Alteration of erythrocyte membrane polyunsaturated fatty acids in preterm newborns with retinopathy of prematurity

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Abstract

Extremely preterm infants are at high risk for retinopathy of prematurity (ROP), a potentially blinding disease characterized by abnormalities in retinal vascularization. Whereas animal studies revealed that n-3 polyunsaturated fatty acids (PUFAs) may be of benefit in preventing ROP, human studies conducted on preterm infants during the 1 ^st weeks of life showed no association between blood n-3 PUFA bioavailability and ROP incidence and/or severity, probably because of the influence of nutrition on the lipid status of infants. In the OmegaROP prospective cohort study, we characterized the erythrocyte concentrations of PUFAs in preterm infants aged less than 29 weeks gestational age (GA) without any nutritional influence. We show that GA is positively associated with the erythrocyte n-6 to n-3 PUFA ratio, and particularly with the ratio of arachidonic acid (AA) to docosahexaenoic acid (DHA), in infants with ROP. A time-dependent accumulation of AA at the expense of DHA seems to occur in utero in erythrocytes of preterm infants who will develop ROP, thus reinforcing previous data on the beneficial properties of DHA on this disease. In addition, preliminary data on maternal erythrocyte membrane lipid concentrations suggest modifications in placental transfer of fatty acids. Documenting the erythrocyte AA to DHA ratio at birth in larger cohorts might be useful to set up new prognostic factors for ROP.

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Most cited references 51

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Retinopathy of prematurity.

Ann Hellström, Lois E. H. Smith, Olaf Dammann (2013)

The immature retinas of preterm neonates are susceptible to insults that disrupt neurovascular growth, leading to retinopathy of prematurity. Suppression of growth factors due to hyperoxia and loss of the maternal-fetal interaction result in an arrest of retinal vascularisation (phase 1). Subsequently, the increasingly metabolically active, yet poorly vascularised, retina becomes hypoxic, stimulating growth factor-induced vasoproliferation (phase 2), which can cause retinal detachment. In very premature infants, controlled oxygen administration reduces but does not eliminate retinopathy of prematurity. Identification and control of factors that contribute to development of retinopathy of prematurity is essential to prevent progression to severe sight-threatening disease and to limit comorbidities with which the disease shares modifiable risk factors. Strategies to prevent retinopathy of prematurity will depend on optimisation of oxygen saturation, nutrition, and normalisation of concentrations of essential factors such as insulin-like growth factor 1 and ω-3 polyunsaturated fatty acids, as well as curbing of the effects of infection and inflammation to promote normal growth and limit suppression of neurovascular development. Copyright © 2013 Elsevier Ltd. All rights reserved.

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Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis.

Kip Connor, John SanGiovanni, Chatarina Löfqvist … (2007)

Many sight-threatening diseases have two critical phases, vessel loss followed by hypoxia-driven destructive neovascularization. These diseases include retinopathy of prematurity and diabetic retinopathy, leading causes of blindness in childhood and middle age affecting over 4 million people in the United States. We studied the influence of omega-3- and omega-6-polyunsaturated fatty acids (PUFAs) on vascular loss, vascular regrowth after injury, and hypoxia-induced pathological neovascularization in a mouse model of oxygen-induced retinopathy. We show that increasing omega-3-PUFA tissue levels by dietary or genetic means decreased the avascular area of the retina by increasing vessel regrowth after injury, thereby reducing the hypoxic stimulus for neovascularization. The bioactive omega-3-PUFA-derived mediators neuroprotectinD1, resolvinD1 and resolvinE1 also potently protected against neovascularization. The protective effect of omega-3-PUFAs and their bioactive metabolites was mediated, in part, through suppression of tumor necrosis factor-alpha. This inflammatory cytokine was found in a subset of microglia that was closely associated with retinal vessels. These findings indicate that increasing the sources of omega-3-PUFA or their bioactive products reduces pathological angiogenesis. Western diets are often deficient in omega-3-PUFA, and premature infants lack the important transfer from the mother to the infant of omega-3-PUFA that normally occurs in the third trimester of pregnancy. Supplementing omega-3-PUFA intake may be of benefit in preventing retinopathy.

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Pathophysiology and mechanisms of severe retinopathy of prematurity.

M Hartnett (2015)

Retinopathy of prematurity (ROP) affects only premature infants, but as premature births increase in many areas of the world, ROP has become a leading cause of childhood blindness. Blindness can occur from aberrant developmental angiogenesis that leads to fibrovascular retinal detachment. To treat severe ROP, it is important to study normal developmental angiogenesis and the stresses that activate pathologic signaling events and aberrant angiogenesis in ROP. Vascular endothelial growth factor (VEGF) signaling is important in both physiologic and pathologic developmental angiogenesis. Based on studies in animal models of oxygen-induced retinopathy (OIR), exogenous factors such as oxygen levels, oxidative stress, inflammation, and nutritional capacity have been linked to severe ROP through dysregulated signaling pathways involving hypoxia-inducible factors and angiogenic factors like VEGF, oxidative species, and neuroprotective growth factors to cause phases of ROP. This translational science review focuses on studies performed in animal models of OIR representative of human ROP and highlights several areas: mechanisms for aberrant growth of blood vessels into the vitreous rather than into the retina through over-activation of VEGF receptor 2 signaling, the importance of targeting different cells in the retina to inhibit aberrant angiogenesis and promote physiologic retinal vascular development, toxicity from broad and targeted inhibition of VEGF bioactivity, and the role of VEGF in neuroprotection in retinal development. Several future translational treatments are discussed, including considerations for targeted inhibition of VEGF signaling instead of broad intravitreal anti-VEGF treatment.

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Author and article information

Contributors

Niyazi Acar: niyazi.acar@inra.fr

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 28 May 2019

Publication date PMC-release: 28 May 2019

Publication date Collection: 2019

Volume: 9

Electronic Location Identifier: 7930

Affiliations

[1 ]GRID grid.31151.37, University Hospital, Department of Ophthalmology, ; Dijon, F-21000 France

[2 ]ISNI 0000 0004 0387 2525, GRID grid.462804.c, Centre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRA, Université Bourgogne Franche-Comté, Eye and Nutrition Research Group, ; Dijon, F-21000 France

[3 ]GRID grid.31151.37, University Hospital, Neonatal Intensive Care Unit, ; Dijon, F-21000 France

Author information

Alain M. Bron http://orcid.org/0000-0002-7265-931X

Article

Publisher ID: 44476

DOI: 10.1038/s41598-019-44476-w

PMC ID: 6538605

PubMed ID: 31138879

SO-VID: 3dcd16ad-1219-4b62-8852-84e20ffa361b

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 1 October 2018

Date accepted : 17 May 2019

Funding

Funded by: Inter Regional Group for Clinical Research and Innovation (GIRCI VISIO Foundation

Funded by: FundRef https://doi.org/10.13039/501100004431, Fondation de France;

Award ID: Prix de la Fondation de l'oeil 2016

Award ID: Prix de la Fondation de l'Oeil 2016

Award Recipient : Julie Mazzocco Catherine P. Creuzot-Garcher Alain M. Bron Lionel Bretillon Niyazi Acar

Funded by: FundRef https://doi.org/10.13039/501100006488, Institut National de la Recherche Agronomique (National Institute for Agricultural Research);

Funded by: FundRef https://doi.org/10.13039/501100001665, Agence Nationale de la Recherche (French National Research Agency);

Award ID: ANR-11-LABEX-0021

Award Recipient : Julie Mazzocco Catherine P. Creuzot-Garcher Alain M. Bron Lionel Bretillon Niyazi Acar

Funded by: Inter Regional Group for Clinical Research and Innovation (GIRCI VISIO Foundation European Funding for Regional Economic Development (FEDER) Regional Council of Burgundy

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Keywords: fatty acids,retinopathy of prematurity

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ScienceOpen disciplines: Uncategorized

Keywords: fatty acids, retinopathy of prematurity

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Alteration of erythrocyte membrane polyunsaturated fatty acids in preterm newborns with retinopathy of prematurity

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Most cited references 51

Retinopathy of prematurity.

Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis.

Pathophysiology and mechanisms of severe retinopathy of prematurity.

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Cited by 11