IJE Advance Access originally published online on December 12, 2007
International Journal of Epidemiology 2008 37(1):173-182; doi:10.1093/ije/dym243
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Intake of ruminant trans fatty acids and risk of coronary heart disease
1Research Unit for Dietary Studies at Institute of Preventive Medicine, Copenhagen University Hospital, Centre for Health and Society, Øster Søgade 18, DK-1357 Copenhagen, Denmark.
2Research Centre for Prevention and Health, Glostrup University Hospital, Nordre Ringvej 57, DK-2600 Glostrup, Denmark.
3Department of Clinical Epidemiology, Aarhus University Hospital, Sdr. Skovvej 15, DK-9100 Aalborg, Denmark.
4Center for Cardiovascular Research, Aalborg Hospital, Aarhus University Hospital, Sdr. Skovvej 15, DK-9100, Denmark.
5Department of Human Nutrition, University of Copenhagen, Rolighedsvej 30, DK-1958 Frederiksberg, Denmark and Capio Diagnostik A/S, Nygårdsvej 32, DK-2100 Copenhagen, Denmark.
*Corresponding author. Department of Clinical Epidemiology, Aarhus University Hospital, Sdr. Skovvej 15, DK-9100 Aalborg, Denmark. E-mail: muj{at}dce.au.dk
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Abstract |
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Background: Studies have shown a positive association between trans fatty acids (TFA) intake and risk of coronary heart disease (CHD), primarily accounted for by industrially produced TFA. Some of these studies indicate an inverse association between ruminant TFA (R-TFA) intake and CHD implying that R-TFA intake is innocuous or even protective against CHD. The aim of this study was to describe the association between R-TFA intake and risk of CHD evaluating both the absolute and the energy-adjusted intake.
Methods: The study was an 18-year follow-up study of 3686 Danes, aged 30–71 years, at baseline without previous CHD.
Results: There were no overall associations between absolute or energy-adjusted R-TFA intakes and risk of CHD. However, among women, indications of inverse associations between R-TFA intake and risk of CHD were found: hazard ratio (HR) per 0.5 g increase in absolute R-TFA intake = 0.84 [95% confidence interval (CI): 0.70, 1.01] and HR per 0.5 g increase in energy-adjusted R-TFA intake = 0.77 (95% CI: 0.55, 1.09). No associations between absolute or energy-adjusted R-TFA intakes and CHD were found among men.
Conclusions: This study suggests that R-TFA intake is not associated with a higher risk of CHD. Whether R-TFA intake is even protective against CHD among women cannot be concluded from this study.
Keywords Coronary disease, dietary fats, intake, ruminant, trans fatty acids
Accepted 30 October 2007
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Introduction |
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Epidemiological studies have shown a strong positive association between the intake of trans fatty acids (TFA) and the risk of coronary heart disease (CHD)1–4; in three studies1–3 the positive association was primarily accounted for by industrially produced TFA (IP-TFA) (Table 1). Indeed, one of these three studies found an inverse association between ruminant TFA (R-TFA) and risk of CHD2 and one study indicated an inverse association1 (Table 1). These findings might imply that R-TFA intake is innocuous or even protective against CHD.
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A reduction in the intake of IP-TFA can be achieved by reducing the content of IP-TFA in foods, whereas a change in the intake of R-TFA can only be achieved by changing intake of dairy and ruminant meat products. In Denmark, the content of IP-TFA in margarines has been reduced and consequently the intake of IP-TFA from margarines and shortenings has decreased from 2.2 g/person/day in 1992 to 0.35 g in 1999.5 In contrast, the intake of R-TFA may have been constant, as the amount of milk fat and ruminant meat available for consumption has been rather constant.6
Previous prospective cohort studies of TFA intake and risk of CHD have expressed R-TFA intake relative to energy intake1,2,4 (as a measure of dietary composition). However, whether R-TFA intake in risk assessments should be expressed as relative intake or absolute intake (as a measure of dietary composition and total amount of food/total energy intake) depends on the potential biological relationships between R-TFA intake and risk of CHD. Studies have shown that intake of C18:1 trans isomers from hydrogenated fats unfavourably affect the plasma lipid profile.7 No specific hypotheses have been suggested regarding the effect of intake of R-TFA on CHD risk.
The Danish population may be one of the best populations to study the association between R-TFA intake and risk of CHD due to the wide range of R-TFA intake.8 The aim of this study was to describe the association between the intake of R-TFA and the risk of CHD for both the absolute and the energy-adjusted intake of R-TFA, using data from four Danish cohort studies.
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Materials and Methods |
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Study population
This study is based on data from four Danish cohort studies [the 1914 cohort, the 1936 cohort, the MONICA-I (monitoring of trends and determinants in cardiovascular disease) cohort and the MONICA-III cohort].9 The cohorts met the criterion that habitual dietary intake was determined using a 7-day weighed food record or a dietary history interview. The participants were recruited and examined between 1964 and 1991, with a participation of 70–88%. The examinations included self-administered questionnaires containing detailed questions concerning sociodemographic factors, lifestyle and health, as well as a general clinical health examination. Participants from the 1914 cohort, the 1936 cohort and the MONICA-I cohort have been invited and examined several times and new participants have been added to the 1914 cohort.9,10 At the first examination or at the re-examination, all or random subsets of the participants from the different cohorts were requested also to provide information regarding their habitual diet. In total, information on diet was obtained from 3959 participants, aged 30–71 years, examined between 1974 and 1993.10 Further details of the study participants are given by Jakobsen et al.10
Exclusions
Persons for whom the recorded sum of saturated fatty acids (SFA), monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA) intake was greater than the total fat intake were excluded. Persons with a previous diagnosis of CHD and persons reporting diabetes mellitus were also excluded.
Dietary variables
Part of the participants was given comprehensive oral and written instructions on how to complete a 7-day weighed food record and part of the participants underwent a dietary history interview by the same trained dietician. The interviews were conducted by asking non-leading, open-ended questions on dietary intake during the previous month. Quantities were explored by averages of food models, photo series and household measures. The methods have been described previously and it has been shown that the methods yield comparable data on intake of energy and macronutrients.11
Nutrient calculation into daily intake averages was done using the Micro Camp, DANKOST 1 and DANKOST 2 computer programs (Danish Catering Center A/S, Herlev, Denmark) based on Danish food composition tables.12,13 R-TFA calculation was achieved by combining information on food intake with the content of TFA in milk fat8 and the content of TFA in ruminant meat products.14
A weighted intake of foods containing high amounts of IP-TFA was calculated for each participant. The foods were selected and weighted according to estimates of the content of IP-TFA in Danish foods.5,15 It was assumed that the weighted intake would rank the study participants according to IP-TFA intake, in spite of the fact that the content of IP-TFA in margarines has changed since the dietary information was obtained.5
Non-dietary variables
Information on family history of myocardial infarction, education, leisure-time physical activity and smoking habits was obtained by a self-administered questionnaire. Blood pressure, height and weight were measured. Blood pressure was measured after at least 5 min rest. Body mass index (BMI) was calculated as weight (kg)/height (m2).
Identification of events
Fatal and non-fatal CHD events were defined according to International Classification of Diseases, Eighth Revision, diagnosis codes 410–414 until December 31, 1994, and subsequently by International Classification of Diseases, Tenth Revision, codes I20–I25. Events were identified by record linkage to the Cause of Death Registry, including information regarding all deaths since 1943,16 and the National Patient Registry, including information regarding all hospitalizations since 1977.17 Events ascertainment was made by review of medical files for participants from the 1914 cohort who were included in 1974 and thus before 1977.18
Documentation of the validity of the diagnosis of myocardial infarction (International Classification of Diseases, Eighth Revision, code 410) in the National Patient Registry and the Cause of Death Registry has been published earlier.19
Statistical analyses
Analyses were carried out in the whole sample and separately for women and men. Hazard ratios (HR) with 95% confidence intervals (CI) for the incidence of and mortality from CHD were calculated using Cox's proportional hazards regression model with age as the underlying time variable. The observation time for each participant was the period from age at the examination by which information on diet was obtained until age at event (fatal or non-fatal CHD), death of another cause, emigration, or December 31, 2000, whichever came first. Participants from the 1936 cohort who underwent the examination in 1976 were followed from 1977.
Two strategies were used for investigating the association between R-TFA intake and risk of CHD: (i) R-TFA intake was included as absolute intake in g/d (0.5 unit) without adjustment for total energy intake and other important determinants of variation in total energy intake between persons [body size (measured as BMI) and physical activity] and (ii) R-TFA intake was included as energy-adjusted intake in g/d (0.5 unit) for a fixed total energy intake (by including total energy intake as a separate variable in the model). The energy-adjusted R-TFA intake was calculated using the residual method as described by Willett and Stampfer.20 By using the residual method, variation in R-TFA intake due to differences in total energy intake is taken into account. Both strategies included adjustment for cohort identification (as a categorical variable).
Adjustment for non-dietary and dietary CHD risk factors: familial history of myocardial infarction (yes, no, do not know); education (7 years or less, 8 years or more); leisure-time physical activity (sedentary, active); smoking (never smokers, ex-smokers, current smokers of 1–14 g of tobacco per day, current smokers of 15 g of tobacco or more per day); alcohol intake (g/day) (non-drinkers, drinkers by tertiles); percentages of energy intake from protein, SFA, MUFA and PUFA (as continuous variables); dietary fibre intake (g/mega joule (MJ)/day) (as a continuous variable); dietary cholesterol intake (mg/MJ/day) (as a continuous variable); and weighted intake of foods containing high amounts of IP-TFA (g/day) (as a continuous variable), was done according to the described strategies. Adjustment for BMI and systolic blood pressure was done using spline regression.21 The knots were defined using equal events in each line segment. A covariate was included if it changed the beta coefficient for the R-TFA variable 10% or more. In analyses including both women and men, sex was adjusted for by allowing different underlying hazard functions for women and men.
To deal with potential confounding by body size and physical activity level in analyses of absolute R-TFA intake and risk of CHD, BMI and leisure-time physical activity were added in further analyses.
For every Cox model, we checked the proportional hazards assumption with a smoothed plot of scaled Schoenfeld residuals vs age and tested continuous variables for non-linearity in a spline regression model. The spline regression model was also used to obtain figures of the log HR as a function of the intake of R-TFA. An age-dependent variable was added to the models that allowed for different associations between SFA intake and risk of CHD for the two age bands of <60 years and 
60 years. This was done as a previous study, using the same data, showed that the association between SFA intake and risk of CHD was modified by age10 and as the plots of scaled Schoenfeld residuals vs age indicated that the association between SFA intake and risk of CHD was modified by age.
The association between R-TFA intake and risk of CHD may be modified by sex and age due to differences in the underlying hazard functions. To evaluate the possible effect modification by sex, statistical interaction between R-TFA intake and sex was tested using the likelihood ratio test. To evaluate the possible effect modification by age, we added an age-dependent variable for the two age bands of <60 years and 60 years; statistical interaction was tested using the likelihood ratio test.
Data analyses were performed using Stata statistical software, release 9.0 (Stata Corporation, College Station, TX, USA).
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Results |
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Five persons for whom the recorded sum of SFA, MUFA and PUFA intake was greater than the total fat intake were excluded. Eighty persons with a previous diagnosis of CHD and 77 persons reporting diabetes mellitus were also excluded. The final population consisted of 3797 persons (1911 women and 1886 men) of whom 3553 completed a 7-day weighed food record and 244 underwent a dietary history interview. The analyses included the 3686 persons who provided information on all potential confounding variables.
Characteristics of the participants and the relation of R-TFA intake to selected variables are given in Table 2. During the 8–23 years (median, 18 years) of follow-up from 1974 to 2000, 374 participants (121 women and 253 men) with fatal or non-fatal events of CHD were identified.
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There were no overall associations between absolute (Table 3) or energy-adjusted (Table 4) R-TFA intakes and risk of CHD. However, among women indications of inverse associations between the absolute R-TFA intake and the risk of CHD (HR = 0.84, 95% CI: 0.70, 1.01 per 0.5 g increase in absolute R-TFA intake) (Table 3) and between the energy-adjusted R-TFA intake and the risk of CHD (HR = 0.77, 95% CI: 0.55, 1.09 per 0.5 g increase in energy-adjusted R-TFA intake) (Table 4) were found. For absolute R-TFA intake, the P-value for effect modification by age was 0.03 and for energy-adjusted R-TFA intake, the P-value was 0.22. No associations between the absolute R-TFA intake (Table 3) or the energy-adjusted R-TFA intake (Table 4) and the risk of CHD were found among men; for absolute R-TFA intake, the P-value for effect modification by age was 0.44 and for energy-adjusted R-TFA intake, the P-value was 0.17.
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To deal with potential confounding by body size and physical activity level in analyses of absolute R-TFA intake and risk of CHD, BMI and leisure-time physical activity were added in further analyses. Adjustment for BMI and leisure-time physical activity level, however, did not change the measures of association for R-TFA intake (Table 3).
No consistent effect modification by sex was found. In overall analyses, the P-value for effect modification by sex were 0.22 for absolute R-TFA intake and 0.52 for energy-adjusted R-TFA intake. In age-dependent analyses, the association between absolute R-TFA intake and risk of CHD was modified by sex among persons <60 years (P = 0.05) but not among persons 60 years (P = 0.60); for energy-adjusted R-TFA intake, the P-values were 0.29 among persons <60 years and 0.72 among persons 60 years.
Spline regression analyses of the log HR of CHD according to the absolute R-TFA intake is shown in Figure 1 and the energy-adjusted R-TFA intake in Figure 2.
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Linear regression analyses were used to identify the most important food groups contributing to variability in R-TFA intake. Intake of butter explained 62% of the variability in R-TFA among women and 67% among men, whereas milk and milk products, cheese and cheese products and ruminant meat products only explained minor parts of the variation (Table 5). A similar pattern was seen after taking into account the variation explained by the intake of SFA (Table 5).
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Discussion |
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In the present study, there was no overall association between R-TFA intake and risk of CHD within a wide range of intake. Among women, however, indications of inverse associations between both the absolute R-TFA intake and the energy-adjusted R-TFA intake and the risk of CHD were found. No associations between R-TFA and risk of CHD were found among men.
Information bias is unlikely to have affected the results, as events were identified by record linkage to the Cause of Death Registry16 and the National Patient Registry17 and diagnoses were established independently of the dietary records and the dietary history interview of the participants. If censoring is related to both R-TFA intake and risk of CHD, and if the true associations between R-TFA and CHD and between R-TFA and censoring are in the same directions, then censoring may lead to underestimation of the true associations between R-TFA and CHD. This may be the case if censoring is due to e.g. thrombotic stroke. In the present study, loss to follow-up was 14%, mainly due to death from other causes. In Denmark, stroke is the cause of about 9% of total mortality. However, censoring could also lead to overestimation if the true associations between R-TFA and CHD and between R-TFA and censoring are in opposite directions. This scenario, however, seems less likely.
A number of limitations should be noted. First, the relatively small number of events caused wide CIs and limited the possibility to further assess possible effect modification. Second, a potential source of random measurement error arises from dietary self-reporting methods. Generally, random measurement error leads to underestimation on the true risk and to the loss of statistical power for testing associations. In the present study, dietary intake was determined using a 7-day weighed food record (among 3449 persons) or a dietary history interview (among 237 persons) conducted by asking questions on dietary intake during the previous month. Quantities were explored by averages of food models, photo series and household measures. The dietary history interview may reflect habitual eating pattern whereas the 7-day weighed food record is at best representative of food intake during the recording period and may not necessarily be strongly correlated with the habitual eating pattern. However, it has been shown that the two dietary assessment methods yield comparable data on intake of energy and macronutrients.11 Third, only baseline information regarding dietary habits was available. The lack of repeated assessment of dietary intake excludes possible analytic approaches to reduce measurement error.
Control for non-dietary and dietary CHD risk factors did not change the measures of association for R-TFA intake among neither women nor men. However, after additional adjustment for SFA intake, the indication of an inverse association between absolute R-TFA intake and risk of CHD among women was strengthened, and an indication of an inverse association between energy-adjusted R-TFA intake and risk of CHD among women was found. SFA intake is a risk factor of CHD at least partially mediated by the effect of SFA on low-density lipoprotein cholesterol concentration in plasma. The R-TFA intake was directly correlated to SFA intake (r = 0.80), partly because of shared food sources. By adjustment for SFA intake, the models address the effects of R-TFA independent of SFA intake, but the variation in R-TFA intake is restricted to variation in food sources not directly overlapping the food sources contributing to variation in SFA intake; thereby probably referring to other underlying dietary patterns. Linear regression analyses were used to identify the most important food groups contributing to variability in R-TFA intake and variability in R-TFA intake after taking into account the variation explained by the intake of SFA. The results indicated that the underlying dietary patterns may be similar before and after adjustment for the intake of SFA. Confounding from other dietary components in dairy products cannot be excluded.
Other epidemiological studies have shown a strong positive association between the intake of TFA and the risk of CHD;1–4 in three studies1–3 the positive association was primarily accounted for by IP-TFA (Table 1). In agreement with the present findings, one previous study indicated an inverse association between energy-adjusted R-TFA intake and risk of CHD among women1 and one study found no association between energy-adjusted R-TFA intake and risk of CHD among men3 (Table 1). One previous study, however, found an inverse association between energy-adjusted R-TFA intake and risk of CHD among men2 and another study indicated a positive association between energy-adjusted R-TFA intake and risk of CHD among men4 (Table 1). It has been suggested that the lack of a higher risk of CHD associated with the intake of R-TFA as compared with the intake of IP-TFA may be due to lower levels of intake.22 The upper limit for R-TFA intake in these previous studies was around 2.5 g/day whereas the upper limit for IP-TFA intake was around 5.1 g/day. Biologically, however, there is no rationale for a threshold effect. Furthermore, in the present study, we found no evidence of a higher risk associated with R-TFA intake within the wide range of intake among both women (90% central range: 0.5–3.1 g/day) and men (90% central range: 0.6–4.1 g/day) (Figures 1 and 2). The lack of a higher risk of CHD associated with the intake of R-TFA in contrast to the higher risk of CHD associated with the intake of IP-TFA may be due to the distinct structure of the major C18:1 trans isomer in ruminant fat, vaccenic acid, which has a double bond in the 11th position as opposed to the 9th position in elaidic acid, the major C18:1 trans isomer in industrially produced, partially hydrogenated fats.23,24
We estimated the associations between both the absolute and the energy-adjusted intake of R-TFA and the risk of CHD. Whether intake of R-TFA in risk assessments should be expressed as absolute intake or relative intake depends on the potential biological relationships between R-TFA intake and risk of CHD. If R-TFA selectively affects an organ system that is uncorrelated with body size and if body size and physical activity do not affect the metabolism of R-TFA, the absolute intake may be most relevant. If R-TFA is metabolized in approximate proportion to body size and physical activity, the relative intake may be, however, the most relevant. No specific hypotheses have been suggested regarding the effect of R-TFA intake on CHD risk. Therefore, at present the optimal epidemiologic approaches for obtaining further insight into the association between R-TFA intake and risk of CHD may be to evaluate both the absolute and the energy-adjusted intake.
In conclusion, the present results suggest that intake of R-TFA is not associated with a higher risk of CHD; a high intake of TFA from dairy and ruminant meat products may thus be an issue of no concern to public health. Whether R-TFA intake is even protective against CHD among women cannot be concluded from this study.
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Acknowledgements |
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This study was financed by The Danish Heart Foundation (grants: 03-2-9-4-22087 and 04-10-B127-A187-22170) and the Female Researchers in Joint Action (FREJA) program from The Danish Medical Research Council. The FREJA program also financed the establishment of the Research Unit for Dietary Studies.
Conflicts of interest: None declared.
KEY MESSAGES
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Notes |
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The originally published version of this paper was incorrect. There was an error in the legends of Figure 2 which said "Log HRs were adjusted for the variables listed as model 3 in Table 3" but should be ""...model 3 in Table 4."
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  D. Mozaffarian Commentary: Ruminant trans fatty acids and coronary heart disease--cause for concern? Int. J. Epidemiol., February 1, 2008; 37(1): 182 - 184. [Full Text] [PDF]
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