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(Stroke. 1996;27:813-818.)
© 1996 American Heart Association, Inc.
Articles |
Effect of Dietary Calcium and Milk Consumption on Risk of Thromboembolic Stroke in Older Middle-aged Men
The Honolulu Heart Program
From the Division of Biostatistics, University of Virginia School of Medicine, Charlottesville (R.D.A.); the Honolulu Heart Program, Kuakini Medical Center, Honolulu, Hawaii (R.D.A., J.D.C., B.L.R., K.Y.); the Department of Medicine, John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu (J.D.C., B.L.R.); and the Honolulu Epidemiology Research Section, Epidemiology and Biometry Program, National Heart, Lung, and Blood Institute, Honolulu, Hawaii (D.S.S., C.M.B.).
Correspondence to Robert D. Abbott, Division of Biostatistics, Box 432, University of Virginia School of Medicine, Charlottesville, VA 22908.
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Abstract |
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Background and Purpose Evidence suggests that dietary calcium is protective against hypertension. This report examines whether the effect has an influence on thromboembolic stroke.
Methods Since 1965, the Honolulu Heart Program has followed a cohort of men in a study of cardiovascular disease. This report examines the effect of baseline dietary calcium and milk intake on stroke risk in 22 years of follow-up in 3150 older middle-aged men (55 to 68 years).
Results Men who were nondrinkers of milk experienced stroke at twice the rate (P<.05) of men who consumed 16 oz/d or more (7.9 versus 3.7 per 100, respectively). While the rate of stroke decreased with increasing milk intake (P<.05), the decline in stroke risk with increased consumption was modest for those who consumed under 16 oz/d. Intake of dietary calcium was also associated with a reduced risk of stroke (P<.01), although its association was confounded with milk consumption. Calcium intake from nondairy sources was not related to stroke, suggesting that other constituents or covariates related to milk consumption may be important.
Conclusions We conclude that an association between milk consumption and a reduced risk of stroke in older middle-aged men cannot be explained by intake of dietary calcium. Since milk is often part of a diverse pattern of dietary intake, it is difficult to determine whether milk consumption has a direct role in reducing the risk of stroke. Data suggest that consumption of milk in older middle age is not harmful, and when combined with a balanced diet, weight control, and physical activity, reductions in the risk of stroke may occur.
Key Words: calcium • diet • risk factors • stroke outcome
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Introduction |
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Epidemiological studies have shown that dietary calcium is inversely associated with blood pressure.1 2 3 4 5 Although equivocal,6 experimental evidence has suggested that the intake of calcium supplementation is effective in controlling mild to moderate hypertension.7 8 Dietary calcium is also thought to improve lipid metabolism,9 10 while extreme excesses in calcium intake have been linked to a variety of adverse health consequences.11 12 13 With much of the epidemiological literature suggesting a cross-sectional relation between dietary calcium and blood pressure, it would seem reasonable to expect that the intake of dietary calcium could reduce the risk of cardiovascular events, such as stroke, that are commonly associated with hypertension.
In this report we examine the effect of dietary calcium and milk consumption (as a major source of dietary calcium) on the risk of thromboembolic stroke while controlling for hypertension and other risk factors for cardiovascular disease. Findings presented are based on 22 years of follow-up of the cohort of older middle-aged men (55 to 68 years) who were originally enrolled in the Honolulu Heart Program.
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Subjects and Methods |
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From 1965 to 1968, the Honolulu Heart Program began following 8006 men of Japanese ancestry living on the island of Oahu, Hawaii, for the development of coronary artery disease and stroke.14 At the time of study enrollment, subjects were aged 45 to 68 years. Each participant was given a baseline physical examination, including a complete cardiovascular evaluation. Initial screening consisted of documentation of cardiac and neurological conditions to identify prevalent cases of coronary artery disease and stroke. Procedures followed were in accordance with institutional guidelines and approved by an institutional review committee. Informed consent was obtained from the study participants.
For this report, analysis is limited to older middle-aged men who were 55 to 68 years old at the time of study inception and free of preexisting and coexisting morbidity due to coronary artery disease and stroke. Younger men were not considered for follow-up, since stroke was less common in the absence of major risk factors for stroke, including hypertension, diabetes, and cigarette smoking.15 There were 3150 men aged 55 to 68 years (mean±SD age, 60.0±3.5 years) at the time of study enrollment who provided information on nutrient intake.
Information on the intake of dietary calcium and milk was obtained by a dietitian based on 24-hour recall methods.16 Collected data were validated against a 7-day diet record in 329 of the 8006 men in the original cohort.17 There were no significant differences between the methods of assessing dietary intake for 15 nutrient categories, and day-to-day variation was less than typical among Western cultures.17 Nutrient intake levels were estimated by grouping foods into standard portions in 54 categories. Levels of nutrient intake for each category were then obtained from the US Department of Agriculture Handbook No. 818 and from a food table specifically designed for the Honolulu Heart Program. Other dietary information considered in this report includes potassium and sodium intake and the usual monthly intake of alcohol.19 Data on other electrolytes that have been associated with blood pressure, such as magnesium and phosphorus, could not be examined because they were available in only a small subset of the cohort.20
Up to 22 years of follow-up data are available on each subject to examine the relation between levels of calcium and milk intake at the baseline examination and the risk of stroke. Information on cardiovascular events was obtained through a comprehensive surveillance of hospital discharges, death certificates, autopsy records, and at repeated examinations given at 2 and 6 years into follow-up. As of 1990, 62 men in the original cohort had moved off the island of Oahu, resulting in an out-migration rate of approximately 1/1000 per year. The current survival status is unknown in only four men.
In this report, subjects were followed for the first occurrence of a fatal or nonfatal stroke. A diagnosis of stroke was made by a neurologist when a neurological deficit was accompanied by blood in cerebrospinal fluid or by evidence of an infarct or hemorrhage on nuclear brain scan or CT. Probable strokes included neurological deficits that persisted for at least 2 weeks or until death but were not accompanied by positive cerebrospinal fluid, brain scan, or CT findings. Based on this evidence, as well as clinical and pathological information from hospitalization, surgery, or autopsy, it was usually possible to classify strokes as thromboembolic or hemorrhagic. Possible strokes (neurological deficits lasting at least 24 hours but less than 2 weeks or of unknown duration) were not included among the stroke events because diagnostic certainty was lower and classification by stroke type was accomplished in only a small proportion of patients. A stroke was considered thromboembolic if the focal neurological deficit occurred usually without prolonged unconsciousness, nuchal rigidity, fever, pronounced leukocytosis, or blood in the spinal fluid. Identification of hemorrhagic stroke was based on a focal neurological deficit accompanied by loss of consciousness, headache, and blood present in the spinal fluid obtained by an atraumatic lumbar puncture or on the basis of CT or surgical findings. Subjects who experienced neurological episodes attributed to other conditions, such as blood dyscrasias, neoplastic disease, head injury, surgical accident, meningoencephalitis, fat embolism, epilepsy, or cardiac arrest, were not included among the stroke victims. Since CT was not used in the diagnosis of stroke until later in the course of follow-up in Hawaii, an effect on the classification of stroke as thromboembolic or hemorrhagic could have been introduced when this technology first appeared. Studies of stroke patients in Japan21 and autopsy data from the Honolulu Heart Program, however, indicate that the effect is small. Further details on the diagnosis of stroke are provided in an earlier publication.22
To help isolate the independent effect of dietary calcium and milk intake on the risk of stroke, several risk factors were considered possible confounding sources. In addition to alcohol consumption and the dietary intake of potassium and sodium, other factors examined included age, cigarette smoking, levels of physical activity, body mass index, systolic blood pressure, total cholesterol, serum glucose, serum uric acid, and hematocrit. Body mass index was defined as weight (kilograms) divided by height (meters) squared. Serum glucose was measured in a nonfasting state 1 hour after a 50-g challenge. Assessment of physical activity was based on the use of an index to quantify overall metabolic output that occurred during a typical 24-hour period.15 23 24 25 High levels of the index indicated active lifestyles and low levels inactive lifestyles. Further description of the other risk factors considered in this report is provided elsewhere.26
For the purpose of describing how risk factors change with increases in the intake of dietary calcium and milk, age-adjusted mean levels of each risk factor were compared across quartiles of the daily intake of dietary calcium and across various levels of milk consumption with the use of ANCOVA and logistic regression models.27 The cumulative incidence of stroke within the various ranges of calcium and milk intake was derived from estimated survival curves according to the methods of Kaplan and Meier.28
To assess the effect of dietary calcium on the risk of stroke, Cox regression models29 30 were used to provide estimates of relative risk that compare the risk of stroke in each of the bottom three quartiles of the intake of dietary calcium with the top quartile. Similar methods were used to make comparisons across various levels of milk consumption. Adjustments were made for age plus the other risk factors and for age alone. Although comparisons were made among ranges of calcium intake and milk consumption for purposes of illustration, they were also used to allow for flexibility in modeling the unknown dose-response or nonlinear relation that might exist between calcium and milk intake and the risk of stroke. Modeling milk consumption and dietary calcium as a continuous variable did not alter the findings that are reported here. All reported probability values were based on two-sided tests of significance.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Table 1
shows the ranges of daily intake of dietary
calcium that define each quartile of calcium consumed from nondairy and
dairy sources in the older middle-aged men in the Honolulu cohort
at the time of study enrollment. More than 25% of the study sample
consumed less than 300 mg/d of dietary calcium from both sources
combined. The majority of men consumed less than 600 mg/d. Excess
levels of calcium consumption were rare. Approximately 1% of the men
consumed more than 1500 mg/d of dietary calcium, and approximately 95%
consumed less than 1000 mg/d. A third of the calcium consumed was
derived from dairy sources. Although statistically significant
(P<.001), the correlation between calcium consumed from
dairy and nondairy sources was low (.08).
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During 22 years of follow-up, 229 of the 3150 men at risk
experienced a thromboembolic stroke. Table 1
also provides the crude
incidence of such events that was observed over the course of
follow-up by each quartile of intake of dietary calcium. The median
time to the occurrence of a thromboembolic stroke was 11.9 years.
For nondairy sources of calcium, the incidence of thromboembolic stroke over 22 years of follow-up did not differ across the quartiles of intake of dietary calcium. Incidence rates averaged near 7.3 per 100. In contrast, the incidence of thromboembolic stroke decreased significantly with increasing levels of dietary calcium intake from dairy sources (P<.01). Differences in the risk of stroke between adjacent quartiles were similar between the first through third quartiles, where the absolute reduction in the incidence of stroke increased gradually from 8.6 to 7.1 per 100. The largest change in the reduced risk of stroke among adjacent quartiles was observed between the third and fourth quartiles (7.1 versus 5.6 per 100). Men in the bottom and second quartiles had significantly higher rates of stroke than men in the top quartile (P<.05).
Tables 2 and 3 describe the relation
between the intake of dietary calcium from dairy sources and the intake
of potassium and sodium and putative risk factors for
cardiovascular disease. Data for nondairy calcium
intake are similar except for the instances noted below.
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The consumption of dietary potassium and sodium increased
consistently with increasing levels of dietary calcium intake
(Table 2). Men who fell in the top quartile of intake of dietary
calcium had significantly greater intakes of potassium and sodium than
men who fell in any of the other quartiles (P<.001).
Alcohol consumption also changed consistently with increasing
levels of calcium intake. Men who fell in the bottom three quartiles of
calcium intake consumed significantly more alcohol (11.4 to 15.4 oz/mo)
than men who consumed the most calcium (8.9 oz/mo, P<.05).
In contrast to calcium from dairy sources, alcohol consumption appeared
to be unrelated to the intake of nondairy calcium.
Use of cigarettes was also less frequent in the highest quartile of calcium intake relative to the other quartiles, although differences were not statistically significant. Differences in physical activity were modest, with levels of activity being highest in men who consumed the most calcium. Men who consumed amounts of calcium in the top quartile were significantly more active than men whose calcium intake fell in the first and third quartiles (P<.05).
Table 3 describes the relation between the intake of dietary calcium
from dairy sources and other known or potential risk factors for
stroke. Most of the differences in the risk factors across the
quartiles of intake of dietary calcium were not large. Nevertheless,
men who consumed the smallest amounts of calcium had significantly
higher levels of body mass index relative to men who consumed the
highest levels of calcium (P<.05). Systolic blood
pressure was also significantly higher in men who fell in the first and
second quartiles of calcium intake compared with men in the top
quartile (P<.01). Serum uric acid was at its lowest level
among men who consumed the highest levels of calcium. It was
significantly reduced in the top quartile compared with the first and
second quartiles (P<.01). There were no clear associations
between calcium intake from dairy sources and total
cholesterol, serum glucose, and hematocrit. There were also
no clear relations between the intake of calcium from nondairy sources
and body mass index, systolic blood pressure, and serum uric
acid.
To help determine whether the association of dietary calcium with the
risk of thromboembolic stroke could be attributed to the association
between calcium intake and the other risk factors, Cox regression
models were estimated in an attempt to control for possible confounding
influences. Table 4 shows the estimated relative risk of
thromboembolic stroke, comparing the expected risk that occurred in
each of the bottom three quartiles of calcium intake for dairy and
nondairy sources with the risk that was observed in the top quartile.
Adjustments to the relative risk estimates were made for age, dietary
potassium and sodium, alcohol, cigarette smoking, physical activity
index, systolic blood pressure, total cholesterol,
serum glucose, serum uric acid, and hematocrit. Adjustments made for
each of the risk factors alone had little effect on the reported
findings.
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Increases in the intake of dietary calcium from dairy sources appeared to have a protective effect against thromboembolic stroke that was independent of concomitant systolic blood pressure and the other risk factors (P<.05). When sources of calcium are combined, there was a statistically significant excess of thromboembolic stroke on the order of 80% in the lowest quartile of dietary calcium intake compared with the top quartile (P<.05). Men whose intake of calcium placed them in the second quartile also experienced a significant excess of stroke compared with the fourth quartile of intake (P<.05). Although not statistically significant, men in the third quartile had a near 50% excess risk of stroke compared with the top quartile.
Findings for milk consumption in terms of relations with other risk factors and the risk of stroke are similar to those described for calcium intake from dairy sources. As with dietary calcium, milk intake tended to be low. A third of the men consumed no milk, while less than 10% consumed 16 oz/d or more. Mean±SD daily milk consumption was 4.9±6.7 ounces. Approximately 5% of the milk consumed was skimmed. From 1965 to 1968, when the dietary data were collected, it is likely that the remaining percentage of milk consumed was largely whole milk. The correlation between milk consumption and calcium intake derived from dairy sources was high (.93, P<.001).
The cumulative incidence of thromboembolic stroke that was observed
during the course of follow-up in the Honolulu Heart Program is
shown in the Figure for four levels of milk consumption.
Throughout the course of follow-up, the incidence curve for men who
consumed the largest amounts of milk (16 oz/d or more) was
significantly less than the curves for the other levels of milk
consumption (P<.05). When adjustments were made for risk
factors, a twofold excess risk of stroke persisted in nondrinkers
versus those who consumed 16 oz/d or more (P<.05). During
the last 8 years of follow-up, nondrinkers of milk had the highest
cumulative incidence of thromboembolic stroke, followed by men who
consumed milk but whose intake was less than 8 oz/d. Except for the
first 4 years of follow-up, men who consumed 8 oz/d or more but
fewer than 16 oz/d were associated with an incidence curve that fell
between the curves for men who consumed more and less milk. Although
the rate of stroke decreased significantly with increasing milk intake
(P<.05), among men who consumed less than 16 oz/d, the
decline in the risk of stroke with increased consumption was modest and
not statistically significant.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The findings presented in this report are limited to lower ranges of dietary calcium intake that are less typical of other population-based samples. In the men of Japanese ancestry in the Honolulu Heart Program, the mean±SD daily intake of dietary calcium was 477±290 mg/d. From the Third National Health and Nutrition Examination Survey, the estimated average intake of calcium in the general US population is 854 mg/d in men aged 50 to 59 years and 875 mg/d in those aged 60 to 69 years.31 In a study that examined the effects of dietary calcium on lipoprotein concentrations, the average baseline intake of calcium was 946 mg/d in hypertensive men and 1038 mg/d in those who were normotensive.32 Among Dutch civil servants,33 the 20th percentile of dietary calcium intake (585 mg/d) was near the 75th percentile of intake that was observed in Hawaii (606 mg/d). Fewer than 12% of the Japanese-American men in the Honolulu Heart Program consumed at least the average daily allowance of dietary calcium (800 mg/d) that is recommended by the National Research Council.34 In a recent consensus report from the National Institutes of Health,13 recommended intake for men aged 25 to 65 years is 1000 mg/d. Presumably, men in the Honolulu Heart Program also consumed smaller amounts of milk than men in other ethnic groups, although data on levels of milk consumption in older middle-aged men are not readily available in a format that can be used for comparison purposes. In the general US population, milk consumption averages approximately 6.8 oz/d compared with 4.9 oz/d in the Honolulu cohort.35
Because of the low intake of dietary calcium in the cohort of men enrolled in the Honolulu Heart Program, the effects of greater intakes of dietary calcium that are commonly observed in other communities (or the effects of dietary supplementation) cannot be examined. Evidence from Hawaii, however, suggests that for the ranges of calcium that were consumed, calcium intake was unrelated to the risk of stroke. Although calcium from dairy sources had an association with stroke, it appears to have been mediated through a protective effect derived from milk consumption. While the protective constituent of milk cannot be identified, it would seem logical that it is not due to calcium, since calcium does not appear to be protective when consumed from nondairy sources. When amounts of calcium from dairy sources and milk intake are adjusted for the effects of each other, neither shows a significant relation to stroke. Since the correlation between calcium intake from dairy sources and milk consumption is high (.93, P<.001), this is to be expected. Jointly, however, they remain significantly related to stroke with and without adjustment for other risk factors (P<.05), and since calcium from nondairy sources is unrelated to stroke, it would seem more likely that other constituents or covariates related to milk consumption may be important. Increased bioavailability of calcium through milk is an unlikely confounder, since calcium absorption from all sources is probably maximized in the sunny environment of Hawaii.
The relation between milk and stroke is also unexplained by other nutritional information collected by the Honolulu Heart Program. The relation is left unexplained by potassium, sodium, and the diuretic effects of alcohol intake. Control for the intake of carbohydrates, saturated fatty acids, dietary cholesterol, and protein also provides little additional insight from the Honolulu cohort.
In conjunction with reports which suggest that dietary calcium is inversely associated with blood pressure,1 2 3 4 5 7 8 it would seem reasonable to suspect that dietary calcium or milk consumption could be protective against cardiovascular events that are often the consequence of hypertension. In terms of stroke, however, there is no effect of calcium from nondairy sources even when unadjusted for systolic blood pressure. Since milk consumption continues to have a beneficial effect on reducing the risk of stroke after adjustment for hypertension, this finding is consistent with mechanisms that do not involve hypertension. Milk consumption and intake of calcium from either nondairy or dairy sources are also unrelated to strokes that have a hemorrhagic origin. Since hemorrhagic stroke is strongly associated with hypertension,36 37 it would seem reasonable to rule out hypertension as an explanatory factor for the relation between milk consumption and stroke.
Since dietary calcium affects only thromboembolic events independent of hypertension, mechanisms may be related to coagulation factors or lipid metabolism. Associations involving coagulation are not known. Some evidence suggests that intake of dietary calcium results in favorable lipoprotein concentrations,9 10 possibly through increases in fecal fat content.9 In the Honolulu Heart Program, however, men who consumed higher amounts of dietary calcium and milk tended to have higher concentrations of total cholesterol, although the excess was not large. Data on levels of high- and low-density lipoprotein cholesterol were not available in Hawaii at the time of study enrollment, and triglyceride levels (measured in a nonfasting state) had no effect on the reported findings.
Whether changes in diet over time have a role in affecting the risk of stroke is unknown. At an examination that occurred approximately 15 years after study enrollment, changes in dietary patterns were observed in only a small sample of men. Thus, an assessment of changes in food intake over time could not be addressed.
It is possible that deficits in milk consumption are associated with stroke through induced changes in other important risk factors over time. Increases in blood pressure or acute phases of hypertension could occur with greater frequency, longer duration, or less tolerance during the aging process in those who are nondrinkers of milk. Excluding subjects with atrial fibrillation at baseline failed to alter the reported findings from Hawaii. Although excluding men who were enrolled in the Honolulu Heart Program with hypertension or diabetes (and the treatment of either condition) reduced statistical power, those who were nondrinkers of milk had the highest risk of thromboembolic stroke, significantly higher than men who drank 16 oz/d or more (P<.05). The effect of milk intake did not appear to interact with physical activity or with past or current cigarette smoking status. Milk consumption was also unrelated to the incidence of coronary artery disease.
For younger men who were not considered in this report (aged 45 to 54 years), a significant effect of milk and calcium intake on the risk of stroke could not be identified, although both tended to be protective. This lack of statistical significance was not unexpected, since the rate of stroke in those who were younger was much lower than in those who were older. In addition, since only 16 of 147 thromboembolic strokes in the younger men were unaffiliated with hypertension, diabetes, or cigarette smoking (compared with 48 of 229 in those who were older), it becomes difficult to identify an effect of milk or dietary calcium intake on the risk of stroke in the presence of some of the most potent stroke risk factors. When the younger and older men were combined, the effects of milk and calcium intake are diluted, primarily because of the addition of a larger cohort of younger men (4439), in whom disease was uncommon even in those whose intake of calcium and milk was low, to a smaller cohort of individuals who were older (3150).
Although specific explanations for the association between the consumption of milk and stroke cannot be identified in this kind of study, drinking milk appears to be associated with a reduced risk of stroke. Milk consumption, however, is likely to be associated with the improved intake of other nutrients and with health behavior involving numerous other factors, most of which would be difficult to identify. As a result, it would be inappropriate to recommend that milk consumption be increased to reduce the risk of stroke because of the inability to eliminate other explanatory factors. Nevertheless, data suggest that the consumption of milk in older middle age is not harmful, and when combined with a balanced diet, weight control, and physical activity, reductions in the risk of stroke may occur.
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Acknowledgments |
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This study was supported by grant NO1-HC-05102 (to the Honolulu Heart Program) from the National Heart, Lung, and Blood Institute, Bethesda, Md.
Received December 18, 1995; revision received February 8, 1996; accepted February 8, 1996.
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References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. McCarron D, Morris C, Holly J, Stanton J. Blood pressure and nutrient intake in the United States. Science. 1984;224:1392-1398.
2. Stitt FW, Crawford M, Clayton DG, Morres JN. Clinical and biochemical indicators of cardiovascular disease among men living in hard and soft water areas. Lancet. 1973;1:122-126. [Medline] [Order article via Infotrieve]
3.
McCarron D, Morris D, Cole C. Dietary calcium
in human hypertension. Science. 1982;217:267-269.
4.
Ackley S, Barrett-Connor E, Suarez L. Dairy
products, calcium and blood pressure. Am J Clin
Nutr. 1983;38:457-461.
5.
Criqui MH, Langer RD, Reed DM. Dietary alcohol,
calcium, and potassium: independent and combined effects on blood
pressure. Circulation. 1989;80:609-614.
6. Cutler JA, Brittain E. Calcium and blood pressure: an epidemiologic perspective. Am J Hypertens. 1990;3:137S-146S. [Medline] [Order article via Infotrieve]
7.
Belizan JM, Villar J, Pineda O, Gonzalez AE, Sainz E,
Garrera G, Sibrian R. Reduction of blood pressure with calcium
supplementation in young adults. JAMA. 1983;249:1161-1165.
8. McCarron DA. Epidemiological evidence and clinical trials of dietary calcium's effect on blood pressure. Contrib Nephrol.. 1991;90:2-10. [Medline] [Order article via Infotrieve]
9. Denke MA, Fox MM, Schulte MC. Short-term dietary calcium fortification increases saturated fat content and reduces serum lipids in men. J Nutr. 1993;123:1047-1053.
10.
Karanja N, Morris CD, Illingworth DR, McCarron
DA. Plasma lipids and hypertension: response to calcium
supplementation. Am J Clin Nutr. 1987;45:60-65.
11.
Cappuccio FP. The
epidemiology of diet and blood
pressure. Circulation. 1992;86:1651-1653.
12. Seely S. Is calcium excess in Western diet a major cause of arterial disease? Int J Cardiol. 1991;33:191-198. [Medline] [Order article via Infotrieve]
13. Optimum calcium intake. NIH Consens Statement. 1994;12:1-31.
14.
Yano K, Reed DM, McGee DL. Ten-year
incidence of coronary heart disease in the Honolulu Heart
Program: relationship to biologic and lifestyle
characteristics. Am J Epidemiol. 1984;119:653-666.
15.
Abbott RD, Rodriguez BL, Burchfiel CM, Curb JD.
Physical activity in older middle-aged men and reduced risk of
stroke: the Honolulu Heart Program. Am J Epidemiol. 1994;139:881-893.
16.
Tillotson J, Kato H, Nichaman M, Miller DC, Gay ML,
Johnson KG, Rhoads GG. Epidemiology of
coronary heart disease and stroke in Japanese men living in
Japan, Hawaii and California: methodology for comparison of
diet. Am J Clin Nutr. 1973;26:177-184.
17.
McGee D, Rhoads G, Hankin J, Yano K, Tillotson
J. Within person variability of nutrient intake in a group of
Hawaiian men of Japanese ancestry. Am J Clin Nutr. 1982;36:657-663.
18. Watt BK, Merrill ALP. Composition of Foods: Raw, Processed, Prepared. Washington, DC: US Dept of Agriculture; 1963. Agriculture Handbook No. 8.
19.
Donahue RP, Abbott RD, Reed DM, Yano K. Alcohol
and hemorrhagic stroke: the Honolulu Heart Program.
JAMA. 1986;255:2311-2314.
20.
Joffres MR, Reed DM, Yano K. Relationship of
magnesium intake and other dietary factors to blood pressure: the
Honolulu Heart Study. Am J Clin Nutr. 1987;45:469-475.
21.
Tanaka H, Ueda Y, Hayashi M, Date C, Baba T, Yamashita
H, Shoji H, Tanaka Y, Owada K, Detels R. Risk factors for
cerebral hemorrhage and cerebral infarction in a Japanese rural
community. Stroke. 1982;13:62-73.
22.
Kagan A, Popper JS, Rhoads GG. Factors related
to stroke incidence in Japanese men: the Honolulu Heart Study.
Stroke. 1980;11:14-21.
23.
Donahue RP, Abbott RD, Reed DM, Yano K. Physical
activity and coronary heart disease in middle-aged and
elderly men: the Honolulu Heart Program. Am J Public
Health.. 1988;78:683-685.
24.
Kannel WB, Sorlie PD. Some health benefits of
physical activity: the Framingham Study. Arch Intern
Med.. 1979;139:857-861.
25. Garcia-Palmieri MR, Costas R, Cruz-Vidal M, Sorlie PD, Havlik RJ. Increased physical activity: a protective factor against heart attack in Puerto Rico. Am J Cardiol. 1982;50:749-755. [Medline] [Order article via Infotrieve]
26. Kagan A, Harris BR, Winkelstein W Jr, Johnson KG, Kato H, Syme SL, Rhoads GG, Gay ML, Nichaman MZ, Hamilton HB, Tillotson J. Epidemiologic studies of coronary heart disease and stroke in Japanese men living in Japan, Hawaii and California: demographic, physical, dietary, and biochemical characteristics. J Chron Dis. 1974;27:345-364. [Medline] [Order article via Infotrieve]
27. Lane PW, Nelder JA. Analysis of covariance and standardization as instances of prediction. Biometrics. 1982;38:613-621.[Medline] [Order article via Infotrieve]
28. Kaplan E, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc.. 1958;53:457-481.
29. Cox DR. Regression models and life tables. J R Stat Soc. 1972;34(series B):187-202.
30. Kalbfleisch JD, Prentice KL. The Statistical Analysis of Failure Time Data. New York, NY: John Wiley & Sons, Inc; 1980.
31. Alaimo K, McDowell MA, Briefel RR, Bischof AM, Caughman CR, Loria CM, Johnson CL. Dietary Intake of Vitamins, Minerals, and Fiber of Persons Ages 2 Months and Over in the United States: Third National Health and Nutrition Examination Survey, Phase 1, 1988-1991. Hyattsville, Md: National Center for Health Statistics; 1994. Advance Data From Vital and Health Statistics, No. 258.
32.
Karanja N, Morris CD, Rufolo P, Snyder G, Illingworth
DR, McCarron DA. Impact of increasing calcium in the diet on
nutrient consumption, plasma lipids, and lipoproteins in
humans. Am J Clin Nutr. 1994;59:900-907.
33.
Van Der Vijver LPL, Van Der Waal MAE, Weterings KGC,
Dekker JM, Schouten EG, Kok FJ. Calcium intake and 28-year
cardiovascular and coronary heart disease
mortality in Dutch civil servants. Int J Epidemiol. 1992;21:36-39.
34. National Research Council. Recommended Dietary Allowance. 10th ed. Washington, DC: National Academy Press; 1989.
35. Interagency Board for Nutrition Monitoring and Related Research; Ervin B, Reed D, eds. Nutrition Monitoring in the United States: Chartbook I: Selected Findings From the National Nutrition Monitoring and Related Research Program. Hyattsville, Md: Public Health Service; 1993.
36.
Wolf PA. Risk factors for stroke.
Stroke. 1985;16:359-360.
37. Kagan A, Popper JS, Rhoads GG. Factors related to stroke incidence in Hawaii Japanese men: the Honolulu Heart Program. Stroke. 1980;11:14-21.
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 K. F. Hilpert, S. G. West, D. M. Bagshaw, V. Fishell, L. Barnhart, M. Lefevre, M. M. Most, M. B. Zemel, M. Chow, A. L. Hinderliter, et al. Effects of Dairy Products on Intracellular Calcium and Blood Pressure in Adults with Essential Hypertension J. Am. Coll. Nutr., April 1, 2009; 28(2): 142 - 149. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. C. Elwood, D. I. Givens, A. D. Beswick, A. M. Fehily, J. E. Pickering, and J. Gallacher The Survival Advantage of Milk and Dairy Consumption: an Overview of Evidence from Cohort Studies of Vascular Diseases, Diabetes and Cancer J. Am. Coll. Nutr., December 1, 2008; 27(6): 723S - 734S. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Lamarche Review of the Effect of Dairy Products on Non-Lipid Risk Factors for Cardiovascular Disease J. Am. Coll. Nutr., December 1, 2008; 27(6): 741S - 746S. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Umesawa, H. Iso, J. Ishihara, I. Saito, Y. Kokubo, M. Inoue, S. Tsugane, and for the JPHC Study Group Dietary Calcium Intake and Risks of Stroke, Its Subtypes, and Coronary Heart Disease in Japanese: The JPHC Study Cohort I Stroke, September 1, 2008; 39(9): 2449 - 2456. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Jauhiainen and R. Korpela Milk Peptides and Blood Pressure J. Nutr., March 1, 2007; 137(3): 825S - 829S. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Umesawa, H. Iso, C. Date, A. Yamamoto, H. Toyoshima, Y. Watanabe, S. Kikuchi, A. Koizumi, T. Kondo, Y. Inaba, et al. Dietary Intake of Calcium in Relation to Mortality From Cardiovascular Disease: The JACC Study Stroke, January 1, 2006; 37(1): 20 - 26. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Alonso, J. J. Beunza, M. Delgado-Rodriguez, J A. Martinez, and M. A. Martinez-Gonzalez Low-fat dairy consumption and reduced risk of hypertension: the Seguimiento Universidad de Navarra (SUN) cohort Am. J. Clinical Nutrition, November 1, 2005; 82(5): 972 - 979. [Abstract] [Full Text] [PDF]
|
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|
|
 |
|
 P. C Elwood Time to value milk Int. J. Epidemiol., October 1, 2005; 34(5): 1160 - 1162. [Full Text] [PDF]
|
|
|
|
 |
|
 P C Elwood, J J Strain, P. J Robson, A. M Fehily, J. Hughes, J. Pickering, and A. Ness Milk consumption, stroke, and heart attack risk: evidence from the Caerphilly cohort of older men J Epidemiol Community Health, June 1, 2005; 59(6): 502 - 505. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. K. Choi, W. C. Willett, M. J. Stampfer, E. Rimm, and F. B. Hu Dairy Consumption and Risk of Type 2 Diabetes Mellitus in Men: A Prospective Study Arch Intern Med, May 9, 2005; 165(9): 997 - 1003. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Rajaram The effect of vegetarian diet, plant foods, and phytochemicals on hemostasis and thrombosis Am. J. Clinical Nutrition, September 1, 2003; 78(3): 552S - 558. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Fraser Commentary: Protection from stroke by eating animal foods? Surely not! Int. J. Epidemiol., August 1, 2003; 32(4): 543 - 545. [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Pereira, D. R. Jacobs Jr, L. Van Horn, M. L. Slattery, A. I. Kartashov, and D. S. Ludwig Dairy Consumption, Obesity, and the Insulin Resistance Syndrome in Young Adults: The CARDIA Study JAMA, April 24, 2002; 287(16): 2081 - 2089. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. K. Massey Dairy Food Consumption, Blood Pressure and Stroke J. Nutr., July 1, 2001; 131(7): 1875 - 1878. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A R Ness, G D. Smith, and C Hart Milk, coronary heart disease and mortality J Epidemiol Community Health, June 1, 2001; 55(6): 379 - 382. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Miller, J. K. Jarvis, and L. D. McBean The Importance of Meeting Calcium Needs with Foods J. Am. Coll. Nutr., April 1, 2001; 20(2): 168S - 185. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Schrezenmeir and A. Jagla Milk and Diabetes J. Am. Coll. Nutr., April 1, 2000; 19(90002): 176S - 190. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Iso, M. J. Stampfer, J. E. Manson, K. Rexrode, C. H. Hennekens, G. A. Colditz, F. E. Speizer, and W. C. Willett Prospective Study of Calcium, Potassium, and Magnesium Intake and Risk of Stroke in Women Stroke, September 1, 1999; 30(9): 1772 - 1779. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Ascherio, E. B. Rimm, M. A. Hernan, E. L. Giovannucci, I. Kawachi, M. J. Stampfer, and W. C. Willett Intake of Potassium, Magnesium, Calcium, and Fiber and Risk of Stroke Among US Men Circulation, September 22, 1998; 98(12): 1198 - 1204. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. Sacco, E. J. Benjamin, J. P. Broderick, M. Dyken, J. D. Easton, W. M. Feinberg, L. B. Goldstein, P. B. Gorelick, G. Howard, S. J. Kittner, et al. Risk Factors Stroke, July 1, 1997; 28(7): 1507 - 1517. [Full Text]
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