Eggs, Dietary Choline, and Nonalcoholic Fatty Liver Disease in the Framingham Heart Study

Abstract

Background: Eggs are rich in bioactive compounds, including choline and carotenoids that may benefit cardiometabolic outcomes. However, little is known about their relationship with nonalcoholic fatty liver disease (NAFLD).

Objectives: We investigated the association between intakes of eggs and selected egg-rich nutrients (choline, lutein, and zeaxanthin) and NAFLD risk and changes in liver fat over ∼6 y of follow-up in the Framingham Offspring and Third Generation cohorts.

Methods: On 2 separate occasions (2002-2005 and 2008-2011), liver fat was assessed using a computed tomography scan to estimate the average liver fat attenuation relative to a control phantom to create the liver phantom ratio (LPR). In 2008-2011, cases of incident NAFLD were identified as an LPR ≤0.33 in the absence of heavy alcohol use, after excluding prevalent NAFLD (LPR ≤0.33) in 2002-2005. Food frequency questionnaires were used to estimate egg intakes (classified as <1, 1, and ≥2 per week), dietary choline (adjusted for body weight using the residual method), and the combined intakes of lutein and zeaxanthin. Multivariable modified Poisson regression and general linear models were used to compute incident risk ratios (RR) of NAFLD and adjusted mean annualized liver fat change.

Results: NAFLD cumulative incidence was 19% among a total of 1414 participants. We observed no associations between egg intake or the combined intakes of lutein and zeaxanthin with an incident NAFLD risk or liver fat change. Other diet and cardiometabolic risk factors did not modify the association between egg intake and NAFLD risk. However, dietary choline intakes were inversely associated with NAFLD risk (RR for tertile 3 compared with tertile 1: 0.69, 95% CI: 0.51, 0.94).

Conclusions: Although egg intake was not directly associated with NAFLD risk, eggs are a major source of dietary choline, which was strongly inversely associated with NAFLD risk in this community-based cohort.

Keywords: dietary choline; eggs; liver fat; lutein; nonalcoholic fatty liver disease; zeaxanthin.

FIGURE 1

Flowchart of study participants for the analyses related to liver fat changes and incident NAFLD risk. Abbreviations: CT, computed tomography; FFQ, food frequency questionnaire; HTN, hypertension; T2DM/IFG, type 2 diabetes mellitus or impaired fasting glucose, and TEE, total energy expenditure. ∗These criteria were developed by FHS investigators.

FIGURE 2

Annualized liver fat changes (SE) associated with egg and egg-rich nutrients in females and males in a combined study sample of Offspring and Third Generation. A: Liver fat changes associated with egg intake. B: Liver fat changes associated with body weight-adjusted choline intakes. C: Liver fat changes associated with lutein and zeaxanthin intakes. Analyses for egg intakes were adjusted for age, sex (in all participants’ model only), TEE, education level, red meat intakes, baseline BMI, prevalent T2DM/IFG, HTN, and baseline LPR. Analyses for egg-rich nutrients were adjusted for age, sex (in all participants’ model only), education level, baseline waist-to-height ratio, and baseline LPR. The scale on the y-axis represents the amount of LPR decline (SE); e.g., 0.001 annualized liver fat increase indicates 0.001 unit decrease in LPR. Abbreviations: HTN, hypertension; LPR, liver phantom ratio; T2DM/IFG, type 2 diabetes or impaired fasting glucose, and TEE, total energy expenditure.

FIGURE 3

Independent and combined associations of egg intake categories with other risk or diet factors on incident NAFLD risk in a combined sample of Offspring and Third Generation cohorts. Each panel indicates a different risk factor as follows: (A) BMI; (B) elevated TG:HDL; (C) T2DM/IFG; (D) fiber intake; (E) dairy intake; and (F) red and processed meat intake. Analyses were adjusted for age, sex, TEE (except in the analyses for BMI), education level, red meat intakes (except in the analyses for red meat), baseline BMI (except in the analyses for BMI, lipids, and diabetes) and prevalent T2DM/IFG (except in the analyses for T2DM/IFG) and hypertension. Additive interaction was estimated through RERI for risk factors, and none reached statistical significance. Abbreviations: NAFLD, nonalcoholic fatty liver disease; RERI, relative excess risk due to interaction; T2DM/IFG, type 2 diabetes mellitus or impaired fasting glucose; TEE, total energy expenditure, and TG:HDL, triglyceride to high density lipoprotein ratio.

FIGURE 4

Independent and combined associations of body weight-adjusted choline intake categories with other risk or diet factors on incident NAFLD risk in a combined sample of Offspring and Third Generation cohorts. Each panel indicates a different risk factor as follows: (A) BMI, (B) physical activity, (C) fruit and vegetable intake, (D) fiber intake, and (E) legumes, nuts, and seeds intake. Analyses were adjusted for age, sex, and education level. Analyses for fruits and vegetables, fiber, and legumes, nuts and seeds were additionally adjusted for TEE. Moderate and vigorous physical activity was classified as low (Q1-Q2) and high (Q3-Q5) METs per hour. Additive interaction was estimated through RERI for risk factors, and none reached statistical significance. Abbreviations: MV, moderate to vigorous; METs, metabolic equivalents; NAFLD, nonalcoholic fatty liver disease; RERI, relative excess risk due to interaction; and TEE, total energy expenditure.