 |
|
Legume Consumption and Risk of Coronary Heart Disease in US Men and Women
NHANES I Epidemiologic Follow-up Study
Lydia A. Bazzano, PhD;
Jiang He, MD, PhD;
Lorraine G. Ogden, MS;
Catherine Loria, PhD, MS;
Suma Vupputuri, PhD, MPH;
Leann Myers, PhD;
Paul K. Whelton, MD, MSc
Arch Intern Med. 2001;161:2573-2578.
ABSTRACT
| |
Background Soybean protein and dietary fiber supplementation reduce serum cholesterol
in randomized controlled trials. Consumption of legumes, which are high in
bean protein and water-soluble fiber, may be associated with a reduced risk
of coronary heart disease (CHD).
Methods A total of 9632 men and women who participated in the First National
Health and Nutrition Examination Survey Epidemiologic Follow-up Study (NHEFS)
and were free of cardiovascular disease (CVD) at their baseline examination
were included in this prospective cohort study. Frequency of legume intake
was estimated using a 3-month food frequency questionnaire, and incidence
of CHD and CVD was obtained from medical records and death certificates.
Results Over an average of 19 years of follow-up, 1802 incident cases of CHD
and 3680 incident cases of CVD were documented. Legume consumption was significantly
and inversely associated with risk of CHD (P = .002
for trend) and CVD (P = .02 for trend) after adjustment
for established CVD risk factors. Legume consumption 4 times or more per week
compared with less than once a week was associated with a 22% lower risk of
CHD (relative risk, 0.78; 95% confidence interval, 0.68-0.90) and an 11% lower
risk of CVD (relative risk, 0.89; 95% confidence interval, 0.80-0.98).
Conclusions Our study indicates a significant inverse relationship between legume
intake and risk of CHD and suggests that increasing legume intake may be an
important part of a dietary approach to the primary prevention of CHD in the
general population.
INTRODUCTION
EACH YEAR, approximately 1.1 million Americans are expected to have
a new or recurrent coronary heart disease (CHD) event.1
Even with great improvements in the treatment of CHD in recent years, the
likelihood of disability or death following CHD events remains high. For instance,
25% of men and 38% of women will die within 1 year following a recognized
myocardial infarction, and 22% of men and 46% of women will be disabled with
heart failure within 6 years of a recognized myocardial infarction.1 Therefore, primary prevention should be a major element
of public health strategies aimed at reducing societal burden due to CHD-related
morbidity and mortality in the United States and worldwide.
Consumption of legumes, which are high in bean protein and water-soluble
fiber, may reduce the risk of CHD. Soluble fiber has been shown to reduce
total and low-density lipoprotein cholesterol levels as well as insulin resistance.2 In addition, legumes are generally low in sodium and
rich in minerals such as potassium, calcium, and magnesium.3
Low dietary intake of sodium and high dietary intake of potassium, calcium,
and magnesium have been associated with a reduced risk of cardiovascular disease
(CVD) in epidemiologic studies.4-6
Additionally, randomized clinical trials have shown that substituting protein
from vegetable sources, specifically soybean, for protein from animal sources
reduces serum cholesterol levels.7
However, most studies of the relationship between diet and CVD, like
those mentioned above, have focused on nutrients rather than examining food
items or dietary patterns. Because men and women manipulate their diet through
food choices, it may be more instructive to examine relationships between
food intake and disease. Nutritional recommendations are easier to understand
and follow when phrased in terms of the consumption of foods rather than nutrients.
Moreover, food items are biochemically complex and may not be adequately represented
by their content of a single nutrient. We took advantage of the large sample
size and extended follow-up experience of participants in the First National
Health and Nutrition Examination Survey (NHANES I) Epidemiologic Follow-up
Study (NHEFS) to examine the association between legume consumption and risk
of subsequent CHD.
METHODS
STUDY POPULATION
The NHANES I used a multistage, stratified probability sampling design
to select a representative sample of the US civilian noninstitutionalized
population aged 1 to 74 years.8-9
Certain population subgroups, including those with a low income, women of
childbearing age (25-44 years), and elderly persons (65 years or older) were
oversampled. The NHEFS is a prospective cohort study of NHANES I participants
who were 25 to 74 years old when the survey was conducted between 1971 and
1975. Of the 14 407 persons in this age range at baseline, we excluded
(1) 1347 who had a self-reported history of heart attack, heart failure, or
stroke at baseline or had used medication for heart disease during the preceding
6 months, (2) 2853 NHANES I Augmentation Survey participants for whom the
study protocol did not include a dietary assessment, and (3) 189 who lacked
legume intake information. Among the remaining participants, 386 (3.9%) were
lost to follow-up, leaving a total of 9632 participants who contributed 159 599
person-years to this analysis.
MEASUREMENT
Baseline data collection included a dietary assessment, standardized
medical examination, anthropometric measurements, medical history, and laboratory
tests.8-9 The dietary assessment
included a 3-month food frequency questionnaire on participants' usual consumption
of food groups in 13 major categories including legume intake. The primary
item used in this investigation asked participants how often "dry beans and
peas like pinto beans, red beans, black-eye [sic]
peas, peanuts and peanut butter" were usually consumed in the past 3 months
excluding periods of illness or dieting.10
Information on portion size was not collected. In addition to the food frequency
questionnaire, a single 24-hour dietary recall was conducted by trained NHANES
I personnel using a standardized protocol and 51 three-dimensional models
to estimate portion size. Trained personnel coded the dietary recall questionnaires
using nutrient information from the Department of Agriculture Handbook No.
8 or other resources. Saturated fat and total energy intake was calculated
for each participant by the National Center for Health Statistics. Blood pressure,
body weight, and height were obtained using standard protocols.8
Frozen serum samples were sent to the Centers for Disease Control and Prevention
for measurement of serum total cholesterol levels.
The baseline questionnaire on medical history included questions about
selected health conditions and medications used for these conditions during
the preceding 6 months. Data on education, physical activity, and alcohol
consumption were obtained by means of interviewer-administered questionnaires.
Baseline information on smoking status was obtained for 6913 participants
who underwent a more detailed baseline examination.8-9
For the remaining study participants, information on smoking status at baseline
was derived from responses to questions on lifetime smoking history obtained
at their follow-up interviews from 1982 to 1984 or later.11-12
The validity of information obtained using this approach has been documented.13-14
FOLLOW-UP PROCEDURES
Follow-up data were collected between 1982 and 1984 and in 1986, 1987,
and 1992.11-12,15-16
Each follow-up examination included tracking a participant or his/her proxy
to a current address; performing an in-depth interview; obtaining hospital
and nursing home records, including pathology reports and electrocardiograms;
and, for decedents, acquiring a death certificate. Incident CVD was based
on documentation of an event that met prespecified study criteria and occurred
during the period between the participant's baseline examination and last
follow-up interview. Validity of study outcome data has been documented.17
Incident CHD was based on a death certificate report in which the underlying
cause of death was coded as an International Classification
of Diseases, Ninth Revision (ICD-9) code of
410 to 414, or by 1 or more hospital and/or nursing home stays in which the
participant had a discharge diagnosis with these codes. Incident CVD was based
on a death certificate report in which the underlying cause of death was recorded
using an ICD-9 code of 390 to 459, or 1 or more hospital
and/or nursing home stays in which the participant had a discharge diagnosis
with these codes. The date of record for incident events was identified by
the date of first hospital admission with an established study event or date
of death from a study event in the absence of hospital or nursing home documentation
of such an event.
STATISTICAL ANALYSIS
Based on the distribution of participants' responses, legume intake
was grouped into the following 4 categories: intake less than once a week,
once a week, 2 to 3 times a week, and at least 4 times a week. For each baseline
characteristic, the mean value or corresponding percentage of study participants
was calculated by category of legume intake. The statistical significance
of differences was examined by analysis of variance (continuous variables)
and by the  2 test (categorical variables). The cumulative
incidence of CVD by category of legume intake was calculated using the Kaplan-Meier
method,18 and differences in the cumulative
rates were examined using the log-rank test for trend.19
Cox proportional hazard models were used to explore the relationship between
categories of legume intake and risk of CVD.20
Age was used as the time scale in all time-to-event analyses.21
Cox proportional hazard models were stratified by birth cohort using 10-year
intervals to control for calendar period and cohort effects.21
Methods to estimate variance that take into account sample clustering and
stratification of the NHANES I sample were used in the Cox proportional hazards
models.21 Data from the small number of participants
who had reached 85 years of age were censored.
RESULTS
Baseline characteristics of the study participants are given by category
of legume intake in Table 1. Compared
with those with a lower intake, participants with a higher intake of legumes
tended to be younger and male. Persons with more frequent legume intake had,
on average, a lower systolic blood pressure, less hypertension, lower levels
of total cholesterol and hypercholesterolemia, less diabetes, and a lower
body mass index (BMI) than their counterparts who consumed legumes less often.
In addition, participants with more frequent legume intake tended to be more
physically active, more likely to smoke, and less likely to have completed
high school. They also tended to consume more saturated fat and to have a
higher total energy intake. The average amount of legumes consumed in 24 hours
increased with frequency of legume intake from the 3-month food questionnaire.
The average serving size of legumes consumed in this cohort calculated from
the 24-hour dietary recall was 98.6 g with an SD of 97.6 g.
|
|
|
|
Table 1. Baseline Characteristics of 9632 NHEFS Participants According
to Frequency of Legume Intake*
|
|
|
Over the course of 159 599 person-years of follow-up between 1971
and 1992, 1802 CHD events and 3680 CVD events were documented. Relative risks
(RRs) and corresponding 95% confidence intervals (CIs) for CHD and CVD by
category of legume intake are given in Table 2. In age-, sex-, race-, and energy-adjusted analyses, risk
of CHD was significantly and inversely related to frequency of legume consumption
at baseline (P = .02 for trend). After additional
adjustment for history of diabetes, recreational physical activity, level
of education, regular alcohol consumption, and current cigarette smoking,
frequency of legume consumption at baseline was again significantly and inversely
related to risk of CHD (P = .002 for trend). In the
latter model, those with an intake of legumes at least 4 times a week had
a 22% lower risk of CHD (RR, 0.78; 95% CI, 0.68-0.90) compared with their
counterparts consuming legumes less than once a week. Further adjustment for
systolic blood pressure, total serum cholesterol, BMI, frequency of meat and
poultry consumption, frequency of fruit and vegetable consumption, and saturated
fat intake did not materially alter the risk estimates. For instance, those
consuming legumes at least 4 times a week had a 20% lower risk of CHD (RR,
0.80; 95% CI, 0.69-0.91) compared with those consuming legumes less than once
a week. Risk of CVD was inversely related to participants' frequency of legume
consumption with borderline significance (P = .07
for trend) in models adjusted for age, sex, race, and energy intake. After
additional adjustment for history of diabetes, recreational physical activity,
level of education, regular alcohol consumption, and current cigarette smoking,
risk of CVD was significantly and inversely related to legume consumption
at baseline (P = .02 for trend). Intake of legumes
at least 4 times per week was associated with an 11% lower risk of CVD events
compared with intake of legumes less than once a week (RR, 0.89; 95% CI, 0.80-0.98).
Further adjustment for systolic blood pressure, serum cholesterol, BMI, frequency
of meat and poultry consumption, frequency of fruit and vegetable consumption,
and saturated fat intake produced little change in risk estimates but was
associated with borderline statistical significance (P
= .06 for trend).
|
|
|
|
Table 2. Relative Risk of Coronary Heart Disease and Cardiovascular
Disease According to Frequency of Legume Intake in 9632 NHEFS Participants*
|
|
|
Relative risks and 95% CIs for the comparison of legume intake at least
4 times a week to less than once a week by selected subgroups are given in Table 3. Relative risks for CHD and CVD
were lower among persons consuming legumes at least 4 times a week than for
their counterparts consuming legumes less than once a week across subgroups
based on sex, recreational physical activity, smoking status, vitamin use,
hypertension status, serum cholesterol levels, and BMI.
|
|
|
|
Table 3. Relative Risk for Coronary Heart Disease and Cardiovascular
Disease in NHEFS Participants Who Consumed Legumes 4 or More Times vs Less
Than Once a Week
|
|
|
However, estimates of risk differed significantly by category of age
at entry. When participants were stratified by age at entry into 2 groups
(60 years or older at the baseline examination and younger than 60 years at
baseline) significant associations were detected in the older group but not
in the younger group. For instance, in the older group, those with an intake
of legumes at least 4 times a week had a 38% lower risk of CHD (RR, 0.62;
95% CI, 0.50-0.77) and a 27% lower risk of CVD (RR, 0.73; 95% CI, 0.62-0.87)
compared with those whose intake of legumes was less than once a week. However,
after adjustment for time from dietary measurement to event, effect modification
was no longer statistically significant for either CHD or CVD (P>.05), while estimates of risk associated with legume consumption
categories were not considerably changed.
COMMENT
Our study found a strong and independent inverse association between
dietary intake of legumes and risk of CHD in a representative sample of the
noninstitutionalized adult US population. These findings have important clinical
and public health implications. Coronary heart disease is the single largest
killer of men and women in the United States, and although improved, the CHD
case-fatality rate is still high.1 In addition,
CHD is one of the leading causes of premature, permanent disability in the
US population, accounting for 19% of disability allowances by the Social Security
Administration.1 Moreover, Medicare beneficiaries
were paid $10.5 billion in 1996 for CHD events and, per discharge, amounts
ranged from $3843 to $11 130.1 Because
of the high mortality from CHD, high prevalence of disability due to CHD,
and substantial financial burden to individual patients and for society, the
primary prevention of CHD is an essential element of any attempt to tackle
the problem of CVD in the United States. Our findings suggest that increasing
legume intake may be an important part of dietary interventions to reduce
heart disease.
To our knowledge, this is the first study examining the relationship
between legume intake as foods and the development of CVD. Most studies of
legume intake have focused on specific nutritional components of legumes,
such as protein, fiber, and phytochemicals,2, 22-23
or have not used clinical events as end points. However, it may be more instructive
and useful to investigate of the relationship between dietary patterns or
specific food intakes and risk of CHD events because the results of such studies
may have more direct public health implications. In addition, studies focusing
on nutrient intake may fail to consider the biochemical complexity and possibility
of nutrient interactions in food items.
The present study was conducted in a representative sample of the adult
noninstitutionalized US population, so our findings are highly generalizable.
Additional strengths include the assessment of incidence of CVD over an average
of 19 years of follow-up, with experience available for more than 96% of the
study participants. Moreover, because legume intake was measured at baseline,
temporal relationships can be established with confidence. Further, the use
of a food frequency method allowed for the assessment of usual legume intake
during the baseline examination.
Limitations of the study include a lack of portion size information
for legume intake. We were not able to estimate the RR of CVD associated with
servings of legumes per day using data derived from the food frequency questionnaire.
However, several studies have shown that portion size estimation using food
frequency methods may not be accurate24-27
and may introduce measurement error.28 Average
portion size was estimated using data from the 24-hour dietary recall.
Additionally, changes in legume intake during follow-up were not measured.
This might have contributed to misclassification of legume intake because
dietary practices may have changed during the 19-year follow-up period.29-30 Consequently, the interaction observed
here between legume intake and age may be due to greater measurement error
in legume intake for persons whose age at entry to the study was younger than
60 years. While the median time from baseline dietary assessment to CVD events
was 7.6 years in participants 60 years or older at baseline, the median time
to events was 10.3 years in participants younger than 60 years at baseline.
Moreover, in models adjusted for time from dietary measurement to event, age
interactions were not statistically significant.
Given the above information, it is likely that changes in dietary pattern
over the course of prolonged follow-up reduced our ability to assess the relationship
between legume intake and CVD in younger participants. Therefore, the apparent
age group interaction should be interpreted with caution.
It is possible that persons with a more frequent intake of legumes may
have other dietary and nondietary habits that promote health, such as not
smoking, regular exercise, and a low dietary intake of cholesterol and saturated
fat. However, in our study population, persons consuming legumes more frequently
were also more likely to smoke and consumed higher levels of saturated fat
than their counterparts with a less frequent intake of legumes, while vitamin
use was not significantly different across categories of legume consumption.
Additionally, the estimates of risk in this study were adjusted for
important potential confounders of CVD, such as age, sex, race, recreational
physical activity, education level, cigarette smoking status, diabetic status,
regular alcohol consumption, and total energy intake. Further adjustment for
dietary factors (such as frequency of intake of meat, frequency of intake
of fruits and vegetables, and intake of saturated fat) and biological factors
(such as serum cholesterol level, BMI, and systolic blood pressure) resulted
in minimal change in risk estimates and linear trends. The inverse association
between legume intake and risk of CHD and CVD was consistent across strata
of vitamin use and level of recreational activity, both markers of a healthy
lifestyle. These findings suggest that legume intake may be related to a lower
risk of CHD and CVD, independent of other health habits.
Many constituents of legumes could contribute to the potential protective
effect of legume intake on CVD. For instance, soybean protein has been shown
to reduce serum total and low-density lipoprotein cholesterol levels in a
meta-analysis of 29 clinical trials.7 Soybean
protein intake averaged 47 g/d across the studies. In 19 of the 29 studies,
intakes of energy, total fat, saturated fat, and cholesterol were similar
between the control and soybean-containing diets. In a pooled analysis of
the results from all 29 trials, soybean protein administration was associated
with a reduction in serum total cholesterol concentrations (a decrease of
23.2 mg/dL [0.60 mmol/L]; 95% CI, 13.5-32.9 mg/dL [0.35-0.85 mmol/L]), and
a net reduction in serum low-density lipoprotein cholesterol of 21.7 mg/dL
(0.56 mmol/L) (95% CI, 11.2-31.7 mg/dL [0.29-0.82 mmol/L]).
In addition, soybean protein diets significantly decreased serum triglyceride
concentrations by 13.3 mg/dL (0.15 mmol/L) (95% CI, 0.3-25.7 mg/dL [0.003-0.29
mmol/L]). While soybean protein did not significantly affect serum high-density
lipoprotein cholesterol levels, a net increase of 1.2 mg/dL (0.03 mmol/L)
was seen across the 29 trials. Legume intake other than soybean has also been
associated with a reduction in serum cholesterol in clinical studies, possibly
due to the high soluble fiber content of legumes.31-34
A half cup of cooked beans contains an average of 6 g of total fiber and 2
g of soluble fiber, which is more total fiber than the same amount of soluble
fiber as s contained in one-third cup of dry oat bran.31
Soluble fiber has been associated with reduced cholesterol levels and risk
of CHD as well as better glycemic control.3, 23, 31, 35
Furthermore, legumes are a major source of dietary folate.36
Both folate and vitamin B12 are important for the metabolism of
homocysteine, and dietary intake of folate has been inversely associated with
plasma homocysteine levels.37 Elevated levels
of plasma homocysteine have been related to an increased risk of CHD.38-39 In addition, serum folate levels
have been inversely associated with mortality from CHD and CVD.40-41
In conclusion, our study found a strong inverse relationship between
legume intake and risk of CHD. Future specifically designed prospective studies
with detailed measurements of legume intake at baseline and during follow-up
will provide more definitive information on this association. However, based
on our current knowledge and national and international recommendations to
increase fruit and vegetable intake, increasing legume consumption may be
an important part of dietary interventions to reduce the risk of CHD. Additionally,
increasing legume consumption may be a novel approach to culturally tailor
dietary interventions aimed at reducing CHD.
AUTHOR INFORMATION
Accepted for publication April 10, 2001.
This study was supported by grant R03 HL61954 (Dr He) and in part by
grant R01HL60300 from the National Heart, Lung, and Blood Institute.
The NHEFS has been developed and funded by the National Center for Health
Statistics, Hyattsville, Md; the National Institute on Aging, National Cancer
Institute, National Institute of Child Health and Human Development, National
Heart, Lung, and Blood Institute, National Institute of Mental Health, National
Institute of Diabetes and Digestive and Kidney Diseases, National Institute
of Arthritis and Musculoskeletal and Skin Diseases, National Institute of
Allergy and Infectious Diseases, and the National Institute of Neurological
and Communicative Disorders and Stroke, Bethesda, Md; the Centers for Disease
Control and Prevention, Atlanta, Ga; and the US Department of Agriculture,
Washington, DC.
Corresponding author and reprints: Jiang He, MD, PhD, Department
of Epidemiology, Tulane University School of Public Health and Tropical Medicine,
1430 Tulane Ave, SL18, New Orleans, LA 70112 (e-mail: jhe{at}tulane.edu).
From the Departments of Epidemiology (Drs Bazzano, He, Vupputuri, and
Whelton) and Biostatistics (Ms Ogden and Dr Myers), Tulane University School
of Public Health and Tropical Medicine, New Orleans, La; and the National
Institutes of Health, National Heart, Lung, and Blood Institute, Bethesda,
Md (Dr Loria).
REFERENCES
| |
1. American Heart Association. 2000 Heart and Stroke Statistical Update. Dallas, Tex: American Heart Association; 1999.
2. Glore SR, Van Treeck D, Knehans AW, Guild M. Soluble fiber and serum lipids: a literature review. J Am Diet Assoc. 1994;94:425-436.
FULL TEXT
|
ISI
| PUBMED
3. Anderson JW, Smith BM, Washnock CS. Cardiovascular and renal benefits of dry bean and soybean intake. Am J Clin Nutr. 1999;70:464S-474S.
4. He J, Ogden LG, Vupputuri S, Bazzano LA, Loria C, Whelton PK. Dietary sodium intake and subsequent risk of cardiovascular disease
in overweight adults. JAMA. 1999;282:2027-2034.
FREE FULL TEXT
5. Ascherio A, Rimm EB, Hernan MA, et al. Intake of potassium, magnesium, calcium, and fiber and risk of stroke
among US men. Circulation. 1998;98:1198-1204.
ISI
| PUBMED
6. Sasaki S, Zhang XH, Kesteloot H. Dietary sodium, potassium, saturated fat, alcohol, and stroke mortality. Stroke. 1995;26:783-789.
FREE FULL TEXT
7. Anderson JW, Johnstone BM, Cook-Newell M. Meta-analysis of the effects of soy protein intake on serum lipids. N Engl J Med. 1995;333:276-282.
FREE FULL TEXT
8. Miller HW. Plan and Operation of the Health and Nutrition Examination
Survey: United States, 1971-1973. Hyattsville, Md: National Center for Health Statistics; 1978. Data
From Vital and Health Statistics, No. 1(10a).
9. Engel A, Murphy RS, Maurer K, Collins E. Plan and Operation of the NHANES I Augmentation Survey
of Adults 25-74 Years: United States, 1974-1975. Hyattsville, Md: National Center for Health Statistics; 1978. Data
From Vital and Health Statistics, No. 1(14).
10. Miller HW. Plan and Operation of the Health and Nutrition Examination
Survey: United States, 1971-1973. Hyattsville, Md: National Center for Health Statistics; 1978. Data
From Vital and Health Statistics, No. 1(10b).
11. Cohen BB, Barbano HE, Cox CS, et al. Plan and Operation of the NHANES I Epidemiologic
Follow-up Study, 1982-1984. Hyattsvile, Md: National Center for Health Statistics; 1987. Data
From Vital and Health Statistics, No. 1(22).
12. Finucane FF, Freid VM, Madans JH, et al. Plan and Operation of the NHANES I Epidemiologic
Follow-up Study, 1986. Hyattsville, Md: National Center for Health Statistics; 1990. Data
From Vital and Health Statistics, No. 1(25).
13. McLaughlin JK, Dietz MS, Mehl ES, Blot WJ. Reliability of surrogate information on cigarette smoking by type of
informant. Am J Epidemiol. 1987;126:144-146.
FREE FULL TEXT
14. Machlin SR, Kleinman JC, Madans JH. Validity of mortality analysis based on retrospective smoking information. Stat Med. 1989;8:997-1009.
ISI
| PUBMED
15. Cox CS, Rothwell ST, Madans JH, et al. Plan and Operation of the NHANES I Epidemiologic
Follow-up Study, 1987. Hyattsville, Md: National Center for Health Statistics; 1992. Data
From Vital and Health Statistics, No. 1(27).
16. Cox CS, Mussolino ME, Rothwell ST, et al. Plan and Operation of the NHANES I Epidemiologic
Follow-up Study, 1992. Hyattsville, Md: National Center for Health Statistics; 1997. Data
From Vital and Health Statistics, No. 1(35).
17. Madans JH, Reuben CA, Rothwell ST, Eberhardt MS. Differences in morbidity measures and risk factor identification using
multiple data sources: the case of coronary heart disease. Stat Med. 1995;14:643-653.
ISI
| PUBMED
18. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53:457-481.
FULL TEXT
|
ISI
19. Tarone RE. Tests for trend in life table analysis. Biometrika. 1975;62:679-682.
FREE FULL TEXT
20. Cox RD. Regression models and life tables (with discussion). J R Stat Soc B. 1972;34:187-220.
21. Korn EL, Graubard BI, Midthune D. Time-to-event analysis of longitudinal follow-up of a survey: choice
of the time-scale. Am J Epidemiol. 1997;145:72-80.
FREE FULL TEXT
22. Bingham SA, Atkinson C, Liggins J, Bluck L, Coward A. Phyto-oestrogens: where are we now? Br J Nutr. 1998;79:393-406.
FULL TEXT
|
ISI
| PUBMED
23. Rimm EB, Ascherio A, Giovannucci E, Spiegelman D, Stampfer MJ, Willett WC. Vegetable, fruit and cereal fiber intake and risk of coronary heart
disease among men. JAMA. 1996;275:447-451.
ABSTRACT
24. Guthrie HA. Selection and quantification of typical food portions by young adults. J Am Diet Assoc. 1984;84:1440-1444.
ISI
| PUBMED
25. Blake AJ, Guthrie HA, Smiciklas-Wright H. Accuracy of food portion estimation by overweight and normal-weight
subjects. J Am Diet Assoc. 1989;89:962-964.
ISI
| PUBMED
26. Faggiano F, Vineis P, Cravanzola D, et al. Validation of a method for the estimation of food portion size. Epidemiology. 1992;3:379-382.
ISI
| PUBMED
27. Smith AF, Jobe JB, Mingay DJ. Question-induced cognitive biases in reports of dietary intake by college
men and women. Health Psychol. 1991;10:244-251.
FULL TEXT
|
ISI
| PUBMED
28. Flegal KM. Evaluating epidemiologic evidence of the effects of food and nutrient
exposures. Am J Clin Nutr. 1999;69:1339S-1344S.
29. Tsubono Y, Nishino Y, Fukao A, Hisamichi S, Tsugane S. Temporal change in the reproducibility of a self-administered food
frequency questionnaire. Am J Epidemiol. 1995;142:1231-1235.
FREE FULL TEXT
30. Thompson FE, Lamphiear DE, Metzner HL, Hawthorne VM, Oh MS. Reproducibility of reports of frequency of food use in the Tecumseh
Diet Methodology Study. Am J Epidemiol. 1987;125:658-671.
FREE FULL TEXT
31. Van Horn L. Fiber, lipids, and coronary heart disease: a statement for healthcare
professionals from the nutrition committee, the American Heart Association. Circulation. 1997;95:2701-2704.
ISI
| PUBMED
32. Anderson JW, Gustafson NJ, Spencer DB, Tietyen J, Bryant CA. Serum lipid response of hypercholesterolemic men to single and divided
doses of canned beans. Am J Clin Nutr. 1990;51:1013-1019.
FREE FULL TEXT
33. Anderson JW, Gustafson NJ. Hypocholesterolemic effects of oat and bean products. Am J Clin Nutr. 1988;48:749-753.
FREE FULL TEXT
34. Anderson JW, Story L, Sieling B, Chen WJ, Petro MS, Story J. Hypocholesterolemic effects of oat-bran or bean intake for hypercholesterolemic
men. Am J Clin Nutr. 1984;40:1146-1155.
FREE FULL TEXT
35. Pietinen P, Rimm EB, Dorhonen P, et al. Intake of dietary fiber and risk of coronary heart disease in a cohort
of Finnish men: the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Circulation. 1996;94:2720-2727.
ISI
| PUBMED
36. Messina MJ. Legumes and soybeans: overview of their nutritional profiles and health
effects. Am J Clin Nutr. 1999;70:439S-450S.
FREE FULL TEXT
37. Selhub J, Jacques PF, Wilson PWF, Rush D, Rosenberg IH. Vitamin status and intake as primary determinants of homocysteinemia
in an elderly population. JAMA. 1993;270:2693-2698.
ABSTRACT
38. Stampfer MJ, Malinow MR, Willett WC, et al. A prospective study of plasma homocyst(e)ine and risk of myocardial
infarction in US physicians. JAMA. 1992;268:877-881.
ABSTRACT
39. Selhub J, Jacques PF, Bostom AG, et al. Association between plasma homocysteine concentrations and extracranial
carotid-artery stenosis. N Engl J Med. 1995;332:286-291.
FREE FULL TEXT
40. Ford ES, Byers TE, Giles WH. Serum folate and chronic disease risk: findings from a cohort of United
States adults. Int J Epidemiol. 1998;27:592-598.
FREE FULL TEXT
41. Loria CM, Ingram DD, Feldman JJ, Wright JD, Madans JH. Serum folate and cardiovascular disease mortality among US men and
women. Arch Intern Med. 2000;160:3258-3262.
FREE FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
|
Isoflavone intake in persons at high risk of cardiovascular events: implications for vascular endothelial function and the carotid atherosclerotic burden
Chan et al.
Am. J. Clin. Nutr. 2007;86:938-945.
ABSTRACT
| FULL TEXT
Effects of a Controlled Diet Supplemented with Chickpeas on Serum Lipids, Glucose Tolerance, Satiety and Bowel Function
Pittaway et al.
J. Am. Coll. Nutr. 2007;26:334-340.
ABSTRACT
| FULL TEXT
Pinto Beans Are a Source of Highly Bioavailable Copper in Rats
Saari et al.
J. Nutr. 2006;136:2999-3004.
ABSTRACT
| FULL TEXT
Protein, body weight, and cardiovascular health
Hu
Am. J. Clin. Nutr. 2005;82:242S-247S.
ABSTRACT
| FULL TEXT
Decreased Consumption of Dried Mature Beans Is Positively Associated with Urbanization and Nonfatal Acute Myocardial Infarction
Kabagambe et al.
J. Nutr. 2005;135:1770-1775.
ABSTRACT
| FULL TEXT
Soy Product Intake Is Inversely Associated with Serum Homocysteine Level in Premenopausal Japanese Women
Nagata et al.
J. Nutr. 2003;133:797-800.
ABSTRACT
| FULL TEXT
Copper in Legumes May Lower Heart Disease Risk
Klevay et al.
Arch Intern Med 2002;162:1780-1781.
FULL TEXT
|
