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The Impact of Formulation on Lutein, Zeaxanthin, and Meso-Zeaxanthin Bioavailability: a Randomised Double-Blind Placebo-Controlled Study

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The Impact of Formulation on Lutein, Zeaxanthin, and Meso-Zeaxanthin Bioavailability: a Randomised Double-Blind Placebo-Controlled Study antioxidants Article The Impact of Formulation on Lutein, Zeaxanthin, and meso-Zeaxanthin Bioavailability: A Randomised Double-Blind Placebo-Controlled Study Marina Green-Gomez 1 , Alfonso Prado-Cabrero 1 , Rachel Moran 1, Tommy Power 1, Laura G. Gómez-Mascaraque 2 , Jim Stack 1 and John M. Nolan 1,* 1 Nutrition Research Centre Ireland, School of Health Sciences, Carriganore House, Waterford Institute of Technology West Campus, X91 X236 Waterford, Ireland; [email protected] (M.G.-G.); [email protected] (A.P.-C.); [email protected] (R.M.); [email protected] (T.P.); [email protected] (J.S.) 2 Teagasc Food Research Centre, Moorepark, Fermoy, P61 C996 Co. Cork, Ireland; [email protected] * Correspondence: [email protected]; Tel.: +353-(0)51-845-505 Received: 30 July 2020; Accepted: 15 August 2020; Published: 18 August 2020 Abstract: Lutein (L), zeaxanthin (Z), and meso-zeaxanthin (MZ) have been the focus of research and commercial interest for their applications in human health. Research into formulations to enhance their bioavailability is merited. This 6 month randomised placebo-controlled trial involving 81 healthy volunteers compared the bioavailability of different formulations of free L, Z, and MZ in sunflower or omega-3 oil versus L, Z, and MZ diacetates (Ld, Zd, and MZd) in a micromicellar formulation. Fasting serum carotenoids, macular pigment, and skin carotenoid score were analysed at baseline and 6 months. Serum L, Z, and MZ concentrations increased in all active interventions compared to placebo (p < 0.001 to p = 0.008). The diacetate micromicelle formulation exhibited a significantly higher mean response in serum concentrations of Z and MZ compared to the other active interventions (p = 0.002 to 0.019). A micromicellar formulation with solubilised Z and MZ diacetates is a promising technology advancement that enhances the bioavailability of these carotenoids when compared to traditional carotenoid formulations (ISRCTN clinical trial registration number: ISRCTN18206561). Keywords: meso-zeaxanthin; zeaxanthin; lutein; carotenoid diacetates; bioavailability; micromicelles 1. Introduction Lutein (L), zeaxanthin (Z), and meso-zeaxanthin (MZ) are xanthophyll carotenoids (XC) that singularly deposit in the human macula lutea [1], where they are known as macular pigment (MP). L and Z are obtained solely through dietary intake [2]. MZ has been proposed to be obtained from the endogenous conversion of L in the retinal pigment epithelium [3], but it can be also found in trace amounts in diet [4]. Over the last two decades, intervention trials have studied the role of L, Z, and MZ in human health using nutritional supplements [2]. Reports confirmed that these carotenoids enhance visual performance [5–12] and cognitive function [13], and are potential preventive and therapeutic agents in retinal pathology, such as non-advanced age-related macular degeneration (AMD) [14]. L used in nutritional supplements is extracted from the marigold flower (Tagetes erecta L.) [15], while Z is obtained from specific varieties of this flower [16] and peppers [17]. MZ is obtained from L through a process that promotes the migration of a double bond that turns the "-ring of L into a β-ring [18]. In every case, the final purification step forms XC microcrystals [17,19] (Figure1). Nutraceutical companies continually seek to develop new methods to protect these microcrystals from oxidation, improve their solubility in aqueous matrices, and increase their bioavailability in the Antioxidants 2020, 9, 767; doi:10.3390/antiox9080767 www.mdpi.com/journal/antioxidants Antioxidants 2020, 9, x FOR PEER REVIEW 2 of 16 Antioxidants 2020, 9, 767 2 of 15 Nutraceutical companies continually seek to develop new methods to protect these microcrystals from oxidation, improve their solubility in aqueous matrices, and increase their bioavailability in the digestive system.system. AmongAmong thethe methodsmethodsdescribed described to to protect protect the the XC XC microcrystals microcrystals are are the the dispersion dispersion in ediblein edible oils, oils, encapsulation encapsulation with with biopolymers biopolymers [20] or [20] mechanochemical or mechanochemical complexation complexation [21,22]. To[21,22]. increase To bioavailabilityincrease bioavailability and solubility and solubility in different in matrices,different researchersmatrices, researchers have emulsified have emulsified the XC following the XC difollowingfferent methods different [ 23methods,24]. However, [23,24]. noneHowever, of these none methods of these manage methods to dissolve manage the to microcrystalsdissolve the completely.microcrystals Recently, completely. a new Recently, method esterifying a new method the XCs esterifying with short the organic XCs acids,with short claimed organic to keep acids, XCs solubilisedclaimed to withoutkeep XCs the solubilised formation ofwithout microcrystals the formation under environmental of microcrystals conditions under ofenvironmental temperature andconditions pressure of [temperature23,25]. In this and process, pressure XCs [23,25]. are esterified In this process, with acetate XCs are or esterified propionate with to formacetate L, or Z, andpropionate MZ diacetates to form (Ld,L, Z, Zd,and andMZ MZd,diacetates respectively). (Ld, Zd, and After MZd, this respec reactiontively). takes After place, this XC reaction derivatives takes areplace, then XC homogenised derivatives are in theirthen naturalhomogenised original in flowertheir natural matrix original in the presence flower matrix of lipids, in the phospholipids, presence of fattylipids, acids, phospholipids, and emulsifiers fatty toacids, keep and XCs emulsifiers soluble. In to the keep digestive XCs soluble. system, In this the soluble digestive state system, facilitates this thesoluble incorporation state facilitates of XCs the into incorporation micromicelles, of XCs which into aremicromicelles, spherical aggregates which are ofspherical lipid molecules aggregates in theof lipid presence molecules of amphiphilic in the presence compounds of amphiphilic known as compounds surfactants [known24,26]. as This surfactants formulation [24,26]. has beenThis previouslyformulation tested has [been27–29 previously] in clinical trialstested and [27–29] compared in clinical to crystallised trials and formulations compared (free to crystallised lutein). formulations (free lutein). Figure 1. Formation of lutein (L) from marigold flower flower as free L (microcrystals) and as a diacetatediacetate derivative. In In the flower, flower, L is present as esterifiedesterified L with fatty acids. To extractextract this carotenoid, it is de-esterifiedde-esterified and purifiedpurified by crystallisation.crystallisation. To solubilisesolubilise these crystals and facilitate absorption in the digestive system, L and otherother xanthophyllxanthophyll carotenoids (XCs) can be re-esterifiedre-esterified with acetate or propionate upon crystallisation and re-suspended inin the flower’sflower’s lipid matrix with added surfactants to maintain thethe XCsXCs solubilisedsolubilised underunder ambientambient conditions.conditions. Here, we present the findings of the Carotenoid-Omega Availability Study (COAST), which was Here, we present the findings of the Carotenoid-Omega Availability Study (COAST), which was performed to compare the bioavailability of Ld, Zd and MZd in a micromicelle formulation with performed to compare the bioavailability of Ld, Zd and MZd in a micromicelle formulation with classical formulations containing the free carotenoids as microcrystals suspended in oil. classical formulations containing the free carotenoids as microcrystals suspended in oil. 2. Materials and Methods 2. Materials and Methods 2.1. Design and Study Population 2.1. Design and Study Population COAST was a 6 month, double-blind, block-randomised placebo-controlled study involving 81 healthyCOAST participants was a 6 between month, 18double-blind, and 65 years block-randomised old. Participant recruitment placebo-controlled and assessment study involving commenced 81 inhealthy December participants 2017 and between ended in 18 December and 65 2018.years Recruitmentold. Participant was achievedrecruitment through and localassessment media, andcommenced advertisement in December at the Waterford2017 and ended Institute in December of Technology, 2018.local Recruitment fitness centres, was achieved and with through employees local Antioxidants 2020, 9, 767 3 of 15 of an industry based in Waterford, Ireland. Participants were excluded if they had a medical diagnosis of a critical or acute medical condition and/or if they were taking nutritional supplements containing L, Z, MZ, or omega-3 fatty acids. Every participant enrolled in the study provided written informed consent prior to commencement. The study protocol was approved in May 2017 by the Research Ethics Committees of the Waterford Institute of Technology (Waterford, Ireland; +353-51-302000; [email protected]), ref: 17/HS-MPRG/01 and the HSE, South Eastern Area (University Hospital Waterford, Waterford, Ireland; +353-51-842026). Industrial Organica, S.A. de C.V., the manufacturer of the nutritional supplements, had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript. All authors vouch for the accuracy of the data and the fidelity of the study to the protocol. 2.2. Interventions COAST was a five-arm intervention study, where participants were randomly allocated, with equal probability and separately for men and women, to one
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