Rye Bran Modified with Cell Wall–Degrading Enzymes Influences
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The Journal of Nutrition Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions Rye Bran Modified with Cell Wall–Degrading Enzymes Influences the Kinetics of Plant Lignans but Not of Enterolignans in Multicatheterized Pigs Anne K Bolvig,1 Natalja P Nørskov,1 Sophie van Vliet,1 Leslie Foldager,1,2 Mihai V Curtasu,1 Mette S Hedemann,1 Jens F Sørensen,3 Helle N Lærke,1 and Knud E Bach Knudsen1 Downloaded from https://academic.oup.com/jn/article/147/12/2220/4728058 by guest on 30 September 2021 1Department of Animal Science and 2Bioinformatics Research Centre, Faculty of Science and Technology, Aarhus University, Aarhus, Denmark; and 3DuPont Industrial Biosciences, Brabrand, Denmark Abstract Background: Whole-grain intake is associated with a lower risk of chronic Western-style diseases, possibly brought about by the high concentration of phytochemicals, among them plant lignans (PLs), in the grains. Objective: We studied whether treatment of rye bran with cell wall–degrading enzymes changed the solubility and kinetics of PLs in multicatheterized pigs. Methods: Ten female Duroc 3 Danish Landrace 3 Yorkshire pigs (60.3 6 2.3 kg at surgery) fitted with permanent catheters were included in an incomplete crossover study. The pigs were fed 2 experimental diets for 1–7 d. The diets were rich in PLs and based on nontreated lignan-rich [LR; lignan concentration: 20.2 mg dry matter (DM)/kg] or enzymatically treated lignan-rich (ENZLR; lignan concentration: 27.8 mg DM/kg) rye bran. Plasma concentrations of PLs and enterolignans were quantified with the use of targeted LC-tandem mass spectrometry. Data were log transformed and analyzed with mixed-effects, 1-compartment, and asymptotic regression models. Results: The availability of PLs was 38% greater in ENZLR than in LR, and the soluble fraction of PLs was 49% in ENZLR compared with 35% in LR diets. PLs appeared in the circulation 30 min after intake of both the ENZLR and LR diets. Postprandially, consumption of ENZLR resulted in a 4-times-greater (P < 0.0001) plasma PL concentration compared with LR. The area under the curve (AUC) measured 0–360 min after ENZLR intake was ;2 times higher than after LR intake. A 1-compartment model could describe the postprandial increase in plasma concentration after ENZLR intake, whereas an asymptotic regression model described the plasma concentrations after LR intake. Despite increased available and soluble PLs, ENZLR did not increase plasma enterolignans. Conclusion: The modification of rye bran with cell wall–degrading enzymes resulted in significantly greater plasma concentrations of PLs and the 4-h AUC, particularly syringaresinol, in multicatheterized pigs. JNutr2017;147:2220–7. Keywords: lignans, cell wall–degrading enzymes, kinetics, catheterized pigs, syringaresinol Introduction disease, and type 2 diabetes, is well established and has been The link between a high intake of whole grains and a lower risk documented in a number of epidemiological studies (1–3). One of chronic Western-style diseases, including cancer, heart of the active components that may play a role in the health- beneficial properties of whole grains and their consumption is Funding was provided by Innovation Fund Denmark (ELIN: 0603-00580B). the lignans. Lignans are diphenolic compounds found in high Author disclosures: AKB, NPN, SvV, LF, MVC, MSH, JFS, HNL, and KEBK, no conflicts of interest. concentrations in such common foods as seeds, grains, berries, Supplemental Tables 1–6 are available from the ‘‘Online Supporting Material’’ and vegetables (4–6). As concerns cereal grains, the concentra- link in the online posting of the article and from the same link in the online table of contents at http://jn.nutrition.org. tion of lignans is higher in rye than in wheat, oats, and barley (5), Address correspondence to AKB (e-mail: [email protected]). and the lignan content in grain is found mainly in the outer bran Abbreviations used: DM, dry matter; End, enterodiol; Enl, enterolactone; ENZLR, layer (pericarp or testa and aleurone) (7, 8). enzymatically treated lignan-rich diet; Hydr, 7-hydroxymatairesinol; I-Lari, iso-lariciresinol; Lari, lariciresinol; LR, lignan-rich diet; Mata, matairesinol; Med, medioresinol; Pino, pinoresinol; Commonly identified plant lignans (PLs) are matairesinol PL, plant lignan; PLOther, plant lignans other than Syr; PLTotal, total plant lignans; SDG, (Mata), pinoresinol (Pino), medioresinol (Med), lariciresinol (Lari), secoisolariciresinol diglycoside; Seco, secoisolariciresinol; Syr, syringaresinol; WO, washout. iso-lariciresinol (I-Lari), syringaresinol (Syr), secoisolariciresinol ã 2017 American Society for Nutrition. 2220 Manuscript received July 18, 2017. Initial review completed August 18, 2017. Revision accepted September 12, 2017. First published online October 4, 2017; doi: https://doi.org/10.3945/jn.117.258483. (Seco), and the glycosylated form of Seco, secoisolariciresinol The pigs were transferred to individual pens (1.25 3 3.75 m) without diglycoside (SDG). Absorption of PLs has not been well charac- bedding material but with elevated plastic grids, which allowed the pigs terized; however, recent studies in rats (9) and pigs (10), along to rest and remain dry. The pigs were acclimatized for 4 d before being with studies in humans, fed a lignan-rich (LR) diet or a single surgically fitted with permanent catheters in the portal and hepatic veins dose of SDG (11, 12) have shown rapid postprandial absorption and in the mesenteric artery. A flow probe was fitted around the portal vein (17), but because of technical problems, flow probe data were not of PLs and reported peak concentrations within 0–2.5 h from included in the present study. intake. The rapid absorption implies that part of the PLs is The pigs had a 7–9-d recovery period after the surgery, at which time absorbed from the small intestine to the circulation, which is the pigs entered the experimental period. Originally, the study was in contrast to the enterolignans [enterodiol (End) and enterolactone designed as a crossover study; however, because of the malfunctioning (Enl)], which are produced by the gut microbiota and are absorbed catheters, the crossover was not completed and the experiment was mainly from the large intestine (13). terminated on day 16. The pigs were fed the WO diet on days 1–4. This The lignans in cereals are concentrated to a large extent in the was followed by intake of one of the LR diets (LR or ENZLR) on days dietary fiber–rich outer bran fraction, which also contains a high 5–11. On days 12–15, the WO was fed again, and on the last day of the concentration of other phenolic compounds. Bioprocessing with experimental period (day 16), the pigs were fed the LR diet (LR or xylanases alone or in combination with arabinofuranosidase has ENZLR) that was not fed on days 5–11. Ten pigs completed the been shown to make a substantial part of the insoluble ferulic postprandial profile conducted on days 5 and 16 on each diet, whereas Downloaded from https://academic.oup.com/jn/article/147/12/2220/4728058 by guest on 30 September 2021 5 pigs/diet completed days 5–11 during which the samples collected acid available for absorption in the small intestine (14). Further- when the pigs were feed deprived were sampled. The experiment was more, enzymatic treatment with xylanases has resulted in the terminated after the postprandial profile was completed on day 16. enrichment of PLs in soluble rye bran extract (15). The effect of The pigs were offered water ad libitum and were allowed physical enzyme modification of the lignan source has not been investi- and visual contact through the railings of the pens. The pigs were gated in vivo, however, and its influence on the kinetic param- weighed 1 time/wk, and an iron supplement (400 mg; Uniferon, eters is unknown. Pharmacosmos) was administered intramuscularly weekly and addi- We hypothesized that the treatment of rye bran with cell tionally on profile days. wall–degrading enzymes would result in the increased solubili- Blood samples were collected (0 min) from the catheters of feed- zation of PLs, which would lead to an altered absorption kinetic. deprived pigs on days 5–16. On days 5 and 16, additional postprandial The aim of the present study was to investigate the absorption blood samples were collected at 30, 60, 120, 180, 240, 300, and 360 min relative to the morning meal. On days 12–15, a single sample was and elimination kinetics of PLs upon intake of an LR diet collected 360 min after the morning meal in addition to the 0-min sample modified with a cocktail of cell wall–degrading enzymes: xylanases, taken after feed deprivation for 12 h. After sampling was completed, the b -glucanases, and cellulases. The enzyme-modified rye bran or indwelling catheters were treated as described by Ingerslev et al. (16). nontreated rye bran was incorporated into a low-lignan wheat Blood samples were collected into sodium heparin Vacutainers (Becton- flour–based diet replacing refined wheat–concentrated fiber at an Dickinson), centrifuged at 2000 3 g for 10 min at 4°C, and plasma was iso-dietary fiber level. The effect of the enzyme treatment was stored at 280°C until analysis. Hematocrit levels were measured on days assessed in terms of absorption kinetic consequences for PLs and 5, 12, and 16. The pigs were killed with an overdose of sodium enterolignans in a catheterized pig model. pentobarbital followed by exsanguination (18). The animal experiment was conducted according to the protocols approved by the Danish Animal Experiments Inspectorate and complied with the guidelines of the Ministry of Food, Agriculture, and Fisheries concerning animal Methods experiments and the care of animals under study. Diets Analytical methods Three experimental diets were produced: a washout (WO) diet low in PLs Chemical analyses of the diets were performed in duplicate on freeze- based on white wheat flour supplemented with purified wheat fiber (Vitacel dried samples.