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Increased Bioavailability of Hesperetin-7-Glucoside Compared with Hesperidin Results in More Efficient Prevention of Bone Loss in Adult Ovariectomised Rats

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Increased Bioavailability of Hesperetin-7-Glucoside Compared with Hesperidin Results in More Efficient Prevention of Bone Loss in Adult Ovariectomised Rats Downloaded from British Journal of Nutrition (2009), 102, 976–984 doi:10.1017/S0007114509338830 q The Authors 2009 https://www.cambridge.org/core Increased bioavailability of hesperetin-7-glucoside compared with hesperidin results in more efficient prevention of bone loss in adult ovariectomised rats . IP address: Ve´ronique Habauzit1, Inge-Lise Nielsen2, Angel Gil-Izquierdo3, Anna Trzeciakiewicz1, Christine Morand1, 2 2 1 1 2 Winnie Chee †, Denis Barron , Patrice Lebecque , Marie-Jeanne Davicco , Gary Williamson , 170.106.202.126 Elizabeth Offord2,Ve´ronique Coxam1 and Marie-Noe¨lle Horcajada1* 1Human Nutrition Unit, UMR 1019, ASM, INRA, Clermont-Ferrand/Theix, St-Gene`s Champanelle F-63122, France 2Nestle´ Research Center, Vers Chez Les Blanc, 1000 Lausanne 26, Switzerland , on 3Departamento de Ciencia y Tecnologı´a de Alimentos, CEBAS – CSIC, 30100 Espinardo, Murcia, Spain 29 Sep 2021 at 04:11:40 (Received 3 September 2008 – Revised 9 March 2009 – Accepted 11 March 2009 – First published online 27 April 2009) Hesperidin (Hp), a citrus flavonoid predominantly found in oranges, shows bone-sparing effects in ovariectomised (OVX) animals. In human subjects, the bioavailability of Hp can be improved by the removal of the rhamnose group to yield hesperetin-7-glucoside (H-7-glc). The aim , subject to the Cambridge Core terms of use, available at of the present work was to test whether H-7-glc was more bioavailable and therefore more effective than Hp in the prevention of bone loss in the OVX rat. Adult 6-month-old female Wistar rats were sham operated or OVX, then pair fed for 90 d a casein-based diet supplemented or not with freeze-dried orange juice enriched with Hp or H-7-glc at two dose equivalents of the hesperetin aglycone (0·25 and 0·5 %). In the rats fed 0·5 %, a reduction in OVX-induced bone loss was observed regarding total bone mineral density (BMD): þ 7·0 % in OVX rats treated with Hp (HpOVX) and þ6·6 % in OVX rats treated with H-7-glc (H-7-glcOVX) v. OVX controls (P,0·05). In the rats fed 0·25 % hesperetin equivalents, the H-7-glcOVX group showed a 6·6 % improvement in total femoral BMD v. the OVX controls (P,0·05), whereas the Hp diet had no effect at this dose. The BMD of rats fed 0·25 % H-7-glc was equal to that of those given 0·5 % Hp, but was not further increased at 0·5 % H-7-glc. Plasma hesperetin levels and relative urinary excretion were significantly enhanced in the H-7-glc v. Hp groups, and the metabolite profile showed the absence of eriodictyol metabolites and increased levels of hesperetin sulphates. Taken together, improved bioavailability of H-7-glc may explain the more efficient bone protection of this compound. Bioavailability: Bone mineral density: Hesperidin: Flavanones: Rats British Journal of Nutrition Nutrition plays an important role in the dietary management Hesperidin (Hp), a monomethoxylated flavanone found and prevention of osteoporosis, a major public health problem. abundantly in citrus fruits such as oranges(10), is highly https://www.cambridge.org/core/terms While it is established that Ca, vitamin D and micronutrients consumed in Western countries. Indeed, in Finland, Hp con- are essential for bone health, other compounds such as sumption was estimated to be 28 mg/d, contributing to 50 % polyphenols, found abundantly in fruit and vegetables, show of total flavonoid intake(11). Hp and metabolites show promis- potential for bone-protective effects. For example, rodent ing health benefits due to their antioxidant, anti-inflammatory studies have shown that quercetin and quercetin-3-rhamnoglu- and lipid-lowering properties demonstrated in preclinical coside (rutin) from onions(1,2), resveratrol from red wine(3) and models(12 – 14). Furthermore, Hp shows bone-sparing effects isoflavones from soya(4) inhibit ovariectomised (OVX)- in OVX mice and rats of various ages, when provided in the induced bone loss. Until now, most of the human intervention diet at 0·5 %(15,16), and citrus juice consumption has been studies have been carried out with high levels of soya isofla- shown to prevent bone loss in male orchidectomised rats(17). vones (80–90 mg), some studies showing prevention of bone Flavonoids are commonly conjugated to glycosides when https://doi.org/10.1017/S0007114509338830 loss in postmenopausal women(5,6), while others not(7,8). The present in plants. Hp is one such conjugated glycoside consist- level of consumption of soya products is rather low in Western ing of the aglycone hesperetin (40-methoxy-30,5,7-trihydroxy- countries compared with Asian ones, whose daily intakes flavanone) bound to rutinose (i.e. one molecule of rhamnose (9) (18) average 20–40 mg . Therefore, it would be of interest to and one molecule of glucose) in the C7-position . Hp has identify commonly consumed polyphenols with bone-protec- limited bioavailability in human subjects, due to the delayed tive effects, as soya is not used as a staple in the Western diet. action of the colonic microflora needed to release the rutinose Abbreviations: BMD, bone mineral density; D-BMD, diaphyseal BMD; dM-BMD, distal metaphyseal BMD; DPD, deoxypyridinoline; H-7-glc, hesperetin-7- glucoside; Hp, hesperidin; M-BMD, metaphyseal BMD; OC, osteocalcin; OVX, ovariectomy; pM-BMD, proximal BMD; T-BMD, total BMD. * Corresponding author: Marie-Noe¨lle Horcajada, fax þ33 473 62 46 38, email [email protected] † Present address: Department of Nutrition and Dietetics, International Medical University, Plaza Komanwel, Bukit Jalil, 50 700 Kuala Lumpur, Malaysia. Downloaded from Hesperidin bioavailability and bone density 977 moiety of Hp before absorption of its aglycone hesperetin. of diet given to each rat per day was adjusted to the mean food https://www.cambridge.org/core Indeed, consumption of 1 litre of orange juice containing intake registered in SH animals (pair feeding). The animals 450 mg Hp led to circulating plasma concentrations of had free access to water during the entire study, and their hesperetin of approximately 1 mM with a peak at 5 h body weights and food intake were measured weekly. Urine post-ingestion(19). Monoglucuronides of hesperetin were the of each animal was collected over a 24-h period on day 0 major forms present in plasma after the ingestion of orange and the day before killing, to measure urinary excretion of juice(19). We have recently demonstrated that enzymatic deoxypyridinoline (DPD), a marker for bone resorption. removal of the rhamnose sugar from Hp to yield hesperetin- At killing, on day 90, blood samples were collected into ice- 7-glucoside (H-7-glc) improves its bioavailability by 3-fold cooled heparinised plastic tubes containing 200 peptidase . IP address: in human subjects(20). The removal of the terminal rhamnose inhibitory units of aprotinin (Iniprol, Choay, Paris, France) sugar changes the absorption site from the colon to the per millilitre blood, and centrifuged immediately (3500 g for small intestine, as it has been previously demonstrated with 5 min at 48C). Then plasma samples were frozen at 2208C 170.106.202.126 rutin and quercetin-4-glucoside in onions(21). until measurements of osteocalcin (OC), a marker of osteo- The aim of the present study was to test whether H-7-glc blastic activity. Before freezing at 2208C, plasma samples was more bioavailable than Hp in the OVX rat (as in human dedicated to the analysis of hesperetin metabolites were subjects) and whether this correlated with improved efficiency acidified with acetic acid (0·1 M, 1 %) in order to protect the in prevention of bone loss. structure of these metabolites. Uterine horns were removed , on and immediately weighed. Femurs were separated from adja- 29 Sep 2021 at 04:11:40 cent tissue, cleaned and used for physical measurements Experimental methods (mechanical testing and bone mineral density (BMD)). Animals and diets Bone measurements The study was carried out in accordance with the recommen- dations of the Regional Ethical Committee on animal exper- Bone mineral density. BMD was assessed by dual-energy , subject to the Cambridge Core terms of use, available at imentation in France. Fifty-eight adult, 6-month-old virgin X-ray absorptiometry, with the Hologic QDR-4500 A X-ray female Wistar rats were purchased from Institut National de bone densitometer. The total right femur BMD (T-BMD), as la Recherche Agronomique (Clermont-Ferrand/Theix, well as the BMD of two subregions, one corresponding to St-Gene`s Champanelle, France). Five groups of ten rats the metaphyseal zone (M-BMD), rich in cancellous bone, were surgically OVX and one group of eight rats was sham and the other to the diaphyseal zone (D-BMD), rich in cortical operated (SH) under anaesthesia, using chloral hydrate bone, were determined(22). In each femur scan, distal (Fluka Chemie AG, Buchs, Switzerland; 80 g/l in saline sol- (dM-BMD) and proximal (pM-BMD) metaphyseal regions ution; 0·4 ml/100 g body weight intraperitonealy). The animals of interest were positioned at the same distance from the were housed individually in plastic cages allowing separation distal and proximal femur extremity, respectively, and with and collection of urine and faeces at 218C with relative humid- the same height. The region of interest between the two ity of 55 % and under a 12 h:12 h light:dark cycle. preliminary delimited metaphyseal zones corresponds to the The animals were fed a semipurified standard diet devoid of diaphyseal subregion. Results are given in g/cm2. British Journal ofany Nutrition soya proteins (Institut National de la Recherche Femoral mechanical testing. Immediately after collection Agronomique, Jouy en Josas, France). The control diet con- in NaCl (9 g/l), the length of the left femur and the mean tained 150 g casein/kg, 50 g rapeseed oil/kg, 16·8 g diameter of the diaphysis (i.e.
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