Table 1.
Markers of Oxidative Stress in Patients with Psoriasis.
| Authors and Year | Country | Type of Study | Sample Size (Psoriasis/Controls) | Mean Disease Duration (Years) | Mean Age (Years) | Sample | Measured Parameters | Main Results (Psoriasis Versus Control Group) | |
|---|---|---|---|---|---|---|---|---|---|
| 1. | Kirmit et al. 2020 [14] | Turkey | Case–control study | 147 (87/60) | 7 (0–37) | 32.8 ± 15.6 | Venous blood | CRP, CAT, MPO, FOX, IMA | ↑CAT, FOX, IMA (p < 0.001), CRP (p = 0.04) ↑MPO (p = 0.123) |
| 2. | Oszukawska et al. 2020 [15] |
Poland | Case–control study | 96 (66/30) | 21–73 years | Venous blood | PON-1, alpha-tocopherol, uric acid, homocysteine | ↑Uric acid, homocysteine ↓PON-1 (p < 0.001), alpha tocopherol (p < 0.05) |
|
| 3. | Skutnik-Radziszewska et al. 2020 [16] |
Poland | Case–control study | 80 (40/40) | 12.7 ± 9 | 45.6 ± 20.2 | Venous blood, stimulated/unstimulated saliva | Px, CAT, SOD (saliva), TOS, OSI, AGE, AOPP, MDA, LOOH (blood and saliva) | ↑TOS, OSI, AGE, AOPP, MDA, LOOH (p < 0.001) (venous blood and saliva) ↑ROS (p < 0.001) (saliva) |
| 4. | Kiafar et al. 2020 [17] |
Iran | Observational study | 20 (20/0) | - | 38.9 ± 12.6 | Skin biopsy samples | TrxR | ↓TrxR (p < 0.01) |
| 5. | Skoie et al. 2019 [18] |
Norway | Case–control study | 168 (84/84) | 14 (8–24) | 45 | Venous blood | AOPP, MDA, CRP | AOPP unmodified ↓MDA (p = 0.03) |
| 6. | Kizilyel et al. 2019 [19] |
Turkey | Case–control study | 95 (50/45) | 8.8 ± 6.9 | 32.5 ± 14.5 | Venous blood | TOS, TAS, MDA, 8H2D | ↑TOS (p < 0.001) |
| 7. | Ergun et al. 2019 [20] |
Turkey | Case–control stody | 72 (50/20) | - | - | None (non-invasive measurements) | AGE | ↑AGE (p = 0.05) |
| 8. | Wojcik et al. 2019 [21] |
Poland | Case–control study | 48 (32/16) | - | 35 (Ps) 37(PsA) |
Venous blood | NADPH oxidase, Xanthine oxidase, ROS, CAT, GSH-Px, GSH | ↑NADPH, xanthine oxidase, ROS (PsA > Ps) (p < 0.05) ↓CAT, GSH (p < 0.05) |
| 9. | Esmaeili et al. 2019 [22] |
Iran | Case–control study | 20 (10/10) | 18.5 ± 3.1 (mild Ps), 13.5 ± 7.8 (moderate/severe Ps) |
37 (mild Ps) 27 (moderate/severe Ps) |
Venous blood | GSH, ROS, TAS, FRAP | ↑ROS (p = 0.04) ↓CAT (p = 0.02) |
| 10. | Elaine Husni et al. 2018 [23] |
USA | Cross sectional study | 688 (343 (198PsA, 143 Ps)/345) |
15.5 ± 13.2 (Ps), 21.1 ± 14.9 (PsA) | 45.7 ± 15.3 (Ps), 50.4 ± 11.8 (PsA) | Venous blood | PON-1, AS | ↓AS (p < 0.001), similar PON-1 levels |
| 11. | Haberka et al. 2018 [24] |
Poland | Case–control study | 119 (80/39) |
15.3 ± 11.2 | 43 ± 13.5 | Venous blood | Visfatin, Nesfatin, AOPP |
↑AOPP, visfatin |
| 12. | Ambrozewicz et al. 2018 [25] |
Poland | Case–control study | 102 (68/34) |
- | 38.2 | Venous blood | NADPH oxidase, Xanthine oxidase, GSH-Px, GSH-R, SOD, TrxR, GSH, Vitamin C | ↑NADPH oxidase, xanthine oxidase (Ps and PsA), SOD (only in Ps) (p < 0.05) ↓Trx, TrxR, GSH, Vitamin C (Ps and PsA), GSH-Px (only in PsA) (p < 0.05) |
| 13. | El-Rifaie et al. 2018 [26] |
Egypt | Case–control study | 101 (51/50) |
- | 45.6 ± 15.1 | Venous blood | HO | ↑HO (p < 0.001) |
| 14. | Asha et al. 2017 [27] |
India | Case–control study | 300 (150/150) |
- | 39.6 ± 11.9 | Venous blood | OxLDL, GSH, FRAP, MDA | ↑OxLDL, OxLDL/LDL (p < 0.01), MDA(p < 0.001) ↓GSH |
| 15. | Emre et al. 2017 [28] |
Turkey | Case–control study | 166 (90/76) |
- | 36.0 | Venous blood | Native SH, Total SH, SS | ↑Native SH (p = 0.013), Total SH (p = 0.04) |
| 16. | Papagrigoraki et al. 2017 [29] |
Italy | Cross sectional study | 160 (120 (80 Ps, 40 eczema)/40) |
- | 48 ± 8 (severe Ps). 47 ± 11 (mild Ps) | Venous blood | AGE(s) AGE(p) |
↑AGE(s) (p = 0.01) AGE(p) (p = 0.01) |
| 17. | Shahidi-Dadras et al. 2017 [30] |
Iran | Case–control study | 80 (40/40) |
10.1 ± 8.3 | 36.7 ± 14.8 | Venous blood | Cu, Fe, Trf, Cp | ↓Fe, Trf (p < 0.01) ↑Cp (p = 0.02) |
| 18. | Bakry et al. 2016 [31] |
India | Case–control study | 115 (85/30) |
0.3 ± 0.2 | 39.8 ± 18.1 | Urine | Urinary biopyrrins | ↑Urinary biopyrrins (p < 0.001) |
| 19. | Sunitha et al. 2016 [32] |
India | Cross sectional study | 90 (45/45) |
3.7 ± 5.1 | 44.9 ± 14.3 | Venous blood | AuAb-oxLDL, oxLDL | ↑AuAb-oxLDL, OxLDL (p < 0.001) |
| 20. | Dilek et al. 2016 [33] |
Turkey | Case–control study | 75 (50/25) |
- | 36.8 ± 8.2 | Venous blood, skin biopsy samples | iNOS, MPO | ↑MPO (p < 0.05) |
| 21. | Yazici et al. 2016 [34] |
Turkey | Case–control study | 43 (29/14) |
11.4 ± 9.3 | 39.1 ± 12.4 | Venous blood | MPO, PCC, AOPP, LOOH, PP | ↑MPO, PCC, AOPP, LOOH, PP (p < 0.05) |
| 22. | Zhou et al. 2015 [35] |
China | Case–control study | 379 (214/165) | - | 41.0 ± 12.6 | Venous blood | TB, CRP | ↓TB (p < 0.001) ↑CRP (p < 0.001) |
| 23. | Ikonomidis et al. 2015 [36] |
Greece | Cross sectional study | 158 (118 (59 Ps, 59 CAD)/40) |
- | 51 ± 12.2 | Venous blood | MDA, IL-6 | ↑MDA, IL-6 (p < 0.05) |
| 24. | Surucu et al. 2015 [37] |
Turkey | Case–control study | 87 (40/47) |
10.1 ± 7.7 | 37.9 ± 10.8 | Venous blood | Prolidase, TOS, TAS, OSI | ↓TAS (p = 0.01) ↑Prolidase, TOS (p = 0.01), OSI (p < 0.001) |
| 25. | Chandrashekar et al. 2015 [38] |
India | Cross sectional study | 86 (43/43) |
4.1 ± 4 | 44.6 ± 12.0 | Venous blood | 25-OH-vitD, CRP, IMA | ↓25-OH-vitD (p = 0.004) ↑CRP (p = 0.002), IMA (p < 0.001) |
| 26. | Nemati et al. 2014 [39] |
Iran | Case–control study | 200 (100/100) |
4.5 ± 2.4 | 35.7 ± 10 | Venous blood | PON-1, SOD, CAT, MDA | ↓PON-1, SOD, CAT (p < 0.05) ↑MDA |
| 27. | Pujari et al. 2014 [40] |
India | Case–control study | 180 (90/90) |
- | 20–60 | Venous blood | MDA, vitamin E, CAT | ↓Vitamin E, CAT (p < 0.001) ↑MDA (p < 0.001) |
| 28. | Balta et al. 2014 [41] |
Turkey | Case–control study | 115 (60/55) |
7.5 ± 9.1 | 36.8 ± 12.8 | Venous blood | TB, DB, IB, CRP | ↓TB (p < 0.08), DB (p < 0.001) ↑IB (p < 0.05), CRP (p < 0.001) |
| 29. | Meki et Shobaili, 2014 [42] |
Saudi Arabia | Case–control study | 80 (60/22) |
10.3 ± 0.9 | 30.2 ± 1.4 | Venous blood | NO | ↑NO (p < 0.001) |
| 30. | He et al. 2014 [43] |
China | Cross sectional study | 50 (25/25) |
- | 43.04 ± 11.15 | Venous blood | MDA, PON-1 | ↓PON-1 (p < 0.01) ↑MDA (p < 0.05) |
| 31. | Kaur et al. 2013 [44] |
Estonia | Case–control study | 107 (60/47) |
18.6 ± 11.0 | 43.2 ± 12.4 | Venous blood | TPX, TAS, OSI, Methylglycoxal | ↓TAS (p < 0.001) ↑TPX, OSI (p < 0.001), Methylglycoxal (p = 0.01) |
| 32. | Damasiewicz-Bodzek et Wielkoszynski, 2012 [45] |
Poland | Case–control study | 160 (80/80) |
10.2 ± 8.1 | 37.1 ± 10.8 | Venous blood | AGE, Ab anti CEL, Ab anti CML | ↑AGE, Ab anti CEL, Ab anti CML (p < 0.05) |
| 33. | Emre et al. 2012 [46] |
Turkey | Case–control study | 116 (54 (28 smokers, 26 non-smokers)/62) |
9.51 ± 7,19 (non-smokers), 9.715 ± 7.84 (smokers) | 39.9 ± 11.1 (non-smokers), 39.6 ± 12.9 (smokers) | Venous blood | TOS, TAS, AS, OSI | ↓TAS (p < 0.01), PON-1 (p = 0.01—in smokers) ↑TOS, OSI (p < 0.01) |
| 34. | Gabr and Al-Ghadir, 2012 [47] |
Egypt | Case–control study | 75 (55/20) |
4.72 ± 1.7 | 29 ± 13.6 | Venous blood | MDA, NO, SOD, CAT, TAS | ↓TAS, SOD, CAT (p < 0.001) ↑MDA, NO (p < 0.001) |
| 35. | Ozdemir et al. 2012 [48] |
Turkey | Case–control study | 52 (26/26) |
6.6 ± 5.8 | 38.9 ± 11.5 | Venous blood | IMA | ↑IMA (p = 0.001) |
| 36. | Lima et Kimball, 2011 [49] |
USA | Cross sectional study | 116 (42/72) |
- | 49.4 | None (non-invasive measurements) | Skin Carotenoid level | ↓Skin carotenoid level (p = 0.003) |
| 37. | Usta et al. 2011 [50] |
Turkey | Cross sectional study | 77 (52 (27 without MS, 25 with MS)/25) |
10 (without MS), 10 (with MS) | - | Venous blood | TAS, TOS, PON-1, AS | ↓PON-1, AS |
| 38. | Ferretti et al. 2011 [51] |
Italy | Case–control study | 48 (23/25) |
- | 47.5 ± 13.5 | Venous blood | PON-1, AS, LOOH | ↓PON-1, AS ↑LOOH (p < 0.001) |
| 39. | Sikar Akturk et al. 2011 [52] |
Turkey | Case–control study | 46 (23/23) |
- | 42.8 ± 16.5 | Venous blood, skin biopsy samples | NO, MDA | ↑NO, MDA (p < 0.001) |
| 40. | Basavaraj et al. 2011 [53] |
India | Case–control study | 40 (30/10) |
- | 25–45 | Venous blood | 8-OHdG, TAS |
↑8-OHdG (p < 0.05) |
| 41. | Kadam et al. 2010 [54] |
India | Case–control study | 120 (90/30) |
- | - | Venous blood | MDA, NO, SOD, CAT, TAS | ↓TAS, SOD, CAT (p < 0.01) ↑MDA, NO (p < 0.01) |
| 42. | Abeyakirthi et al. 2010 [55] |
Scotland | Case–control study | 16 (8/8) |
- | 21–50 | Skin tape strips | Ornithine, Arginine | ↑Ornithine (p < 0.001) ↓Arginine (p = 0.005) |
| 43. | Hashemi et al. 2009 [56] |
Iran | Case–control study | 86 (40/46) |
- | 30.6 (8–80) | Venous blood | ADA, s-TIC, TAS | ↓TAS (p = 0.02) ↑ADA (p < 0.001), s-TIC (p < 0.001) |
| 44. | Nakai et al. 2009 [57] |
Japan | Case–control study | 70 (49 (29 Ps, 21 AD)/20) | - | 55 (21–76) | Urine | Nitrate, 8-OHdG, MDA | ↑Nitrate (p = 0.03), 8-OHdG (p = 0.03) (Ps versus control) |
| 45. | Toker et al. 2009 [58] |
Turkey | Case–control study | 53 (30/23) | 7.2 | 30.4 ± 10.6 | Venous blood | MDA, TAS, PON-1, AS | ↑PON-1, sodium stimulated PON-1 (p < 0.05), AS (p < 0.01) |
| 46. | Kaur et al. 2008 [59] |
Estonia | Case–control study | 44 (22/22) | - | 48 | Venous blood | Adiponectin, GSH, GSSG | ↑GSSG/GSH |
| 47. | Tekin et al. 2007 [60] |
Turkey | Case–control study | 124 (84/40) | - | 39 (17–58) | Skin biopsy samples | Ox-LDL | ↑Ox-LDL |
| 48. | Karaman et al. 2007 [61] |
Turkey | Case–control study | 66 (36/30) | 7.08 ± 4.52 | 39.3 ± 13.4 | Venous blood | SOD, GSH-Px(e), CAT | ↓SOD (p < 0.001), CAT (p < 0.05) ↑GSH-Px(e) (p < 0.05) |
| 49. | Rocha-Pereira et al. 2004 [62] |
Portugal | Case–control study | 100 (60/40) | 0.5–50 | 46 ± 12 | Venous blood | TBA, TAS, Transferrin, Ceruloplasmin, CRP | ↓TAS (p < 0.001) |
| 50. | Kural et al. 2003 [63] |
Turkey | Case–control study | 70 (35/35) | - | 27–43 | Venous blood | AuAb-oxLDL, CRP, MDA, LOOH, TAS, SOD, GSH-Px, GSH-R, CAT | ↓CAT(e)(p = 0.001), SOD (e-p = 0.01, p-p = 0.003), GSH-Px(e) (p = 0.02), TAS(p) (p = 0.03) ↑AuAb-oxLDL (p = 0.002), MDA (from LDL p = 0.018, from oxLDL-p < 0.001, from e-p < 0.001), LOOH (p = 0.001) |
| 51. | Baz et al. 2003 [64] |
Turkey | Case–control study | 59 (35/24) | 7.83 ± 8.14 | 42.5 ± 13.7 | Venous blood | MDA, SOD, TAS | ↓TAS (p = 0.001) ↑SOD (p = 0.01), MDA (p = 0.005) |
| 52. | Yldirim et al. 2003 [65] |
Turkey | Case–control study | 44 (22/22) | 10 | 37 | Venous blood, skin biopsy samples | SOD(e), GSH-Px(e), CAT(p), MDA(p and skin) | ↓SOD (e) (p < 0.05) ↑CAT(p) (p < 0.05), MDA skin (p < 0.01) |
| 53. | Relhan et al. 2002 [66] |
India | Case–control study | 80 (40/40) | 5.6 | - | Venous blood | MDA, Thiols | ↓Thiols (p < 0.001) ↑MDA (p < 0.001) |
CRP—C-reactive protein, CAT—catalase, MPO—myeloperoxidase, FOX—ferroxidase, IMA—ischemia modified albumin, PON-1—paraoxonase 1, TOS—total oxidant status, TAS—total antioxidant status, MDA—malondialdehyde, 8H2D—8-hydroxy 2′-deoxyguanosine, AOPP—advanced oxidation protein products, NADPH oxidase—nicotinamide adenine dinucleotide phosphate, ROS—reactive oxygen species, GSH-Px—glutathione peroxidase, GSH—glutathione, TrxR—thioredoxin reductase, FRAP—ferric reducing ability of plasma, AS—arylesterase, OSI—oxidative stress index, Px—salivary peroxidase, SOD—superoxide dismutase, AGE—advanced glycation end-products, LOOH—lipid hydroperoxides, OxLDL—oxidized low-density lipoproteins, NO—nitric oxide, 8-OHdG—8-hydroxy guanosine, iNOS—inducible nitric oxide, GSH-R—glutathione reductase, MS—metabolic syndrome, 25-OH-vitD—25-hydroxy-vitamin D, ADA—adenosine deaminase, s-TIC—serum trypsin inhibitory capacity, TBA—thiobarbituric acid, AD—atopic dermatitis, TPX—total peroxide concentration, PCC—protein carbonyl compounds, PP—pyrrolized protein, GSSG—oxidized glutathione, HO—hemoxygenase, TB—total bilirubin, DB—direct bilirubin, IB—indirect bilirubin, Cu—copper, Fe—iron, Trf—transferrin, Cp—ceruloplasmin, AuAb-oxLDL—autoantibodies anti-oxidized LDL, SH—thiol, SS—disulfide, CAD—coronary artery disease, IL-6—interleukin-6, Ab anti-CEL—anti-carboxyethyllysine antibodies, Ab anti CML—anti-carbocymethyllysine antibodies. e—erythrocyte, p—plasma, s—skin. ↑, increased. ↓, decreased.