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( Citrus Bergamia Risso ) As a Source of Nutraceuticals: Limonoids And

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( Citrus Bergamia Risso ) As a Source of Nutraceuticals: Limonoids And Journal of Functional Foods 20 (2016) 10–19 Available online at www.sciencedirect.com ScienceDirect journal homepage: www.elsevier.com/locate/jff Bergamot (Citrus bergamia Risso) as a source of nutraceuticals: Limonoids and flavonoids Marina Russo a,b, Adriana Arigò a, Maria Luisa Calabrò a, Sara Farnetti c, Luigi Mondello a,b,d, Paola Dugo a,b,d,* a “Scienze del Farmaco e Prodotti per la Salute” Department, University of Messina, Viale Annunziata, 98168 Messina, Italy b Chromaleont s.r.l., c/o “Scienze del Farmaco e Prodotti per la Salute” Department, University of Messina, Viale Annunziata, 98168 Messina, Italy c Division of Cellular Transplantation of Surgery, Diabetes Research Institute, University of Miami, Miami, FL 33136, USA d University Campus Bio-Medico of Rome, Via Álvaro del Portillo, 21-00128 Rome, Italy ARTICLE INFO ABSTRACT Article history: Limonoids are human health promoters, and have many pharmacological properties: an- Received 22 June 2015 ticancer, antioxidant, antibacterial and antifungal. To the best of the authors’ knowledge, Received in revised form 5 October there are no previous reports on the composition of limonoids in bergamot fruits, so the 2015 aim of this work was to characterize bergamot peel, pulp, seed and juice. Samples analysed Accepted 13 October 2015 showed the presence of both limonoids aglycones and glucosides. Limonoid aglycones are Available online 10 November 2015 the most abundant in seeds and peels (70 and 80% of the total, respectively), while limonoid glucosides are the more abundant in juices and pulps (61 and 76% of the total, respec- Keywords: tively). Moreover a method to isolate pure limonoids from bergamot seeds and juice by means Bergamot of a 2D-HPLC/PDA/MS preparative system is proposed. Pure molecules isolated were used Limonoids to build calibration curves to quantify limonoids in real samples. Isolation of nutraceuticals Bioactive molecules from seeds and juices can represent an advantageous way to re-evaluate these by-products. RP-HPLC © 2015 Elsevier Ltd. All rights reserved. By-products Multidimensional preparative HPLC logical properties: anticancer, antimicrobial, antiviral and anti- 1. Introduction inflammatory activities, effects on capillary fragility, inhibition of human platelet aggregation and reduction of oxidative stress Bergamot (Citrus bergamia, C.b), a typical fruit grown wildly in (Benavente-Garcia, Castillo, Marin, Ortunõ, & Del Rìo, 1997; Delle Calabria (Italy), is a rich source of flavonoids, as recently pub- Monache et al., 2013; Filocamo et al., 2015; Navarra et al., 2014). lished by Sommella et al. (2014), and by other authors (Di Donna The most abundant flavonoids in bergamot fruits are naringin, et al., 2009; Gattuso, Barreca, Caristi, Gargiulli, & Leuzzi, 2007; neohesperidin and neoeriocitrin (Di Donna et al., 2009); naringin Gattuso, Barreca, Gargiulli, Leuzzi, & Caristi, 2007; Gattuso et al., in particular has been evaluated for its probable protective 2006; Sommella et al., 2013). Flavonoids have shown many bio- actions on pre-neoplastic lesions (Kaur & Kaur, 2015). Naringin, * Corresponding author. University Campus Bio-Medico of Rome, Via Álvaro del Portillo, 21-00128 Rome, Italy. Tel.: +39 090 6766541; fax: +39 090 358220. E-mail address: [email protected] (P. Dugo). http://dx.doi.org/10.1016/j.jff.2015.10.005 1756-4646/© 2015 Elsevier Ltd. All rights reserved. Journal of Functional Foods 20 (2016) 10–19 11 neohesperidin and neoeriocitrin possess flavanone-7-O- analysis of limonoids in Citrus fruits was reversed phase liquid neohesperidoside structure, responsible for a bitter taste of the chromatography coupled with a UV–vis detector, and in many fruit and in particular of the juice (Puri, Marwaha, Kothari, & cases with a mass spectrometer. Generally electrospray mass Kennedy, 1996). However they are not the only bitter compo- ionization (ESI) is used for identification of Citrus limonoid glu- nents of bergamot fruits, or of Citrus fruits in general. In fact, cosides (Breksa et al., 2009; Breksa, Zukas, & Manners, 2005), limonin is an intensely bitter triterpenoid dilactone deriva- while atmospheric pressure chemical ionization (APCI) is pre- tive belonging to the limonoids group, widely distributed ferred for identification of Citrus limonoid aglycones (Balestrieri throughout the Citrus fruits. Because it is mainly responsible et al., 2011; Jayaprakasha, Dandekar, Tichy, & Patil, 2011; for the delayed development of bitterness in Citrus juices Manners & Breksa, 2004). (Hasegawa, Bennett, & Verdon, 1980), the presence of this mol- There are many literature data on the composition of ecule in bergamot fruits increases the bitter taste. Limonoids limonoids in different Citrus fruits: sweet orange (Breksa et al., are human health promoters, and have many pharmacologi- 2005; Fong, Hasegawa, Coggins, Atkin, & Miyake, 1992; Herman, cal properties: anticancer, antioxidant, antibacterial and Fong, Ou, & Hasegawa, 1990), lemon (Ronneberg, Hasegawa, antifungal (Kaur & Kaur, 2015). A recent study (Kelley et al., 2015) Suhayda, & Ozaki, 1995), grapefruit (Breksa et al., 2005; Hsu, has demonstrated that limonin glucoside consumption may Berhow, Robertson, & Hasegawa, 1998; Manners et al., 2003; Yu prevent and reverse chronic inflammatory diseases, includ- et al., 2005), lime (Jitpukdeebodintra, Chantachum, Ratanaphan, ing non-alcoholic fatty liver and cardiovascular diseases, type-2 & Chantrapromma, 2005), sour orange (Breksa, Kahn, Zukas, diabetes mellitus, and metabolic syndromes; moreover, supple- Hidalgo, & Lee Yuen, 2011), pummelo (Liu et al., 2015; Xiang menting the diet of overweight and obese human subjects et al., 2014), calamondin (Manners & Breksa, 2004), but there with limonin glucoside significantly decreased circulating is a lack of investigation on the content of limonoids in ber- concentrations of gamma-glutamyl transferase, alanine ami- gamot fruits. There is only one article based on the isolation notransferase and alkaline phosphatase (Kelley et al., 2015). of limonin and nomilin from bergamot seeds, aimed to the in- Nomilin glucoside, limonin glucoside, obacunone gluco- vestigation of the antiretroviral activity of limonoids (Balestrieri side, limonin and nomilin inhibit chemically induced et al., 2011). carcinogenesis in a series of human cancer cell lines, with re- In this work, the qualitative and quantitative characteriza- markable cytotoxicity against colon, oral cavity, lung and skin tion of limonoids (both aglycones and glucosides) in juice, peels, cancer in animal test system and human breast cancer cells pulps and seeds of two bergamot cultivars (Fantastico and (Kaur & Kaur, 2015; Manners, Breksa, Schoch, & Hidalgo, 2003; Femminello) by means of RP-HPLC/PDA/MS is reported. More- Miller et al., 1989; Tanaka, Kohno, & Tsukio, 2000). Limonin and over, a method to isolate pure limonoids from bergamot juice nomilin, present in high concentration in bergamot seeds, have by means of an HPLC–HPLC/PDA/MS preparative system is shown good ability in the inhibition of HIV and HTLV-1 reverse proposed. transcriptases (Balestrieri et al., 2011). Moreover limonin has Cold-pressed essential oil represents the main product of antimicrobial activity (Govindachari et al., 1995), offers some the bergamot industry, while bergamot juice is considered a protection capacity against low-density lipoprotein (LDL) oxi- by-product of the bergamot essential oil production (Gardana, dation, and like other limonoid aglycones, possesses a stronger Nalin, & Simonetti, 2008; Pernice et al., 2009), so isolation of antioxidant capacity than limonoid glucosides (Yu et al., 2005). nutraceuticals from bergamot juice can represent a way to re- Limonoids occur in Citrus both in glucosidic and aglyconic evaluate this by-product. As previously reported by Russo, Dugo, form. Limonoid aglycones are water-insoluble and respon- Marzocco, Inferrera, and Mondello (2015), bergamot juice rep- sible for a bitter taste of the Citrus fruits, while limonoid resents an excellent raw material for the isolation of flavones glucosides are water-soluble and tasteless. These molecules are and flavanones, and could be a good source of limonoids too. present in considerable amounts in Citrus fruits, the highest “Pastazzo”, the other by-product of bergamot essential oil concentration was found in seeds, but these are also present production, which represents roughly 55% of the fruit, is com- in peels, pulps and juices (Kaur & Kaur, 2015). Limonoid glu- posed of seeds, pulps and exhausted peels. Part of the “pastazzo” cosides (limonin glucoside, nomilin glucoside, obacunone is industrially dried, both to produce pectin and for cattle glucoside, nomilinic acid glucoside, deacetylnomilinic acid glu- feeding. An infusion of dried peels and seeds could be an al- coside) are more abundant in juices and pulps because they ternative to the use of dried “pastazzo”, and therefore could be are water-soluble, while limonoid aglycones (limonin, nomilin, another way to re-evaluate this by-product. obacunone, ichangin, deacetyl nomilin) are water-insoluble and are present mainly in seeds and peels (Breksa, Hidalgo, & Lee Yuen, 2009; Manners & Breksa, 2004). 2. Materials and methods Analytical techniques used to identify and quantify Citrus limonoids include: thin-layer chromatography (TLC) with silica 2.1. Materials and samples gel plates, in which the chromatograms were sprayed with Ehrlich’s reagent, a highly selective detection reagent for This research was carried out on two cultivars of bergamot
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