Effects of conventional laser photocoagulation and subthreshold micropulse laser photocoagulation on concentration of vascular endothelial growth factor, interleukin-33 and NO in vitreous of proliferative diabetic retinopathy eyes_Chinese Journal of Ocular Fundus Diseases

Authors：

Lian Haiyan , Chen Xiao , Ding Qin , Yan Ming , Huang Zhen , Yan Ying ,  Song Yanping

Department of Ophthalmology, Central Theater Command General Hospital, Clinical Research Center for Fundus Laser in Hubei Province, Wuhan 430070, China;

Corresponding author：

Song Yanping, Email: songyanping@medmail.com.cn

Keywords：

Diabetic retinopathy/therapy; Laser coagulation; Vascular endothelial growth factors; Interleukins; Nitric oxide

DOI：

10.3760/cma.j.issn.1005-1015.2019.02.004

Video：

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ObjectiveTo analyze the expression of VEGF, IL-33 and NO concentration after laser photocoagulation and subthreshold micropulse laser photocoagulation conventional in proliferative diabetic retinopathy (PDR) patients.MethodsA case control study. The clinical data of 39 patients of PDR and 11 patients of idiopathic macular pucker (IMP) from Department of Ophthalmology, Central Theater General Hospital during November 2015 were collected in this study. PDR patients were assigned randomly into three groups. Fifteen PDR patients with 15 eyes were treated with conventional laser as group A. Thirteen PDR patients with 13 eyes were treated with subthreshold micropulse laser as group B. Eleven PDR patients with 11 eyes without any laser therapy were grouped as C. Eleven IMP patients were grouped as D. There was no difference of age (F=0.53, P=0.23), gender ratio (χ²=0.55, P=0.91), body mass index (F=2.62, P=0.07), duration diabetes (F=0.29, P=0.75), glycoslated hemglobin (F=1.72, P=0.19) in four groups. All PDR patients were examined with FFA. Total protein was quantified by a bicinchoninic acid assay kit. Levels of VEGF, IL-33, NO were determined using enzyme-linked immunosorbent assay kits.ResultsThere was no difference of total protein in four groups (F=1.78, P=0.17). Group C had a higher VEGF level than group A and B (F=7.84, P=0.002). Group A had a higher IL-33 level than group C (t=4.15, P=0.02). There was no difference of IL-33 level in group B and C (t=1.34, P=0.20). Group D had a lower NO level than group A, B, C (F=38.42, P＜0.001). There was no difference of NO level in group A, B and C (F=3.29, P=0.06).ConclusionsBoth conventional laser photocoagulation and subthreshold micropulse laser photocoagulation can decrease vitreous VEGF level and subthreshold micropulse laser photocoagulation can induce less IL-33 level.

Citation： Lian Haiyan, Chen Xiao, Ding Qin, Yan Ming, Huang Zhen, Yan Ying, Song Yanping. Effects of conventional laser photocoagulation and subthreshold micropulse laser photocoagulation on concentration of vascular endothelial growth factor, interleukin-33 and NO in vitreous of proliferative diabetic retinopathy eyes. Chinese Journal of Ocular Fundus Diseases, 2019, 35(2): 124-128. doi: 10.3760/cma.j.issn.1005-1015.2019.02.004 Copy

1.	Klein R, Davis MD, Moss SE, et al. The Wisconsin epidemiologic study of diabetic retinopathy: a comparison of retinopathy in younger and older onset diabetic persons[J]. Adv Exp Med Biol, 1985, 189: 321-335. DOI: 10.1007/978-1-4757-1850-8.
2.	Matri KE, Chebbi Z, Falfoul Y, et al. Treatment of diabetic macular edema with micropulse laser therapy[J]. Acta Ophthalmol, 2017, 95 Suppl 259: S1. DOI: 10.1111/j.1755-3768.2017.0F031.
3.	Matri LE, Falfoul Y, Chebbi Z, et al. Improvement of diabetic macular edema after micropulse laser therapy[J]. Acta Ophthalmol Scand, 2016, 94 Suppl 256: S1. DOI: 10.1111/j.1755-3768.2016.0535.
4.	Barquet LA. Role of VEGF in diseases of the retina[J]. Arch Soc Esp Oftalmol, 2015, 90 Suppl 1: S3-5. DOI: 10.1016/S0365-6691(15)30002-2.
5.	Ha JM, Jin SY, Lee HS, et al. Regulation of retinal angiogenesis by endothelial nitric oxide synthase signaling pathway[J]. Korean J Physiol Pharmacol, 2016, 20(5): 533-538. DOI: 10.4196/kjpp.2016.20.5.533.
6.	Choi YS, Choi HJ, Min JK, et al. Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production[J]. Blood, 2009, 114(14): 3117-3126. DOI: 10.1182/blood-2009-02-203372.
7.	Chamberlain JJ, Johnson EL, Leal S, et al. Cardiovascular disease and risk management: review of the American diabetes association standards of medical care in diabetes 2018[J]. Ann Intern Med, 2018, 168(9): 640-650. DOI: 10.7326/M18-0222.
8.	陈喆, 张士胜, 朱惠敏. 糖尿病视网膜病变的国际临床分类分析[J]. 国际眼科杂志, 2011, 11(8): 1394-1401. DOI: 10.3969/j.issn.1672-5123.2011.08.025.Chen Z, Zhang SS, Zhu HM. Analysis of international clinical diabetic retinopathy disease severity scale[J]. Int Eye Sci, 2011, 11(8): 1394-1401. DOI: 10.3969/j.issn.1672-5123.2011.08.025.
9.	Hwang JU, Sohn J, Moon BG, et al. Assessment of macular function for idiopathic epiretinal membranes classified by spectral-domain optical coherence tomography[J]. Invest Ophthalmol Vis Sci, 2012, 53(7): 3562-3569. DOI: 10.1167/iovs.12-9762.
10.	Ohkoshi K, Tsuiki E, Kitaoka T, et al. Visualization of subthreshold micropulse diode laser photocoagulation by scanning laser ophthalmoscopy in the retro mode[J]. Am J Ophthalmol, 2010, 150(6): 856-862. DOI: 10.1016/j.ajo.2010.06.022.
11.	Funatsu H, Noma H, Mimura T, et al. Association of vitreous inflammatory factors with diabetic macular edema[J]. Ophthalmology, 2009, 116(1): 73-79. DOI: 10.1016/j.ophtha.2008.09.037.
12.	Lip PL, Belgore F, Blann AD, et al. Plasma VEGF and soluble VEGF receptor FLT-1 in proliferative retinopathy: relationship to endothelial dysfunction and laser treatment[J]. Invest Ophthalmol Vis Sci, 2000, 41(8): 2115-2119.
13.	Wilson AS, Hobbs BG, Shen WY, et al. Argon laser photocoagulation-induced modification of gene expression in the retina[J]. Invest Ophthalmol Vis Sci, 2003, 44(4): 1426-1434. DOI: 10.1167/iovs.02-0622.
14.	Luttrull JK, Sramek C, Palanker D, et al. Long-term safety, high-resolution imaging, and tissue temperature modeling of subvisible diode micropulse photocoagulation for retinovascular macular edema[J]. Retina, 2012, 32(2): 375-386. DOI: 10.1097/IAE.0b013e3182206f6c.
15.	Li Z, Song Y, Chen X, et al. Biological modulation of mouse RPE cells in response to subthreshold diode micropulse laser treatment[J]. Cell Biochem Biophys, 2015, 73(2): 545-552. DOI: 10.1007/s12013-015-0675-8.
16.	Bromberg-White JL, Glazer L, Downer R, et al. Identification of VEGF-independent cytokines in proliferative diabetic retinopathy vitreous[J]. Invest Ophthalmol Vis Sci, 2013, 54(10): 6472-6480. DOI: 10.1167/iovs.13-12518.
17.	Li J, Hu WC, Song H, et al. Increased vitreous chemerin levels are associated with proliferative diabetic retinopathy[J]. Ophthalmologica, 2016, 236(2): 61-66. DOI: 10.1159/000447752.
18.	Manaviat MR, Rashidi M, Afkhami-Ardekani M, et al. Effect of pan retinal photocoagulation on the serum levels of vascular endothelial growth factor in diabetic patients[J]. Int Ophthalmol, 2011, 31(4): 271-275. DOI: 10.1007/s10792-011-9448-6.
19.	Mohamed TA, Mohamed Sel-D. Effect of pan-retinal laser photocoagulation on plasma VEGF, endothelin-1 and nitric oxide in PDR[J]. Int J Ophthalmol, 2010, 3(1): 19-22. DOI: 10.3980/j.issn.2222-3959.2010.01.05.
20.	Itaya M, Sakurai E, Nozaki M, et al. Upregulation of VEGF in murine retina via monocyte recruitment after retinal scatter laser photocoagulation[J]. Invest Ophthalmol Vis Sci, 2007, 48(12): 5677-5683. DOI: 10.1167/iovs.07-0156.
21.	Konac E, Sonmez K, Bahcelioglu M, et al. Does pattern scan laser (PASCAL) photocoagulation really induce less VEGF expression in murine retina than conventional laser treatment?[J]. Gene, 2014, 549(1): 156-160. DOI: 10.1016/j.gene.2014.07.062.
22.	Riddell JR, Maier P, Sass SN, Peroxiredoxin 1 stimulates endothelial cell expression of VEGF via TLR4 dependent activation of HIF-1α[J/OL]. PLoS One, 2012, 7(11): 50394[2012-11-21]. https://doi.org/10.1371/journal.pone.0050394. DOI: 10.1371/journal.pone.0050394.
23.	Flaxel C, Bradle J, Acott T, et al. Retinal pigment epithelium produces matrix metalloproteinases after laser treatment[J]. Retina, 2007, 27(5): 629-634. DOI: 10.1097/01.iae.0000249561.02567.fd.
24.	Lavinsky D, Sramek C, Wang J, et al. Subvisible retinal laser therapy: titration algorithm and tissue response[J]. Retina, 2014, 34(1): 87-97. DOI: 10.1097/IAE.0b013e3182993edc.
25.	Arany PR, Nayak RS, Hallikerimath S, et al. Activation of latent TGF-beta1 by low-power laser in vitro correlates with increased TGF-beta1 levels in laser-enhanced oral wound healing[J]. Wound Repair Regen, 2007, 15(6): 866-874. DOI: 10.1111/j.1524-475X.2007.00306.x.
26.	Szymanska J, Goralczyk K, Klawe JJ, et al. Phototherapy with low-level laser influences the proliferation of endothelial cells and vascular endothelial growth factor and transforming growth factor-beta secretion[J]. J Physiol Pharmacol, 2013, 64(3): 387-391.
27.	Mandriota SJ, Menoud PA, Pepper MS. Transforming growth factor beta 1 down-regulates vascular endothelial growth factor receptor 2/flk-1 expression in vascular endothelial cells[J]. J Biol Chem, 1996, 271(19): 11500-11505. DOI: 10.1074/jbc.271.19.11500.
28.	Arend WP, Palmer G, Gabay C. IL-1, IL-18, and IL-33 families of cytokines[J]. Immunol Rev, 2008, 223: 20-38. DOI: 10.1111/j.1600-065X.2008.00624.x.
29.	Schmitz J, Owyang A, Oldham E, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines[J]. Immunity, 2005, 23(5): 479-490. DOI: 10.1016/j.immuni.2005.09.015.
30.	Takeuchi M, Sato T, Tanaka A, et al. Elevated levels of cytokines associated with Th2 and Th17 cells in vitreous fluid of proliferative diabetic retinopathy patients[J/OL]. PLoS One, 2015, 10(9): 137358[2015-09-09]. https://doi.org/10.1371/journal.pone.0137358. DOI: 10.1371/journal.pone.0137358.
31.	Shimura M, Yasuda K, Nakazawa T, et al. Panretinal photocoagulation induces pro- inflammatory cytokines and macular thickening in high-risk proliferative diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2009, 247(12): 1617-1624. DOI: 10.1007/s00417-009-1147-x.
32.	Han JW, Choi J, Kim YS, et al. Comparison of the neuroinflammatory responses to selective retina therapy and continuous-wave laser photocoagulation in mouse eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(2): 341-353. DOI: 10.1007/s00417-017-3883-7.
33.	Chidlow G, Shibeeb O, Plunkett M, et al. Glial cell and inflammatory responses to retinal laser treatment: comparison of a conventional photocoagulator and a novel, 3-nanosecond pulse laser[J]. Invest Ophthalmol Vis Sci, 2013, 54(3): 2319-2332. DOI: 10.1167/iovs.12-11204.
34.	Ito A, Hirano Y, Nozaki M, et al. Short pulse laser induces less inflammatory cytokines in the murine retina after laser photocoagulation[J]. Ophthalmic Res, 2015, 53(2): 65-73. DOI: 10.1159/000366520.
35.	Inagaki K, Shuo T, Katakura K, et al. Sublethal photothermal stimulation with a micropulse laser induces heat shock protein expression in ARPE-19 cells[J/OL].J Ophthalmol, 2015, 2015: 729792[2015-11-30]. http://dx.doi.org/10.1155/2015/729792. DOI: 10.1155/2015/729792.
36.	Yenari MA, Liu J, Zheng Z, et al. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection[J]. Ann N Y Acad Sci, 2010, 1053(1): 74-83. DOI: 10.1111/j.1749-6632.2005.tb00012.x.
37.	Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability[J]. J Cell Sci, 2008, 121(Pt 13): 2115-2122. DOI: 10.1242/jcs.017897.
38.	Hernández C, Lecube A, Segura RM, et al. Nitric oxide and vascular endothelial growth factor concentrations are increased but not related in vitreous fluid of patients with proliferative diabetic retinopathy[J]. Diabetic Medicine, 2010, 19(8): 655-660. DOI: 10.1046/j.1464-5491.2002.00768.x.
39.	Kulaksizoglu S, Karalezli A. Aqueous humour and serum levels of nitric oxide, malondialdehyde and total antioxidant status in patients with type 2 diabetes with proliferative diabetic retinopathy and nondiabetic senile cataracts[J]. Can J Diabetes, 2016, 40(2): 115-119. DOI: 10.1016/j.jcjd.2015.07.002.
40.	Er H, Doganay S, Turkoz Y, et al. The levels of cytokines and nitric oxide in rabbit vitreous humor after retinal laser photocoagulation[J]. Ophthalmic Surg Lasers, 2000, 31(6): 479-483.

1. Klein R, Davis MD, Moss SE, et al. The Wisconsin epidemiologic study of diabetic retinopathy: a comparison of retinopathy in younger and older onset diabetic persons[J]. Adv Exp Med Biol, 1985, 189: 321-335. DOI: 10.1007/978-1-4757-1850-8.
2. Matri KE, Chebbi Z, Falfoul Y, et al. Treatment of diabetic macular edema with micropulse laser therapy[J]. Acta Ophthalmol, 2017, 95 Suppl 259: S1. DOI: 10.1111/j.1755-3768.2017.0F031.
3. Matri LE, Falfoul Y, Chebbi Z, et al. Improvement of diabetic macular edema after micropulse laser therapy[J]. Acta Ophthalmol Scand, 2016, 94 Suppl 256: S1. DOI: 10.1111/j.1755-3768.2016.0535.
4. Barquet LA. Role of VEGF in diseases of the retina[J]. Arch Soc Esp Oftalmol, 2015, 90 Suppl 1: S3-5. DOI: 10.1016/S0365-6691(15)30002-2.
5. Ha JM, Jin SY, Lee HS, et al. Regulation of retinal angiogenesis by endothelial nitric oxide synthase signaling pathway[J]. Korean J Physiol Pharmacol, 2016, 20(5): 533-538. DOI: 10.4196/kjpp.2016.20.5.533.
6. Choi YS, Choi HJ, Min JK, et al. Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production[J]. Blood, 2009, 114(14): 3117-3126. DOI: 10.1182/blood-2009-02-203372.
7. Chamberlain JJ, Johnson EL, Leal S, et al. Cardiovascular disease and risk management: review of the American diabetes association standards of medical care in diabetes 2018[J]. Ann Intern Med, 2018, 168(9): 640-650. DOI: 10.7326/M18-0222.
8. 陈喆, 张士胜, 朱惠敏. 糖尿病视网膜病变的国际临床分类分析[J]. 国际眼科杂志, 2011, 11(8): 1394-1401. DOI: 10.3969/j.issn.1672-5123.2011.08.025.Chen Z, Zhang SS, Zhu HM. Analysis of international clinical diabetic retinopathy disease severity scale[J]. Int Eye Sci, 2011, 11(8): 1394-1401. DOI: 10.3969/j.issn.1672-5123.2011.08.025.
9. Hwang JU, Sohn J, Moon BG, et al. Assessment of macular function for idiopathic epiretinal membranes classified by spectral-domain optical coherence tomography[J]. Invest Ophthalmol Vis Sci, 2012, 53(7): 3562-3569. DOI: 10.1167/iovs.12-9762.
10. Ohkoshi K, Tsuiki E, Kitaoka T, et al. Visualization of subthreshold micropulse diode laser photocoagulation by scanning laser ophthalmoscopy in the retro mode[J]. Am J Ophthalmol, 2010, 150(6): 856-862. DOI: 10.1016/j.ajo.2010.06.022.
11. Funatsu H, Noma H, Mimura T, et al. Association of vitreous inflammatory factors with diabetic macular edema[J]. Ophthalmology, 2009, 116(1): 73-79. DOI: 10.1016/j.ophtha.2008.09.037.
12. Lip PL, Belgore F, Blann AD, et al. Plasma VEGF and soluble VEGF receptor FLT-1 in proliferative retinopathy: relationship to endothelial dysfunction and laser treatment[J]. Invest Ophthalmol Vis Sci, 2000, 41(8): 2115-2119.
13. Wilson AS, Hobbs BG, Shen WY, et al. Argon laser photocoagulation-induced modification of gene expression in the retina[J]. Invest Ophthalmol Vis Sci, 2003, 44(4): 1426-1434. DOI: 10.1167/iovs.02-0622.
14. Luttrull JK, Sramek C, Palanker D, et al. Long-term safety, high-resolution imaging, and tissue temperature modeling of subvisible diode micropulse photocoagulation for retinovascular macular edema[J]. Retina, 2012, 32(2): 375-386. DOI: 10.1097/IAE.0b013e3182206f6c.
15. Li Z, Song Y, Chen X, et al. Biological modulation of mouse RPE cells in response to subthreshold diode micropulse laser treatment[J]. Cell Biochem Biophys, 2015, 73(2): 545-552. DOI: 10.1007/s12013-015-0675-8.
16. Bromberg-White JL, Glazer L, Downer R, et al. Identification of VEGF-independent cytokines in proliferative diabetic retinopathy vitreous[J]. Invest Ophthalmol Vis Sci, 2013, 54(10): 6472-6480. DOI: 10.1167/iovs.13-12518.
17. Li J, Hu WC, Song H, et al. Increased vitreous chemerin levels are associated with proliferative diabetic retinopathy[J]. Ophthalmologica, 2016, 236(2): 61-66. DOI: 10.1159/000447752.
18. Manaviat MR, Rashidi M, Afkhami-Ardekani M, et al. Effect of pan retinal photocoagulation on the serum levels of vascular endothelial growth factor in diabetic patients[J]. Int Ophthalmol, 2011, 31(4): 271-275. DOI: 10.1007/s10792-011-9448-6.
19. Mohamed TA, Mohamed Sel-D. Effect of pan-retinal laser photocoagulation on plasma VEGF, endothelin-1 and nitric oxide in PDR[J]. Int J Ophthalmol, 2010, 3(1): 19-22. DOI: 10.3980/j.issn.2222-3959.2010.01.05.
20. Itaya M, Sakurai E, Nozaki M, et al. Upregulation of VEGF in murine retina via monocyte recruitment after retinal scatter laser photocoagulation[J]. Invest Ophthalmol Vis Sci, 2007, 48(12): 5677-5683. DOI: 10.1167/iovs.07-0156.
21. Konac E, Sonmez K, Bahcelioglu M, et al. Does pattern scan laser (PASCAL) photocoagulation really induce less VEGF expression in murine retina than conventional laser treatment?[J]. Gene, 2014, 549(1): 156-160. DOI: 10.1016/j.gene.2014.07.062.
22. Riddell JR, Maier P, Sass SN, Peroxiredoxin 1 stimulates endothelial cell expression of VEGF via TLR4 dependent activation of HIF-1α[J/OL]. PLoS One, 2012, 7(11): 50394[2012-11-21]. https://doi.org/10.1371/journal.pone.0050394. DOI: 10.1371/journal.pone.0050394.
23. Flaxel C, Bradle J, Acott T, et al. Retinal pigment epithelium produces matrix metalloproteinases after laser treatment[J]. Retina, 2007, 27(5): 629-634. DOI: 10.1097/01.iae.0000249561.02567.fd.
24. Lavinsky D, Sramek C, Wang J, et al. Subvisible retinal laser therapy: titration algorithm and tissue response[J]. Retina, 2014, 34(1): 87-97. DOI: 10.1097/IAE.0b013e3182993edc.
25. Arany PR, Nayak RS, Hallikerimath S, et al. Activation of latent TGF-beta1 by low-power laser in vitro correlates with increased TGF-beta1 levels in laser-enhanced oral wound healing[J]. Wound Repair Regen, 2007, 15(6): 866-874. DOI: 10.1111/j.1524-475X.2007.00306.x.
26. Szymanska J, Goralczyk K, Klawe JJ, et al. Phototherapy with low-level laser influences the proliferation of endothelial cells and vascular endothelial growth factor and transforming growth factor-beta secretion[J]. J Physiol Pharmacol, 2013, 64(3): 387-391.
27. Mandriota SJ, Menoud PA, Pepper MS. Transforming growth factor beta 1 down-regulates vascular endothelial growth factor receptor 2/flk-1 expression in vascular endothelial cells[J]. J Biol Chem, 1996, 271(19): 11500-11505. DOI: 10.1074/jbc.271.19.11500.
28. Arend WP, Palmer G, Gabay C. IL-1, IL-18, and IL-33 families of cytokines[J]. Immunol Rev, 2008, 223: 20-38. DOI: 10.1111/j.1600-065X.2008.00624.x.
29. Schmitz J, Owyang A, Oldham E, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines[J]. Immunity, 2005, 23(5): 479-490. DOI: 10.1016/j.immuni.2005.09.015.
30. Takeuchi M, Sato T, Tanaka A, et al. Elevated levels of cytokines associated with Th2 and Th17 cells in vitreous fluid of proliferative diabetic retinopathy patients[J/OL]. PLoS One, 2015, 10(9): 137358[2015-09-09]. https://doi.org/10.1371/journal.pone.0137358. DOI: 10.1371/journal.pone.0137358.
31. Shimura M, Yasuda K, Nakazawa T, et al. Panretinal photocoagulation induces pro- inflammatory cytokines and macular thickening in high-risk proliferative diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2009, 247(12): 1617-1624. DOI: 10.1007/s00417-009-1147-x.
32. Han JW, Choi J, Kim YS, et al. Comparison of the neuroinflammatory responses to selective retina therapy and continuous-wave laser photocoagulation in mouse eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(2): 341-353. DOI: 10.1007/s00417-017-3883-7.
33. Chidlow G, Shibeeb O, Plunkett M, et al. Glial cell and inflammatory responses to retinal laser treatment: comparison of a conventional photocoagulator and a novel, 3-nanosecond pulse laser[J]. Invest Ophthalmol Vis Sci, 2013, 54(3): 2319-2332. DOI: 10.1167/iovs.12-11204.
34. Ito A, Hirano Y, Nozaki M, et al. Short pulse laser induces less inflammatory cytokines in the murine retina after laser photocoagulation[J]. Ophthalmic Res, 2015, 53(2): 65-73. DOI: 10.1159/000366520.
35. Inagaki K, Shuo T, Katakura K, et al. Sublethal photothermal stimulation with a micropulse laser induces heat shock protein expression in ARPE-19 cells[J/OL].J Ophthalmol, 2015, 2015: 729792[2015-11-30]. http://dx.doi.org/10.1155/2015/729792. DOI: 10.1155/2015/729792.
36. Yenari MA, Liu J, Zheng Z, et al. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection[J]. Ann N Y Acad Sci, 2010, 1053(1): 74-83. DOI: 10.1111/j.1749-6632.2005.tb00012.x.
37. Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability[J]. J Cell Sci, 2008, 121(Pt 13): 2115-2122. DOI: 10.1242/jcs.017897.
38. Hernández C, Lecube A, Segura RM, et al. Nitric oxide and vascular endothelial growth factor concentrations are increased but not related in vitreous fluid of patients with proliferative diabetic retinopathy[J]. Diabetic Medicine, 2010, 19(8): 655-660. DOI: 10.1046/j.1464-5491.2002.00768.x.
39. Kulaksizoglu S, Karalezli A. Aqueous humour and serum levels of nitric oxide, malondialdehyde and total antioxidant status in patients with type 2 diabetes with proliferative diabetic retinopathy and nondiabetic senile cataracts[J]. Can J Diabetes, 2016, 40(2): 115-119. DOI: 10.1016/j.jcjd.2015.07.002.
40. Er H, Doganay S, Turkoz Y, et al. The levels of cytokines and nitric oxide in rabbit vitreous humor after retinal laser photocoagulation[J]. Ophthalmic Surg Lasers, 2000, 31(6): 479-483.

Chinese Journal of Ocular Fundus Diseases

Effects of conventional laser photocoagulation and subthreshold micropulse laser photocoagulation on concentration of vascular endothelial growth factor, interleukin-33 and NO in vitreous of proliferative diabetic retinopathy eyes

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