Margine or butter

Butter healthier than
margarine? Nope.
Evidence refuting butter-is-healthy
claims
[Updated January 2016]
Registered dietitian, M.Sc, MBA
Reijo Laatikainen
www.pronutritionist.net
www.pronutritionistblog.com
www.twitter.com/pronutritionist
Page 1

Impetus to this slide deck; pro-butter
doctors in media
• General practioner (GP) John Briffa’s text in Times newspaper
and the followed discussion at his blog
• Cardiologist Aseem Malhotra’s comment on BBC TV Channel
“Butter is healthier than low-fat spreads or margarine”
• Diet Doctor’s, GP Andreas Eenfeldt, posts
• Finnish doctors, such as Antti Heikkilä’s and Taija Somppi’s,
numerous comments in the media
• And more …
www.pronutritionist.net2

My position
• Modern margarines are healthier than butter. However,
margarines are not miraculous. Extra virgin olive oils and canola
oils are very likely healthier than margarine
• Some scientific evidence on dietary fats is controversial
• Butter or saturated fat per se have not been shown to be
superior to modern vegetable oils or margarines in meta-
analyses examining cardiovascular disease, cancer or type 2
diabetes
• There is enough scientific evidence to refute the claim ”butter is
healthy”
•

First, some scientific data that is
often emphasized by pro-butter
doctors

Siri-Tarino’s meta-analysis of prospective
cohorts: Saturated does not increase the
risk of coronary heart disease risk nor does
it reduce the risk
Siri-Tarino PW et al. Am J Clin Nutr (January 13, 2010). doi:10.3945/ajcn.
5

Chowdhury’s meta-analysis of prospective,
observational studies and randomized,
controlled trials.
Chowdhury R, Warnakula S, Kunutsor S, et al. Association of dietary, circulating, and
supplement fatty acids with coronary risk. A systematic review and meta-analysis. Ann
Intern Med 2014; 160;398-406
6
“Conclusion: Current evidence does not clearly
support cardiovascular guidelines that encourage
high consumption of polyunsaturated fatty acids
and low consumption of total saturated fats.”

Sydney Diet Heart Study: Cardiac mortality
was increased in vegetable oil/margarine
group (re-evaluation of the study published
originally 1978 )
Page 7
74 %
increased
risk in PUFA
group
PUFA
Safflower oil/margarine
Control Diet, high in SFA
Ramsden CE, Zamora D, Leelarthaepin B, Majchrzak-Hong SF, Faurot KR, Suchindran CM, et al. Use of dietary linoleic
acid for secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet
Heart Study and updated meta-analysis. BMJ 2013;346:e8707

Risk of death is not increased nor
reduced among butter users. Meta-
analysis of prospective cohorts
8
O’Sullivan T et al. Food sources of saturated fat and the association with mortality: a meta-analysis. Am J
Public Health. 2013;103:e31-42
1,17* 1,21*
1.01 1.03
0,96**
0
0.2
0.4
0.6
0.8
1
1.2
1.4
Meat Processed meat Milk Cheese Butter
*) p<0,001, **) p=0,5 (not significant)

The rest of this slide deck depicts
scientific evidence which pro-
butter doctors usually dismiss or
downplay

Point #1
World has changed since 1970s when
Sydney Diet Heart Study and many other fat
replacement studies were done.

1960 1970 1990 2013
Era of the pivotal fat modification trials
Oslo Diet
Heart 1958-
1964
MRC Soy 1968
STARS 1992
Minnesota
Coronary Survey
1968-1973
LA Veterans
1969
DART 1989
Rose Corn Oil
1965
Margarines per se and use of oils have
changed since 1970s
*) if not given, the publication date
Sydney Diet
Heart Study
1966-73

You cannot translate data from 1960’s
directly to modern world because
margarines per se, use of oils and
background diet has changed
dramatically

Sunflower
oil /100 g
Corn oil
/100 g
Soy oil /
100 g
Canola oil
/100 g
Olive oil /
100 g
Linoleic acid
(omega-6)
62 g 53 g 52 g 22 g 10 g
ALA (omega-
3)
0,5 g 1 g 7 g 11 g 0,5 g
PUFA 63 g 54 g 59 g 33 g 11 g
SFA 11 g 13 g 15 g 6 g 14 g
MUFA 22 g 27 g 22 g 60 g 68 g
Oils of 1970s have different fatty
acid composition
Oils losing market share Modern dominating oils

By using canola oil instead of sunflower oil
you’ll get >20 times more omega-3 fats. In
addition you don’t even get half of the
amount of omega-6 linoleic acid
In 1970s sunflower, corn, soy and other omega-6 rich oils were used in clinical
trials. Canola oil and olive oil are dominating clinical trials today. They also
dominate European cuisines

IN ADDITION. MARGARINES
ARE WAY BETTER TODAY

Modern margarines in UK, or in most
European countries, do not commonly
contain trans fat. Boy, it was a different
story in 1970s
21.8 %
0.22%
0.0 %
5.0 %
10.0 %
15.0 %
20.0 %
25.0 %
Margarines 1970s* Margarines 2012 (UK)**
Median trans fat content of tube
margarines/spreads
*) Beare-Rogers JL et al. The linoleic acid and trans fatty acids of margarines. Am J Clin Nutr. 1979
Sep;32(9):1805-9.
**) Roe M, et al Trans fatty acids in a range of UK processed foods. Food Chem. 2013 Oct 1;140(3):427-31. .
← 1970s vs now →

Median trans fat content of margarines
is currently very low. Finland today vs
US 1970s
1970s
(US*)
2012
(FIN**)
Trans fat content
of margarines
21.8% 0.34%
*) Beare-Rogers JL et al. The linoleic acid and trans fatty acids of margarines. Am J
Clin Nutr. 1979 Sep;32(9):1805-9.
**) Ritvanen, T., Putkonen, T. , Peltonen, K. A comparative study of the fatty acid
composition of dairy products and margarines with reduced or substituted fat content.
Food and Nutrition Sciences, Vol. 3, 2012, pp. 1189-1196

Trans fat content of
margarines/spreads has plummeted
during the last 50 years
Source: Ravinder Reddy, American Heart Association. Trans Fat Conference. October 10-11, 2006
Trans fat
Saturated fat
PUFA
Omega-3

Point #2
Meta-analyses of the classic fat replacement
trials have shown that combination of omega-
3 fatty acids and omega-6 linoleic acid reduce
cardiovascular mortality

Meta-analysis: high intake of both linoleic
acid AND omega-3 fats reduce cardiovascular
deaths by 21 % in randomized trials.
Ramsden CE, Zamora D, Leelarthaepin B, Majchrzak-Hong SF, Faurot KR, Suchindran CM, et al. Use of dietary linoleic acid for
secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet Heart Study and updated
meta-analysis. BMJ 2013;346:e8707.

Supplementing omega-3 fats alone
does not reduce cardiac deaths. Meta-
analysis
• ”Overall, omega-3 PUFA supplementation was not
associated with a lower risk of all-cause mortality, cardiac
death, sudden death, myocardial infarction, or stroke
based on relative and absolute measures of association”
Rizos EC, et al. Association between omega-3 fatty acid supplementation and risk of major
cardiovascular disease events: a systematic review and meta-analysis. JAMA. 2012 Sep
12;308(10):1024-33

Guidelines recommend increase in
both omega-3 fatty acids and omega-6
linoleic acid intake
• Dietary recommendations underline the adequate
intake of BOTH omega-3 AND omega-6 fatty acids
(linoleic acid), exactly in the line with the beneficial
outcomes of meta-analysis by Ramsden 2013
• You can increase your intake of omega-3 fatty acids
by using canola oil, walnuts and oily fish without fear
of increasing too much linoleic acid intake; exactly as
the nutrition recommendations tell us to do

Point #3
Sydney Diet Heart Study has important
limitations
(This study is the only randomized study
showing increased cardiovascular mortality
on vegetable oils/margarine)

Lead investigator of Sydney Diet Heart
Study, Chris Ramsden:
“The really important limitations were; …
2) The median intake of omega-6 linoleic acid was
almost 15% of calories. In the United States,
consumption of omega-6 linoleic acid has increased
from about 2% of calories in the early 20th century to
about 7% of calories currently. So in the SDHS [Sydney
Diet Heart Study] it ended up approximately twice as
much as the average American consumes nowadays.”
The PUFA Investigation: An Expert Interview
Linda Brookes, MSc, Christopher E. Ramsden, March 18, 2013
www.medscape.com

New systematic review: median global
intake of linoleic acid (LA) 5,5 E %
Harika RK, Eilander A, Alssema M, Osendarp SJ, Zock PL. Intake of Fatty Acids in General Populations
Worldwide Does Not Meet Dietary Recommendations to Prevent Coronary Heart Disease: A Systematic Review
of Data from 40 Countries. Ann Nutr Metab. 2013 Oct 29;63(3):229-238

Margarines used at time of Sydney Diet
Heart Study contained trans fat 12-65
% of all fatty acids
Beare-Rogers JL et al. The linoleic acid and trans fatty acids of margarines. Am J Clin Nutr. 1979 Sep;32(9):1805-
9.

Different realities 1970s vs NOW
Omega-6 linoleic
acid intake as of
total calories
Trans fat content of
margarines
In Sydney Diet Heart Study,
ie. 1970s
15% ~20%
Now 5.5% <1% (at least in
Western Europe)

Point #4
Use of either olive oil, margarine or soy oil
alone, or as a part of multifactorial
intervention has reduced cardiovascular
morbidity/mortality

In 4 large successful randomized
trials, butter and saturated fat
reduction has been the key
Study Fat given for
free to active
group
Comment
Los Angeles Veterans
Administration Study
Corn, Safflower,
sunflower and
soy oil (mix)
Pure fat replacement study. Combined
fatal strokes, amputations and heart
attacks reduced by 31%. (p<0,05)
Lyon Diet Heart
Study
Margarine Med Diet Study, ie multifactorial design
but only canola oil based margarine given
for free. Cardiovascular mortality reduced
by 76% (p=0,029)
Oslo Diet Heart Study Soy oil (and oily
fish occasionally)
Multifactorial design but only oil and some
oily fish given for free. Fatal heart attacks
reduced by 56% (p=0,029)
Predimed Olive oil (extra
virgin olive oil
group)
Med Diet Study, ie multifactorial design
but only fats given for free. Cardiovascular
events reduced by 30%

Summary on large randomized CVD
trials
Favoring
saturated fat
Draw Favoring
vegetable
oils and/or
margarine
Name of the
study
Sydney Diet
Heart Study
DART,
Minnesota CS,
MRC Soy, St
Thomas
Atherosclerosis
, Rose Corn Oil
Los Angeles
Veterans, Oslo
Diet Heart,
Lyon Diet
Heart,
Predimed
Number of
randomized
studies
(w/mortality or
morbidity end
points)
1 5 4

Point #5
Margarine, canola oil and olive oil all induce better
total cholesterol/HDL –ratio and apoB levels than
butter. This is proven at the level of meta-analysis.
If you replace butter with oils/margarine you win. Also
if you replace carbohydrates with oils/modern
margarine you win. But you lose or have a draw if you
replace carbohydrates with butter.

Total cholesterol is strong risk factor
for ischemic heart disease (IHD)
mortality but total cholesterol/HDL –
ratio is even stronger
Prospective Studies Collaboration,. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-
analysis of individual data from 61 prospective studies. Lancet. 2007 Dec 1;370(9602):1829-39.
e studies with 55,000 vascular deaths.
,
Total cholesterol as
a risk marker
Total cholesterol/HDL
as a risk marker

Meta-analysis: Canola oil and even
margarine produce clearly better Total
Cholesterol/HDL ratios than butter
33
Mensink et al. Effects of dietary fatty acids and carbohydrates on the ratio of serum total to
HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled
trials. Am J Clin Nutr. 2003 May;77(5):1146-55.
Canolaoil=

Effects of replacing potatoes with
butter or canola oil in an isocaloric
situation
34
?

-9.3 %
-0.7 %
0.4 %
2.8 %
6.8 %
-12.0 %
-10.0 %
-8.0 %
-6.0 %
-4.0 %
-2.0 %
0.0 %
2.0 %
4.0 %
6.0 %
8.0 %
Carbohydrate Protein* PUFA MUFA SFA
Change in macronutrient intake when 10% of daily energy as carbs
(boiled potatoes) is replaced by animal fat (butter)
Changes in macronutrient intake when
butter replaces potatoes
35
*Protein is considered neutral in the following calculations (no data in Mensink). Therefore actual
amount of carbs replaced is 9.3 E%-0.7 E%= 8.6 E%. It follows that the ‘replaceable’ fat intake is
also reduced by 0.7 E%, and this reduction is splitted to all 3 fatty acid classes in the following
calcutions.

Changes in macronutrient intake when
canola oil replaces potatoes
36
-9.3 %
-0.7 %
2.8 %
6.4 %
0.7 %
-12.0 %
-10.0 %
-8.0 %
-6.0 %
-4.0 %
-2.0 %
0.0 %
2.0 %
4.0 %
6.0 %
8.0 %
Carbohydrate Protein PUFA MUFA SFA
Change in macronutrient intake when 10% of daily energy as carbs
(boiled potatoes) is replaced by canola oil

Change in LDL when potatoes are
replaced with butter or canola oil
37
0.1808
-0.0883
-0.15
-0.1
-0.05
0
0.05
0.1
0.15
0.2
Carbs replaced by butter Carbs replaced by canola oil
Change in LDL (mmol/L)
mmol/L (For mg/DL multiply by 38.67)
Mensink RP, Zock PL, Kester AD, Katan MB. Effects of dietary fatty acids and carbohydrates on
the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-
analysis of 60 controlled trials. Am J Clin Nutr. 2003 May;77(5):1146-55 (calculated from Table 1)

Change in HDL when potatoes are
38
0.087
0.0694
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09
0.1
Change in HDL (mmol/L)
mmol/L (For mg/DL multiply by 38.67)

Change in total cholesterol:HDL –ratio
when potatoes are replaced with butter
or canola oil
39
-0.0545
-0.2403
-0.3
-0.25
-0.2
-0.15
-0.1
-0.05
0
Change in TOT CHOL:HDL -ratio

Change in apoB when potatoes are
40
2.88
-48
-60
-50
-40
-30
-20
-10
0
10
Change in apoB (mg/L)
mg/L

Point #6
Replacing saturated fat with polyunsaturated
fat (PUFA) reduces coronary heart disease
mortality in prospective cohorts

Pooled analysis of 11 prospective cohorts:
“replacing SFAs with PUFAs rather than MUFAs
or carbohydrates prevents CHD [Coronary Heart
Disease]”
Page 42
Jakobsen M et al. Major types of dietary fat and risk of coronary heart disease: a pooled analysis of 11 cohort
studies. Am J Clin Nutr. 2009 May;89(5):1425-32.
replace
SFA: Saturated fat; PUFA: Polyunsaturated fat, ie. Omega-6 and
omega-3 fatty acids

1.1.2016
43
-21 %
-9 %
“Comparing the highest to
the lowest category, dietary
linoleic acid was associated
with 21% lower risk of CHD
deaths”
Farvid MS, Ding M, Pan A, Sun Q, Chiuve SE, Steffen LM, Willett WC, Hu FB.. Dietary
Linoleic Acid and Risk of Coronary Heart Disease: A Systematic Review and Meta-Analysis
of Prospective Cohort Studies. Circulation. 2014;130(18):1568-1578
“A 5% of energy
increment in linoleic acid
intake replacing energy
from saturated fat intake
was associated with a
9% lower risk of CHD
events”
“A 5% of energy
increment in linoleic acid
intake replacing energy
from saturated fat intake
was associated with a
13% lower risk of CHD
deaths “
-10 %
Meta-analysis of 13 prospective cohorts
published between 1992-2011: linoleic acid
(prominent PUFA) is associated with reduced
risk of CHD.

Point #7
Omega-6 fats are not pro-inflammatory in
humans in contrast to common claims by pro-
butter doctors

Meta-analysis of 15 clinical trials
• ” This review clearly demonstrates that virtually no
data are available from randomized, controlled
intervention studies among healthy, noninfant human
beings to show that the addition of LA [linoleic acid] to
diets increases markers of inflammation.”
• Linoleic acid does not even increase arachidonic acid (AA)
levels because conversion to AA is extremely low. Only 0.3-
0.6% of linoleic acid is converted to AA in humans
Johnson & Fritsche. Effect of Dietary Linoleic Acid on Markers of Inflammation in Healthy Persons: A
Systematic Review of Randomized Controlled Trials. Journal of the Academy of Nutrition and Dietetics
2012; 112: 1029-1041
Rett & Whelan. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults
consuming Western-type diets: a systematic review. Nutr Metab (Lond). 2011 Jun 10;8:36

Butter and saturated fat per se pose
either deleterious or neutral effects on
inflammation
• Butter induced pro-inflammatory changes versus sunflower oil in clinical trial
– Bjermo H, et al. Effects of n-6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation
in abdominal obesity: a randomized controlled trial. Am J Clin Nutr. 2012 May;95(5):1003-12.
• ”Consumption of a saturated fat reduces the anti-inflammatory potential of HDL”
– Nicholls SJ, et al. Consumption of saturated fat impairs the anti-inflammatory properties of high-density
lipoproteins and endothelial function. Margarine reduces post-prandial inflammation in proportion to
butter J Am Coll Cardiol. 2006 Aug 15;48(4):715-20
• Exchanging SFA from butterfat for sunflower oil in a mixed meal decrease
postprandial concentrations of IL-6, TNFα, sTNFr-I and -II, and sVCAM-1 in
overweight men.
– Masson CJ, Mensink RP Exchanging saturated fatty acids for (n-6) polyunsaturated fatty acids in a
mixed meal may decrease postprandial lipemia and markers of inflammation and endothelial activity in
overweight men.. J Nutr. 2011 May;141(5):816-21.)
• Sterol containing margarine and butter produce similar effects on inflammatory
markers
– Gagliardi AC et al. Effects of margarines and butter consumption on lipid profiles, inflammation
markers and lipid transfer to HDL particles in free-living subjects with the metabolic syndrome. Eur J
Clin Nutr. 2010 Oct;64(10):1141-9.

Point #8
Omega-6 fats are not associated with cancer
in contrast to claims by pro-butter doctors.
Results from meta-analyses

Very high intake of linoleic acid. No
increase in cancer risk in clinical trials
Zock PL, Katan MB. Linoleic acid intake and cancer risk: a review and meta-analysis. Am J Clin Nutr. 1998
Jul;68(1):142-53.

Meta-analyses by World Cancer Research
Fund: Omega-6 fats not linked to cancer. If
anything, butter is linked to lung cancer
(limited evidence)
World Cancer Research Fund / American Institute for Cancer Research.
Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective.
Washington DC: AICR, 2007

Point #9
Lower intake of saturated fat during low carb
diet improves parameters of cardiovascular
health, when the major source of protein is
beef

Ronald Krauss with co-workers:
lowering SFA content of low carb diet
improves cardiovascular risk profile
Run in period Low SFA + Low
carb diet high in
beef
High SFA + Low
carb diet high in
beef
TG, mmol/l 1,22 1.0 1.1
LDL, mmol/l 2,87 2.5* 2.86*
HDL, mmol/l 1,08 1.04* 1.07*
Small LDL, nmol/l 207 187* 222*
Medium LDL, “ 284 214* 304*
Large LDL, “ 698 655 712
ApoB, g/l 0,74 0.68* 0.73*
*) p<0.05 low vs high SFA diets
http://twitter.com/pronutritionistPage 51
Mangravite LM, Chiu S, Wojnoonski K, Rawlings RS, Bergeron N, Krauss RM. Changes in atherogenic dyslipidemia induced by
carbohydrate restriction in men are dependent on dietary protein source.J Nutr. 2011 Dec;141(12):2180-5
“… reductions in the other lipoprotein-related risk factors, including apoB and small LDL, were
greatest following consumption of a Low Carbohydrate Low Saturated Fat Diet”

Point #10
Scientific data in the field of nutrition is almost
never perfectly clear due to very complex
interplay of nutrients, phytochemicals,
cooking methods, biological variation and
research methods.
You either accept this or deny it. Choice is
yours

Dietary pattern loaded with butter
is likely to be unhealthier than
otherwise similar food pattern with
vegetables oils or margarine as
main edible fat.
However, used sparingly, butter is
far from poison
53

Wellcome aboard!
http://twitter.com/pronutritionist
http://www.facebook.com/pronutritionist
http://www.pronutritionist.net
Reijo Laatikainen, RD, MBA
Images bought and licensed from BigStockPhoto. Snapshots from papers and sites refered to.
Page 54

1. Randomized mortality &
morbidity trials
2. Prospective cohorts
3. Randomized risk
marker studies
4. Cross-sectional and
case-control cohorts
5 Ecological & animal
studies
Strengthofevidence Meta-analyses of 1,2 & 3
Modified from: Micha & Mozaffarian.
Lipids. 2010; 45(10): 893–905 and
Evidence Analysis Manual.
Academy of Nutrition and Dietetics
January 2012

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