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Clinical Applications of Astaxanthin in the Treatment of Ocular Diseases: Emerging Insights

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Clinical Applications of Astaxanthin in the Treatment of Ocular Diseases: Emerging Insights marine drugs Review Clinical Applications of Astaxanthin in the Treatment of Ocular Diseases: Emerging Insights Giuseppe Giannaccare 1 , Marco Pellegrini 2 , Carlotta Senni 2, Federico Bernabei 2, Vincenzo Scorcia 1 and Arrigo Francesco Giuseppe Cicero 3,* 1 Department of Ophthalmology, University Magna Graecia of Catanzaro, 88100 Catanzaro, Italy; [email protected] (G.G.); [email protected] (V.S.) 2 Ophthalmology Unit, S.Orsola-Malpighi Hospital, University of Bologna, 40138 Bologna, Italy; [email protected] (M.P.); [email protected] (C.S.); [email protected] (F.B.) 3 Medical and Surgical Sciences Department, Alma Mater Studiorum University of Bologna, 40138 Bologna, Italy * Correspondence: [email protected] Received: 3 April 2020; Accepted: 29 April 2020; Published: 1 May 2020 Abstract: Astaxanthin is a naturally occurring red carotenoid pigment belonging to the family of xanthophylls, and is typically found in marine environments, especially in microalgae and seafood such as salmonids, shrimps and lobsters. Due to its unique molecular structure, astaxanthin features some important biologic properties, mostly represented by strong antioxidant, anti-inflammatory and antiapoptotic activities. A growing body of evidence suggests that astaxanthin is efficacious in the prevention and treatment of several ocular diseases, ranging from the anterior to the posterior pole of the eye. Therefore, the present review aimed at providing a comprehensive evaluation of current clinical applications of astaxanthin in the management of ocular diseases. The efficacy of this carotenoid in the setting of retinal diseases, ocular surface disorders, uveitis, cataract and asthenopia is reported in numerous animal and human studies, which highlight its ability of modulating several metabolic pathways, subsequently restoring the cellular homeostatic balance. To maximize its multitarget therapeutic effects, further long-term clinical trials are warranted in order to define appropriate dosage, route of administration and exact composition of the final product. Keywords: astaxanthin; carotenoids; eye; age-related macular degeneration; glaucoma; cataract; dry eye disease; oxidative stress; nutritional supplements 1. Introduction Astaxanthin (3,3’-dihydroxy-β,β-carotene4,4’-dione; molar mass 596.84 g/mol) is a naturally occurring carotenoid whose structural and functional characteristics make it a promising bioactive compound in the prevention of several human diseases as well as in the maintenance of a good health status [1]. It belongs to the family of xanthophylls (the oxygenated derivatives of carotenoids) and is especially common in marine environments where it looks like a red pigment. This contributes to the pinkish-red color of salmonids, shrimps, lobsters, and crayfish’s flesh [2]. Once biosynthesized by phytoplankton and microalgae, such as Haematococcus pluvialis, Chlorella zofingiensis and Xanthophyllomyces dendrorhous, it accumulates in various aquatic species, which represent the main dietary sources of such valuable nutrient. As a member of xanthophylls, it consists of two terminal rings joined by a polyene chain, plus two asymmetric carbons located at the 3,30 positions of the β-ionone ring with hydroxyl group (-OH) on either end of the molecule, which provide both lipophilic and hydrophilic properties. Each double polyene bond can exist either as cis- or trans-geometric isomers. Further, due to the presence of two stereogenic carbon atoms at the Mar. Drugs 2020, 18, 239; doi:10.3390/md18050239 www.mdpi.com/journal/marinedrugs Mar. Drugs 2020, 18, 239 2 of 13 3,3’ positions, three different stereoisomers of astaxanthin, including a pair of enantiomers (3R,3’R- and 3S,3’S-astaxanthin) and an optically inactive mesoform (3R,3’S-astaxanthin) may be found, as shown inMar. Figure Drugs1 2020[1]., 18, x 2 of 13 FigureFigure 1. SkeletalSkeletal structure structure of of astaxa astaxanthinnthin that that consists consists of ofa β a,ββ-carotene-4,4’-dione,β-carotene-4,4’-dione bearing bearing two twohy- hydroxydroxy substituents substituents at atpositions positions 3 and 3 and 3’. 3’. ApplicationApplication fieldsfields of of astaxanthin astaxanthin range range from from the the food-coloring food-coloring industry, industry, for for its naturalits natural intense intense red colorred color brightness, brightness, to aquaculture to aquaculture and and poultry poultry industries industries for itsfornatural its natural feed feed addictive addictive properties properties [3]. Furthermore,[3]. Furthermore, the the use use of astaxanthinof astaxanthin in in the the medical medical field field is is of of recent recent interest, interest, with with thethe purposepurpose of improvingimproving healthhealth status.status. Not by chance, chance, it it has has show shownn multiple multiple beneficial beneficial effects effects including including anticancer, anticancer, antidiabetic,antidiabetic, anti-inflammatoryanti-inflammatory and antioxidant activities,activities, as well as protective actions for skin andand nervousnervous and cardiovascular systemssystems [[1,4,5].1,4,5]. Currentl Currently,y, 95%95% ofof astaxanthinastaxanthin availableavailable in world market isis producedproduced syntheticallysynthetically usingusing petrochemicalspetrochemicals due to cost-ecost-efficiencyfficiency for mass production;production; recently however,however, thethe interestinterest inin naturalnatural sourcessources ofof thethe pigmentpigment isis increasingincreasing substantiallysubstantially [ 6[6,7].,7]. UnlikeUnlike mostmost antioxidantsantioxidants whichwhich workwork inin thethe innerinner (e.g.,(e.g., vitaminvitamin EE andand ββ-carotene) oror in the outer sideside ofof thethe membranemembrane (e.g.,(e.g., vitamin vitamin C), C), astaxanthin astaxanthin stretches stretches through through the the bilayer bilayer membrane, membrane, providing provid- protectioning protection against against oxidative oxidative stress stress by scavenging by scavenging reactive reactive oxygen oxygen species species (ROS) (ROS) in both in both the inner the inner and outerand outer layers layers of the of cellular the cellular membrane membrane [4,5]. [4,5]. SeveralSeveral recent clinical trials highlight the potential role of astaxanthin in promoting eye health, asas suggestedsuggested byby thethe significantsignificant improvementimprovement in thethe outcomesoutcomes ofof variousvarious ocularocular diseasesdiseases includingincluding diabeticdiabetic retinopathy,retinopathy, age-relatedage-related macularmacular degeneration,degeneration, glaucoma glaucoma and and cataract. cataract. TheThe aim of of the the present present paper paper is to is provide to provide a comp a comprehensiverehensive review review of the of current the current clinical clinical appli- applicationscations of astaxanthin of astaxanthin in the in treatment the treatment of a wide of a wide range range of ocular of ocular diseases. diseases. 2. Literature Review: Methods 2. Literature Review: Methods Relevant articles published to March 2020 were searched using PubMed, Scopus and Medline Relevant articles published to March 2020 were searched using PubMed, Scopus and Medline databases, as well as through the reference lists of identified publications. Search terms included the databases, as well as through the reference lists of identified publications. Search terms included the following key phrases: astaxanthin; carotenoids; eye; age-related macular degeneration; glaucoma; following key phrases: astaxanthin; carotenoids; eye; age-related macular degeneration; glaucoma; cataract; dry eye disease; oxidative stress; nutritional supplements. cataract; dry eye disease; oxidative stress; nutritional supplements. 3. Mechanism of Action 3. Mechanism of Action 3.1. Antioxidant Activity 3.1. Antioxidant Activity Oxidative stress results from a disturbance of the delicate balance between cellular pro- and anti-oxidantOxidative reactions,stress results and from acts a as disturbance a key mediator of the in delicate the pathogenesis balance between of several cellular human pro- and diseases. anti- Indeed,oxidant reactions, the excess and of oxidativeacts as a key agents mediator may in react the withpathogenesis proteins, of lipids several and human nucleic diseases. acids throughIndeed, athe chain excess reaction of oxidative with subsequent agents may functionalreact with andproteins, structural lipids damage.and nucleic A commonacids through carotenoid a chain exerts reac- itstion antioxidant with subsequent activity functional either by and disrupting structural free-radical damage. A chain common reactions carotenoid or by reacting exerts its with antioxidant them to produceactivity either harmless by disrupting products, free-radical whereas astaxanthin chain reacti neutralizesons or by reacting single oxygens with them and to scavenges produce harmless radicals toproducts, prevent whereas chain reactions, astaxanthin thus neut preservingralizes membranesingle oxygens structure and scavenges [5]. Naguib radicals and coauthors to prevent showed chain thatreactions, astaxanthin thus preserving has a higher membrane antioxidant structure activity [5 compared]. Naguib and to other coauthors carotenoids showed such that as astaxanthinα-carotene, lycopene,has a higher lutein, antioxidant and β-carotene activity [compared8]. Furthermore, to other another carotenoids study such evaluated as α-carotene, the effects lycopene, of astaxanthin, lutein, and β-carotene [8]. Furthermore,
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