Top

Graefe's Archive for Clinical and Experimental Ophthalmology

Published in:

01-09-2009 | Basic Science

A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats

Authors: Coralie Schnebelen, Bruno Pasquis, Manuel Salinas-Navarro, Corinne Joffre, Catherine P. Creuzot-Garcher, Manuel Vidal-Sanz, Alain M. Bron, Lionel Bretillon, Niyazi Acar

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 9/2009

Abstract

Background

To evaluate the effect of a dietary combination of omega-3 and omega-6 polyunsaturated fatty acids (PUFAs) compared to single PUFA supplementations on the outcome of a substantial elevation of intraocular pressure (IOP) in rats.

Methods

Sprague Dawley rats were fed for 6 months with either a control diet, a diet enriched with omega-3 PUFAs (eicosapentaenoic acid, EPA, and docosahexaenoic acid, DHA), a diet enriched with omega-6 PUFAs (γ-linolenic acid, GLA) or a diet enriched with both omega-3 and omega-6 PUFAs (EPA + DHA and GLA). After 3 months of feeding, elevation of IOP was induced by photocoagulation of the episcleral veins, limbus and trabecular meshwork using a 532-nm laser. IOP and scotopic electroretinograms (ERGs) were monitored after the induction of IOP elevation until the end of the nutritional supplementation. Retinal morphometry and GFAP immunohistochemistry were performed 3 months after laser photocoagulation. Retinal ganglion cells (RGCs) were quantified using retrograde labelling.

Results

A significant rise in IOP was observed in the laser-treated eyes. PUFA supplementation did not influence the time course of IOP in the laser-treated eyes. Three months after laser photocoagulation, the activation of glial cells observed in the laser-treated eyes was significantly lower in animals fed with the EPA + DHA + GLA diet when compared to those fed the control diet, while single supplementations with either EPA + DHA or GLA were not effective. The same protective effect of the EPA + DHA + GLA combination was observed on retinal structures in the laser-treated eyes. However, PUFA supplementation did not influence either ERG b-wave amplitude or the RGC loss in the laser-treated eyes.

Conclusions

This study demonstrates that a 6-month supplementation with a combination of omega-3 and omega-6 PUFAs is more effective than single supplementations, since the EPA + DHA + GLA dietary combination prevented retinal cell structure and decreased glial cell activation induced by the elevation of IOP in rats.

Weinreb RN, Khaw PT (2004) Primary open-angle glaucoma. Lancet 363:1711–1720, doi:10.1016/S0140-6736(04)16257-0 PubMedCrossRef

Lafuente MP, Villegas-Perez MP, Selles-Navarro I, Mayor-Torroglosa S, Miralles de Imperial J, Vidal-Sanz M (2002) Retinal ganglion cell death after acute retinal ischemia is an ongoing process whose severity and duration depends on the duration of the insult. Neuroscience 109:157–168, doi:10.1016/S0306-4522(01)00458-4 PubMedCrossRef

Selles-Navarro I, Villegas-Perez MP, Salvador-Silva M, Ruiz-Gomez JM, Vidal-Sanz M (1996) Retinal ganglion cell death after different transient periods of pressure-induced ischemia and survival intervals. A quantitative in vivo study. Invest Ophthalmol Vis Sci 37:2002–2014PubMed

Grozdanic SD, Kwon YH, Sakaguchi DS, Kardon RH, Sonea IM (2004) Functional evaluation of retina and optic nerve in the rat model of chronic ocular hypertension. Exp Eye Res 79:75–83, doi:10.1016/j.exer.2004.02.011 PubMedCrossRef

Grozdanic SD, Sakaguchi DS, Kwon YH, Kardon RH, Sonea IM (2003) Functional characterization of retina and optic nerve after acute ocular ischemia in rats. Invest Ophthalmol Vis Sci 44:2597–2605, doi:10.1167/iovs.02-0600 PubMedCrossRef

Mukaida Y, Machida S, Masuda T, Tazawa Y (2004) Correlation of retinal function with retinal histopathology following ischemia-reperfusion in rat eyes. Curr Eye Res 28:381–389, doi:10.1080/02713680490503679 PubMedCrossRef

Mayor-Torroglosa S, De la Villa P, Rodriguez ME, Lopez-Herrera MP, Aviles-Trigueros M, Garcia-Aviles A, de Imperial JM, Villegas-Perez MP, Vidal-Sanz M (2005) Ischemia results 3 months later in altered ERG, degeneration of inner layers, and deafferented tectum: neuroprotection with brimonidine. Invest Ophthalmol Vis Sci 46:3825–3835, doi:10.1167/iovs.05-0392 PubMedCrossRef

Kim IB, Kim KY, Joo CK, Lee MY, Oh SJ, Chung JW, Chun MH (1998) Reaction of Muller cells after increased intraocular pressure in the rat retina. Exp Brain Res 121:419–424, doi:10.1007/s002210050476 PubMedCrossRef

Lam TT, Abler AS, Tso MO (1999) Apoptosis and caspases after ischemia-reperfusion injury in rat retina. Invest Ophthalmol Vis Sci 40:967–975PubMed

10.

Smith W, Mitchell P, Leeder SR (2000) Dietary fat and fish intake and age-related maculopathy. Arch Ophthalmol 118:401–404PubMed

11.

Seddon JM, Cote J, Rosner B (2003) Progression of age-related macular degeneration: association with dietary fat, transunsaturated fat, nuts, and fish intake. Arch Ophthalmol 121:1728–1737, doi:10.1001/archopht.121.12.1728 PubMedCrossRef

12.

Seddon JM, Rosner B, Sperduto RD, Yannuzzi L, Haller JA, Blair NP, Willett W (2001) Dietary fat and risk for advanced age-related macular degeneration. Arch Ophthalmol 119:1191–1199PubMed

13.

Bas O, Songur A, Sahin O, Mollaoglu H, Ozen OA, Yaman M, Eser O, Fidan H, Yagmurca M (2007) The protective effect of fish n-3 fatty acids on cerebral ischemia in rat hippocampus. Neurochem Int 50:548–554, doi:10.1016/j.neuint.2006.11.005 PubMedCrossRef

14.

Miyauchi O, Mizota A, Adachi-Usami E, Nishikawa M (2001) Protective effect of docosahexaenoic acid against retinal ischemic injury: an electroretinographic study. Ophthalmic Res 33:191–195, doi:10.1159/000055669 PubMedCrossRef

15.

Murayama K, Yoneya S, Miyauchi O, Adachi-Usami E, Nishikawa M (2002) Fish oil (polyunsaturated fatty acid) prevents ischemic-induced injury in the mammalian retina. Exp Eye Res 74:671–676, doi:10.1006/exer.2002.1151 PubMedCrossRef

16.

Nguyen CT, Vingrys AJ, Bui BV (2008) Dietary omega-3 fatty acids and ganglion cell function. Invest Ophthalmol Vis Sci 49:3586–3594, doi:10.1167/iovs.08-1735 PubMedCrossRef

17.

Nguyen CT, Bui BV, Sinclair AJ, Vingrys AJ (2007) Dietary omega 3 Fatty acids decrease intraocular pressure with age by increasing aqueous outflow. Invest Ophthalmol Vis Sci 48:756–762, doi:10.1167/iovs.06-0585 PubMedCrossRef

18.

Kang JH, Pasquale LR, Willett WC, Rosner BA, Egan KM, Faberowski N, Hankinson SE (2004) Dietary fat consumption and primary open-angle glaucoma. Am J Clin Nutr 79:755–764PubMed

19.

Tezel G, Wax MB (2000) Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci 20:8693–8700PubMed

20.

Zhou X, Li F, Kong L, Tomita H, Li C, Cao W (2005) Involvement of inflammation, degradation, and apoptosis in a mouse model of glaucoma. J Biol Chem 280:31240–31248, doi:10.1074/jbc.M502641200 PubMedCrossRef

21.

Leventhal LJ, Boyce EG, Zurier RB (1993) Treatment of rheumatoid arthritis with gammalinolenic acid. Ann Intern Med 119:867–873PubMed

22.

Dirks J, van Aswegen CH, du Plessis DJ (1998) Cytokine levels affected by gamma-linolenic acid. Prostaglandins Leukot Essent Fatty Acids 59:273–277, doi:10.1016/S0952-3278(98)90141-7 PubMedCrossRef

23.

Furse RK, Rossetti RG, Zurier RB (2001) Gammalinolenic acid, an unsaturated fatty acid with anti-inflammatory properties, blocks amplification of IL-1 beta production by human monocytes. J Immunol 167:490–496PubMed

24.

Schnebelen C, Viau S, Gregoire S, Joffre C, Creuzot-Garcher C, Bron A, Bretillon L, Acar N (2009) Nutrition for the eye: different susceptibility of the retina and the lacrimal gland to dietary omega-6 and omega-3 polyunsaturated fatty acid incorporation. Ophthalmic Res (in press).

25.

Levkovitch-Verbin H, Quigley HA, Martin KR, Valenta D, Baumrind LA, Pease ME (2002) Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol Vis Sci 43:402–410PubMed

26.

Biel M, Seeliger M, Pfeifer A, Kohler K, Gerstner A, Ludwig A, Jaissle G, Fauser S, Zrenner E, Hofmann F (1999) Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proc Natl Acad Sci USA 96:7553–7557, doi:10.1073/pnas.96.13.7553 PubMedCrossRef

27.

Bretillon L, Acar N, Seeliger MW, Santos M, Maire MA, Juaneda P, Martine L, Gregoire S, Joffre C, Bron AM, Creuzot-Garcher C (2008) ApoB100, LDLR-/- mice exhibit reduced electroretinographic response and cholesteryl esters deposits in the retina. Invest Ophthalmol Vis Sci 49:1307–1314, doi:10.1167/iovs.07-0808 PubMedCrossRef

28.

Salinas-Navarro M, Mayor-Torroglosa S, Jimenez-Lopez M, Aviles-Trigueros M, Holmes TM, Lund RD, Villegas-Perez MP, Vidal-Sanz M (2009) A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Res 49:115–126, doi:10.1016/j.visres.2008.09.029 PubMedCrossRef

29.

Osborne NN, Ugarte M, Chao M, Chidlow G, Bae JH, Wood JP, Nash MS (1999) Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol 43(Suppl 1):S102–S128, doi:10.1016/S0039-6257(99)00044-2 PubMedCrossRef

30.

Levkovitch-Verbin H, Dardik R, Vander S, Nisgav Y, Kalev-Landoy M, Melamed S (2006) Experimental glaucoma and optic nerve transection induce simultaneous upregulation of proapoptotic and prosurvival genes. Invest Ophthalmol Vis Sci 47:2491–2497, doi:10.1167/iovs.05-0996 PubMedCrossRef

31.

Pang IH, Clark AF (2007) Rodent models for glaucoma retinopathy and optic neuropathy. J Glaucoma 16:483–505, doi:10.1097/IJG.0b013e3181405d4f PubMedCrossRef

32.

Bui BV, Edmunds B, Cioffi GA, Fortune B (2005) The gradient of retinal functional changes during acute intraocular pressure elevation. Invest Ophthalmol Vis Sci 46:202–213, doi:10.1167/iovs.04-0421 PubMedCrossRef

33.

Pinilla I, Cuenca N, Salinas-Navarro M, Fernandez-Sanchez L, Alarcon-Martinez L, Aviles-Trigueros M, Villegas-Perez M, Vidal-Sanz M (2008) Changes in the outer retina after acute increase of the intraocular pressure in adult mice. Invest Ophthalmol Vis Sci 40:E-Abstract 5482

34.

Takita H, Yoneya S, Gehlbach PL, Duh EJ, Wei LL, Mori K (2003) Retinal neuroprotection against ischemic injury mediated by intraocular gene transfer of pigment epithelium-derived factor. Invest Ophthalmol Vis Sci 44:4497–4504, doi:10.1167/iovs.03-0052 PubMedCrossRef

35.

Quigley HA (1999) Neuronal death in glaucoma. Prog Retin Eye Res 18:39–57, doi:10.1016/S1350-9462(98)00014-7 PubMedCrossRef

36.

Woldemussie E, Wijono M, Ruiz G (2004) Muller cell response to laser-induced increase in intraocular pressure in rats. Glia 47:109–119, doi:10.1002/glia.20000 PubMedCrossRef

37.

Nakazawa T, Matsubara A, Noda K, Hisatomi T, She H, Skondra D, Miyahara S, Sobrin L, Thomas KL, Chen DF, Grosskreutz CL, Hafezi-Moghadam A, Miller JW (2006) Characterization of cytokine responses to retinal detachment in rats. Mol Vis 12:867–878PubMed

38.

Tezel G, Li LY, Patil RV, Wax MB (2001) TNF-alpha and TNF-alpha receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis Sci 42:1787–1794PubMed

39.

Tezel G, Wax MB (2003) Glial modulation of retinal ganglion cell death in glaucoma. J Glaucoma 12:63–68, doi:10.1097/00061198-200302000-00014 PubMedCrossRef

40.

Wallace FA, Miles EA, Calder PC (2000) Activation state alters the effect of dietary fatty acids on pro-inflammatory mediator production by murine macrophages. Cytokine 12:1374–1379, doi:10.1006/cyto.2000.0735 PubMedCrossRef

41.

Dooper MM, van Riel B, Graus YM, M’Rabet L (2003) Dihomo-gamma-linolenic acid inhibits tumour necrosis factor-alpha production by human leucocytes independently of cyclooxygenase activity. Immunology 110:348–357, doi:10.1046/j.1365-2567.2003.01749.x PubMedCrossRef

42.

Umeda-Sawada R, Fujiwara Y, Ushiyama I, Sagawa S, Morimitsu Y, Kawashima H, Ono Y, Kiso Y, Matsumoto A, Seyama Y (2006) Distribution and metabolism of dihomo-gamma-linolenic acid (DGLA, 20:3n–6) by oral supplementation in rats. Biosci Biotechnol Biochem 70:2121–2130, doi:10.1271/bbb.60057 PubMedCrossRef

43.

Kim HY, Akbar M, Lau A, Edsall L (2000) Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n–3). Role of phosphatidylserine in antiapoptotic effect. J Biol Chem 275:35215–35223, doi:10.1074/jbc.M004446200 PubMedCrossRef

44.

Rotstein NP, Politi LE, German OL, Girotti R (2003) Protective effect of docosahexaenoic acid on oxidative stress-induced apoptosis of retina photoreceptors. Invest Ophthalmol Vis Sci 44:2252–2259, doi:10.1167/iovs.02-0901 PubMedCrossRef

45.

Mizota A, Sato E, Taniai M, Adachi-Usami E, Nishikawa M (2001) Protective effects of dietary docosahexaenoic acid against kainate-induced retinal degeneration in rats. Invest Ophthalmol Vis Sci 42:216–221PubMed

46.

Moriguchi K, Yuri T, Yoshizawa K, Kiuchi K, Takada H, Inoue Y, Hada T, Matsumura M, Tsubura A (2003) Dietary docosahexaenoic acid protects against N-methyl-N-nitrosourea-induced retinal degeneration in rats. Exp Eye Res 77:167–173, doi:10.1016/S0014-4835(03)00114-3 PubMedCrossRef

47.

Bazan NG (2006) Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci 29:263–271, doi:10.1016/j.tins.2006.03.005 PubMedCrossRef

48.

Phillis JW, Horrocks LA, Farooqui AA (2006) Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders. Brain Res Brain Res Rev 52:201–243, doi:10.1016/j.brainresrev.2006.02.002 CrossRef

49.

Bayer AU, Danias J, Brodie S, Maag KP, Chen B, Shen F, Podos SM, Mittag TW (2001) Electroretinographic abnormalities in a rat glaucoma model with chronic elevated intraocular pressure. Exp Eye Res 72:667–677, doi:10.1006/exer.2001.1004 PubMedCrossRef

50.

Fortune B, Bui BV, Morrison JC, Johnson EC, Dong J, Cepurna WO, Jia L, Barber S, Cioffi GA (2004) Selective ganglion cell functional loss in rats with experimental glaucoma. Invest Ophthalmol Vis Sci 45:1854–1862, doi:10.1167/iovs.03-1411 PubMedCrossRef

51.

Mittag TW, Danias J, Pohorenec G, Yuan HM, Burakgazi E, Chalmers-Redman R, Podos SM, Tatton WG (2000) Retinal damage after 3 to 4 months of elevated intraocular pressure in a rat glaucoma model. Invest Ophthalmol Vis Sci 41:3451–3459PubMed

52.

Li RS, Tay DK, Chan HH, So KF (2006) Changes of retinal functions following the induction of ocular hypertension in rats using argon laser photocoagulation. Clin Experiment Ophthalmol 34:575–583, doi:10.1111/j.1442-9071.2006.01237.x PubMedCrossRef

53.

Whitmore AV, Libby RT, John SW (2005) Glaucoma: thinking in new ways-a role for autonomous axonal self-destruction and other compartmentalised processes? Prog Retin Eye Res 24:639–662, doi:10.1016/j.preteyeres.2005.04.004 PubMedCrossRef

54.

Cordeiro MF, Guo L, Luong V, Harding G, Wang W, Jones HE, Moss SE, Sillito AM, Fitzke FW (2004) Real-time imaging of single nerve cell apoptosis in retinal neurodegeneration. Proc Natl Acad Sci USA 101:13352–13356, doi:10.1073/pnas.0405479101 PubMedCrossRef

55.

Hood DC, Kardon RH (2007) A framework for comparing structural and functional measures of glaucomatous damage. Prog Retin Eye Res 26:688–710, doi:10.1016/j.preteyeres.2007.08.001 PubMedCrossRef

Title: A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats
Authors: Coralie Schnebelen
Bruno Pasquis
Manuel Salinas-Navarro
Corinne Joffre
Catherine P. Creuzot-Garcher
Manuel Vidal-Sanz
Alain M. Bron
Lionel Bretillon
Niyazi Acar
Publication date: 01-09-2009
Publisher: Springer-Verlag
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 9/2009
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-009-1094-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 9/2009

Effect of epigallocatechin-gallate on inner retinal function in ocular hypertension and glaucoma: A short-term study by pattern electroretinogram

Construct validation of the Amblyopia and Strabismus Questionnaire (A&SQ) by factor analysis

Relationship between oculomotor scanning determined by the DEM test and a contextual reading test in schoolchildren with reading difficulties

Intravitreal ranibizumab (Lucentis®) in the treatment of retinal angiomatous proliferation (RAP)

Change in ocular alignment after topical anesthetic cataract surgery

Intravitreal bevacizumab for CNV-complicated tilted disk syndrome