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Serum carbon and nitrogen stable isotopes as potential biomarkers of dietary intake and their relation with incident type 2 diabetes: the EPIC-Norfolk study.

Abstract

BACKGROUND

Stable-isotope ratios of carbon (¹³C/¹²C, expressed as δ¹³C) and nitrogen (¹⁵N/¹⁴N, or δ¹⁵N) have been proposed as potential nutritional biomarkers to distinguish between meat, fish, and plant-based foods.

OBJECTIVE

The objective was to investigate dietary correlates of δ¹³C and δ¹⁵N and examine the association of these biomarkers with incident type 2 diabetes in a prospective study.

DESIGN

Serum δ¹³C and δ¹⁵N (‰) were measured by using isotope ratio mass spectrometry in a case-cohort study (n = 476 diabetes cases; n = 718 subcohort) nested within the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk population-based cohort. We examined dietary (food-frequency questionnaire) correlates of δ¹³C and δ¹⁵N in the subcohort. HRs and 95% CIs were estimated by using Prentice-weighted Cox regression.

RESULTS

Mean (±SD) δ¹³C and δ¹⁵N were -22.8 ± 0.4‰ and 10.2 ± 0.4‰, respectively, and δ¹³C (r = 0.22) and δ¹⁵N (r = 0.20) were positively correlated (P < 0.001) with fish protein intake. Animal protein was not correlated with δ¹³C but was significantly correlated with δ¹⁵N (dairy protein: r = 0.11; meat protein: r = 0.09; terrestrial animal protein: r = 0.12, P ≤ 0.013). δ¹³C was inversely associated with diabetes in adjusted analyses (HR per tertile: 0.74; 95% CI: 0.65, 0.83; P-trend < 0.001], whereas δ¹⁵N was positively associated (HR: 1.23; 95% CI: 1.09, 1.38; P-trend = 0.001).

CONCLUSIONS

The isotope ratios δ¹³C and δ¹⁵N may both serve as potential biomarkers of fish protein intake, whereas only δ¹⁵N may reflect broader animal-source protein intake in a European population. The inverse association of δ¹³C but a positive association of δ¹⁵N with incident diabetes should be interpreted in the light of knowledge of dietary intake and may assist in identifying dietary components that are associated with health risks and benefits.

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    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    ,

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    From the MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, United Kingdom (PSP, AJMC, SB, NJW, and NGF); the Department of Archaeology & Anthropology, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO); the McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, United Kingdom (TCO and CKK); the University of Reading, Reading, United Kingdom (GGCK); and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom (AMM, RNL, K-TK, and GGCK).

    Source

    MeSH

    Adult
    Aged
    Biomarkers
    Carbon Isotopes
    Case-Control Studies
    Cohort Studies
    Diabetes Mellitus, Type 2
    Diet
    Dietary Proteins
    England
    Female
    Fish Proteins
    Follow-Up Studies
    Humans
    Incidence
    Male
    Middle Aged
    Nitrogen Isotopes
    Risk Factors
    Surveys and Questionnaires

    Pub Type(s)

    Journal Article
    Observational Study
    Research Support, Non-U.S. Gov't

    Language

    eng

    PubMed ID

    24990425

    Citation

    Patel, Pinal S., et al. "Serum Carbon and Nitrogen Stable Isotopes as Potential Biomarkers of Dietary Intake and Their Relation With Incident Type 2 Diabetes: the EPIC-Norfolk Study." The American Journal of Clinical Nutrition, vol. 100, no. 2, 2014, pp. 708-18.
    Patel PS, Cooper AJ, O'Connell TC, et al. Serum carbon and nitrogen stable isotopes as potential biomarkers of dietary intake and their relation with incident type 2 diabetes: the EPIC-Norfolk study. Am J Clin Nutr. 2014;100(2):708-18.
    Patel, P. S., Cooper, A. J., O'Connell, T. C., Kuhnle, G. G., Kneale, C. K., Mulligan, A. M., ... Forouhi, N. G. (2014). Serum carbon and nitrogen stable isotopes as potential biomarkers of dietary intake and their relation with incident type 2 diabetes: the EPIC-Norfolk study. The American Journal of Clinical Nutrition, 100(2), pp. 708-18. doi:10.3945/ajcn.113.068577.
    Patel PS, et al. Serum Carbon and Nitrogen Stable Isotopes as Potential Biomarkers of Dietary Intake and Their Relation With Incident Type 2 Diabetes: the EPIC-Norfolk Study. Am J Clin Nutr. 2014;100(2):708-18. PubMed PMID: 24990425.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Serum carbon and nitrogen stable isotopes as potential biomarkers of dietary intake and their relation with incident type 2 diabetes: the EPIC-Norfolk study. AU - Patel,Pinal S, AU - Cooper,Andrew J M, AU - O'Connell,Tamsin C, AU - Kuhnle,Gunter G C, AU - Kneale,Catherine K, AU - Mulligan,Angela M, AU - Luben,Robert N, AU - Brage,Soren, AU - Khaw,Kay-Tee, AU - Wareham,Nicholas J, AU - Forouhi,Nita G, Y1 - 2014/07/02/ PY - 2014/7/4/entrez PY - 2014/7/6/pubmed PY - 2015/4/22/medline SP - 708 EP - 18 JF - The American journal of clinical nutrition JO - Am. J. Clin. Nutr. VL - 100 IS - 2 N2 - BACKGROUND: Stable-isotope ratios of carbon (¹³C/¹²C, expressed as δ¹³C) and nitrogen (¹⁵N/¹⁴N, or δ¹⁵N) have been proposed as potential nutritional biomarkers to distinguish between meat, fish, and plant-based foods. OBJECTIVE: The objective was to investigate dietary correlates of δ¹³C and δ¹⁵N and examine the association of these biomarkers with incident type 2 diabetes in a prospective study. DESIGN: Serum δ¹³C and δ¹⁵N (‰) were measured by using isotope ratio mass spectrometry in a case-cohort study (n = 476 diabetes cases; n = 718 subcohort) nested within the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk population-based cohort. We examined dietary (food-frequency questionnaire) correlates of δ¹³C and δ¹⁵N in the subcohort. HRs and 95% CIs were estimated by using Prentice-weighted Cox regression. RESULTS: Mean (±SD) δ¹³C and δ¹⁵N were -22.8 ± 0.4‰ and 10.2 ± 0.4‰, respectively, and δ¹³C (r = 0.22) and δ¹⁵N (r = 0.20) were positively correlated (P < 0.001) with fish protein intake. Animal protein was not correlated with δ¹³C but was significantly correlated with δ¹⁵N (dairy protein: r = 0.11; meat protein: r = 0.09; terrestrial animal protein: r = 0.12, P ≤ 0.013). δ¹³C was inversely associated with diabetes in adjusted analyses (HR per tertile: 0.74; 95% CI: 0.65, 0.83; P-trend < 0.001], whereas δ¹⁵N was positively associated (HR: 1.23; 95% CI: 1.09, 1.38; P-trend = 0.001). CONCLUSIONS: The isotope ratios δ¹³C and δ¹⁵N may both serve as potential biomarkers of fish protein intake, whereas only δ¹⁵N may reflect broader animal-source protein intake in a European population. The inverse association of δ¹³C but a positive association of δ¹⁵N with incident diabetes should be interpreted in the light of knowledge of dietary intake and may assist in identifying dietary components that are associated with health risks and benefits. SN - 1938-3207 UR - https://www.unboundmedicine.com/medline/citation/24990425/Serum_carbon_and_nitrogen_stable_isotopes_as_potential_biomarkers_of_dietary_intake_and_their_relation_with_incident_type_2_diabetes:_the_EPIC_Norfolk_study_ L2 - https://academic.oup.com/ajcn/article-lookup/doi/10.3945/ajcn.113.068577 DB - PRIME DP - Unbound Medicine ER -