular fluid; TAC, total antioxidant capacity; TBARS, thiobarbituric acid reacting substances; 8-HOdG, 8-hydroxydeoxyguanosine; GPx, glutathione peroxidase; GSH, reduced glutathione; GSSG, oxidized glutathione; PC, protein carbonyls; MDA, malondialdehyde; TOS, total oxidant status; SOD, superoxid dismutase; OSI, oxidative stress index; IL-1beta, interleukin 1beta; ROM, reactive oxygen metabolites; ROS, reactive oxygen species; FRAP, ferric reducing antioxidant power; 4-HNE, 4-hydroxy-2-nonenal; CAT, catalase; CRP, C-reactive protein; AOPP, advanced oxidation protein products; TRAP, total radical-trapping antioxidant potential; MPO, myeloperoxidase; mtDNA, mitochondrial DNA.