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Eur J Clin Nutr. Author manuscript; available in PMC 2014 August 01.
Published in final edited form as:
Eur J Clin Nutr. 2014 February ; 68(2): 178–183. doi:10.1038/ejcn.2013.248.
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Serum concentrations of cholesterol, apolipoprotein A-I, and
apolipoprotein B in a total of 1 694 meat-eaters, fish-eaters,
vegetarians, and vegans
Kathryn E Bradbury, PhD1, Francesca L Crowe, PhD1, Paul N Appleby, MSc1, Julie A
Schmidt, MSc1, Ruth C Travis, DPhil1, and Timothy J Key, DPhil1
1Cancer Epidemiology Unit, University of Oxford, Oxford, UK
Abstract
BACKGROUND—The objective of this study was to describe serum lipid concentrations,
including apolipoproteins A-I and B, in different diet groups.
METHODS—A cross-sectional analysis of a sample of 424 meat-eaters, 425 fish-eaters, 423
vegetarians, and 422 vegans, matched on sex and age, from the European Prospective
Investigation into Cancer and Nutrition (EPIC)-Oxford cohort. Serum concentrations of total, and
HDL cholesterol, as well as apolipoproteins A-I and B were measured, and serum non-HDL
cholesterol was calculated.
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RESULTS—Vegans had the lowest BMI, and the highest and lowest intakes of polyunsaturated
and saturated fat, respectively. After adjustment for age, alcohol and physical activity, compared
to meat-eaters, fish-eaters and vegetarians, serum concentrations of total and non-HDL
cholesterol, and apolipoprotein B were significantly lower in vegans. Serum apolipoprotein A-I
concentrations did not differ between the diet groups. In males, the mean serum total cholesterol
concentration was 0.87 nmol/L lower in vegans than in meat-eaters; after further adjustment for
BMI this difference was 0.76 nmol/L. In females, the difference in total cholesterol between these
two groups was 0.60 nmol/L, and after further adjustment for BMI was 0.55 nmol/L.
CONCLUSIONS—In this study, which included a large number of vegans, serum total
cholesterol and apolipoprotein B concentrations were lower in vegans compared to meat-eaters,
fish-eaters and vegetarians. A small proportion of the observed differences in serum lipid
concentrations was explained by differences in BMI, but a large proportion is most likely due to
diet.
Keywords
lipids; cholesterol; apolipoproteins; vegetarian diet; vegan diet
INTRODUCTION
Serum concentrations of total cholesterol and non-HDL cholesterol are well-established risk
factors for cardiovascular disease.1 Apolipoprotein A-I and apolipoprotein B represent the
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Corresponding author: Kathryn E Bradbury Cancer Epidemiology Unit Nuffield Department of Population Health Richard Doll
Building University of Oxford Roosevelt Drive Oxford OX3 7LF, UK Tel: +44 (0) 1865289647 Fax: +44 (0) 1865289610
kathryn.bradbury@ceu.ox.ac.uk.
CONFLICT OF INTEREST The authors declare no conflict of interest.
Bradbury et al.
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number of circulating anti-atherogenic and atherogenic particles, respectively. Serum
concentrations of these apolipoproteins have also been associated with the risk of
cardiovascular disease,2 and may provide some additional, physiologically-relevant,
information to aid in the prediction of cardiovascular disease risk.3, 4
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A comparison of serum lipid profiles in different diet groups, for example vegetarians and
omnivores, can provide insight into the net effect of habitual diets that have distinctly
different compositions. Previous studies have generally shown that vegetarians have
relatively low serum concentrations of total cholesterol and LDL cholesterol,5, 6 but
differences in serum concentrations of apolipoproteins A-I and B between diet groups are
not well characterised. In addition, previous studies have only included a small number of
vegans, and relatively little is known about the serum lipid profiles of vegans – who exclude
all animal products from their diet.
The objective of this study is to describe serum concentrations of lipids and apolipoproteins
A-I and B, in a representative sample of meat-eaters, fish-eaters, vegetarians, and vegans
participating in the European Prospective Investigation into Cancer and Nutrition (EPIC)Oxford cohort.
MATERIALS AND METHODS
The EPIC-Oxford cohort is a prospective study of 65 411 men and women aged 20 years or
older. The study has been described in detail elsewhere.7 Briefly, the study was designed to
investigate diet, lifestyle and risk of cancer and other chronic diseases in people with
different dietary habits, and thus the aim was to recruit a large number of vegetarians and
vegans. Recruitment was carried out between 1993 and 2001. Eleven percent of participants,
mainly non-vegetarians, were recruited through general practice surgeries. Postal methods
were used to recruit all other participants, including a large number of vegetarians and
vegans. The study was approved by a Multicenter Research Ethics Committee, and all
participants gave written informed consent.
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In the baseline questionnaire, participants were asked if they ate meat, fish, dairy products
and eggs, and were classified accordingly into meat-eaters (reported consuming meat), fisheaters (reported consuming fish but no meat), vegetarians (reported consuming dairy
products and/or eggs but no meat or fish), and vegans (reported no consumption of meat,
fish, dairy products, or eggs). The recruitment questionnaire also included a 130-item semiquantitative Food Frequency Questionnaire (FFQ). Food intakes were calculated by
multiplying the reported frequency of consumption of food items by standard portion sizes.
Data from the fifth edition of McCance and Widdowson’s The Composition of Food and its
supplements 8-17 were used to estimate nutrient intakes.
Height and weight were self-reported in the baseline questionnaire. In a sub-sample of the
cohort, height and weight were measured (n = 4 808); measured and self-reported values
showed excellent agreement (r > 0.90).18 Measured (where available) or self-reported height
and weight were used to calculate BMI (kg/m2). The baseline questionnaire collected
information on occupational and leisure activities. This information was combined into a
physical activity index, and participants were categorised into one of four groups: inactive,
or low, moderate, or high level of activity. This index has been shown to rank participants
according to objectively measured physical activity energy expenditure.19, 20
The present study consists of a sub-sample drawn from participants younger than 90 years
who provided a blood sample at recruitment to the EPIC-Oxford cohort between 1993 and
1998. In addition, to be eligible for the current study, participants had to have: responded to
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at least 80% of the relevant questions in the FFQ (in total, 130 relevant questions for meateaters and fish-eaters, and 113 relevant questions for vegetarians and vegans) and have a
daily energy intake between 3.3 and 16.7 MJ (800 and 4000 kcal) for men or between 2.1
and 14.7 MJ (500 and 3500 kcal) for women 21; information on smoking and diet group;
follow-up data; no self-reported or prevalent malignant cancer at recruitment; no selfreported history of MI, stroke, or angina at recruitment, or missing information for these
variables; and, not been receiving treatment for a long-term illness at recruitment or missing
information for this variable. In addition, women who were pregnant or using oral
contraceptives or hormone replacement therapy at recruitment were excluded from the
present study. In order to include a wide range of dietary exposures in this cross-sectional
analysis, eligible participants were stratified by sex and 10-year age categories and
approximately equal numbers of participants in each of the four diet groups were randomly
selected within each strata. The final sample includes 424 meat-eaters (168 men, 256
women), 425 fish-eaters (168 men, 257 women), 423 vegetarians (168 men, 255 women),
and 422 vegans (167 men and 255 women in total).
At recruitment or shortly after, participants attended their local general practice surgeries
where a blood sample was taken. Participants were not required to fast prior to the blood
sample. Blood was transported overnight to a laboratory in Norfolk by mail at ambient
temperature, where samples were centrifuged and serum was aliquoted into 0.5 mL plastic
straws. These were heat-sealed at both ends and stored in liquid nitrogen (−196°C) until
2010-2011 and subsequently in electric freezers (−80°C) until analysis later in 2011.
Beckman Synchron CX autoanalyzers (Beckman Coulter, High Wycombe, UK) were used
to measure apolipoprotein A-I and B by immunoturbimetric assay, HDL cholesterol was
measured directly, and total cholesterol was measured by enzymatic assay. Pooled serum
samples (n = 196) were included in each run; the laboratory technicians were blinded to the
diet groups and to the pooled samples. The coefficients of variation were 1.9% for total
cholesterol, 1.9% for HDL cholesterol, 2.8% for apolipoprotein A-I, and 2.6% for
apolipoprotein B.
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STATA Statistical software, release 12 (StataCorp LP; College Station, USA), was used for
all statistical analyses. All analyses were conducted for males and females separately.
Participant characteristics and dietary intakes were compared between diet groups. Chisquared tests were used to test for differences in proportions between diet groups, and for
continuous variables ANOVA was used to test for differences in means between diet groups.
Multiple linear regression was used to calculate the mean serum lipid concentrations in the
four diet groups. In the basic model age (as a continuous variable), alcohol consumption
(continuous), and physical activity (categorical: inactive, low activity, moderate activity, or
high level of activity) were included as covariates; in the second model BMI (continuous)
was also included as a covariate. If there was significant heterogeneity between the four diet
groups, post-hoc pairwise comparisons were used to test for significant differences in serum
lipid concentrations between each of the diet groups, using the Bonferroni adjustment for
multiple comparisons. All p values were two-sided and p < 0.05 was considered statistically
significant.
RESULTS
Selected characteristics and dietary intakes of male and female participants in each diet
group are shown in Table 1 and Table 2. In both males and females, mean BMI differed
significantly between diet groups (p < 0.001, for both). Compared to the other diet groups,
vegans had a lower mean BMI and a much higher proportion of vegans had a BMI of less
than 20 kg/m2 (p for difference between diet groups < 0.001, for all). The distribution of
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physical activity differed significantly between diet groups in males (p = 0.015), but not in
females (p = 0.168). In males, a higher proportion of vegans was considered to be very
active (28.1%) compared to meat-eaters (22.0%), fish-eaters (17.3%) and vegetarians
(17.3%), whereas the proportion of males who were inactive was similar in vegans (19.2%)
and meat-eaters (19.6%), and lower in fish-eaters (11.9%) and vegetarians (12.5%). In both
males and females, compared to the other diet groups, vegans had a lower energy and
alcohol intake, and a lower proportion of energy from saturated fat (p for difference between
diet groups < 0.001, for all). Vegans had a higher fiber intake, and a higher proportion of
energy from carbohydrate and polyunsaturated fat (p for difference < 0.001, for all). Ninetysix percent of participants were of white European origin.
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In the basic model adjusted for age, alcohol intake, and physical activity, in both males and
females, compared to meat-eaters, fish-eaters and vegetarians the mean serum
concentrations of total cholesterol, non-HDL cholesterol, and apolipoprotein B were each
lower in vegans (p for pairwise comparison < 0.001, for all) (Tables 3 and 4). In men,
compared to meat-eaters, vegans had a 0.87 mmol/L lower mean total cholesterol
concentration, a 0.85 mmol/L lower mean non-HDL cholesterol concentration, and an 18
mg/dL lower mean apolipoprotein B concentration. In women, compared to meat-eaters,
vegans had a 0.60 mmol/L lower mean total cholesterol concentration, a 0.49 mmol/L lower
mean non-HDL cholesterol concentration, and an 11 mg/dL lower mean apolipoprotein B
concentration. In women, compared to meat-eaters and fish-eaters, mean HDL cholesterol
was lower in vegans (p for pairwise comparison = 0.001 for meat-eaters vs vegans, and p =
0.014 for fish-eaters vs vegans). In the basic model, there were no statistically significant
differences in the mean apolipoprotein A-I concentration between diet groups in men (p for
difference = 0.690) or women (p = 0.092). In men, there were significant differences in the
ratio of total:HDL cholesterol and in the ratio of apolipoprotein B:apolipoprotein A-I
between the diet groups; in both cases compared to meat-eaters the ratio was lower in the
vegans (p for pairwise comparison < 0.001 for both). In women, there was no statistically
significant difference in the ratio of total:HDL cholesterol between the diet groups (p for
difference = 0.053). However, compared to meat-eaters, the ratio of apolipoprotein
B:apolipoprotein A-I was lower in vegans (p for pairwise comparison < 0.001).
After further adjustment for BMI the differences in serum lipid concentrations between the
diet groups were, in most cases, slightly attenuated (Tables 3 and 4). In men, compared to
meat-eaters, vegans had a 0.76 nmol/L lower mean total cholesterol concentration, a 0.68
nmol/L lower mean non-HDL cholesterol concentration, and a 14 mg/dL lower mean
apolipoprotein B concentration (p for pairwise comparison < 0.001, for all). In women,
compared to meat-eaters, vegans had a 0.55 nmol/L lower mean total cholesterol
concentration, a 0.40 nmol/L lower mean non-HDL cholesterol concentration, and a 9 mg/
dL lower mean apolipoprotein B concentration (p for pairwise comparison < 0.001, for all).
However, the non-significant association between diet group and mean apolipoprotein A-I
concentration in women became significant after further adjustment for BMI (p for
heterogeneity = 0.092 before and p = 0.003 after adjustment for BMI).
DISCUSSION
In this cross-sectional study, which included a large number of vegetarians and vegans,
serum concentrations of total cholesterol, non-HDL cholesterol, and apolipoprotein B were
significantly lower in vegans compared to meat-eaters, fish-eaters and vegetarians. In
women, compared to meat-eaters and fish-eaters, the mean HDL cholesterol concentration
was lower in vegans. In men, there were no significant differences in apolipoprotein A-I
concentrations between the diet groups. In women, after additional adjustment for BMI,
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there were significant differences in apolipoprotein A-I concentrations between the diet
groups; vegans had a lower mean apolipoprotein A-I concentration than meat-eaters.
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Previous studies have also documented lower total cholesterol concentrations in vegetarians
compared to omnivores.5, 6, 22-30 Five studies that included vegans as a separate diet group
observed the lowest total cholesterol concentrations in this diet group, although the number
of vegans in these studies (ranging from 8 to 114) was much smaller than in the present
study (n = 422).6, 22, 24, 29-30
In accordance with our findings on non-HDL cholesterol – the majority of which is LDL
cholesterol – in the Oxford Vegetarian Study serum LDL cholesterol concentrations were
shown to be highest in meat-eaters (n = 1 198), followed by fish-eaters (n = 415),
vegetarians (n = 1 550), and vegans (n = 114).6 Other much smaller cross-sectional studies
carried out in Hong Kong5, Brazil26, 28-29, Taiwan27, and Australia30 also observed higher
LDL cholesterol concentrations in omnivores compared to vegetarians.
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Most previous studies have found no difference in serum HDL cholesterol concentrations
between omnivores and vegetarians.26-29 The study of Hong Kong Chinese by Lee et al.5
found lower HDL cholesterol concentrations in vegetarians (1.20 mmol/L) compared to
omnivores (1.32 mmol/L, p < 0.05). The Oxford Vegetarian Study found significant
differences in HDL cholesterol concentrations between diet groups; HDL cholesterol
concentrations were similar in meat-eaters (1.49 mmol/L), vegetarians (1.50 mmol/L) and
vegans (1.49 mmol/L), but higher in fish-eaters (1.56 mmol/L, p for difference between diet
groups < 0.01).6 Although in our study there were only small differences in HDL cholesterol
concentrations between the diet groups, in males the ratio of total to HDL cholesterol was
lower in vegans compared with meat-eaters and vegetarians, owing to the very low mean
total cholesterol concentration in vegans relative to the other diet groups. In females, the
differences in the ratio of total to HDL cholesterol concentrations between the diet groups
were not statistically significant. Although the ratio of total to HDL cholesterol has been
shown to predict cardiovascular disease risk1, a recent Mendelian randomisation study has
brought into question the view that HDL is causally related to risk of cardiovascular
disease.31 In this Mendelian randomisation study, genetic variants that give rise to a high
HDL concentration were not associated with a reduced risk of myocardial infarction.31
In our study, vegans had a lower BMI than meat-eaters, and there is good evidence that BMI
is positively related to serum non-HDL cholesterol concentrations.32 However, adjustment
for BMI only slightly attenuated the difference in serum lipid concentrations between the
diet groups, indicating that differences in BMI explained only a small proportion of the
differences between the diet groups. However, BMI is not a perfect measure of body
composition, and future studies should include more comprehensive measures of body
composition such as body fat percentage. In our study, vegans had the lowest saturated fat
intakes and the highest polyunsaturated fat intakes. Evidence from metabolic ward studies33
and dietary intervention trials34 demonstrates that isocaloric replacement of carbohydrate
with saturated fat increases serum total and LDL cholesterol concentrations, whereas
isocaloric replacement of carbohydrate with polyunsaturated fat has the opposite effect. In
addition, vegans had a higher mean daily fiber intake than meat-eaters, and fiber may have a
modest cholesterol lowering effect.35 Taken together, these findings strongly suggest that a
large proportion of the difference in serum lipid concentrations between diet groups is
explained by differences in the nutrient composition of the diets, especially differences in
saturated and polyunsaturated fat intakes.
We have recently reported a 32% lower risk of hospital admission or death from ischaemic
heart disease (IHD) in vegetarians and vegans combined, compared to meat-eaters and fish-
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eaters combined.36 The reduced risk of ischaemic heart disease among vegetarians and
vegans combined was shown in both men and women.36 Using the serum lipid
concentrations of meat-eaters and vegans in our study we are able to predict the difference in
IHD mortality between these two distinct diet groups. Data from the Prospective Studies
Collaboration1 indicates that in males, a 0.85 mmol/L difference in non-HDL cholesterol
concentrations (observed between male meat-eaters and vegans in our study) would be
associated with an approximately 37% lower risk of IHD mortality, and in females a 0.49
mmol/L difference in non-HDL cholesterol concentrations (observed between female meateaters and vegans in our study) would be associated with an approximately 25% lower risk
of IHD mortality.
The strengths of this study include the large number of participants, especially vegan
participants, and the inclusion of the apolipoproteins A-I and B in the analysis of lipid
profiles. The sample used in this analysis was randomly selected from the larger EPICOxford cohort, but the EPIC-Oxford cohort was recruited mainly through postal recruitment
targeted toward vegetarians, the health-conscious public and their friends and family
members. We have previously established that the meat-eaters participating in EPIC-Oxford
are healthier than the general British population (most of whom are meat-eaters) 37, but it is
difficult to judge whether our fish-eaters, vegetarians, and vegans are generally
representative of these diet groups in Britain. Nearly all (96%) of the participants in this
analysis were of white European origin, and our findings may not apply to diet groups of
other ethnicities, for example Indian vegetarians. This study was cross-sectional and
therefore we cannot infer causality; however our findings are consistent with meta-analyses
of controlled dietary studies on the effects of saturated and polyunsaturated fats on serum
cholesterol concentrations. We did not directly measure LDL cholesterol, instead we report
non-HDL cholesterol. However, the majority of non-HDL cholesterol is LDL, and non-HDL
cholesterol is an established risk factor for ischaemic heart disease mortality1. We collected
non-fasting blood samples and therefore we did not measure triglycerides.
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In conclusion, this study compares the serum lipid concentrations of British meat-eaters,
fish-eaters, vegetarians, and vegans, and finds lower serum concentrations of total and nonHDL cholesterol in vegans. Vegans also had very low saturated fat intakes, and higher
intakes of polyunsaturated fat and fiber. Variation in the intake of these dietary components
most likely explains a large proportion of the difference in serum lipid concentrations
between diet groups. To the best of our knowledge, this is the first time that serum
concentrations of apolipoproteins A-I and B have been reported for a large number of
vegans. Our results show that vegans had the lowest apolipoprotein B concentrations. In
men, there were no significant differences in apolipoprotein A-I concentrations between the
diet groups. In women, after further adjustment for BMI, apolipoprotein A-I concentrations
were lower in vegans compared to meat-eaters. The serum lipid profile of vegans in our
study would be expected to confer a much lower risk of IHD mortality compared with meateaters.
Acknowledgments
The authors thank the participants of EPIC-Oxford for their contribution to the study. We also acknowledge
Wolfson Laboratories, Clinical Trial Service Unit and Epidemiological Studies Unit, University of Oxford for the
measurement of serum lipid concentrations.
Sources of support: Funding was provided by Cancer Research UK. The funder played no role in designing or
conducting the study or in the collection, management, analysis, and interpretation of the data, nor did they have
any input into the preparation, review, or approval of this manuscript.
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Bradbury et al.
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Table 1
Characteristics of male participants by diet group
Europe PMC Funders Author Manuscripts
Diet group
Meateaters
Fish-eaters
Vegetarians
Vegans
n = 168
n = 168
n = 168
n = 167
p value1
Age category (years)
20 to 29
11 (6.6)
10 (6.0)
11 (6.6)
10 (6.0)
30 to 39
48 (28.6)
48 (28.6)
48 (28.6)
48 (28.7)
40 to 49
63 (37.5)
63 (37.5)
63 (37.5)
62 (37.1)
50 to 59
22 (13.1)
23 (13.7)
23 (13.7)
23 (13.8)
60 +
24 (14.3)
24 (14.3)
23 (13.7)
24 (14.4)
24.9 (3.1)
23.2 (2.9)
23.3 (2.6)
22.4 (3.2)
4 (2.4)
16 (9.5)
9 (5.4)
28 (16.8)
20 to 22.5
34 (20.2)
51 (30.4)
61 (36.3)
64 (38.3)
22.5 to 25
50 (29.8)
56 (33.3)
49 (29.2)
49 (29.3)
25 to 27.5
47 (28.0)
24 (14.3)
27 (16.1)
16 (9.6)
27.5+
33 (19.6)
21 (12.5)
22 (13.1)
10 (6.0)
Inactive
33 (19.6)
20 (11.9)
21 (12.5)
32 (19.2)
Low activity
53 (31.6)
72 (42.9)
61 (36.3)
39 (23.4)
Moderate activity
32 (19.1)
36 (21.4)
46 (27.4)
37 (22.2)
Very active
37 (22.0)
29 (17.3)
29 (17.3)
47 (28.1)
1.00
BMI (kg/m2)
Mean (SD)
< 20
< 0.001
< 0.001
Physical activity
0.015
Daily dietary intakes2
Europe PMC Funders Author Manuscripts
Energy (MJ)
9.25 (2.35)
9.04 (2.32)
9.11 (2.37)
8.00 (2.34)
< 0.001
Protein (% of energy)
16 (2)
14 (2)
13 (2)
13 (2)
< 0.001
Carbohydrate (% of energy)
48 (6)
50 (7)
51 (7)
54 (7)
< 0.001
32 (6)
31 (6)
31 (6)
29 (7)
0.003
Saturated
12 (3)
11 (3)
11 (3)
6 (2)
< 0.001
Monounsaturated
11 (2)
10 (2)
10 (2)
10 (3)
0.003
Polyunsaturated
6 (2)
7 (2)
7 (2)
10 (3)
< 0.001
0.57 (0.26)
0.73 (0.34)
0.73 (0.33)
1.56 (0.39)
< 0.001
19 (7)
23 (8)
23 (7)
27 (9)
< 0.001
