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Absorption and Pharmacokinetics of Grapefruit Flavanones in Beagles

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Absorption and Pharmacokinetics of Grapefruit Flavanones in Beagles Downloaded from British Journal of Nutrition (2007), 98, 86–92 doi: 10.1017/S0007114507707262 q The Authors 2007 https://www.cambridge.org/core Absorption and pharmacokinetics of grapefruit flavanones in beagles Maria de Lourdes Mata-Bilbao1, Cristina Andre´s-Lacueva1, Elena Roura1, Olga Ja´uregui2, Elvira Escribano3, 4 1 Celina Torre and Rosa Maria Lamuela-Ravento´s * . IP address: 1Department of Nutrition and Food Science, CerTA, Faculty of Pharmacy, University of Barcelona, Av. Joan XXIII s/n, Barcelona, Spain 2 Scientific and Technical Services, University of Barcelona, Barcelona, Spain 170.106.35.229 3Biopharmaceutics and Pharmacokinetics Unit, Faculty of Pharmacy, University of Barcelona, Av. Joan XXIII s/n, Barcelona, Spain 4Affinity Pet-care, Barcelona, Spain , on (Received 25 August 2006 – Revised 8 January 2007 – Accepted 24 January 2007) 29 Sep 2021 at 02:36:36 The present study evaluated the pharmacokinetics of three different grapefruit flavanone forms in dog plasma and demonstrated their absorption after an oral intake of a grapefruit extract; pharmacokinetic parameters of these forms were also determined. Ten healthy beagles were adminis- tered 70 mg citrus flavonoids as a grapefruit extract contained in capsules, while two additional dogs were used as controls and given an excipient. The grapefruit flavanone naringin, along with its metabolites naringenin and naringenin glucuronide, was detected in dog plasma. Blood , subject to the Cambridge Core terms of use, available at samples were collected between 0 and 24 h after administration of the extract. Naringin reached its maximun plasma concentration at around 80 min, whereas naringenin and naringenin glucuronide reached their maximun plasma concentrations at around 20 and 30 min, respectively. Maximum plasma concentrations of naringin, naringenin and naringenin glucuronide (medians and ranges) were 0·24 (0·05–2·08), 0·021 (0·001–0·3) and 0·09 (0·034–0·12) mmol/l, respectively. The areas under the curves were 23·16 l (14·04–70·62) min £ mmol/for nariningin, 1·78 (0·09–4·95) min £ mmol/l for naringenin and 22·5 (2·74–99·23) min £ mmol/l for naringenin glucuronide. The median and range values for mean residence time were 3·3 (1·5–9·3), 2·8 (0·8–11·2) and 8·0 (2·3–13·1) h for naringin, naringenin and naringenin glucuronide, respectively. The results of the present study demonstrate the absorption of grapefruit flavanones via the presence of their metabolites in plasma, thus making an important contribution to the field since the biological activities ascribed to these compounds rely on their specific forms of absorption. Absorption: Flavanone: Bioavailability: Dog: Grapefruit: Pharmacokinetics: Plasma Flavonoids are a group of polyphenolic compounds with et al. 2004, 2005), CYP3A4 being a type of cytochrome health-related properties that are widely distributed in fruits, P450. These studies suggest a potential therapeutic benefit https://www.cambridge.org/core/terms vegetables, fruit juices, cocoa, teas and wines. Citrus fruits from using the active constituents of grapefruit to increase are rich in flavonoids that have been investigated for their bio- drug bioavailability. Lowering the effective dose will also logical activity. The use of citrus flavonoids as anti-inflamma- reduce drug costs, although potential clinical problems tory, anticarcinogenic and antitumour agents has been reported remain (Dahan & Altman, 2004). (Middleton & Kandaswami, 1994; Benavente-Garcı´a et al. One of the most common flavonoids found in grapefruit 1997; Montanari et al. 1998). Recent research shows that (Citrus paradisi) is the flavanone glycoside naringin (narin- the citrus flavonoid naringenin stimulates DNA repair in pros- genin 7-O-neohesperidoside; Fig. 1). Naringin is also known tate cancer cells (Gao et al. 2006), whereas the flavanone gly- to be the agent responsible for the bitterness of grapefruit coside naringin has proved to be a potent inhibitor of juice. Narirutin and naringenin (Fig. 1) are also present in . angiogenic peptide vascular endothelial growth factor, which grapefruit but to a lesser extent (Macheix et al. 1990). https://doi.org/10.1017/S0007114507707262 is released in human tumour cells (Schindler & Mentlein, Most of the molecular forms of flavonoids that reach the 2006). These studies suggest a novel mechanism for mammary peripheral circulation and tissues are different from those pre- cancer prevention, which is considered the most common sent in foods (Day & Williamson, 2001; Day et al. 2001; cancer in female dogs. Graefe et al. 2001; Natsume et al. 2003; Zhang et al. 2003). Several studies have shown that grapefruit juice elevates the In general, the predominant forms in plasma are conjugates blood levels of some orally taken drugs, primarily by inhibit- (glucuronates or sulphates, with or without methylation). ing intestinal CYP3A4-mediated first-pass metabolism (Fuhr These conjugates are chemically distinct from their parent et al. 2002; Dahan & Altman, 2004; Lilja et al. 2004; Paine compounds, differing in size, polarity and ionic form. Abbreviations: AUC, area under the curve; Cmax, maximum plasma concentration; LC, liquid chromatography; MRT, mean residence time; m/z, mass-to-charge ratio. * Corresponding author: Dr R. M. Lamuela-Ravento´s, fax þ34 93 4035931, email [email protected] Downloaded from Grapefruit flavanones in beagles 87 https://www.cambridge.org/core . IP address: 170.106.35.229 , on 29 Sep 2021 at 02:36:36 , subject to the Cambridge Core terms of use, available at Fig. 1. Structures and molecular weights (MW) of (A) naringin, (B) narirutin and C naringenin. Consequently, their physiological behaviour is likely to be for flavonoid analysis (Roura et al. 2005; Urpı´-Sarda` et al. different from that of the native compounds (Kroon et al. 2005; Fang et al. 2006). 2004), and their biological effect will ultimately depend on The use of dogs as a model has been shown to be helpful in the cellular effects of their circulating metabolites (Harada evaluating the absorption of flavonoids from green tea et al. 1999; Spencer et al. 2001a, b). (Swezey et al. 2003). Thus, the present study aims to assess Very little is known about the biological activities of these the major flavanone forms in plasma after the oral adminis- conjugated metabolites. Glucuronides of isoflavones and epi- tration of a grapefruit extract; and to evaluate the kinetics of catechin have been shown to have a much weaker oestrogenic these metabolic forms in the plasma by considering biotrans- activity and to provide no protection against oxidative stress formation, thus providing a general model that can be used in cells grown in vitro (Zhang et al. 1999; Spencer et al. for studies on flavonoid bioavailability. 2001a, b), whereas additional studies have shown that the 5- O-b-D-glucuronide of catechin and epicatechin excreted in rat urine does not interfere with their antioxidant properties, Methods https://www.cambridge.org/core/terms as assesed by their ability to scavenge superoxide (Harada Chemicals et al. 1999; Okushio et al. 1999), thus suggesting that in plasma they may still act as antioxidants. Although glucuro- Naringin (naringenin-7-O-rhamnoglucoside) and blank dog nides do not readily enter cells, it is also possible that they plasma were purchased from Sigma-Aldrich (St Louis, MO, 0 might be cleaved by the action of b-glucuronidases located USA). Naringenin (4 ,5,7-trihydroxyflavanone), narirutin (nar- in human tissues such as the liver (O’Leary et al. 2001) or ingenin-7-O-rutinoside) and the internal standard taxifolin by neutrophils that release b-glucuronidases when activated were purchased from Extrasynthese (Genay, France). Metha- (Shimoi et al. 1998; Simio et al. 2001). nol and acetonitrile, HPLC grade and formic acid were pur- Initially, only free flavonoids without a sugar molecule, so- chased from Scharlau Chemie S. A. (Barcelona, Spain). called aglycones, were considered to be able to pass across the Ultrapure water (Milli-Q) was obtained from a Millipore https://doi.org/10.1017/S0007114507707262 gut wall (Hollman & Katan, 1997). However, the absorption system (Millipore, Bedford, MA, USA). of quercetin glycosides from onions in human subjects (Holl- man et al. 1995) and the presence of the flavanone glycoside Animals and study design naringin in plasma and urine after oral administration (Ishii et al. 2000; Fang et al. 2006) have now been demonstrated. Animals. Ten healthy adult beagle dogs were randomly Liquid chromatography (LC)-MS/MS has emerged as the chosen. The dogs had a mean weight of 13·97 (SD 2·96) kg preferred technology for the quantitative determination of and were deprived of food overnight before the experiment. metabolites in different biomatrices, due to its sensitivity Two capsules containing 200 mg grapefruit extract (70 mg fla- and selectivity through MS/MS experiments and the fact that vanones) were orally administered to the dogs; two additional it enables structural identification (Murphy et al. 1994). Ion- dogs were chosen as controls and were given an excipient con- spray ionization, together with tandem MS for structural taining talc. The grapefruit extract contained naringin, nari- characterization, has become a popular and versatile method rutin and naringenin as citrus flavanones. Blood was drawn Downloaded from 88 M. de Lourdes Mata-Bilbao et al. before capsule administration and at the following times after MS/MS data. TurboIonspray source settings were as follows: https://www.cambridge.org/core administrations: 10 min, 20 min, 30 min, 40 min, 80 min, 2 h, capillary voltage, 23500 V; nebulizer gas (N2), 10 (arbitrary 4 h, 6 h, 8 h and 24 h. The dogs were fed with a polyphenol- units); curtain gas (N2), 12 (arbitrary units); collision gas free diet 2 h after the capsules were given. Blood samples (N2), 10 (arbitrary units); focusing potential, 2200 V; (5 ml) were collected in vacutainer tubes containing EDTA entrance potential, 10 V; drying gas (N2), heated to 4008C as anticoagulant (Becton, Dickinson, Franklin Lakes, NJ, and introduced at a flow rate of 8000 cm3/min.
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