Abstract
Background & Aims:
Diet modification is a major component of non-pharmacological coronary heart disease (CHD) prevention. Few studies have examined the association between consumption of different dairy products with subclinical coronary artery disease. We sought to examine whether milk, yogurt, or cheese consumption is associated with calcified atherosclerotic plaques in the coronary arteries.
Methods:
We cross-sectionally examined 2278 participants from the National Heart, Lung, and Blood Institute Family Heart Study. Dairy consumption was assessed by a semiquantitative food frequency questionnaire. Coronary artery calcium (CAC) was estimated by cardiac computed tomography. We used an Agatston score of ≥100 to indicate prevalent CAC and fitted multivariable logistic regression to calculate adjusted odds ratios.
Results:
Mean age was 58±13 years and 45% were male. The frequency of milk (≤1/week, 2-4/week, and ≥5/week; 22%, 14%, and 64%, respectively), yogurt (almost never, <1/week, and ≥1/week; 54%, 20%, and 26%, respectively), and cheese consumption (<1/week, 1/week, 2-4/week, and ≥5/week; 15%, 17%, 41%, and 27%, respectively) varied in the cohort. We observed an inverse association of cheese consumption with prevalent CAC: odds ratio (95% CI) of 0.63 (0.42-0.94) when comparing cheese intake of ≥5 servings/week with <1/week, adjusting for sex, age, body mass index, cigarette pack years, presence of CHD, family income, and education (p for linear trend 0.007). In contrast, there was no association between yogurt or milk consumption and CAC (p for linear trend 0.51 and 0.87, respectively).
Conclusion:
Our data suggest that cheese consumption but not yogurt or milk is associated with a lower odds of CAC in men and women.
Keywords: Dairy consumption, cheese, yogurt, milk, coronary artery disease, coronary artery calcium score
Introduction
Coronary heart disease (CHD) is a leading cause of mortality and disability worldwide [1]. Dietary modification in addition to smoking cessation, weight loss, and increase in physical activity are the most important non-pharmacological strategies for CHD prevention [2]. A variety of dairy products, such as milk, yogurt, and cheese, have been associated with a lower incidence of CHD [3, 4] as well as other diseases related to atherosclerosis [5, 6].
Radiographically detectable coronary-artery calcium (CAC) is a marker of subclinical CHD. Coronary calcification, being part of the intravascular healing process, occurs as a consequence of atheroma instability and rupture [7] and is frequently observed near the surface of fibroatheroma or more complicated lesions (type 5 or 6 atherosclerotic lesions, respectively) [7, 8]. CAC is associated with coronary artery disease severity [9, 10], but also with incident CHD, independent of traditional risk factors [11-14]. In clinical practice, CAC possesses good cardiovascular risk reclassification capacity (net reclassification improvement index 0.55 [95% CI 0.42-0.69]) [15] and is therefore recommended for treatment guidance in patients with intermediate cardiovascular risk [2]. Hence, the association between CAC and nutrition becomes more relevant as CAC directly impacts patient management.
The relation of dairy consumption with CAC remains unclear. In the Multi-Ethnic Study of Atherosclerosis, whole milk consumption (≥1x/month) was inversely associated with CAC progression [16], however no significant association between milk consumption and incident CHD events was observed in the European Prospective Investigation into Cancer and Nutrition (EPIC; n=409,885) [3]. The relationship of cheese and yogurt consumption with CAC has not been investigated although a large Swedish cohort study (n=106,772) reported an inverse association between cheese and cardiovascular mortality in women [17] and the EPIC study found an inverse association of cheese and yogurt consumption with incident CHD [3].
Given the paucity of data on dairy consumption on CAC, we therefore investigated the association between milk, yogurt, and cheese consumption and CAC among participants of the National Heart, Lung, and Blood Institute Family Heart Study (NHLBI FHS).
Material and Methods
Study population
We analyzed data collected on participants of the NHLBI FHS, a multi-center, population-based cross-sectional cohort study aiming to identify genetic and non-genetic determinants of preclinical atherosclerosis, CHD, and cardiovascular risk factors. The details of the NHLBI FHS have been described in detail elsewhere [18]. In short, families contributing to the study were randomly selected (random group) or selected due to a higher-than-expected risk of CHD (high-risk group) from existing population-based cohort studies [19] (Supplemental Figure 1). The largest families that underwent additional typing of genome-wide anonymous markers by the Mammalian Genotyping Service were invited between 2002 and 2003 for further examination that included cardiac-gated multi-detector computed tomography (cardiac CT) with coronary artery calcium (CAC) scoring. Of the 3360 participants with cardiac CT, 2278 participants had dairy consumption data available at baseline examination (1994-1995). Each participant gave informed consent and the study protocol of the parent NHLBI FHS was reviewed and approved by each participating institution. The Institutional Review Board of Brigham and Women’s Hospital approved the current project (2005P002385, Djousse, PI).
Assessment of dairy consumption
Dairy consumption was assessed through a staff-administered semi-quantitative food frequency questionnaire designed by Willett et al. [20]. The questionnaire has been validated in other cohorts [20-22]. Each participant was asked the following question: “In the past year, how often on average did you consume whole milk [237 ml] (low fat milk [237 ml], ricotta and cottage cheese [113 g], other cheese [28 g], or yogurt [245 g], respectively)? Pre-specified responses were: almost never, 1-3/month, 1/week, 2-4/week, 5-6/week, 1/day, 2-3/day, 4-6/day, and >6/day. Dairy products were defined as total milk (whole milk and low-fat milk), cheese (ricotta, cottage cheese, and other cheese), and yogurt. For total milk and cheese consumption, we summed frequencies of corresponding categories. Due to sparse data in some categories, we combined adjacent categories for stable estimates.
Assessment of relevant variables
Information on demographics, cigarette smoking, family income, and education was obtained by the interview during the initial clinical visit. Resting blood pressure was measured three times on seated participants after a 5-minute rest using a random zero sphygmomanometer and an appropriate cuff size. For analyses, average systolic and diastolic blood pressures from the second and third measurement were used. The seventh Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure classification was used to define hypertension or if the study participant reported contemporary treatment for hypertension. Further assessment of traditional cardiovascular disease risk factors has been described elsewhere [23]. Anthropometric data were collected with subjects wearing scrub suits. Prevalence of CHD was assessed via questionnaire. All variables were ascertained during the initial examination (1994-1995).
Calcified atherosclerotic plaque quantification in the coronary arteries
Cardiac computed tomography scans were performed with four different scanner systems (General Electric LightSpeed Plus and LightSpeed, GE Healthcare Technologies, Chicago, US; Siemens Somaton Volume Zoom, Siemens Medical Solutions, Erlangen, Germany; and Philips MX 8000, Philips Healthcare, Best, Netherlands). The scan protocol was consistent with NHLBI’s Multi-Ethnic Study of Atherosclerosis Study (MESA) protocol [24]. Scan parameters and data acquisition are described by Djoussé et al. [23].
CT images were electronically transmitted and read at the core lab at Wake Forest University Health Science, Winston-Salem, NC, USA. Images were interpreted by trained readers using dedicated software (GE Smartscore) and hardware (GE Advantage Windows Workstation). The Agatston method was used to calculate the CAC score based on the area and density of calcified plaques [25]. CAC scores of each of two scans per participant were averaged to obtain the final CAC score.
Statistical Analysis
We used logistic regression to calculate the age- and multivariable adjusted odds ratios (ORs) of CAC for each category of dairy consumption, using the lowest category of each type of dairy as reference. CAC was dichotomized using the cut-off ≥100 Agatston score, as previously described [23]. Additionally cut-points >0, ≥50, ≥150, ≥200, and ≥300 were evaluated in sensitivity analyses. In the multivariable model, we adjusted for age, sex, body mass index, cigarette pack years, presence of CHD, family income (<$25K, $25K to $75K, ≥$75K), and education (high school or less, bachelor or some college, advanced degree). Further variables were tested for confounding applying a change-in-estimate criterion with a 10% cutoff [26]. All statistical analyses were conducted using SAS (Release 9.3, SAS Institute Inc, Cary, North Carolina, USA) and R (Page version 4.0, R foundation for Statistical Computing, Vienna, Austria). A two-sided p-value of <0.05 was considered statistically significant.
Results
Of the 2278 participants analyzed, 45% were men, and the mean age was 58±13 years. The median consumption of milk, yogurt, and cheese was ≥5, <1, and 2-4 servings/week, respectively. Characteristics of the NHLBI FHS participants are provided according to consumption of cheese (Table 1) as well as milk and yogurt (Supplementary Table 1).
Table 1.
Characteristics among 2277 participants of the NHLBI Family Heart Study according to cheese consumption.
Frequency of cheese consumption | ||||
---|---|---|---|---|
<1/week n=343 |
1/week n=382 |
2-4/week n=931 |
≥5/week n=621 |
|
Age (years) | 61.6±11.9 | 60.4±12.6 | 58.5±11.9 | 54.2±12.6 |
Male (%) | 45 | 46 | 46 | 43 |
BMI (kg/m2) | 27.3±5.3 | 27.7±4.9 | 27.8±5.3 | 27.3±4.9 |
Hypertension (%) | 42.9 | 45.3 | 43.0 | 33.7 |
SBP (mmHg) | 138.6±18.5 | 139.2±18.0 | 137.8± 18.5 | 134.7±18.0 |
DBP (mmHg) | 89.3±13.0 | 89.7±12.6 | 90.6±13.0 | 90.3±12.6 |
Antihypertensive treatment (%) | 21.3 | 24.1 | 21.1 | 15.5 |
Hypercholesterolemia (%) | 39.9 | 34.2 | 30.3 | 27.3 |
Total/HDL cholesterol ratio | 4.2±3.0 | 4.5±3.3 | 5.1±3.1 | 6.7±4.8 |
Statin treatment (%) | 2 | 1 | 0.6 | 0.6 |
Calorie intake (kcal/day) | 1449±601 | 1566±680 | 1722±599 | 2121±936 |
Diabetes mellitus (%) | 12.8 | 11.5 | 12.7 | 11.9 |
Antidiabetic treatment (%) | 3.5 | 2.1 | 3.7 | 3.9 |
Current Smoker (%) | 11.7 | 11.8 | 11.9 | 13.2 |
Current Drinker (%) | 52.2 | 50.9 | 50.3 | 50.7 |
Cigarette pack years | 14.2±24.7 | 14.3±25.0 | 10.5±24.7 | 8.0±25.0 |
CHD prevalence (%) | 12 | 11 | 8 | 6 |
Family income (%) | ||||
<$25,000 | 19 | 18 | 15 | 14 |
$25,000 - <$75,000 | 63 | 66 | 66 | 68 |
≥$75,000 | 19 | 16 | 20 | 19 |
Education (%) | ||||
High school or less | 41 | 42 | 34 | 30 |
Bachelor or some college | 12 | 9 | 11 | 11 |
Advanced degree | 47 | 49 | 55 | 59 |
Data are presented as mean ± SD or percentage. CHD, coronary heart disease defined as composite of myocardial infarction, percutaneous coronary angioplasty, coronary artery bypass surgery, or death secondary to coronary heart disease.
Odds ratios showed an inverse association between cheese consumption and CAC (Table 2). People reporting consumption of ≥5 servings of cheese per week had a 37% lower odds of CAC (95% Confidence Interval [CI]: 6% to 58%) when compared to participants that almost never consumed cheese after multivariable adjustment (p-trend = 0.007). Addition of traditional CVD risk factors, hypercholesterolemia treatment or calorie intake as covariates did not alter the ORs in a meaningful way (Supplementary Table 2). Additional control for physical activity, milk, yogurt, fruit or vegetable intake as potential confounding factors did not alter the effect size and conclusions [data not shown]. The association between cheese consumption and CAC persisted upon exclusion of people with prevalent CHD from analyses (multivariable adjusted OR: 0.63 [95% CI: 0.41 - 0.96]; Supplementary Table 3). In a sensitivity analysis, we observed an inverse relationship between cheese consumption and prevalent CAC using CAC cut-off points of 300, 200, 150, 50 [i.e., multivariable adjusted OR [95% CI] for ≥5 cheese servings/week: 0.57 [0.37-88], 0.49 [0.32-0.74], 0.52 [0.34-0.79], 0.59 [0.40-0.88], respectively], but not the CAC cut-off of 0 (Supplementary Table 4). We observed no relationship between yogurt or milk consumption and CAC (Table 2).
Table 2.
Prevalence odds ratios (95% confidence intervals) of calcified atherosclerotic plaque in the coronary arteries according to cheese, yogurt, and milk consumption in 2278 participants of the NHLBI Family Heart Study.
CAC prevalence, cases/n (%) |
Crude | Age/sex-adjusted | Multivariable adjusted model1 |
|
---|---|---|---|---|
Frequency of cheese consumption | ||||
Almost never or <1/week | 145 / 343 (42%) | 1.0 | 1.0 | 1.0 |
1/week | 153 / 382 (40%) | 0.91 (0.68 to 1.23) | 0.98 (0.67 to 1.42) | 0.95 (0.62 to 1.44) |
2-4/week | 300 / 931 (32%) | 0.65 (0.50 to 0.84) | 0.77 (0.56 to 1.05) | 0.83 (0.58 to 1.18) |
≥5/week | 131 / 621 (21%) | 0.37 (0.27 to 0.49) | 0.58 (0.40 to 0.83) | 0.63 (0.42 to 0.94) |
P for linear trend | - | <0.001 | 0.002 | 0.007 |
Frequency of yogurt consumption | ||||
Almost never | 463 / 1238 (37%) | 1.0 | 1.0 | 1.0 |
<1/week | 120 / 448 (27%) | 0.61 (0.48 to 0.78) | 0.92 (0.68 to 1.24) | 1.18 (0.84 to 1.66) |
≥1/week | 146 / 592 (25%) | 0.55 (0.44 to 0.68) | 0.80 (0.61 to 1.05) | 0.95 (0.69 to 1.29) |
P for linear trend | - | 0.26 | 0.07 | 0.87 |
Frequency of total milk consumption | ||||
Almost never or ≤1/week | 161 / 509 (32%) | 1.0 | 1.0 | 1.0 |
2-4/week | 111 / 315 (35%) | 1.18 (0.87 to 1.58) | 1.13 (0.77 to 1.66) | 1.33 (0.87 to 2.04) |
≥5/week | 457 / 1454 (31%) | 0.99 (0.80 to 1.23) | 0.90 (0.68 to 1.18) | 1.22 (0.89 to 1.67) |
P for linear trend | - | 0.99 | 0.76 | 0.51 |
adjusted for age, sex, body mass index, cigarette pack years, presence of coronary heart disease, family income (<$25K, $25K to $75K, ≥$75K), education (high school or less, bachelor or some college, advanced degree). CAC, coronary artery calcium; NHLBI, National Heart, Lung, and Blood Institute. Cheese consumption data was only available in 2277 study participants. One hundred twenty-nine participants (5%) had missing data on covariates (including overlap of missing values: 3 body mass index, 75 pack years, 3 presence of CHD, 44 family income, 5 education).
Discussion
Main findings
Our study showed that frequency of cheese consumption is inversely related to the odds of calcified coronary artery plaque after adjustment for potential confounders. On the other hand, we did not observe an association between yogurt or milk consumption and prevalent CAC.
Association of cheese with CAC
Given the lack of prior studies on dairy consumption and CAC, our findings provide new insight into the relation between cheese and stable coronary artery disease. Hyperlipidemia and diabetes including associated pathophysiological processes may be in the causal pathway between cheese consumption and CAC.
Low LDL levels are associated with CAC regression and stagnation [27] and suboptimal glycemic control (HbA1c >7.5%) in type 1 diabetes patients is associated with increased CAC progression [28]. Both risk factors, hyperlipidemia and diabetes, associate inversely with cheese consumption. In a small cross-over study, Soerensen et al. documented that a diet rich in cheese increased LDL cholesterol less than an isocaloric control diet (0.47±0.12 and 0.84±0.11 mmol/L, respectively) in the context of increased fecal fat excretion [29]. Similarly, Brassard et al. observed a lesser LDL increase in a multicenter, crossover randomized controlled trial when comparing an isocaloric cheese and butter diet with the same saturated fatty acid contents (+3.8% and +4.7%, respectively) [30]. A nested case-cohort study published by Sluijs et al. showed that cheese intake had an inverse association with incidence of diabetes (Hazard Ratio 0.88, [95%CI 0.76-1.02]) [31]. Furthermore, Ericson et al. showed in 16427 female participants of the MalmöDiet and Cancer Cohort, that cheese intake was inversely associated with incidence of type 2 diabetes mellitus (p=0.02) [32].
Association of milk or yogurt with CAC
Contrary to our study, Ghosh et al. observed an inverse relation of milk consumption with CAC in MESA [16]. Reasons for this difference are likely multifactorial. The authors reported a significant CAC difference at baseline between participants with (n=1272; 24%) and without whole milk intake frequency ≥1x/month (n=4001; 76%). Potentially influenced by our total milk consumption approach, we observed milk intake >1/week in 1769 participants (78%) of the NHLBI FHS cohort with CAC measurements. Furthermore, application of the cut-off CAC >100 provide a 5% difference between those with and without milk intake frequency ≥1x/month in MESA, whereas in our study the difference between those with and without milk intake >1/week was only 1%. An association between yogurt consumption and CAC has not been reported in the literature.
Limitations strengths
Our study has some limitations. The number of participants with frequent yogurt intake was small, which might have prevented us from detecting a small, yet clinically relevant effect size [3]. Furthermore, given the cross-sectional design, we are unable to infer causality between cheese consumption and CAC and cannot rule out unmeasured or residual confounding as a reason for observed findings. We assumed that participants kept a stable dietary pattern in our analyses. However, it is possible that study participants could have changed their dietary intake of dairy products and thereby introducing exposure misclassification in our data. Furthermore, the food questionnaire did not capture all dishes that include cheese, yogurt, or milk as ingredients. Consequentially, the exposure to these dietary components might be underestimated. The current investigation also has several strengths including a large sample size allowing for greater statistical power, availability of data on key covariates to control for confounding by lifestyle factors and anthropometric measurements, participant recruitment from several US geographical regions to support generalizability of our findings, and a standardized and validated approach to CAC measurement [24].
Conclusion
Our study shows an inverse association of cheese consumption but not milk or yogurt with prevalent CAC in men and women.
Supplementary Material
Acknowledgements
This report is presented on behalf of the investigators of the NHLBI FHS. We thank the Family Heart Study participants and staff for their valuable contributions.
Funding Statement
The NHLBI Family Heart Study was supported by the NHLBI co-operative agreement grants U01 HL 67893, U01 HL67894, U01 HL67895, U01 HL67896, U01 HL67897, U01 HL67898, U01 HL67899, U01 HL67900, U01 HL67901, and U01 HL67902. Dr. Djoussé was supported by grant R01 HL131687 from the National Heart, Lung, and Blood Institute, Bethesda, MD.
List of abbreviations
- CAC
Coronary-artery calcium
- CHD
Coronary heart disease
- CI
Confidence interval
- CT
Computed tomography
- EPIC
European Prospective Investigation into Cancer and Nutrition
- LDL
Low-density lipoprotein
- MESA
Multi-Ethnic Study of Atherosclerosis
- NHLBI FHS
National Heart, Lung, and Blood Institute Family Heart Study
- OR
Odds ratio
Footnotes
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Conflict of Interest
Ulf Neisius – no conflicts of interest
Guohai Zhou – no conflict of interest
Rachel E Ward – no conflict of interest
R Curtis Ellison – no conflict of interest
J Michael Gaziano – no conflict of interest
Luc Djoussé – no conflict of interest
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