Review Article

Meta-Analysis of Assessment of Total Oxidative Stress and Total Antioxidant Capacity in Patients with Periodontitis

Table 3

The mean values of TAC in various biological fluid samples between healthy controls and patients with periodontitis in the included studies included in the meta-analysis.

Author name and YearCountryStudy designCriteriaAge years case/control mean ± SD or rangeSample typeUnitPeriodontitisControlp-ValueMethod of assessment
Mean ± SD or median (upper–lower value)Sample size (M/F)Mean ± SD or median (upper–lower value)Sample size (M/F)

Chapple et al. [5]UKCSGustafsson et al. [49]46.1/46.9Plasmaµmol TEq/l501.8 ± 12310 (5/5)577.9 ± 99.810 (5/5)>0.05Chapple et al. [54]
Brock et al. [6]UKCCPPD ≥ 5 mm at least two sites per quadrant, BOP, radiographic LB ≥ 30%43.5 (23–60) /44.7 (24–63)Salivanmol/30s sample0.18 ± 0.0817 (7/10)0.14 ± 0.0617 (7/10)NSChapple et al. [54]
GCFµmol0.14 ± 0.060.18 ± 0.08<0.001
Baltacıoğlu et al. [7]TurkeyComparative studyArmitage [47]37.4 ± 5.4/37.1 ± 4.2SerummM Trolox equivalent0.53 ± 0.1931 (F)0.72 ± 0.2126 (F)<0.05Erel [55]
GCF0.07 ± 0.030.12 ± 0.05
GCF TAOC/30 s0.36 ± 0.120.50 ± 0.16
Chapple et al. [8]UKInterventionalBrock et al. [6]32–60Plasmaµmol TEq507 ± 9235
(12/23)
520 ± 10032 (N/A)0.57Chapple et al. [54] Maxwell et al. [56]
GCF680 ± 3711129 ± 722<0.0001
Konopka et al. [10]PolandCCLindhe et al. [50]31.5/33.2Venous Bloodmmol/l1.68 ± 0.1330
(15/15)
1.94 ± 0.1225
(10/15)
<0.001ABTS reduction method
Gingival Blood1.81 ± 0.181.94 ± 0.130.029
Guentsch et al. [11]GermanyInterventional studyAt least 30% of teeth with PPD >5 mm46.3 ± 13.1/34.1 ± 11.8Salivaμmol/ml0.37 ± 0.2415
(6/9)
0.52 ± 0.2015
(7/8)
<0.05Popov and Lewin [57]
Akalin et al. [12]TurkeyCSArmitage [47]29.3 ± 3.94/29.73 ± 3.71SerummM Trolox equivalent0.59 ± 0.2027 (F)0.75 ± 0.2125(F)<0.005Erel [55]
GCF Conc0.09 ± 0.030.17 ± 0.04
GCF TAC/30s0.40 ± 0.110.59 ± 0.10
Su et al. [13]USACS–CCScully and Langley-Evans [51]52.27 (14.08)/45.39 (18.75) SEMSalivammol0.71 ± 0.0858
(25/33)
0.46 ± 0.04234 (107/126)0.0001Miller et al. [58]
Kim et al. [14]KoreaInterventional studyPPD ≥ 5 mm at least two sites per quadrant, BOP, radiographic LB ≥ 30%50.0 ± 12.5/31.7 ± 8.0SalivaμM335.7 ± 36.67 (3/4)282.7 ± 55.17 (3/4)ImAnOx (TAS) Kit
Sulaiman and Shehadeh [15]SyriaInterventional studyPPD ≥ 5 mm at least two sites per quadrant, BOP, radiographic LB ≥ 30%41/34Plasmaµmol TEq559 ± 53.230
(9/21)
625 ± 88.730
(9/21)
<0.001Erel [55]
Dhotre et al. [17]IndiaCCArmitage [47]52.7 ± 9.27/50.3 ± 9.39Plasmammol/l1.3 ± 0.15100
(60/40)
2.32 ± 0.24100
(60/40)
<0.001Benzie and Strain [59]
Saliva0.46 ± 0.071.07 ± 0.03
Dhotre et al. [18]IndiaCCArmitage [47]52.7 ± 9.27/50.03 ± 9.39Plasmammol/l1.14 ± 0.13502.32 ± 0.2425<0.001Benzie and Strain [59]
Esen et al. [19]TurkeyCSAL ≥ 4 mm and PPD ≥ 5 mm.42.85 ± 9.6/40.05 ± 9.8Serummillimoles trolox equivalent per/l1.980 (1.835– 2.195)20 (4/16)2.510 (2.170– 2.725)20 (4/16)<0.001Erel [55]
GCF0.0875 (0.059 to 0.140)0.105 (0.070– 0.145)
Konuganti et al. [20]IndiaCCPPD ≥ 5 mm at least 2 sites per quadrant, BOP18–40 yearsBloodµg/dl37.13 ± 7.141552.4 ± 9.7115<0.001NBT method
Toker et al. [21]TurkeyInterventional studyCAL > 30% of sites; PPD ≥ 5 mm38.7 ± 5.9/38.0 ± 7.2GCFmmol TEq/l0.12 ± 0.3315 (7/8)0.13 ± 0.2510 (6/4)>0.05Erel [55]
Akpinar et al. [22]TurkeyInterventionalArmitage [47]37.7 ± 5.9/37.0 ± 7.4GCFmmol Trolox equiv./l(0–0.1) 0.115
(7/8)
(0.1–0.1) 0.110
(5/5)
Erel [55]
Novaković et al. [23]SerbiaPSBone loss >30%, at least one pocket; PPD >5 mm per quadrant with BOP39.2 ± 11.5/35.2 ± 7.1Salivaµmol/l0.4 ± 0.2421
(14/7)
0.59 ± 0.1421
(14/7)
>0.05ABTS colorimetric, Ransod kit
Sezer et al. [24]TurkeyCS45.50 ± 7.50/40.75 ± 10.26Serummmol Trolox Eq/l1.15 ± 0.3620
(6/14)
1.30 ± 0.2320
(6/14)
Erel [55]
Azizi et al. [25]IndiaCCArmitage [47]37–50/39.64 ± 5.04Plasmaμmol/l831.75 ± 78.15134 (M)925.2 ± 68.464 (M)0.001Benzie and Strain [59]
Baltacıoğlu et al. [26]TurkeyCS and CCArmitage [47]32.55 ± 5.32/30.10 ± 4.06Serummmol TEq1.08 ± 0.073633
(16/17)
1.5 ± 0.073630
(16/14)
0.001ABTS Erel [55]
Salivammol TEq0.5 ± 0.110.71 ± 0.08<0.05Elisa kit
Bostanci [27]TurkeyInterventional studiesArmitage [47]38.80 ± 4.87/37.33 ± 5.67GCFμmol trolox equivalent/l0.09 (0.07–0.11)15
(6/9)
0.07 (0.05–0.15)15 (7/8)>0.05Erel [55]
Serum1.45 (1.23–2.10)1.44 (1.28–1.68)
Kose et al. [28]TurkeyComparative studyArmitage [47]27–51 yearsSalivammol TEq/l0.77 ± 0.1422 (11/11)0.92 ± 0.2222
(12/10)
<0.05Erel [55]
Serummmol TEq/l1.16 ± 0.291.34 ± 0.32
Miricescu et al. [29]RomaniaCCAt least six sites with PD ≥ 4 mm; bone loss higher than 30% and gingival inflammation51.26 ± 7.4/18.66 ± 2Salivanmol/mg albumin0.75 ± 0.1625
(14/11)
1.24 ± 0.1625
(20/5)
<0.05ABTS colorimetric, Ransod kit
Thomas et al. [31]IndiaInterventionalCAL ≥ 4 mm in at least 30% of sites35–65Serummmol/l0.4972 ± 0.2250251.2585 ± 0.368325<0.001
Almerich-Silla et al [32]SpainCCAt least four zones with PP ≥ 5 mm and LA ≥ 2 mm41–45/38–43Salivammol1.09 ± 0.090533
(19/14)
0.9067 ± 0.11937
(15/22)
<0.001Elisa kit
Baser et al. [33]TurkeyCCArmitage [47]39.9 ± 5.2/37.3 ± 5.4Salivaμmol0.33 ± 0.336
(11/25)
0.57 ± 0.316
(6/10)
<0.05Commercially available calorimetry
Plasmaμmol0.27 ± 0.140.44 ± 0.26
Shankarram et al. [34]IndiaCCSalivammol1.03 ± 0.158250.906 ± 0.11925<0.01Elisa kit
Nguyen et al. [35]VietnamCSArmitage [47]51.04 ± 12.25/51.17 ± 11.88Salivammol0.07 ± 0.0724
(12/12)
0.19 ± 0.1424
(14/10)
<0.001Antioxidant assay kit
Atabay et al. [36]TurkeyCC≥ 30% of sites with PPD ≥ 5 mm; with CAL ≥ 5 mm; ≥ 30% LB42.47 ± 2.99/39.60 ± 5.84GCF ConcentrationµM/ml72.43 ± 6.7915 (9/6)351.60 ± 21.6615
(6/9)
0.001TAOC (ImAnOx-TAS)/TAC Kit
GCF TotalµM69.70 ± 3.3788.01 ± 4.61
Bansel et al. [37]IndiaInterventionalArmitage [47]20–45Plasmaµmol/l792.33 ± 124.33401,076.1 ± 193.8240<0.001Benzie and Strain [59]
Ahmadi-Motamayel et al. [38]IranCCPage and Eke [52]30–50 (Both groups)Salivamol/ml unit0.16 ± 0.0955
(28/27)
0.18 ± 0.156
(28/28)
0.11Riviere and Papagiannoulis [60]
Serummol/ml unit0.36 ± 0.010.37 ± 0.05
Punj et al. [39]IndiaComparative studyArmitage [48]25–65 (Both groups)Salivammol/l0.44 ± 0.14200.48 ± 0.1820>0.05Phosphomolybdenum method
Serummmol/l0.58 ± 0.130.94 ± 0.36<0.001
Narendra et al. [40]IndiaCCArmitage [47]47.13 ± 7.00/36.56 ± 6.26Serummmol/l0.49 ± 0.07546
(29/17)
1.23 ± 0.2250
(33/17)
<0.001Miller et al. [58]
GCFmmol/l0.655 ± 0.161.36 ± 0.11
Tripathi et al. [41]IndiaCCArmitage [47]> 18 yearsSalivamM Trolox equivalent0.60400.78400.04ELISA
Serum1.101.500.03
Vincent et al. [42]IndiaComparative studyArmitage [48]25–65 yearsGCFmmol/l0.75 ± 0.24201.2 ± 0.41200.001Erel [55]
Sánchez-Villamil et al. [43]ColombiaCS and CCPage and Eke [52]45 ± 12/31 ± 10Salivammol0.32 ± 0.2187
(45/42)
0.15 ± 0.114
(6/8)
0.004TAC assay kit (CS0790—Sigma- Aldrich)
Senouci et al. [44]AlgeriaCCPPD ≥ 6 mm; with CAL ≥ 5 mm; Tooth loss due to periodontitis24.06 ± 6.09/24.73 ± 1.38Salivaμmol ascorbic acid eq/l0.46 ± 0.34291.45 ± 0.5728<0.0001Kerboua et al. [61]
Thomas et al. [45]IndiaRCT30–60
(Both)
Serumµg/ml0.5865 ± 0.17011001.1028 ± 0.2600100<0.001Phosphomolybdenum assay
Verghese et al. [46]IndiaLSMinimum 20 natural teeth; PPD at least 30% of sites; CAL >3 mm; bone loss30–60
(Both)
Serum0.56 ± 0.04251.92 ± 0.1025<0.001Phosphomolybdenum assay

SD, standard deviation; Cont, control; TEq, Trolox equivalent; ABTS, 2,2′-azinobis (3-ethylbenzothiazoline-6-sulfonic acid) FRAP, ferric reducing antioxidant power; TAC, total antioxidant capacity; PPD, periodontal pocket depth; BOP, bleeding on probing; LB, loss of bone; CAL, clinical attachment level; CC, case–control; PS, prospective study; CS, cross-sectional study; RCT, randomized controlled trial; LS, longitudinal study.