Meta-analysis investigating associations between healthy diet and fasting glucose and insulin levels and modification by loci associated with glucose homeostasis in data from 15 cohorts

Jennifer A. Nettleton, Marie France Hivert, Rozenn N. Lemaitre, Nicola M. McKeown, Dariush Mozaffarian, Toshiko Tanaka, Mary K. Wojczynski, Adela Hruby, Luc Djoussé, Julius S. Ngwa, Jack L. Follis, Maria Dimitriou, Andrea Ganna, Denise K. Houston, Stavroula Kanoni, Vera Mikkilä, Ani Manichaikul, Ioanna Ntalla, Frida Renström, Emily Sonestedt & 45 others Frank J A Van Rooij, Stefania Bandinelli, Lawrence De Koning, Ulrika Ericson, Neelam Hassanali, Jessica C. Kiefte-De Jong, Kurt K. Lohman, Olli Raitakari, Constantina Papoutsakis, Per Sjogren, Kathleen Stirrups, Erika Ax, Panos Deloukas, Christopher J. Groves, Paul F. Jacques, Ingegerd Johansson, Yongmei Liu, Mark I. McCarthy, Kari North, Jorma Viikari, M. Carola Zillikens, Josée Dupuis, Albert Hofman, Genovefa Kolovou, Kenneth Mukamal, Inga Prokopenko, Olov Rolandsson, Ilkka Seppälä, L. Adrienne Cupples, Frank B. Hu, Mika Kähönen, André G. Uitterlinden, Ingrid B. Borecki, Luigi Ferrucci, David R. Jacobs, Stephen B. Kritchevsky, Marju Orho-Melander, James S. Pankow, Terho Lehtimäki, Jacqueline C M Witteman, Erik Ingelsson, David S. Siscovick, George Dedoussis, James B. Meigs, Paul W. Franks

Research output: Contribution to journalArticle

Abstract

Whether loci that influence fasting glucose (FG) and fasting insulin (FI) levels, as identified by genome-wide association studies, modify associations of diet with FG or FI is unknown. We utilized data from 15 US and European cohort studies comprising 51,289 persons without diabetes to test whether genotype and diet interact to influence FG or FI concentration. We constructed a diet score using study-specific quartile rankings for intakes of whole grains, fish, fruits, vegetables, and nuts/seeds (favorable) and red/processed meats, sweets, sugared beverages, and fried potatoes (unfavorable). We used linear regression within studies, followed by inverse-variance-weighted meta-analysis, to quantify 1) associations of diet score with FG and FI levels and 2) interactions of diet score with 16 FG-associated loci and 2 FI-associated loci. Diet score (per unit increase) was inversely associated with FG (β =-0.004 mmol/L, 95% confidence interval:-0.005,-0.003) and FI (β =-0.008 ln-pmol/L, 95% confidence interval:-0.009,-0.007) levels after adjustment for demographic factors, lifestyle, and body mass index. Genotype variation at the studied loci did not modify these associations. Healthier diets were associated with lower FG and FI concentrations regardless of genotype at previously replicated FG-and FI-associated loci. Studies focusing on genomic regions that do not yield highly statistically significant associations from main-effect genome-wide association studies may be more fruitful in identifying diet-gene interactions.

Original languageEnglish (US)
Pages (from-to)103-115
Number of pages13
JournalAmerican Journal of Epidemiology
Volume177
Issue number2
DOIs
StatePublished - Jan 2013
Externally publishedYes

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Meta-Analysis
Fasting
Homeostasis
Insulin
Glucose
Diet
Healthy Diet
Genome-Wide Association Study
Genotype
Confidence Intervals
Nuts
Beverages
Solanum tuberosum
Vegetables
Life Style
Linear Models
Fruit
Seeds
Fishes
Body Mass Index

Keywords

  • diabetes
  • dietary pattern
  • gene-environment interaction
  • glucose
  • insulin

ASJC Scopus subject areas

  • Epidemiology

Cite this

Meta-analysis investigating associations between healthy diet and fasting glucose and insulin levels and modification by loci associated with glucose homeostasis in data from 15 cohorts. / Nettleton, Jennifer A.; Hivert, Marie France; Lemaitre, Rozenn N.; McKeown, Nicola M.; Mozaffarian, Dariush; Tanaka, Toshiko; Wojczynski, Mary K.; Hruby, Adela; Djoussé, Luc; Ngwa, Julius S.; Follis, Jack L.; Dimitriou, Maria; Ganna, Andrea; Houston, Denise K.; Kanoni, Stavroula; Mikkilä, Vera; Manichaikul, Ani; Ntalla, Ioanna; Renström, Frida; Sonestedt, Emily; Van Rooij, Frank J A; Bandinelli, Stefania; De Koning, Lawrence; Ericson, Ulrika; Hassanali, Neelam; Kiefte-De Jong, Jessica C.; Lohman, Kurt K.; Raitakari, Olli; Papoutsakis, Constantina; Sjogren, Per; Stirrups, Kathleen; Ax, Erika; Deloukas, Panos; Groves, Christopher J.; Jacques, Paul F.; Johansson, Ingegerd; Liu, Yongmei; McCarthy, Mark I.; North, Kari; Viikari, Jorma; Zillikens, M. Carola; Dupuis, Josée; Hofman, Albert; Kolovou, Genovefa; Mukamal, Kenneth; Prokopenko, Inga; Rolandsson, Olov; Seppälä, Ilkka; Cupples, L. Adrienne; Hu, Frank B.; Kähönen, Mika; Uitterlinden, André G.; Borecki, Ingrid B.; Ferrucci, Luigi; Jacobs, David R.; Kritchevsky, Stephen B.; Orho-Melander, Marju; Pankow, James S.; Lehtimäki, Terho; Witteman, Jacqueline C M; Ingelsson, Erik; Siscovick, David S.; Dedoussis, George; Meigs, James B.; Franks, Paul W.

In: American Journal of Epidemiology, Vol. 177, No. 2, 01.2013, p. 103-115.

Research output: Contribution to journalArticle

Nettleton, JA, Hivert, MF, Lemaitre, RN, McKeown, NM, Mozaffarian, D, Tanaka, T, Wojczynski, MK, Hruby, A, Djoussé, L, Ngwa, JS, Follis, JL, Dimitriou, M, Ganna, A, Houston, DK, Kanoni, S, Mikkilä, V, Manichaikul, A, Ntalla, I, Renström, F, Sonestedt, E, Van Rooij, FJA, Bandinelli, S, De Koning, L, Ericson, U, Hassanali, N, Kiefte-De Jong, JC, Lohman, KK, Raitakari, O, Papoutsakis, C, Sjogren, P, Stirrups, K, Ax, E, Deloukas, P, Groves, CJ, Jacques, PF, Johansson, I, Liu, Y, McCarthy, MI, North, K, Viikari, J, Zillikens, MC, Dupuis, J, Hofman, A, Kolovou, G, Mukamal, K, Prokopenko, I, Rolandsson, O, Seppälä, I, Cupples, LA, Hu, FB, Kähönen, M, Uitterlinden, AG, Borecki, IB, Ferrucci, L, Jacobs, DR, Kritchevsky, SB, Orho-Melander, M, Pankow, JS, Lehtimäki, T, Witteman, JCM, Ingelsson, E, Siscovick, DS, Dedoussis, G, Meigs, JB & Franks, PW 2013, 'Meta-analysis investigating associations between healthy diet and fasting glucose and insulin levels and modification by loci associated with glucose homeostasis in data from 15 cohorts', American Journal of Epidemiology, vol. 177, no. 2, pp. 103-115. https://doi.org/10.1093/aje/kws297
Nettleton, Jennifer A. ; Hivert, Marie France ; Lemaitre, Rozenn N. ; McKeown, Nicola M. ; Mozaffarian, Dariush ; Tanaka, Toshiko ; Wojczynski, Mary K. ; Hruby, Adela ; Djoussé, Luc ; Ngwa, Julius S. ; Follis, Jack L. ; Dimitriou, Maria ; Ganna, Andrea ; Houston, Denise K. ; Kanoni, Stavroula ; Mikkilä, Vera ; Manichaikul, Ani ; Ntalla, Ioanna ; Renström, Frida ; Sonestedt, Emily ; Van Rooij, Frank J A ; Bandinelli, Stefania ; De Koning, Lawrence ; Ericson, Ulrika ; Hassanali, Neelam ; Kiefte-De Jong, Jessica C. ; Lohman, Kurt K. ; Raitakari, Olli ; Papoutsakis, Constantina ; Sjogren, Per ; Stirrups, Kathleen ; Ax, Erika ; Deloukas, Panos ; Groves, Christopher J. ; Jacques, Paul F. ; Johansson, Ingegerd ; Liu, Yongmei ; McCarthy, Mark I. ; North, Kari ; Viikari, Jorma ; Zillikens, M. Carola ; Dupuis, Josée ; Hofman, Albert ; Kolovou, Genovefa ; Mukamal, Kenneth ; Prokopenko, Inga ; Rolandsson, Olov ; Seppälä, Ilkka ; Cupples, L. Adrienne ; Hu, Frank B. ; Kähönen, Mika ; Uitterlinden, André G. ; Borecki, Ingrid B. ; Ferrucci, Luigi ; Jacobs, David R. ; Kritchevsky, Stephen B. ; Orho-Melander, Marju ; Pankow, James S. ; Lehtimäki, Terho ; Witteman, Jacqueline C M ; Ingelsson, Erik ; Siscovick, David S. ; Dedoussis, George ; Meigs, James B. ; Franks, Paul W. / Meta-analysis investigating associations between healthy diet and fasting glucose and insulin levels and modification by loci associated with glucose homeostasis in data from 15 cohorts. In: American Journal of Epidemiology. 2013 ; Vol. 177, No. 2. pp. 103-115.
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abstract = "Whether loci that influence fasting glucose (FG) and fasting insulin (FI) levels, as identified by genome-wide association studies, modify associations of diet with FG or FI is unknown. We utilized data from 15 US and European cohort studies comprising 51,289 persons without diabetes to test whether genotype and diet interact to influence FG or FI concentration. We constructed a diet score using study-specific quartile rankings for intakes of whole grains, fish, fruits, vegetables, and nuts/seeds (favorable) and red/processed meats, sweets, sugared beverages, and fried potatoes (unfavorable). We used linear regression within studies, followed by inverse-variance-weighted meta-analysis, to quantify 1) associations of diet score with FG and FI levels and 2) interactions of diet score with 16 FG-associated loci and 2 FI-associated loci. Diet score (per unit increase) was inversely associated with FG (β =-0.004 mmol/L, 95{\%} confidence interval:-0.005,-0.003) and FI (β =-0.008 ln-pmol/L, 95{\%} confidence interval:-0.009,-0.007) levels after adjustment for demographic factors, lifestyle, and body mass index. Genotype variation at the studied loci did not modify these associations. Healthier diets were associated with lower FG and FI concentrations regardless of genotype at previously replicated FG-and FI-associated loci. Studies focusing on genomic regions that do not yield highly statistically significant associations from main-effect genome-wide association studies may be more fruitful in identifying diet-gene interactions.",
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AU - Hivert, Marie France

AU - Lemaitre, Rozenn N.

AU - McKeown, Nicola M.

AU - Mozaffarian, Dariush

AU - Tanaka, Toshiko

AU - Wojczynski, Mary K.

AU - Hruby, Adela

AU - Djoussé, Luc

AU - Ngwa, Julius S.

AU - Follis, Jack L.

AU - Dimitriou, Maria

AU - Ganna, Andrea

AU - Houston, Denise K.

AU - Kanoni, Stavroula

AU - Mikkilä, Vera

AU - Manichaikul, Ani

AU - Ntalla, Ioanna

AU - Renström, Frida

AU - Sonestedt, Emily

AU - Van Rooij, Frank J A

AU - Bandinelli, Stefania

AU - De Koning, Lawrence

AU - Ericson, Ulrika

AU - Hassanali, Neelam

AU - Kiefte-De Jong, Jessica C.

AU - Lohman, Kurt K.

AU - Raitakari, Olli

AU - Papoutsakis, Constantina

AU - Sjogren, Per

AU - Stirrups, Kathleen

AU - Ax, Erika

AU - Deloukas, Panos

AU - Groves, Christopher J.

AU - Jacques, Paul F.

AU - Johansson, Ingegerd

AU - Liu, Yongmei

AU - McCarthy, Mark I.

AU - North, Kari

AU - Viikari, Jorma

AU - Zillikens, M. Carola

AU - Dupuis, Josée

AU - Hofman, Albert

AU - Kolovou, Genovefa

AU - Mukamal, Kenneth

AU - Prokopenko, Inga

AU - Rolandsson, Olov

AU - Seppälä, Ilkka

AU - Cupples, L. Adrienne

AU - Hu, Frank B.

AU - Kähönen, Mika

AU - Uitterlinden, André G.

AU - Borecki, Ingrid B.

AU - Ferrucci, Luigi

AU - Jacobs, David R.

AU - Kritchevsky, Stephen B.

AU - Orho-Melander, Marju

AU - Pankow, James S.

AU - Lehtimäki, Terho

AU - Witteman, Jacqueline C M

AU - Ingelsson, Erik

AU - Siscovick, David S.

AU - Dedoussis, George

AU - Meigs, James B.

AU - Franks, Paul W.

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N2 - Whether loci that influence fasting glucose (FG) and fasting insulin (FI) levels, as identified by genome-wide association studies, modify associations of diet with FG or FI is unknown. We utilized data from 15 US and European cohort studies comprising 51,289 persons without diabetes to test whether genotype and diet interact to influence FG or FI concentration. We constructed a diet score using study-specific quartile rankings for intakes of whole grains, fish, fruits, vegetables, and nuts/seeds (favorable) and red/processed meats, sweets, sugared beverages, and fried potatoes (unfavorable). We used linear regression within studies, followed by inverse-variance-weighted meta-analysis, to quantify 1) associations of diet score with FG and FI levels and 2) interactions of diet score with 16 FG-associated loci and 2 FI-associated loci. Diet score (per unit increase) was inversely associated with FG (β =-0.004 mmol/L, 95% confidence interval:-0.005,-0.003) and FI (β =-0.008 ln-pmol/L, 95% confidence interval:-0.009,-0.007) levels after adjustment for demographic factors, lifestyle, and body mass index. Genotype variation at the studied loci did not modify these associations. Healthier diets were associated with lower FG and FI concentrations regardless of genotype at previously replicated FG-and FI-associated loci. Studies focusing on genomic regions that do not yield highly statistically significant associations from main-effect genome-wide association studies may be more fruitful in identifying diet-gene interactions.

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KW - gene-environment interaction

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KW - insulin

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