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In Vitro Studies of an Aged Black Garlic Extract Enriched in S-Allylcysteine and Polyphenols with Cardioprotective Effects

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In Vitro Studies of an Aged Black Garlic Extract Enriched in S-Allylcysteine and Polyphenols with Cardioprotective Effects journal of functional foods 27 (2016) 189–200 Available online at www.sciencedirect.com ScienceDirect journal homepage: www.elsevier.com/locate/jff In vitro studies of an aged black garlic extract enriched in S-allylcysteine and polyphenols with cardioprotective effects A.L. García-Villalón a, S. Amor a, L. Monge a, N. Fernández a, M. Prodanov b, M. Muñoz c, A.M. Inarejos-García c, M. Granado a,* a Departamento de Fisiología, Facultad de Medicina, Universidad Autónoma de Madrid, Madrid, Spain b Departamento de Química Física Aplicada, Facultad de Ciencias, CIAL (CEI, CSIC-UAM), Universidad Autónoma de Madrid, Madrid, Spain c Pharmactive Biotech Products SL, Parque Científico de Madrid, Madrid, Spain ARTICLE INFO ABSTRACT Article history: Aged black garlic (ABG) exerts metabolic and cardiovascular beneficial effects. The aim of Received 1 April 2016 this work was to analyse the in vitro cardiovascular effects of an ABG extract enriched in Received in revised form 22 August S-allyl-cysteine and polyphenols (ABG10+) in Sprague-Dawley rats. Hearts were pre- 2016 treated either with ABG10+ or vehicle and subjected to 30 min ischaemia followed by 45 min Accepted 29 August 2016 reperfusion (IR) using the Langendorff technique. Segments of aorta and tail artery were Available online used for inflammation/oxidative stress and vascular reactivity experiments respectively in presence/absence of ABG10+. ABG10+ induced a nitric oxide (NO) dependent vasodilating Keywords: effect in tail artery segments and directly increased the release of NO in aorta segments. + Aged black garlic In the heart, ABG10 induced a relaxing effect on coronary arteries before and after IR and Ischaemia–reperfusion prevented the IR induced decrease in myocardial contractility. Functional changes were as- Nitric oxide sociated with increased expression of both pro- and antioxidant and pro- and anti- Antioxidant inflammatory markers in the myocardium and in aorta. Anti-inflammatory © 2016 Elsevier Ltd. All rights reserved. Allicin is highly unstable at pH close to neutral values, at high 1. Introduction temperatures or in the presence of oils and rapidly degrades during processing or during storage, limiting its bioaccessibility Raw garlic has long been used as traditional medicine for treat- (Kim, Nam, Rico, & Kang, 2012). ing a diverse range of human diseases, due to the presence Concerning toxicity, raw garlic must be consumed in mod- of several bioactive components with proven beneficial effects eration because it might be toxic at high doses (Bae, Cho, Won, (Bautista et al., 2005; Rees, Minney, Plummer, Slater, & Skyrme, Lee, & Park, 2014; Kodera et al., 2002). In addition to toxicity, 1993). Among them, the most studied and relevant is allicin the consumption of unprocessed raw garlic is limited due to and its derivatives; allicin is the major thiosulfinate in fresh its characteristic odour, taste and tendency to cause an upset crushed garlic, which is responsible for its characteristic taste stomach (Kodera et al., 2002). Therefore, in recent years, various and aroma (Rosin, Tuorila, & Uutela, 1992; Salazar et al., 2008). processing methods such as heat treatment, ageing and * Corresponding author. Department of Physiology, Faculty of Medicine, Universidad Autónoma de Madrid, C/ Arzobispo Morcillo n°2, 28029 Madrid, Spain. Fax: +34 91 497 5478. E-mail address: [email protected] (M. Granado García). http://dx.doi.org/10.1016/j.jff.2016.08.062 1756-4646/© 2016 Elsevier Ltd. All rights reserved. 190 journal of functional foods 27 (2016) 189–200 fermentation have been used to eliminate the offensive odour 1982) and hypertension (Zhang et al., 2001); therefore these dis- and improve garlic palatability. Heat treatment is the most fre- eases may be improved and/or prevented by garlic products. quently used processing method to improve the taste and Raw garlic extract reduces infarct size in isolated rabbit flavour of garlic. During heating, non-enzymatic browning hearts (Sharma et al., 2012) and rat hearts (Banerjee, Dinda, (Maillard reaction) produces some physical–chemical changes Manchanda, & Maulik, 2002), although high doses were car- such as colour, flavour, texture, macronutrients and minor com- diotoxic and improved oxidative myocardial damage (Ku et al., pounds content (Nencini, Menchiari, Franchi, & Micheli, 2011), 2002). Moreover, it produces arterial dilatation mediated by nitric which results in the production of aged black garlic. oxide (Benavides et al., 2007; Grman et al., 2011) or hydrogen The general procedure to obtain black garlic is by heating sulfide (Chuah, Moore, & Zhu, 2007). These beneficial effects the whole raw garlic bulb at a high temperature and con- might be enhanced in aged garlic, as SAC present in ABG10+ trolled humidity for approximately 1 month. Black garlic is reported to induce myocardial protection during isch- has a rubbery texture and during the browning process the aemia (Numagami, Sato, & Ohnishi, 1996). Indeed, aged garlic soluble solids content (˚Brix) increases and the taste becomes has been shown to protect against ischaemia–reperfusion injury sweet. The pH of the product also decreases from approxi- in rat brain (Augusti, 1996), but the effects of this particular mately 6 in raw garlic to less than 3.8 in aged black garlic; preparation have not been studied during cardiac ischaemia. this effect together with the high processing temperature The preventive and/or therapeutic use of garlic products on explains the longer shelf life of the product (Nencini et al., the cardiovascular system needs to be improved by a better 2011; Toledano-Medina, Perez-Aparicio, Moreno-Rojas, & characterization of their effects as there is evidence that Merinas-Amo, 2016). Another important change during the there may be undesirable effects at high doses (Banerjee et al., ageing process is the increase in polyphenols content (Kim et al., 2001; Egen-Schwind, Eckard, & Kemper, 1992; Joseph, Rao, & 2011; Park, Park, & Park, 2009), and consequently also in its an- Sundaresh, 1989; Nakagawa, Masamoto, Sumiyoshi, Kunihiro, tioxidant capacity (Nencini et al., 2011). & Fuwa, 1980; Robards, Prenzler, Tucker, Swatsitang, & Glover, On the other hand, the increased antioxidant capacity is 1999). also due to the transformation of some of the unstable and The chemical characterization of SAC and its derivatives is odorous components of raw garlic into stable and odourless still a challenge to be overcome in aged black garlic, mainly due compounds during ageing process, mostly organosulfur com- to its complexity and the very limited absorption of ultraviolet pounds such as S-allylcysteine (SAC) (Lee et al., 2009). SAC is (UV) light of these compounds, 205–210 nm. This is the range, a water-soluble bioactive compound known for its high anti- where the most common solvents used in reversed phase HPLC, oxidant capacity (Bae, Cho, Won, Lee, & Park, 2012) formed acetonitrile and/or methanol, also absorb. In addition, fine sepa- during the enzymatic hydrolysis of γ-glutamyl-S-allylcysteine, ration of these compounds requires the use of salt-containing catalyzed by γ-glutamyl transpeptidase (γ-GTP, EC 2.3.2.2). Its mobile phases, which is a serious problem in HPLC mainte- content is about 20–30 μg/g in raw garlic, and rises up to six nance and mass detection (Beato, Sanchez, de Castro, & Montano, times after the ageing process (Bae et al., 2014; Hanum, Sinha, 2012). This is why most of the analytical techniques developed Guyer, & Cash, 1995). Nevertheless, the γ-GTP activity is af- for determination of amino acids are based on their derivatization fected by heat (Munday, James, Fray, Kirkwood, & Thompson, to chromophores (o-phthaldialdehyde, OPA) or fluorophores (9- 1999), and therefore high temperatures can limit its forma- fluorenylmethyl chloroformate, FMOC or 6-aminoquinolyl-N- tion during ageing. hydroxysuccinimidyl carbamate, AQC) (Bae et al., 2012; Cronin, Several studies have reported that SAC has cardioprotective Pizzarello, & Gandy, 1979; Gartenmann & Kochhar, 1999). effects (Banerjee, Mukherjee, & Maulik, 2003; Ried, Frank, & However, while they considerably improve the detection Stocks, 2010; Steiner, Khan, Holbert, & Lin, 1996) although the selectivity and sensitivity, they are also time-consuming, labo- mechanisms involved are not completely understood. As re- rious and/or require specific instrumentation for carrying out active oxygen species (ROS) play a central role in these a pre- or post-column derivatization, which often leads to low alterations, research has focused on the antioxidant proper- reproducibility. Consequently, it is necessary to develop a more ties of garlic products (Yamasaki, Li, & Lau, 1994). simple and efficient methodology for the assessment of these The wide range of beneficial effects of aged black garlic molecules. include the protection of vascular endothelial cells against hy- Therefore, in this study we have used a newly developed drogen peroxide induced injury (Reeve, Bosnic, Rozinova, & fast methodology for the determination of SAC and its main Boehm-Wilcox, 1993), protection against damage caused by ion- derivatives in an aged black garlic extract ABG10+ and analysed izing radiation (Kojima, Toyama, & Ohnishi, 1994)ortoxic its in vitro effects on isolated rat arteries and isolated per- substances (Alkreathy et al., 2010; Lee et al., 2011), inhibition fused rat hearts during coronary ischaemia–reperfusion. of oxidative and inflammatory markers (Weiss, Papatheodorou, Morihara, Hilge, & Ide, 2013) and an increase in nitric
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