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Evaluation of alkylresorcinols in adipose tissue biopsies as a long-term biomarker of whole-grain wheat and rye intake in free-living Swedish men and women

  • Huaxing Wu (a1), Nor Adila Mhd Omar (a2), Niclas Håkansson (a2), Alicja Wolk (a2) (a3), Karl Michaëlsson (a3) and Rikard Landberg (a1) (a2) (a4)...
Abstract
Objective

Wheat and rye, the most consumed whole grains (WG) in the Nordic countries, contain alkylresorcinols (AR) in their bran. AR concentrations in human adipose tissue might reflect long-term WG rye and wheat intake. We aimed to evaluate AR concentrations in adipose tissue biopsies as a long-term biomarker of WG wheat and rye intake in free-living Swedish men and women.

Design

Cross-sectional study. AR concentrations in adipose tissue biopsies were analysed and compared with long-term WG intake assessed by three FFQ (repeated over a period of 14 years in men, 17 years in women) and with plasma AR concentrations.

Setting

The Cohort of Swedish Men between 1997 and 2010 and the Swedish Mammography Cohort between 1987 and 2003, Sweden.

Subjects

Men (n 149) and women (n 109).

Results

Long-term WG rye intake estimated with repeated FFQ correlated (r=0·31–0·41, P<0·01) with adipose-tissue AR concentrations, while WG wheat intake correlated only weakly (r=0·17–0·33, P<0·05). Total AR concentration in adipose tissue was 61 % lower in women than in men at similar energy-adjusted WG wheat and rye intakes, but plasma concentrations were similar. AR concentrations in adipose tissue correlated well with plasma concentrations (r=0·49–0·81, P<0·001).

Conclusions

AR in adipose tissue reflected long-term WG rye but not WG wheat intake, probably due to poor precision in estimating WG wheat intake by FFQ. AR in adipose tissue appears promising as a biomarker of long-term WG rye intake but should be adjusted for sex.

Copyright
Corresponding author
* Corresponding author: Email wuhuaxing@aliyun.com
References
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1. Aune, D, Keum, N, Giovannucci, E et al. (2016) Whole grain consumption and risk of cardiovascular disease, cancer, and all cause and cause specific mortality: systematic review and dose–response meta-analysis of prospective studies. BMJ 353, i2716.
2. Qi, L, van Dam, RM, Liu, S et al. (2006) Whole-grain, bran, and cereal fiber intakes and markers of systemic inflammation in diabetic women. Diabetes Care 29, 207211.
3. Kyrø, C, Skeie, G, Loft, S et al. (2013) Intake of whole grains from different cereal and food sources and incidence of colorectal cancer in the Scandinavian HELGA cohort. Cancer Causes Control 24, 13631374.
4. Kyrø, C, Skeie, G, Dragsted, LO et al. (2012) Intake of whole grain in Scandinavia: intake, sources and compliance with new national recommendations. Scand J Public Health 40, 7684.
5. Andersson, AAM, Andersson, R, Piironen, V et al. (2013) Contents of dietary fibre components and their relation to associated bioactive components in whole grain wheat samples from the HEALTHGRAIN diversity screen. Food Chem 136, 12431248.
6. Saastamoinen, M, Plaami, S & Kumpulainen, J (1989) Pentosan and β-glucan content of Finnish winter rye varieties as compared with rye of six other countries. J Cereal Sci 10, 199207.
7. Hansen, HB, Rasmussen, CV, Bach Knudsen, KE et al. (2003) Effects of genotype and harvest year on content and composition of dietary fibre in rye (Secale cereale L.) grain. J Sci Food Agric 83, 7685.
8. Nurmi, T, Nyström, L, Edelmann, M et al. (2008) Phytosterols in wheat genotypes in the HEALTHGRAIN Diversity Screen. J Agric Food Chem 56, 97109715.
9. Kristal, AR, Peters, U & Potter, JD (2005) Is it time to abandon the food frequency questionnaire? Cancer Epidemiol, Biomarkers Prev 14, 28262828.
10. Thompson, FE & Subar, AF (2008) Dietary assessment methodology. Nutr Prev Treat Dis 2, 339.
11. Kristensen, M, Toubro, S, Jensen, MG et al. (2012) Whole grain compared with refined wheat decreases the percentage of body fat following a 12-week, energy-restricted dietary intervention in postmenopausal women. J Nutr 142, 710716.
12. Ross, AB, Bruce, SJ, Blondel-Lubrano, A et al. (2011) A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects. Br J Nutr 105, 14921502.
13. Tłuścik, F (2015) Localization of the alkylresorcinols in rye and wheat caryopses. Acta Soc Bot Pol 47, 211218.
14. Kozubek, A & Tyman, JH (1999) Resorcinolic lipids, the natural non-isoprenoid phenolic amphiphiles and their biological activity. Chem Rev 99, 126.
15. Chen, Y, Ross, AB, Åman, P et al. (2004) Alkylresorcinols as markers of whole grain wheat and rye in cereal products. J Agric Food Chem 52, 82428246.
16. Linko, AM, Juntunen, KS, Mykkanen, HM et al. (2005) Whole-grain rye bread consumption by women correlates with plasma alkylresorcinols and increases their concentration compared with low-fiber wheat bread. J Nutr 135, 580583.
17. Kyrø, C, Olsen, A, Landberg, R et al. (2014) Plasma alkylresorcinols, biomarkers of whole-grain wheat and rye intake, and incidence of colorectal cancer. J Natl Cancer Inst 106, djt352.
18. Marklund, M, Magnusdottir, OK, Rosqvist, F et al. (2014) A dietary biomarker approach captures compliance and cardiometabolic effects of a healthy Nordic diet in individuals with metabolic syndrome. J Nutr 144, 16421649.
19. Landberg, R, Kamal-Eldin, A, Andersson, SO et al. (2009) Reproducibility of plasma alkylresorcinols during a 6-week rye intervention study in men with prostate cancer. J Nutr 139, 975980.
20. Ross, AB, Bourgeois, A, Macharia, HN et al. (2012) Plasma alkylresorcinols as a biomarker of whole-grain food consumption in a large population: results from the WHOLEheart Intervention Study. Am J Clin Nutr 95, 204211.
21. Linko-Parvinen, A-M, Landberg, R, Tikkanen, MJ et al. (2007) Alkylresorcinols from whole-grain wheat and rye are transported in human plasma lipoproteins. J Nutr 137, 11371142.
22. Magnusdottir, OK, Landberg, R, Gunnarsdottir, I et al. (2014) Plasma alkylresorcinols C17:0/C21:0 ratio, a biomarker of relative whole-grain rye intake, is associated to insulin sensitivity: a randomized study. Eur J Clin Nutr 68, 453458.
23. Aune, D, Norat, T, Romundstad, P et al. (2013) Whole grain and refined grain consumption and the risk of type 2 diabetes: a systematic review and dose–response meta-analysis of cohort studies. Eur J Epidemiol 28, 845858.
24. Wu, H, Kolehmainen, M, Mykkanen, H et al. (2015) Alkylresorcinols in adipose tissue biopsies as biomarkers of whole-grain intake: an exploratory study of responsiveness to advised intake over 12 weeks. Eur J Clin Nutr 69, 12441248.
25. Jansson, E, Landberg, R, Kamal-Eldin, A et al. (2010) Presence of alkylresorcinols, potential whole grain biomarkers, in human adipose tissue. Br J Nutr 104, 633636.
26. Harris, H, Håkansson, N, Olofsson, C et al. (2013) The Swedish mammography cohort and the cohort of Swedish men: study design and characteristics of two population-based longitudinal cohorts. OA Epidemiol 1, 16.
27. Wolk, A, Larsson, SC, Johansson, J et al. (2006) Long-term fatty fish consumption and renal cell carcinoma incidence in women. JAMA 296, 13711376.
28. Larsson, SC, Giovannucci, E & Wolk, A (2005) Diabetes and colorectal cancer incidence in the cohort of Swedish men. Diabetes Care 28, 18051807.
29. Terry, P, Giovannucci, E, Michels, KB et al. (2001) Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst 93, 525533.
30. Khani, BR, Ye, W, Terry, P et al. (2004) Reproducibility and validity of major dietary patterns among Swedish women assessed with a food-frequency questionnaire. J Nutr 134, 15411545.
31. Bergström, L, Kylberg, E, Hagman, U et al. (1991) The food composition database KOST: the National Administration’s information system for nutritive values of food. Vår Föda 43, 439447.
32. Wierzbicka, R, Wu, H, Franek, M et al. (2015) Determination of alkylresorcinols and their metabolites in biological samples by gas chromatography–mass spectrometry. J Chromatogr B 1000, 120129.
33. Hertzmark, E & Spiegelman, D (2010) The SAS ICC9 Macro. Cambridge, MA: Channing Laboratory, Harvard University.
34. Sandvik, P (2017) Rye bread in Sweden: health-related and sensory qualities, consumer perceptions and consumption patterns. PhD Thesis, Uppsala University.
35. Landberg, R, Townsend, MK, Neelakantan, N et al. (2012) Alkylresorcinol metabolite concentrations in spot urine samples correlated with whole grain and cereal fiber intake but showed low to modest reproducibility over one to three years in US women. J Nutr 142, 872877.
36. McKeown, NM, Marklund, M, Ma, J et al. (2016) Comparison of plasma alkylresorcinols (AR) and urinary AR metabolites as biomarkers of compliance in a short-term, whole-grain intervention study. Eur J Nutr 55, 12351244.
37. McKeown, NM, Hruby, A, Landberg, R et al. (2016) Plasma alkylresorcinols, biomarkers of whole-grain intake, are not associated with progression of coronary artery atherosclerosis in postmenopausal women with coronary artery disease. Public Health Nutr 19, 326331.
38. Nybacka, S, Lindroos, AK, Wirfält, E et al. (2016) Carotenoids and alkylresorcinols as objective biomarkers of diet quality when assessing the validity of a web-based food record tool and a food frequency questionnaire in a middle-aged population. BMC Nutr 2, 53.
39. Andersson, A, Marklund, M, Diana, M et al. (2011) Plasma alkylresorcinol concentrations correlate with whole grain wheat and rye intake and show moderate reproducibility over a 2- to 3-month period in free-living Swedish adults. J Nutr 141, 17121718.
40. Marklund, M, Landberg, R, Andersson, A et al. (2013) Alkylresorcinol metabolites in urine correlate with the intake of whole grains and cereal fibre in free-living Swedish adults. Br J Nutr 109, 129136.
41. Cuff, J, Sanders, T, Reidlinger, D et al. (2015) Urinary alkylresorcinol metabolites as a biomarker of dietary wholegrain intake and of compliance in a randomised dietary intervention trial: results from the CRESSIDA Study. Proc Nutr Soc 74, E42.
42. Kyrø, C, Olsen, A, Skeie, G et al. (2014) Plasma alkylresorcinol concentrations, biomarkers of whole-grain wheat and rye intake, in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Br J Nutr 111, 18811890.
43. Ross, AB, Pineau, N, Kochhar, S et al. (2009) Validation of a FFQ for estimating whole-grain cereal food intake. Br J Nutr 102, 15471551.
44. Landberg, R (2009) Alkylresorcinols as biomarkers of whole grain wheat and rye intake. PhD Thesis, Swedish University of Agricultural Sciences.
45. Landberg, R, Kamal-Eldin, A, Andersson, A et al. (2008) Alkylresorcinols as biomarkers of whole-grain wheat and rye intake: plasma concentration and intake estimated from dietary records. Am J Clin Nutr 87, 832838.
46. Sun, Q, Ma, J, Campos, H et al. (2007) Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am J Clin Nutr 86, 7481.
47. Landberg, R, Åman, P, Hallmans, G et al. (2013) Long-term reproducibility of plasma alkylresorcinols as biomarkers of whole-grain wheat and rye intake within Northern Sweden Health and Disease Study Cohort. Eur J Clin Nutr 67, 259263.
48. Mazahery, H & von Hurst, PR (2015) Factors affecting 25-hydroxyvitamin D concentration in response to vitamin D supplementation. Nutrients 7, 51115142.
49. Toth, MJ & Tchernof, A (2000) Lipid metabolism in the elderly. Eur J Clin Nutr 54, Suppl. 3, S121S125.
50. Montonen, J, Landberg, R, Kamal-Eldin, A et al. (2010) Reliability of fasting plasma alkylresorcinol concentrations measured 4 months apart. Eur J Clin Nutr 64, 698703.
51. Ross, AB, Chen, Y, Frank, J et al. (2004) Cereal alkylresorcinols elevate γ-tocopherol levels in rats and inhibit γ-tocopherol metabolism in vitro . J Nutr 134, 506510.
52. Frank, J, Lee, S, Leonard, SW et al. (2008) Sex differences in the inhibition of γ-tocopherol metabolism by a single dose of dietary sesame oil in healthy subjects. Am J Clin Nutr 87, 17231729.
53. Ley, CJ, Lees, B & Stevenson, JC (1992) Sex- and menopause-associated changes in body-fat distribution. Am J Clin Nutr 55, 950954.
54. Strawford, A, Antelo, F, Christiansen, M et al. (2004) Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am J Physiol Endocrinol Metab 286, E577E588.
55. Halliwell, KJ, Fielding, BA, Samra, JS et al. (1996) Release of individual fatty acids from human adipose tissue in vivo after an overnight fast. J Lipid Res 37, 18421848.
56. Menzel, C, Kamal-Eldin, A, Marklund, M et al. (2012) Alkylresorcinols in Swedish cereal food products. J Food Compost Anal 28, 119125.
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