Urinary excretion of Citrus flavanones and their major catabolites after consumption of fresh oranges and pasteurized orange juice: A randomized cross-over study

Molecular Nutrition and Food Research

Volumn 60, Issue 12, 2016, Pages 2602-2610

  Aschoff, Julian K ^a   Riedl, Ken M ^b   Cooperstone, Jessica L ^b   Högel, Josef ^c   Bosy Westphal, Anja ^a   Schwartz, Steven J ^b   Carle, Reinhold ^a,d   Schweiggert, Ralf M ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ULM   (Germany)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Bioavailability; Flavonoids; Hesperetin; Metabolism; Naringenin

Indexed keywords

4-HYDROXYHIPPURIC ACID; FLAVANONE; FLAVANONE DERIVATIVE; HESPERETIN; HESPERIDIN; HIPPURIC ACID; HIPPURIC ACID DERIVATIVE; NARINGENIN;

ADULT; ANALYSIS; BIOAVAILABILITY; CHEMISTRY; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOSE RESPONSE; FOOD ANALYSIS; FRUIT; FRUIT AND VEGETABLE JUICE; HUMAN; PASTEURIZATION; RANDOMIZED CONTROLLED TRIAL; SWEET ORANGE; TANDEM MASS SPECTROMETRY; URINE; YOUNG ADULT;

ADULT; BIOLOGICAL AVAILABILITY; CITRUS SINENSIS; CROSS-OVER STUDIES; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; FOOD ANALYSIS; FRUIT; FRUIT AND VEGETABLE JUICES; HESPERIDIN; HIPPURATES; HUMANS; PASTEURIZATION; TANDEM MASS SPECTROMETRY; YOUNG ADULT;

EID: 84987677782     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201600315     Document Type: Article

References (40)

1. USDA, US Department of Agriculture, Foreign Agricultural Service. Citrus: World Markets and Trade. Available from: http://apps.fas.usda.gov/psdonline/circulars/citrus.pdf (accessed: March 2016).
2. USDA, US Department of Agriculture. Orange juice: production, supply and distribution in selected countries. Available from: http://apps.fas.usda.gov/psdonline/ (accessed: March 2016).
3. AIJN, Association of the Industry of Juices and Nectars from Fruits and Vegetables of the European Union. Market Report. Available from: http://www.aijn.org/files/default/aijn2015-report.pdf (accessed: March 2016).
4. Aschoff, J. K., Kaufmann, S., Kalkan, O., Neidhart, S. et al., In vitro bioaccessibility of carotenoids, flavonoids, and vitamin C from differently processed oranges and orange juices [Citrus sinensis (L.) Osbeck]. J. Agric. Food Chem. 2015, 63, 578–587.
5. Kawaii, S., Tomono, Y., Katase, E., Ogawa, K. et al., Quantitation of flavonoid constituents in Citrus fruits. J. Agric. Food Chem. 1999, 47, 3565–3571.
6. Aschoff, J. K., Rolke, C. L., Breusing, N., Bosy-Westphal, A. et al., Bioavailability of β-cryptoxanthin is greater from pasteurized orange juice than from fresh oranges: a randomized cross-over study. Mol. Nutr. Food Res. 2015, 59, 1896–1904.
7. Erlund, I., Review of the fLavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, bioavailability, and epidemiology. Nutr. Res. 2004, 24, 851–874.
8. Khan, M. K., Zill-E-Huma Dangles, O., A comprehensive review on flavanones, the major Citrus polyphenols. J. Food Comp. Anal. 2014, 33, 85–104.
9. Kumpulainen, J. T., Lehtonen, M., Mattila, P., in: Kumpulainen, J. T., Salonen, J. T. (Eds.), Natural Antioxidants in Nutrition, Health and Disease, The Royal Society of Chemistry, Cambridge 1999, pp. 141–150.
10. Chun, O. K., Chung, S. J., Song, W. O., Estimated dietary flavonoid intake and major food sources of U.S. adults. J. Nutr. 2007, 137, 1244–1252.
11. Cassidy, A., Rimm, E. B., O'Reilly, E. J., Logroscino, G. et al., Dietary flavonoids and risk of stroke in women. Stroke 2012, 43, 946–951.
12. Knekt, P., Kumpulainen, J., Järvinen, R., Rissanen, H. et al., Flavonoid intake and risk of chronic diseases. Am. J. Clin. Nutr. 2002, 76, 560–568.
13. Morand, C., Dubray, C., Milenkovic, D., Lioger, D. et al., Hesperidin contributes to the vascular protective effects of orange juice: a randomized crossover study in healthy volunteers. Am. J. Clin. Nutr. 2011, 93, 73–80.
14. Aptekmann, N. P., Cesar, T. B., Long-term orange juice consumption is associated with low LDL-cholesterol and apolipoprotein B in normal and moderately hypercholesterolemic subjects. Lipids Health Dis. 2013, 12, 119, 1–10.
15. Ghanim, H., Sia, C. L., Upadhyay, M., Korzeniewski, K. et al., Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression. Am. J. Clin. Nutr. 2010, 91, 940–949.
16. Vallejo, F., Larrosa, M., Escudero, E., Zafrilla, M. P. et al., Concentration and solubility of flavanones in orange beverages affect their bioavailability in humans. J. Agric. Food Chem. 2010, 58, 6516–6524.
17. Bredsdorff, L., Nielsen, Inge Lise F., Rasmussen, S. E., Cornett, C. et al., Absorption, conjugation and excretion of the flavanones, naringenin and hesperetin from alpha-rhamnosidase-treated orange juice in human subjects. Br. J. Nutr. 2010, 103, 1602–1609.
18. Actis-Goretta, L., Dew, T. P., Lévèques, A., Pereira-Caro, G. et al., Gastrointestinal absorption and metabolism of hesperetin-7-O-rutinoside and hesperetin-7-O-glucoside in healthy humans. Mol. Nutr. Food Res. 2015, 59, 1651–1662.
19. Selma, M. V., Espín, J. C., Tomás-Barberán, F. A., Interaction between phenolics and gut microbiota: role in human health. J. Agric. Food Chem. 2009, 57, 6485–6501.
20. Borges, G., Lean, Michael E. J., Roberts, S. A., Crozier, A., Bioavailability of dietary (poly)phenols: a study with ileostomists to discriminate between absorption in small and large intestine. Food Funct. 2013, 4, 754–762.
21. Nielsen, Inge Lise F., Chee, Winnie S. S., Poulsen, L., Offord-Cavin, E. et al., Bioavailability is improved by enzymatic modification of the Citrus flavonoid hesperidin in humans: a randomized, double-blind, crossover trial. J. Nutr. 2006, 136, 404–408.
22. Erlund, I., Meririnne, E., Alfthan, G., Aro, A., Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J. Nutr. 2001, 131, 235–241.
23. Brett, G. M., Hollands, W., Needs, P. W., Teucher, B. et al., Absorption, metabolism and excretion of flavanones from single portions of orange fruit and juice and effects of anthropometric variables and contraceptive pill use on flavanone excretion. Brit. J. Nutr. 2009, 101, 664–675.
24. Pereira-Caro, G., Borges, G., Ky, I., Ribas, A. et al., In vitro colonic catabolism of orange juice (poly)phenols. Mol. Nutr. Food Res. 2015, 59, 465–475.
25. Pereira-Caro, G., Borges, G., van der Hooft, Justin, Clifford, M. N. et al., Orange juice (poly)phenols are highly bioavailable in humans. Am. J. Clin. Nutr. 2014, 100, 1378–1384.
26. Clifford, M. N., Copeland, E. L., Bloxsidge, J. P., Mitchell, L. A., Hippuric acid as a major excretion product associated with black tea consumption. Xenobiotica 2000, 30, 317–326.
27. Barthe, G. A., Jourdan, P. S., McIntosh, C. A., Mansell, R. L., Radioimmunoassay for the quantitative determination of hesperidin and analysis of its distribution in Citrus sinensis. Phytochem. 1988, 27, 249–254.
28. Tripoli, E., La Guardia, M., Giammanco, S., Di Majo, D. et al., Citrus flavonoids: molecular structure, biological activity and nutritional properties: a review. Food Chem. 2007, 104, 466–479.
29. Kim, D.-H., Jung, E.-A., Sohng, I.-S., Han, J.-A. et al., Intestinal bacterial metabolism of flavonoids and its relation to some biological activities. Arch. Pharm. Res. 1998, 21, 17–23.
30. Roowi, S., Mullen, W., Edwards, C. A., Crozier, A., Yoghurt impacts on the excretion of phenolic acids derived from colonic breakdown of orange juice flavanones in humans. Mol. Nutr. Food Res. 2009, 53(Suppl 1), S68–S75.
31. Mullen, W., Archeveque, M.-A., Edwards, C. A., Matsumoto, H. et al., Bioavailability and metabolism of orange juice flavanones in humans: impact of a full-fat yogurt. J. Agric. Food Chem. 2008, 56, 11157–11164.
32. Kanaze, F. I., Bounartzi, M. I., Georgarakis, M., Niopas, I., Pharmacokinetics of the Citrus flavanone aglycones hesperetin and naringenin after single oral administration in human subjects. Eur. J. Clin. Nutr. 2007, 61, 472–477.
33. Majumdar, S., Srirangam, R., Solubility, stability, physicochemical characteristics and in vitro ocular tissue permeability of hesperidin: a natural bioflavonoid. Pharm. Res. 2009, 26, 1217–1225.
34. Merck Research Laboratories, The Merck Index, 14th Edition., Merck & Co., Whitehouse Station, NY 2001.
35. IFU, International Federation of Fruit Juice Producers. Method of Analysis no. 58 (1991), Paris, France 1991.
36. Hidalgo, M., Oruna-Concha, M. J., Kolida, S., Walton, G. E. et al., Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J. Agric. Food Chem. 2012, 60, 3882–3890.
37. Hidalgo, M., Martin-Santamaria, S., Recio, I., Sanchez-Moreno, C. et al., Potential anti-inflammatory, anti-adhesive, anti/estrogenic, and angiotensin-converting enzyme inhibitory activities of anthocyanins and their gut metabolites. Genes Nutr. 2012, 7, 295–306.
38. González-Sarrías, A., Núñez-Sánchez, M. Á., Tomé-Carneiro, J., Tomás-Barberán, F. A. et al., Comprehensive characterization of the effects of ellagic acid and urolithins on colorectal cancer and key associated molecular hallmarks: microRNA-cell specific induction of CDKN1A (p21) as a common mechanism involved. Mol. Nutr. Food Res. 2015, 60, 701–716.
39. Larrosa, M., Luceri, C., Vivoli, E., Pagliuca, C. et al., Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models. Mol. Nutr. Food Res. 2009, 53, 1044–1054.
40. Tomás-Navarro, M., Vallejo, F., Sentandreu, E., Navarro, J. L., Tomás-Barberán, F. A., Volunteer stratification is more relevant than technological treatment in orange juice flavanone bioavailability. J. Agric. Food Chem. 2014, 62, 24–27.