CSIRO PUBLISHING

Animal Production Science, 2014, 54, 831–855 Perspectives on Animal Biosciences

http://dx.doi.org/10.1071/AN13536

Should animal fats be back on the table? A critical review

of the human health effects of animal fat

William Barendse

CSIRO Animal, Food and Health Sciences, 306 Carmody Road, St Lucia, Qld 4067, Australia.
School of Veterinary Science, University of Queensland, Gatton, Qld 4343, Australia.
Email: Bill.Barendse@csiro.au

Abstract. Humans hunt or raise a wide variety of animals for meat, which vary from free-range to intensively reared. These
animals form a valuable part of human nutrition. Their tissues, including the fat, contain vitamin and other essential nutrients
necessary for health. However, animal fat from ruminants and other land mammals is usually regarded as saturated. The
purpose of this review is partly to examine the basis for the saturated fat hypothesis of cardiovascular disease given more
recent research, to examine the human health effects of animal fats, and partly to draw into one place the diverse knowledge
about animal fat and the effects of fat on metabolism. Mechanistic understanding of the initiation of the fatty streak and
atherosclerosis calls into question the avoidance of ruminant or porcine fat. Due to high levels of oleic acid, a low n-6 : n-3
fatty acid ratio in some groups, and the presence of specific micronutrients including vitamins and essential fatty acids, animal
fats are of benefit in human nutrition. Animal fats can be obtained in minimally processed form making them a convenient
source of energy and micronutrients.

Additional keywords: cardiovascular disease, docosahexaenoic acid (DHA), ketogenic, obesity, saturated fat.

Submitted 13 December 2013, accepted 27 March 2014, published online 5 May 2014

Introduction agents in chronic disease. Many observers have noted that the
What butter and whiskey will not cure there’s no cure trend of usage of animal fats has been in the opposite direction to
for – Irish Proverb the rise in CVD or obesity (Yudkin 1957; Antar et al. 1964;
Kritchevsky 1976; Enig et al. 1978; Blaxter and Webster 1991;
‘For example, in Framingham, Mass, the more saturated fat one Eisenmann 2003; Carlson et al. 2011; Chapman et al. 2011).
ate, the more cholesterol one ate, the more calories one ate, the Furthermore, with the discovery of the effects on CVD of
lower the person’s serum cholesterol.’ – William Castelli, 3rd industrial trans fats, animal fats have made a resurgence in the
Director of the Framingham Heart Study (1992). popular literature, on the internet, and in low carbohydrate diet
Humans have used animals and animal products for food books (Taubes 2001, 2007). The diet wars of the 1960s and 1970s
including fish, seafood, insects, birds, reptiles, and mammals have reappeared (Yudkin 1964; Keys 1971), with a renewed focus
since time immemorial. These are either caught wild, are on the effects of sucrose and fructose in obesity, CVD, cancer and
harvested as free-range animals, or are raised at varying type 2 diabetes as opposed to fat (Miller et al. 2011; Hoenselaar
degrees of intensity for a wide range of markets. They are a 2012; Lustig et al. 2012; Basu et al. 2013). There is a renewed
source not only of nutrition but also of gustatory pleasure, and popularity of low carbohydrate high fat diets, as well as the
many are symbols or are eaten during special occasions. But, with scientific study of them (Foster et al. 2003; Volek et al. 2003;
high rates of cardiovascular disease (CVD) and, more recently, Yancy et al. 2004). Indeed, it now appears that genes contribute
high rates of obesity in the West, first fat of all kinds and then to whether one will drop out of a low calorie diet depending on
saturated fat have been put under the microscope as aetiological whether it is low fat or high fat (Grau et al. 2009). Despite these

William Barendse is a senior principal research scientist at CSIRO Animal, Food and Health Sciences and an adjunct Professor in the School of
Veterinary Science, the University of Queensland. Bill was born in Cape Town, South Africa, came to Perth as a teenager, and finished a Bachelor’s
Degree in Science in the Zoology Department of the University of Western Australia. That led to a PhD in the same department, in Genetics and Systematics of
the species Mygalopsis, with Mike Johnson. A Macquarie University Fellowship followed, to study the human disorder pre-eclampsia with Des Cooper,
which introduced him to Molecular Genetics and Linkage Analysis. That led to a position in Rockhampton with CSIRO Tropical Animal Production to
make a linkage map of the cow, in Jay Hetzel’s group. The cow maps acted as the seed for the genome sequence and genetic history of the cow, to which he
contributed. He and his group have been involved in the mapping of genes affecting production traits of cattle. These include the Calpastatin gene for
meat tenderness. Since 1994, he has been studying marbling of beef and fatness of cattle, which has led almost inexorably to this review. He has authored
or co-authored more than 140 refereed articles in the primary scientific literature.

Journal compilation
CSIRO 2014 www.publish.csiro.au/journals/an

832 Animal Production Science W. Barendse

changes in society, high quality food has always featured animal CISFA (Couvreur et al. 2006) and would raise serum cholesterol
fats because of their taste and during the past 40 years there has despite butter having a total of more than 60% SFA. Butter differs
been no deviation from that practice (Escoffier 1921; Bocuse from other animal fats in having a large amount of short- and
1988; Carluccio and Contaldo 2012). The purpose of this review medium-chain SFA, which are rapidly oxidised by the liver
is to investigate whether there are any health benefits in putting instead of being stored in adipose tissue or transported by
animal fats back on the table. lipoprotein cholesterol particles (Bach and Babayan 1982;
One justification for the unrestricted use of animal fats is DeLany et al. 2000) – the amount of palmitate in butter is
the archaeological, ethnographic, and historical evidence that similar to other animal fats. The distinguishing features of
for 1–2 million years before the invention of agriculture humans most animal fats, compared with most plant oils, is the low
were omnivorous hunter-gatherers consuming animal tissues variability in proportion of palmitate to the total amount of
including fat (Richards and Trinkaus 2009; Sponheimer and FA, compared with the large range in proportion of other FA,
Dufour 2009; Stiner and Munro 2011; Ungar and Sponheimer the relatively large proportion of FA with odd number of carbons
2011). Some humans still occupy this niche, and their hunting and in the acyl backbone or with variable numbers and locations of
gathering habits have been documented (Murdock 1967; Cordain unsaturated bonds, and the low to very low levels of n-6
et al. 2002a; Rouja et al. 2003). Organs and fat were generally polyunsaturated fatty acids (PUFA), especially in ruminant fat.
preferred to lean meat by these hunter-gatherers who were well
aware of the value of eating animal fat: the side effects of eating
only lean meat have been replicated in the laboratory and they The effects of fat on human blood lipids
include diarrhoea and unsatisfied hunger (Stefansson 1912; Fat and cholesterol are carried by chylomicrons and lipoprotein
McClellan and Du Bois 1930; Phinney 2004). During human cholesterol particles in circulation, and because serum cholesterol
evolution, how much fat was eaten on a daily or yearly basis is a has been associated with risk of CVD, fat intake has been
matter for speculation, and would depend on a host of factors. implicated in CVD, although detailed analyses show results
Given the nausea limit in human responses to large amounts of fat contrary to this expectation. The effect of different FA on the
(Man and Gildea 1932), one suspects as much fat as could be average TSC of the sample, its sub-fractions, fasting
stomached. These ancestral patterns of food use do not prescribe triacylglycerides (FTG) and the number and size of low
any particular modern diet or lifestyle but they do show the likely density lipoprotein cholesterol (LDL-C) particles have been
human nutritional adaptations and responses to food, and point to determined on largely inactive people in studies in metabolic
the nutrients that need to be obtained from food (Cordain et al. wards. The description of these average changes in TSC and FTG
2005; Lindeberg 2009). have been studied for more than 50 years, they are well known and
are predictable using the Keys equation (Man and Gildea 1932;
Saturated fat and cardiovascular disease Havel et al. 1955; Ahrens et al. 1957; Havel 1957a, 1957b; Keys
et al. 1957, 1965; Albrink and Man 1959; Kuo and Carson 1959;
The degree of saturation of animal fat Grande et al. 1970; Acheson et al. 1988; Tholstrup et al. 1994a,
Although animal fats are described as saturated and containing 1994b; de Roos et al. 2001; McDevitt et al. 2001; Mensink et al.
cholesterol, apart from butter and some fatty fish, animal fat 2003; Matthan et al. 2004; Chapman et al. 2011; Miller et al.
is best described as monounsaturated either by content or by 2011). These changes can be summarised by saying, first, that
function (Table 1) for its effect on serum cholesterol. First, dietary substituting MUFA and stearic acid for starch causes no change
cholesterol makes a second order contribution to serum in the average serum cholesterol of a population sample,
cholesterol, that is, its effect is proportional to the square root although LDL-C concentration decreases while high density
of dietary intake, leading to minor changes in serum cholesterol, lipoprotein cholesterol (HDL-C) concentration increases.
its importance has been debunked, and it has long been ignored in Second, average serum cholesterol is increased as the
prediction of CVD risk (Keys et al. 1965, 1974). Second, as can be proportion of CISFA increases and is decreased as the
seen from the table, the major component of the triacylglycerol proportion of PUFA increases. The increases due to CISFA
(TAG, triglycerides) of animal fat is monounsaturated fatty acid are twice the size of decreases due to PUFA for each unit of
(MUFA), mostly oleic acid, irrespective of how solid the fat is at CISFA or PUFA. Third, HDL-C and FTG of an individual are
room temperature, and in some cases oleic acid consists of more inversely related, so high FTG is usually correlated with both
than 50% of all fatty acids (FA). Even when oleic acid is less than low HDL-C and a pattern of low fat plus high carbohydrate
50% of all the FA, there are other MUFA and FA that do not affect intake. High FTG is strongly correlated with small dense LDL-C,
overall serum cholesterol. As an example from one of the hardest to expanded waistlines and to other features of the metabolic
animal fats, approximately only 27% of tallow from pasture-fed syndrome, which is strongly predictive of increased risk of CVD
beef is cholesterol-increasing saturated fatty acid (CISFA) (Castelli 1986; Boerwinkle et al. 1994; Gardner et al. 1996;
(Yang et al. 1999b), i.e. chain length of 12–16 carbons, and Stampfer et al. 1996; Lamarche et al. 1997; Barrows and Parks
which would raise serum cholesterol, 1% is polyunsaturated, ~4% 2006; Roberts et al. 2008). While serum cholesterol and,
is conjugated linoleic acid (CLA), and the rest is either MUFA or particularly, LDL-C concentrations of the individual are used
is the saturated fatty acid (SFA) stearic acid that causes the same to calculate risk of CVD, of more importance to the mechanistic
effect on total serum cholesterol (TSC) as MUFA (Keys et al. development of CVD is the size and number of LDL-C particles in
1965; Grande et al. 1970; Bonanome and Grundy 1988; Tholstrup circulation and the composition of cholesteryl-esters (cf. below).
et al. 1994a, 1994b; de Roos et al. 2001; Mensink et al. 2003). By An overview of fat and cholesterol transport is shown in Fig. 1
comparison, in butter from pasture-fed cows, 42% of the fat is and shows five major phases that are each affected by dietary and
 Table 1. Percentage fatty acid composition of a range of fats and oils
SCF, subcutaneous fat. Other, dependent on species, mainly other monounsaturated fatty acids and small amounts of long-chain polyunsaturated fatty acids (PUFA) and odd-numbered SFA in land animals,
conjugated linoleic acid in ruminants, and long-chain n-3 PUFA in salmon
Animal fats back on the table

Fatty acid <C12:0 C12:0 C14:0 C16:0 C18:0 C18:1 C18:2 (n-6) C18:3 (n-3) Other Reference
Animal
Butter pasture 10.8 3.5 10.9 24.3 11.2 21.6 1.26 0.70 15.74 Couvreur et al. (2006)
Butter corn silage 11.9 3.8 11.8 31.0 10.3 19.4 1.55 0.22 10.03 Couvreur et al. (2006)
Beef SCF pasture – – 3.3 23.4 11.1 43.6 0.70 0.42 17.48 Yang et al. (1999b)
Beef SCF feedlot 100 days – – 3.4 26.2 13.7 41.7 1.00 0.13 13.87 Yang et al. (1999b)
Deer bone marrow – – 0.8 16.3 4.7 54.1 2.35 1.49 20.20 Cordain et al. (2002b)
Antelope SCF – – 3.6 24.0 34.3 24.1 1.73 1.14 11.13 Cordain et al. (2002b)
Elk SCF – – 5.5 34.7 23.3 17.5 1.61 1.12 16.18 Cordain et al. (2002b)
Free-range pig backfat – – 1.1 19.0 8.1 56.4 8.73 0.56 6.11 Rodríguez-Sánchez et al. (2010)
Wild boar intramuscular fat – – 0.9 24.0 10.3 41.1 12.04 0.42 11.24 Razmaite et al. (2011)
Free-range chicken – – 0.8 26.5 6.3 39.6 14.40 1.64 10.76 Givens et al. (2011)
Intensive chicken – – 1.1 21.3 6.0 36.8 22.87 3.75 8.18 Givens et al. (2011)
Intensive duck intramuscular fat – 0.4 0.5 23.4 7.5 43.5 13.49 0.64 10.57 Chartrin et al. (2006)
Atlantic salmon (farmed-fed fish meal) – – 4.2 12.6 2.4 12.0 2.39 1.19 65.22 Sanden et al. (2011)
Margarines
Corn/soy stick – – – 10.5 7.8 48.4A 27.8 2.5 3.0 http://nutritiondata.self.com/facts/fats-and-oils/
635/2 (verified 20 March 2014)
Canola Harvest soft spread – 1.5 0.1 9.2 2.3 54.3 18.0 8.4 6.2 http://nutritiondata.self.com/facts/fats-and-oils/
10038/2 (verified 20 March 2014)
Plant
Canola oil – – – 4.2 1.5 58.6 21.4 10.9 3.4 Ackman and Sebedio (1981)
Cocoa butter – – – 26.2 35.8 33.6 2.7 0.8 0.9 Lipp et al. (2001)
Coconut oil 21.3 48.2 14.6 6.9 2.0 4.5 1.4 0.1 1.0 Bézard et al. (1971)
Olive oil – – – 12.1 2.7 71.8 10.2 0.7 2.5 Van Niekerk and Burger (1985)
Palm oil – – 1.1 43.7 4.5 39.3 10.1 0.2 5.3 Van Niekerk and Burger (1985)
Peanut oil – – – 11.2 3.7 41.1 35.5 0.1 8.4 Van Niekerk and Burger (1985)
Shea butter – – – 3.4 40.8 46.3 6.6 0.1 2.8 Di Vincenzo et al. (2005)
Soybean oil – – – 9.5 4.9 21.9 52.6 7.9 3.2 Van Niekerk and Burger (1985)
Sunflower oil – – – 6.1 5.6 19.3 67.0 0.1 1.9 Van Niekerk and Burger (1985)
A
One-third of this was trans C18:1.
Animal Production Science
833
834 Animal Production Science W. Barendse

Fig. 1. The main dietary influences on the transport of fatty acids in the body. Bold arrows represent transport of lipids, either in lipoprotein cholesterol particles or
bound to albumin. Narrow arrows represent transport of carbohydrate or polar lipids dissolved in serum. Blue arrows represent increases in proteins or particles
relevant to blood cholesterol resulting from dietary manipulation. SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty
acid; NEFA, non-esterified fatty acid; UFA, unsaturated fatty acid; LC, long-chain; CLA, conjugated linoleic acid; CHO, carbohydrate; DNL, de novo lipogenesis;
TRLR, triglyceride-rich lipoprotein remnant; TAG, triacylglycerol (triglycerides); FTG, fasting triglycerides; apo, apolipoprotein; HDL-C, high density
lipoprotein cholesterol; LDL-C, low density lipoprotein cholesterol; VLDL-C, very low density lipoprotein cholesterol; LDLR, low density lipoprotein receptor;
LRP1, low density lipoprotein receptor-related protein 1; SCARB1, scavenger receptor B1; LPL, lipoprotein lipase.

genetic factors. These phases are (1) the entry of FA into remnants and from that synthesised in the liver, requires apoB-
enterocytes and the formation of chylomicrons, (2) the 100, apoC, and apoE for transport (Utermann 1988). As these
transport of fat and cholesterol via chylomicrons in the mature to LDL-C, the apoC and apoE proteins and cholesterol are
circulation to tissues, (3) the processing of chylomicron lost to HDL-C, leaving only apoB-100 as well as progressively
remnants by the liver and the formation of very low density depleted LDL-C (Chapman et al. 2011). The longer the LDL-C
lipoprotein cholesterol (VLDL-C) in the liver, (4) the transport particle stays in circulation the smaller and denser it becomes.
of fat and cholesterol via VLDL-C and its remnant, LDL-C, to HDL-C is part of the reverse transport of cholesterol, carrying it
tissues, and (5) the release of FA from adipocytes to be carried on back to the liver where it is recycled (Fielding and Fielding 1995).
albumin to tissues via the blood (Chapman et al. 2011). Starting Particles with apoE are taken up faster than particles with only
with the enterocytes, for cholesterol and fat transport, the HDL-C apoB, because apoB can only be processed by the LDL receptor
fraction requires apolipoprotein (apo) A series molecules and the (LDLR) (Ishibashi et al. 1994). Thus chylomicrons and VLDL-C
huge chylomicrons require apoB-48, apoC and apoE (Utermann have a faster level of clearance from the circulation than
1988; Chapman et al. 2011). After being carried to all tissues via LDL-C. Finally, when insulin levels decline, fat stored in
the circulation the remnants of chylomicrons are processed by the adipocytes is released as non-esterified fatty acids (NEFA, also
liver. Dietary FA shorter than 12 carbons are not carried by free fatty acids) transported on albumin (Cahill 2006; Hodson
chylomicrons but are dissolved in blood and carried to the liver via et al. 2008; Marinou et al. 2011).
the Portal vein (Bach and Babayan 1982). At the liver, the VLDL- The characteristic LDL-C particle number and LDL-C particle
C fraction, composed of fat and cholesterol from chylomicron size distribution of an individual are affected by both genetics and
Animal fats back on the table Animal Production Science 835

diet. Each LDL-C particle has a single apoB molecule associated concentration of LDL-C per mL of blood is a combination of
with it, and apoB expression is affected by insulin flux and the both the number of LDL particles per mL and the amount of
amount of lipid in the liver (Elam et al. 1999; Veniant et al. 1999), cholesterol contained in each particle. That is, a particular LDL-C
and so APOB gene expression and hence the number of LDL-C concentration of the blood could be made up of many particles
particles is partly driven by carbohydrate intake. It is also each containing a small amount of cholesterol or few particles
inversely related to the amount of apoE in circulation (Smit each containing a large amount of cholesterol. However, what
et al. 1988; Utermann 1988), and although there is a major counts for heightened risk of CVD is the number of LDL particles
genetic effect on apoE expression due to variation at the per mL in circulation rather than LDL-C concentration per se
apolipoprotein E (APOE) coding sequence, apoE expression is (Sniderman et al. 2012). Two individuals with the same LDL-C
positively correlated with dietary cholesterol, oestrogen and SFA can have vastly different risks for CVD if one has many small
(Utermann et al. 1979; Srivastava 1996; Srivastava et al. 1996). dense particles with small amounts of cholesterol while the other
There are three overall patterns of LDL-C particle size has far fewer particles each carrying much larger amounts of
distribution in humans, stable pattern A is biased to larger less cholesterol. LDL-C particles come in a range of densities. The
dense particles, stable pattern B is biased to smaller denser larger the LDL-C particle the higher the concentration of free
particles, and unstable pattern A, where individuals have cholesterol and lipid, the lower the concentration of protein and
pattern A at high fat levels and pattern B at low fat levels cholesteryl-esters, the younger it is, and the longer it takes either
(Campos et al. 1995; Krauss and Dreon 1995; Dreon et al. for the apoB on the surface of the particle to be glycosylated, or
1999). Stable pattern B is governed by mutations at the LDLR for the particle to cross the vascular endothelium or to oxidise
(Austin et al. 1988; Nishina et al. 1992; Zhu et al. 2007), which (Tribble et al. 1992; Reaven et al. 1994; Younis et al. 2013).
causes delays in LDL-C clearance resulting in smaller, denser
particles. Unstable pattern A is due to variation at the APOE locus,
where the e4 allele requires high fat levels to show pattern A The development of cardiovascular disease
(Dreon et al. 1995; Krauss and Dreon 1995), and reductions in Plaque formation and atherosclerosis, which is at the heart of
LDL-C due to low fat diets are not accompanied by reductions in CVD, is mechanistically initiated by the peroxidation of PUFA in
number of LDL-C particles. This is partly because the apoE*E4 the cholesteryl-esters of LDL-C, and the first evidence of this was
protein has a higher affinity for low-density lipoprotein receptor discovered 60 years ago (Glavind et al. 1952). The favoured
related protein 1 as well as for VLDL-C than the E2 and E3 PUFA for incorporation into cholesteryl-esters is linoleic acid
proteins (Egert et al. 2012), so chylomicrons are cleared at a (C18:2 n-6), the most common n-6 PUFA (Esterbauer et al.
faster rate and VLDL-C matures to LDL-C at a faster rate and so 1992). Restricting PUFA in the diet and providing high levels of
over its lifespan a lipoprotein cholesterol particle will be in the oleic acid results in its replacement in cholesteryl-esters by oleic
LDL-C form for longer for carriers of this allele. acid, the latter of which does not peroxidise (Nestel et al. 1992;
High levels of CISFA cause the strongest increase in LDL-C Abbey et al. 1993; Sandker et al. 1993; Reaven et al. 1994). The
particle size but unsaturated lipids also appear to maintain PUFA-based cholesteryl-esters of LDL-C are peroxidised when
increased LDL-C particle size but to a lesser extent (Dreon they cross the endothelium, resulting in stepwise damage to
et al. 1998; Kratz et al. 2002). Stable pattern B individuals apoB-100 on the surface of the LDL-C particle, which results
respond to an increase in CISFA by increasing the number of in the LDL-C particle being taken up by macrophages, where the
small dense LDL-C particles in circulation, as seen by an increase cholesterol accumulates (Brown and Goldstein 1983; Steinberg
in apoB levels (Krauss and Dreon 1995), because the genetic et al. 1989; Esterbauer et al. 1992; Stocker and Keaney 2004).
lesion is a reduction in recycling of LDL-C particles. Discordance The resulting foam cells form the basis of the atherosclerotic
between LDL-C and apoB concentrations in the blood is plaque. HDL-C particles act as antioxidants in this cascade, and in
an indicator of these differences in LDL-C pattern, and addition, do cross the vascular endothelium and accept
discordance in apoB and LDL-C affects strongly the risk of cholesterol from foam cells, reversing the process, returning
CVD, with apoB level being the more accurate indicator cholesterol to the liver where it is converted to bile salts
(Dreon et al. 1995, 1998; Sniderman et al. 2012). (Brown and Goldstein 1983; Fielding and Fielding 1995). The
Unsaturated fatty acids (UFA) are known to increase the smaller HDL3 particles are most efficient at this process, and
expression of the LDLR gene and, in addition, long-chain n-3 their numbers are increased through consumption of CISFA
and n-6 PUFA and CLA increase the availability of the LDLR (Nestel et al. 1992; Kontush et al. 2003). This mechanism
protein compared with CISFA (Fernandez and McNamara 1989; explains to some extent why HDL-C is an independent risk
Yu-Poth et al. 2005; Dorfman and Lichtenstein 2006). This is factor to LDL-C for CVD (Castelli et al. 1986; Stampfer et al.
consistent with the well known reduction of LDL-C concentration 1996; Chapman et al. 2011; Miller et al. 2011). Antioxidants such
with increased UFA. A similar effect is expected for dietary as Vitamins E and C can slow the damage, but they only delay
stearic acid because its effects on serum cholesterol fractions are the peroxidation on the scale of minutes not hours (Esterbauer
not statistically significantly different to that of oleic acid, it is et al. 1992), consistent with the demonstrated weak effect of
associated with a reduction in concentration of apoB-100, and it antioxidant use in cohort trials and the failure of antioxidant
is rapidly converted to oleic acid in the liver where the LDLR gene therapy to control atherosclerosis in random control trials (Jha
is expressed (Bonanome and Grundy 1988; Tholstrup et al. et al. 1995; Knekt et al. 2004). Once the plaque forms,
1994a; Mensink et al. 2003). inflammatory immunological processes are engaged (Stocker
Although LDL-C concentration of the blood is the most and Keaney 2004), and anti-inflammatory and anti-platelet
common risk factor used in prediction of CVD, the treatment can reduce the risk of vascular death (Bousser et al.
836 Animal Production Science W. Barendse

2011). The tendency for LDL-C to cross the vascular endothelium et al. 2011). Average longevity, a key statistic in comparisons of
is increased if it is small dense LDL-C. High levels of CISFA are different diets and lifestyles, does not increase when SFA is
important when they increase the number of small dense LDL-C replaced by either carbohydrate or UFA (Hooper et al. 2011).
molecules, otherwise the damage is done by peroxidation of Nevertheless, these surveys have extra-ordinary statistical power,
PUFA, and both factors can be rescued by having MUFA as covering many hundreds of thousands of people. Any association
the dominant FA. to SFA that is seen is variable and only at the very highest levels of
consumption, which is consistent with the known mechanisms of
the effect of CISFA on LDL-C structure in some individuals.
The epidemiology of cardiovascular disease On the other hand, very high body mass index (BMI: kg/m2) is
and saturated fat reliably and consistently linked within populations to all forms
These factors help to explain the success of the traditional of CVD (Keys et al. 1980; McGee and Diverse Populations
Mediterranean diet and lifestyle, which has been described as Collaboration 2005), a marker of increased food consumption or
largely lacto-vegetarian (Keys 1995). The Mediterranean diet and decreased movement. Indeed, waist circumference and waist to
lifestyle as originally described, is a high lipid (40% of total hip ratio are stronger physical correlates to CVD than BMI by
calories) low protein (10%) diet based on olive oil, vegetables, itself (de Hollander et al. 2012) and the relative risk of a large
fruit, whole-grain cereals and legumes, wine, nuts, full fat cheese, waist circumference easily exceeds the relative risk found for high
fish, and meat, especially pork fat and offal (Keys et al. 1970; consumption of SFA and is similar to being in the top quintile
Keys 1995). The fat in this specification is dominated by MUFA, for non-HDL-C or the bottom quintile for HDL-C (Chapman
with low levels of linoleic acid (2% of total calories), a ratio of n-6 et al. 2011; Hooper et al. 2011). In food overconsumption
to n-3 PUFA of ~2, and with modest levels of SFA (8% of total studies, excess fructose rather than excess glucose leads to an
calories) (Keys and Kimura 1970; Keys et al. 1970, 1980). Given increase in intra-abdominal fat and hence expanded waist
the composition of olive oil and other plant oils, this suggests a circumferences (Stanhope et al. 2009).
substantial part of the lipid (perhaps a third) was from animal The within-cohort argument against animal or saturated fat
sources. What counts is degree of adherence to that traditional became much weaker once the effects of trans fats in margarines
Mediterranean diet and lifestyle (de Lorgeril et al. 1994, 1999; derived from partial hydrogenation of C18 PUFA in vegetable
Trichopoulou et al. 2003; Scarmeas et al. 2006; Féart et al. 2009; oils were separated from animal fats. Animal fats and margarines
Sofi et al. 2012), no single food group is the magic bullet, although had initially been grouped together in analyses, as representatives
there was evaluation of which particular factors are critical that of fats that were solid at room temperature. These margarines
might alleviate the effects of a Western diet and lifestyle (Keys contained substantial amounts of elaidic acid (C18:1 trans 9)
1980; Hertog et al. 1993; Sandker et al. 1993; Evans et al. 1995; (Hunter 2001; Hayes and Pronczuk 2010). The effect of industrial
de Lorgeril et al. 2002). trans fat on risk of heart disease is powerful, the dose response
Altering the effects of large amounts of SFA on serum predictable (Hu et al. 1997), the results marked (Willett et al.
cholesterol by replacing it with large amounts of PUFA to 1993; Dorfman et al. 2009; Mozaffarian et al. 2009), and
control TSC and reduce CVD, which was the subject of a industrial trans fats are the only fat to double the risk of
large random controlled trial (Multiple Risk Factor CVD, all other fats change the risk by a small percentage.
Intervention Trial Research Group 1982), was not envisaged Consequently, cities in the United States have banned trans
as an option to control CVD and was explicitly criticised fats from publically prepared food (http://www.nbcnews.
before it was performed (Keys et al. 1974). The trial was com/id/16051436/ns/health-diet_and_nutrition/t/new-york-city-
unsuccessful because it showed no significant change in rates passes-trans-fat-ban/#.UVpxVBm8yTw, accessed 1 April 2014).
of CVD in the trial versus the control sample. Worryingly, this In effect, C18 trans MUFA, derived from the partial
trial showed increased rates of cancer in the test group compared hydrogenation of C18:2 and C18:3 PUFA, show decreased
to the control (Blaxter and Webster 1991). Indeed, although HDL-C but similar LDL-C levels to CISFA (de Roos et al.
treatment of CVD has greatly improved over the last 50 years, 2001; Matthan et al. 2004), which explained to some extent
the incidence has stayed the same over that time and reductions the previously observed emergence of a pattern of low HDL-C,
in serum cholesterol have played a small (11%) role in postponing high LDL-C and high FTG seen in some populations (Castelli
deaths from CVD (Hunink et al. 1997; Ford et al. 2007; 1986). Many margarines have a large amount of PUFA, which
Gouda et al. 2012). Smaller trials showed some progress in would contribute to peroxidisable cholesteryl-esters, providing
treating CVD where the lipid composition approximated that a double hit. Indeed, once trans fats were controlled, risk of
of the Mediterranean diet by providing to participants rapeseed CVD declined with increased number of beef, lamb, and pork
(canola) oil hydrogenated to a margarine that was dominated by stews consumed per week, implying a beneficial effect of
MUFA, with more SFA and a lower ratio of n-6 to n-3 PUFA than these animal fats on CVD (Willett et al. 1993). Many
olive oil (de Lorgeril et al. 1994, 1999). manufacturers now create margarines with lower trans fat
Although they can be flawed, nutritional surveys have found levels through interesterification of completely hydrogenated
little evidence to link reported fat consumption of any kind and fats and unhydrogenated oils (Hunter 2001; Hayes and
CVD within countries (Siri-Tarino et al. 2010), and meta- Pronczuk 2010). But there is always some level of trans fat
analyses of random controlled trials have shown small or due to the refinement of vegetable oils, while there would still
no benefit to replacing saturated fat with carbohydrate or be a high level of linoleic acid (Table 1).
unsaturated fat (Multiple Risk Factor Intervention Trial Most of the epidemiological evidence for the role of fat in
Research Group 1982; Micha and Mozaffarian 2010; Hooper CVD comes from comparisons between countries and from the
Animal fats back on the table Animal Production Science 837

changes in food usage over time within countries. As noted above, of the year while the West Finland cohort was centred near Turku
if one were to use the evidence of changes in food usage, then and included a substantial proportion of Swedes (Karvonen et al.
animal fat consumption declined and plant oil consumption 1970). During winter the rations were reduced to milk and other
increased as CVD and obesity rates increased, which argues dairy products, bread, and potatoes with small amounts of other
against the role of animal fat in CVD or obesity (Yudkin foodstuffs (Roine et al. 1958), hardly well balanced but hardly a
1957; Antar et al. 1964; Oddy and Yudkin 1969; Kritchevsky death sentence, given the benefits of dairy product consumption
1976; Enig et al. 1978; Eisenmann 2003; Carlson et al. 2011; for CVD and the metabolic syndrome (Evans et al. 1995; Elwood
Chapman et al. 2011). Comparisons between countries are et al. 2010; Livingstone et al. 2013). Indeed, there was little
controversial, called ecological comparisons, because many difference between East and West Finland in their diets, apart
factors change from one country to the next, and such from a small increase in diversity in the West, and reduced vitamin
comparisons result in incorrect inferences due to correlations C, vitamin E, and iodine in the East. Finnish researchers in the
based on mean values (Robinson 1950; Evans 2011). Moreover, 1950s suspected differences in iodine and subsequent goitre as a
the early ecological comparison of six countries was criticised for likely cause of the difference in CHD between the two Finnish
biased selection of countries, which had led to the reporting of samples (Roine et al. 1958; Uotila et al. 1958). Hypothyroidism is
very strong relationships between fat and CVD (Keys 1953; a known cause of elevated FTG with decreased particle size of
Yerushalmy and Hilleboe 1957; Yudkin 1957). Nevertheless, the VLDL fraction (Nikkilä and Kekki 1972; Abrams et al. 1981;
much of the prestige of the argument against SFA is based on a Castelli 1986), although these days vitamins C and E would also
later version of that ecological comparison, the Seven Countries be thought important due to their antioxidant effects (Esterbauer
study, in which individuals within 16 cohorts were evaluated, et al. 1992). Fourth, the East Finland cohort was centred on the
which showed that within each cohort, smoking, blood pressure, town of Ilomantsi, 3 km from the Finno-Russian border in an area
and serum cholesterol were each important risk factors for CVD in which Russians had seized territory and displaced Karelians
(Keys et al. 1980). Importantly, however, food intake of each had been repatriated by the Finnish government to other parts of
individual was not measured, but gross food composition was Finland (Karvonen et al. 1970). While the report stated that the
determined for a representative sample of 30–50 households, cohort itself consisted of a minimum of displaced persons, the
and then cross-cohort correlations were made between average stress associated with such events, which may have involved
nutrient composition and average rates of CVD (Keys et al. 1980). family members, should not be underestimated. Stress is a well
This was justified on the basis of the known relationship between known factor in CVD, especially stress where one is powerless to
average fat composition of a ration and average serum cholesterol alter events (Marmot et al. 1997). None of the other cohorts
of individuals consuming that ration – that individual cholesterol experienced a similar event associated with the Second World
values are too variable for accurate inference (Keys et al. 1980). War. Last, Karelians are a minority ethnic group and have one of
Indeed, the first study of serum cholesterol and atherosclerosis the highest frequencies of the APOE e4 allele in Europe (Fullerton
at autopsy had shown no correlation between individual values et al. 2000). The APOE gene shows a North/South cline in the
for these two variables (Lande and Sperry 1936). The Seven frequency of the e4 allele in Europe, evidence of natural selection,
Countries study is the basis for the Mediterranean diet and while the lowest frequencies of e4 of any population are found on
lifestyle. the islands and shores of the Mediterranean (Corbo and Scacchi
What are the alternative explanations for the extremely high 1999; Singh et al. 2006; Lappalainen et al. 2010). Carriers of
rates of CVD that occurred in the East Finland cohort in the Seven the e4 allele have a 40% increased risk and homozygotes for this
Countries study (Keys et al. 1980), if one were to assume that they allele have approximately double the risk of CHD compared
were not due to SFA. There, the East Finland cohort had the with the APOE e3 homozygotes in Western countries (Menzel
highest proportion of saturated fat in the diet and nearly twice the et al. 1983; Song et al. 2004; Mooijaart et al. 2006). While it may
incidence of coronary heart disease (CHD) compared with any be coincidental that the age-adjusted death rates for CHD in
other cohort, the SFA derived mainly from milk fat. The overall East Finland and Crete were very similar to the frequencies of
ration also had low levels of linoleic acid as a proportion of homozygotes for APOE e4 in these two cohorts, APOE genotype
calories and a low ratio of n-6 to n-3 FA (Keys and Kimura 1970; has been shown to affect CHD in the East and West Finland
Keys et al. 1970). First, the West Finland cohort had the same populations of the Seven Countries study (Stengard et al. 1995).
median TSC value as the East Finland cohort (Keys et al. 1970; The response of APOE e4 to SFA versus MUFA is significantly
Stengard et al. 1995) but had only a third the rate of age adjusted different to the response of APOE e3, with SFA-dominated fats
CHD compared with the East Finland cohort. Furthermore, West resulting in a substantially elevated LDL-C profile for this allele
Finland had a higher average TSC than the Zutphen (Netherlands) (Moreno et al. 2009; Egert et al. 2012). Given that APOE e4 is
or US Railroad cohorts, and the same or more SFA as a proportion ancestral (Hanlon and Rubinsztein 1995; Fullerton et al. 2000),
of calories than either of those, but less CHD than either may be a thrifty allele (Corbo and Scacchi 1999) and that the East
Zutphen or US Railroad. Second, the East Finland cohort had Finland population was actually consuming the most calories per
the most calorie intake per kilogram bodyweight, but this was kilogram bodyweight, there is evidence of a genetic component to
not substantially greater than West Finland. East Finland did the observations and the differences between cohorts. Obviously,
consume 32% more calories per kilo bodyweight than the Crete there would be other genes involved in blood lipids and response
cohort (lowest CHD rate), and although both consumed ~40% of to fat consumption, not just APOE but would also include
calories as fat, this implies substantially more fat in total (Keys mutations such as the Karelian form of the LDLR gene
et al. 1970). Third, the East Finland cohort was located in Karelia (Vuorio et al. 1997), which would have a role in differences
(Keys et al. 1958), then an isolated and icebound region for most between populations (Teslovich et al. 2010). Taken together, any
838 Animal Production Science W. Barendse

or all of these factors could be working to explain this ecological importance of fat soluble vitamins is extremely well known, with
comparison. recommendations to consume less fat and less animal tissues
Perhaps the final word on fat and cholesterol should be given to on the one hand or absence of these foods in some developing
William Castelli (see quote at the beginning) on individuals living countries on the other hand, vitamin supplementation is often
in the real world. In the real world there is only a tenuous link at needed.
best between consumption of SFA and serum cholesterol, with The fat and other tissues of a wide variety of land animals, not
other factors overriding the relationship. For example, ‘The just oily fish, contain long-chain n-3 PUFA (Table 2). Given the
two factors that jump to mind are exercise and weight. In pollution of the ocean by methyl mercury, ocean fish consumption
Framingham, for example, we found that the people who ate needs to be modulated to achieve the benefits of eating oily
the most cholesterol, ate the most saturated fat, ate the most fish (Mozaffarian and Rimm 2006). These PUFA are part of
calories, weighed the least, and were the most physically active’ the phospholipid fraction, hence their presence in substantial
(Castelli 1992). As noted at the start, the more SFA consumed the amounts in tissues such as brain, liver, and egg yolks. Long-chain
lower the serum cholesterol, and in the Framingham Heart study n-3 PUFA have a wide range of well attested health
(Castelli et al. 1986), not only did lower serum cholesterol and benefits, primarily in brain development in young children and
lower BMI equate to lower risk of CVD, but higher HDL-C, as an important modulator of immune system function, especially
consistent with higher consumption of SFA, was shown to have the inflammatory response (Simopoulos 1991). As inflammation
protective effects. is central to many chronic disorders of aging and obesity, this
subject is important and is regularly reviewed (MacLean et al.
2006; Schmitz and Ecker 2008; Simopoulos 2008; Nicholson
Components of animal fat with known health benefits et al. 2013). Although a-linolenic acid (C18:3 n-3) is found in
The most important health benefit of fat is that it is a carrier for the leafy green vegetables, some nuts and some oil seed, it appears
vitamins A, D, E, and K and the precursors b-carotene and that only animals or algae can synthesise the long-chain n-3
cholesterol. The transport of these into the body partly through PUFA docosahexaenoic acid (DHA) and eicosapentaenoic acid
active transport and passive diffusion in fat has been recently (EPA) (Sprecher 2002). The sequence of reactions and rate-
reviewed (Reboul and Borel 2011). Deficiency disorders for limiting steps are shown in Fig. 2. The human metabolism has
these vitamins are well known, blindness, rickets, and bleeding a trivial ability to increase DHA given extra a-linolenic acid in
disorders are the well attested results of frank deficiency, but the diet (Bézard et al. 1994; Brenna 2002; Burdge and Calder
low levels of these vitamins are associated with bone weakness, 2005; Harper et al. 2006), although levels of DHA in the serum of
osteoporosis, calcification of the arteries, CHD, type 2 diabetes, self-reported vegans is higher than expected, which if accurate
depression and other mental disorders (Rimm et al. 1993; suggests regulation of DHA levels and enhanced endogenous
Schaafsma et al. 2000; Holick 2007; Beulens et al. 2010; synthesis of DHA in the absence of dietary intake (Welch et al.
Flore et al. 2013). Animal tissues, especially organs such as 2010). The starting ratio of shorter-chain n-6 to n-3 PUFA in the
the liver and adipose tissue, and dairy products are a valuable diet largely determines the ratio of longer-chain PUFA that are
source for several of these fat soluble vitamins. Although the synthesised, and the ratio stored in tissues or cholesteryl-esters is

Table 2. Amount of tissue from a range of representative animal sources to provide 250 mg of essential long-chain n-3 fatty acids
Amount is the amount of tissue required to obtain 250 mg of long-chain n-3 polyunsaturated fatty acids in the diet consisting of varying ratios of docosahexaenoic
acid (DHA), eicosapentaenoic acid and n-3 docosapentaenoic acid depending on species and tissue

Species Management Tissue Amount Reference

Antelope Wild Brain 2.7 g Cordain et al. (2002b)
Sardine Wild Muscle 6.3 g Usydus et al. (2012)
Salmon Farmed Whole 16.7 g Sanden et al. (2011)
Pig Intensive (linseed supplemented) Backfat 59 g Enser et al. (2000)
Lamb Pasture Subcutaneous fat 89 g Nuernberg et al. (2005b)
Pig Intensive (unsupplemented) Backfat 101 g Enser et al. (2000)
Chicken Intensive (flaxseed supplemented) Breast, skin on 109 g Jia et al. (2010)
Egg Cage/DHA supplemented Yolk/whole egg <2A–3 large eggs Cachaldora et al. (2008); Anderson (2011)
Pig Intensive (unsupplemented) Liver 113 g Enser et al. (2000)
Chicken Intensive (flaxseed supplemented) Wing, skin on 137 g Jia et al. (2010)
Chicken Intensive Breast, skin on 219 g Jia et al. (2010)
Lamb Pasture Longissimus 260 g Nuernberg et al. (2005b)
Chicken Intensive Wing, skin on 316 g Jia et al. (2010)
Pig Intensive (unsupplemented) Sausages 448 g Enser et al. (2000)
Beef (Simmental) Pasture Longissimus 676 g Nuernberg et al. (2005a)
Beef Pasture Perirenal fat 735 g Staerfl et al. (2011)
Chicken Intensive Leg skin off 880 g Givens et al. (2011)
Beef (Charolais) Feedlot Longissimus 1.3 kg Mandell et al. (1997)
A
Chickens supplemented with DHA in their rations.
Animal fats back on the table Animal Production Science 839

n-3 synthesis n-6 synthesis and inflammatory diseases such as rheumatoid arthritis and
inflammatory bowel disease (Godley et al. 1996; Harvei et al.
ALA 18:3 (9,12,15) LA 18:2 (9,12) 1997; Gogos et al. 1998; Simonsen et al. 1998; Yang et al. 1999c;
delta-6 desaturase
rate limiƟng step
Simopoulos 2008; Murff et al. 2011). Intake of many types of fat
18:4 (6,9,12,15) GLA 18:3 (6,9,12) have been examined, with a suggestion of a threshold of n-6
elongase PUFA, and reduced rates of disease for fats or oils low in n-6
20:4 (8,11,14,17) 20:3 (8,11,14) PUFA, including animal fat (Zock and Katan 1998; Freedman
microsomal

delta-5 desaturase
et al. 2008; Alexander et al. 2010; Brennan et al. 2010; Dong et al.
EPA 20:5 (5,8,11,14,17) AA 20:4 (5,8,11,14) 2011; Gilsing et al. 2011; Liu et al. 2011; Psaltopoulou et al.
elongase
2011; Chajes et al. 2012). Moreover, supplementation with long-
DPA 22:5 (7,10,13,16,19) 22:4 (7,10,13,16) chain n-3 FA fails where there are high rates of consumption of
elongase
n-6 PUFA. Many plant oils have OMR >10, some with OMR
24:5 (9,12,15,18,21) 24:4 (9,12,15,18)
delta-6 desaturase
>100 (Table 1). It has been estimated that the general
rate limiƟng step? consumption in Western countries is OMR ~15, while more
24:6 (6,9,12,15,18,21) 24:5 (6,9,12,15,18)
peroxisomal traditional diets have much lower OMR, and the traditional
-oxidaƟon Greek diet, on which the Mediterranean diet was modelled,
rate limiƟng step DPA 22:5 (4,7,10,13,16)
DHA 22:6 (4,7,10,13,16,19) had an OMR of 2–4 (Keys and Kimura 1970; Keys et al.
Fig. 2. The steps in synthesis of long-chain n-3 and n-6 polyunsaturated fatty 1970; Simopoulos 2008). In general, for the shorter 18-carbon
acid (PUFA) in mammalian tissues. Humans have a trivial ability to synthesise n-3 and n-6 FA, animal fat can have much lower OMR than plant
DHA from ALA (see text). The main rate-limiting steps apply to both n-3 and oils, especially if their rations are low in n-6 PUFA. For longer-
n-6 PUFA. The last rate-limiting step involves the translocation of PUFA chain n-3 and n-6 FA the ratio also depends on the tissue and the
from the endoplasmic reticulum to the peroxisomes. Degradation usually species. Ruminant fat has low PUFA due to bio-hydrogenation in
occurs backwards to the previous PUFA in the pathway, except for 24 : 6 (n-3) the rumen, and from animals on pasture has OMR 2 (Table 1)
and 22 : 6 (n-3), the latter of which degrades to either 22 : 5 (n-3) or 20 : 5 (n-3). and increased levels of a-linolenic acid, which suggests that
ALA, a-linolenic acid; LA, linoleic acid; GLA, gamma-linolenic acid; EPA,
ruminant fat has a role in reducing not just the amount of n-6
eicosapentaenoic acid; AA, arachidonic acid; DPA, docosapentaenoic acid;
PUFA but also the OMR. However, the West and other countries
DHA, docosahexaenoic acid. Information taken from Sprecher (2002).
with high rates of obesity have high rates of these diseases, and
being obese greatly increases the risk of these disorders including
therefore a reflection of the intake ratio of these fats (Zock et al. increased rates for higher levels of intra-abdominal fat (Connolly
1997). Nevertheless, there is human genetic variation in the genes et al. 2002; Key et al. 2004; Pischon et al. 2008; Renehan et al.
of these pathways, which bias processing towards n-3 PUFA over 2008). In overfeeding, it is primarily dietary fat that is stored, due
n-6 PUFA (Tanaka et al. 2009). High levels of circulating long- to the high metabolic cost of converting dietary glucose to lipid
chain n-3 PUFA, especially DHA, therefore, generally requires a in humans, ~0.33 Mj per Mj of lipid deposited, although some
dietary source in humans, essentially from fat of other animals, samples of obese people showed a greater ability to convert
with evidence of little additional benefit beyond a threshold carbohydrate to fat than non-obese people (Acheson et al.
intake of ~250 mg per day (Mozaffarian and Rimm 2006). 1988; Pasquet et al. 1992; McDevitt et al. 2001; Stanhope
EPA is interconverted to DHA via the intermediate n-3 et al. 2009). So analyses of the fat of obese individuals will
docosapentaenoic acid (DPA) but not from n-6 DPA, and n-3 usually show a high ratio of n-6 to n-3 fat in countries where seed
DPA is a long-chain PUFA found in ruminant tissues. However, oils are the dominant source of lipids. This acts to confound the
the ratio of the n-6 to n-3 PUFA in the tissue depends largely on analysis. Is it just that increased food consumption has resulted in
the food source of the animal, with grass-fed ruminants having higher BMI, which of itself predisposes the individual to these
approximately a 2 : 1 ratio of n-6 to n-3 FA, much lower than for disorders, or is it truly the type of fat? Mechanistic studies of
grain-fed ruminants (Yang et al. 1999b; Couvreur et al. 2006; n-3 and n-6 fats show their role in respectively inhibiting and
Sinclair 2007), compositional effects seen in other species as well promoting inflammation and tumour growth (Xia et al. 2005;
(Sinclair et al. 2010). Given the decline and pollution of fisheries Kobayashi et al. 2006), while high levels of n-6 fats may inhibit
(Costello et al. 2012; Halpern et al. 2012) there are other ways of the action of delta-9 desaturase (Yang et al. 1999b), critical for
ensuring a sufficient amount of long-chain n-3 PUFA, especially desaturating SFA. So while controlling bodyweight may be the
since many populations, perhaps under the advice to cut back on more important strategy, reducing the level of n-6 PUFA to bring
saturated fat have reduced their consumption of animal fat and down the OMR of the diet appears worthwhile.
are deficient in DHA and EPA (Givens 2010). Better data on In addition to long-chain n-3 PUFA, ruminant fat contains
DHA, n-3 DPA, and EPA concentrations in a variety of animal various types of CLA, a series of bioactive compounds with well
tissues under different management systems would be welcome. known positive effects on human health. CLA are derived
The ratio of n-6 to n-3 PUFA (OMR) in animal fats may make from PUFA in animal feed that had been bio-hydrogenated in
an important contribution to human health although it is not the rumen. Most of the CLA in the animal’s tissues are from
clear whether these are all direct effects or whether they are partial vaccenic acid (C18:1 trans-11) absorbed from the rumen that is
effects due to food overconsumption and obesity. Several studies converted to the CLA rumenic acid (C18:2 cis-9 trans-11) by the
have shown that a high OMR in tissues or cholesteryl-esters is host through the action of delta-9 desaturase, and a minor
associated with several diseases including cancers such as component of the CLA is produced by the rumen flora and
prostate, bowel and breast cancer, CVD, autoimmune diseases absorbed by the host as one of a range of CLA (Griinari and
840 Animal Production Science W. Barendse

Bauman 1999; Pariza et al. 2001). The richest source is ruminant result of improved diet quality may reduce risk of colon cancer
milk fat (Parodi 1997), but CLA are found in all ruminant fat (Steinmetz and Potter 1991; Van Munster et al. 1994; Mathers
depots including substantial amounts in bone marrow (Cordain et al. 2012). Although most butyrate from dairy fat is absorbed
et al. 2002b), a traditional source of food for pre-agricultural from the small intestine and metabolised in the liver, there is clear
humans (Morin 2007). CLA is produced from both n-6 and n-3 speculation about the potential role of dairy butyrate in not just
PUFA, so animals on grain versus pasture do not produce less colon but other cancers, not by surviving into the large colon
CLA, just the kind of CLA is altered. On grain compared with but by increased levels delivered via the circulation (Parodi
pasture, most of the CLA is still cis-9, trans-11 C18:2 but there is a 1997, 2004). The human health effects of dairy derived
reduction of trans-11, cis-13 C18:2 and an increase in trans-7, cis- butyrate, ceramide, and sphingomyelin, as well as other minor
9 C18:2, trans-10, cis-12 C18:2, and cis-9, cis-11 C18:2 (Daley components of animal fat, have not been extensively studied.
et al. 2010; Aldai et al. 2011). This is apparently due to changes in
the bacterial composition of the rumen in response to changes in
pH as a result of the amount of fibre and energy density of the feed Health effects of fat as a macronutrient
(Daley et al. 2010). These CLA isomers have different 3-D and energy source
structures and there is some evidence for different biological Calorie restriction, not lipid restriction, has been shown to affect
activities, with the cis-9, trans-11 C18:2 isomer seen as the most longevity in a wide range of species (Fontana et al. 2010) but
beneficial (Pariza et al. 2001). This CLA isomer is synthesised longevity studies of humans by humans are obviously impractical
directly by humans from vaccenic acid (trans-11 C18:1), through (Hursting et al. 2010), the benefits are questioned relative to
the action of delta-9 desaturase in the liver and other tissues. CLA sanitation and modern medicine (Everitt and LeCouteur 2007),
came to prominence in screens to find carcinogenic molecules and a recent trial in primates failed to find an effect (Mattison
in grilled steak (Ha et al. 1987), and they were targeted because et al. 2012). It is well known that a low fat, low protein whole-
they are trans fats. However, it proved to be one of the most anti- plant diet, when supplemented with the essential nutrients
carcinogenic molecules in cell culture assay. In addition, due to vitamin B12 and long-chain n-3 PUFA, has been associated
the concern with trans fats of industrial hydrogenation, especially with reduction of the thickness of cardiac arteries (Ornish
elaidic acid, any trans fat receives a great deal of interest, and the et al. 1998). While this gives enormous prestige to low fat
health benefits of CLA have been thoroughly studied and whole-plant diets, reduction of the thickness of cardiac arteries
intensively reviewed (Parodi 1997; Pariza et al. 2001; Dilzer can also be achieved using calorie restriction of a high quality
and Park 2012). A wide range of favourable health outcomes diet, including meat, eggs, and dairy products, thereby consuming
have been found, including anti-cancer and anti-obesity effects, animal fat (Fontana et al. 2004, 2007). Furthermore, starvation
improvements in glucose tolerance, cardiovascular health, bone itself also causes a reduction in thickness of cardiac arteries
density, immune system function and inflammation, and gut in addition to generalised tissue wasting, as was found in the
health. Much of this work is now focussed on CLA as a Minnesota Semistarvation Experiment of humans. There, a more
pharmaceutical preparation or food additive, consisting of the than 50% reduction in calories to an extremely low fat ration of
main isomers cis-9, trans-11 C18:2 and trans-10, cis-12 C18:2, root vegetables, cabbage, cereals, and a few grams of animal
with dosages from 0.5 to 7 g per day (Dilzer and Park 2012). Given protein per week also showed substantial negative physical
the concentration of CLA in dairy foods or ruminant fat, and physiological effects (Keys 1950; Taylor and Keys 1950).
therapeutic doses of CLA could be obtained from moderate In calorie-restricted individuals, when protein was reduced to
consumption (e.g. 100 g of full fat matured cheese) of dairy maintenance levels and replaced isocalorically with other
products or ruminant fat (Fogerty et al. 1988; Mushtaq et al. macronutrients, the level of insulin-like growth factor-1
2010). (IGF-1) dropped substantially (Fontana et al. 2008). This
There are minor components of animal fat that have unverified longevity marker, which is associated with cancer, diabetes,
human health benefits (Parodi 1997, 2004). In animals, fat is a and dementia, including Alzheimer’s disease (Paolisso et al.
metabolically active energy store, as adipose tissue, or a nutritive 1997; Arai et al. 2001; Carro et al. 2002; Trejo et al. 2002;
substance, as in milk. Apart from the major TAG and NEFA that Longo and Finch 2003; Pollak et al. 2004; Carro and Torres-
constitute the fat, there are minor components of the fat such as Aleman 2006; Fontana et al. 2010; Guevara-Aguirre et al. 2011;
phospholipids and sphingolipids that constitute part of the lipid Duron et al. 2012; Rajpathak et al. 2012), is raised the least by
structural element of cell membranes, the non-fat components lipids and most by protein consumption (Thissen et al. 1994).
of the adipocyte, or the fat micelles that constitute milk fat. A study of raw food enthusiasts consuming 40% of calories as
Few health benefits have been identified for these except that lipid and a maintenance level of 0.7 g/kg of protein (Rand et al.
phospholipids and sphingolipids do include long-chain n-3 2003), ~10% of calories, showed similar low levels of IGF-I
FA (Lehninger 1982). Pathways involving ceramide and without apparent calorie restriction (Fontana et al. 2008). This
sphingomyelin, components and downstream metabolites of macronutrient composition is similar to the original description of
sphingolipids, are known to be involved in several pathogenic the Mediterranean diet on Crete (Keys et al. 1970).
metabolic processes involved in cancer cell proliferation as well Although calorie restriction is a niche activity in the West,
as insulin resistance (Holland et al. 2007). Butyrate (C4:0), a there is some evidence of increased longevity for communities
short-chain SFA, forms a substantial part of dairy fat. Butyrate is that eat less food not less fat. Studies of the ‘Blue Zones’, areas of
generated by fermentation from plant fibre and resistant starch in the world with proven enhanced aging, increased proportions of
the colon of humans and is the preferred source of fuel for colon centenarians, and reduced morbidity from aging (Fraser and
cells (Scheppach 1994), and increased levels of butyrate as a Shavlik 2001; Poulain et al. 2004), show first a huge range in
Animal fats back on the table Animal Production Science 841

average fat consumption, from <10 to >40% of calories (Willcox (Hunter 2001), and the presence of long-chain PUFA. Second, in
et al. 2007, 2009; Appel 2008; Pes et al. 2013), relatively low a study of a large number of Swiss citizens, the small percentage
levels of protein, a diet that is plant-based but not vegan, with of individuals with great difficulty in passing faeces were
differences in staple foods and wide variations in the amount of statistically more likely to have a high fibre diet than a low
saturated fat consumed. The individuals generally consume fibre diet (Curtin et al. 1998). Although individuals on a high
substantially fewer calories than in the West, and have fat diet were less likely to report difficulty in passing faeces this
traditions of eating until one was not quite full. There is little was not statistically significant. Third, animal fat also contains a
evidence of deficiency in essential nutrients (Polidori et al. 2007; substantial proportion of stearic acid. Up to 20% of stearic acid,
Willcox et al. 2007; Buffa et al. 2010). It is by no means certain depending on the stereoisomeric location of the FA, is not
that the individuals are calorie restricted, and claims to that absorbed by the enterocytes compared with 0–2% for other FA
extent are a source of controversy, because the calorie and (Bracco 1994). The unabsorbed stearic acid will crystallise in the
protein intake in some of these groups is consistent with their lumen of the gut as the pH increases and be excreted as a calcium
smaller size (Keys and Kimura 1970; Willcox et al. 2007; Pes soap (Owen et al. 1995). This reduces the energy of the diet, and
et al. 2013). Nevertheless, these individuals consume on changes the consistency and increases the mass of the faeces
average substantially fewer calories than in the West, and less (Dougherty et al. 1995). This is not to argue that dietary fibre
than individuals in surrounding regions (e.g. Sardinia vs Italy, is unimportant, rather that dietary fibre is often not sufficient to
Okinawa vs Japan). Furthermore, despite the lower calorie intake, cure constipation and other ailments of the colon and rectum.
the individuals were far more physically active than the average in Constipation underlies many of the diseases of the bowel, and it is
the West, although their activity is not usually associated with long known to be a precursor to diverticulitis, varicose veins,
particularly hard work but instead represents activity all day long and haemorrhoids, among other disorders (Burkitt 1973; Cleave
(Fraser and Shavlik 2001; Willcox et al. 2009; Pes et al. 2013). Fat 1974). Colorectal cancer is related to diet quality, risk is reduced
appears not to be important in explaining increases in longevity in through the consumption of vegetables, fruit and resistant starch
these Blue Zones. Moreover, a study of Ashkenazi centenarians (Macquart-Moulin et al. 1987; Steinmetz and Potter 1991; Van
in the US showed that a non-significant smaller proportion of Munster et al. 1994; Archer et al. 1998; Topping and Clifton
the centenarians reported eating a low fat diet (Rajpathak et al. 2001; Mathers et al. 2012), and fat consumption has not been
2011) compared with an age-matched cohort from NHANES I – shown to be linked to its occurrence in large meta-analyses
the only statistically significant difference was that fewer of (Nelson et al. 1999; Liu et al. 2011). As an aside, colorectal
the men smoked. Eating less in the English-speaking West is cancer has been linked to red meat, preserved meat and beer
an unpalatable recommendation that goes against centuries old consumption, which may implicate methods of preparation
traditions of ‘eat, drink and be merry, for tomorrow you die’, and preservation of food involving known factors such as
entrenched overconsumption of food, and the social prestige of nitrosamines and heterocyclic amines (McMichael et al. 1979;
large amounts of lean meat (Dickson Wright 2011). Potter 1999; Aune et al. 2013; Egeberg et al. 2013).
While fat per se is not negatively associated with longevity, The macroscopic structure of a fat and its stereoisomeric
it is positively associated with digestion and gut performance. composition of TAG and their abundances makes a substantial
Low fat high carbohydrate diets of a high glycemic index have difference to the organoleptic and processing characteristics of
been associated with symptomatic gall bladder disease (Tsai that fat (Bracco 1994), there are differences between species and
et al. 2005) likely due to reduced cycling of cholesterol between plants and animals (Hunter 2001), but whether these
through bile salt release. Although fat or oil are often stated make a substantial difference to health is not clear. A TAG is
as affecting gastrooesophagial reflux disease, a systematic review composed of a glycerol molecule covalently bound to three FA,
of the literature failed to find an effect of fat consumption numbered sn-1, sn-2 and sn-3 from the bottom to the top – which
(Dent et al. 2005). In addition, fat has a unique ability to can be imagined as a glycerol molecule displayed vertically on
stimulate colonic contraction, not found for carbohydrate or the left-hand side of a visual image with the three FA displayed
protein, and these contractions are essential to the voiding of horizontally, bound to the hydroxyl groups of the glycerol
faeces (Wright et al. 1980). Indeed, remedies for constipation molecule. The specific sn-x structures and varieties of TAG
before the Second World War recommended, in addition affect the properties of a fat. For example, beef tallow and
to ‘roughage’, water and the avoidance of diuretics, the cocoa butter have similar but not identical mouthfeel, and the
consumption of fat such as bacon fat, butter, or olive oil, property of melting on the tongue is due mainly to the reduced
especially if the faeces was small and dry (Hutchison 1936), types of TAG and their specific combinations in cocoa butter
and for spastic colon no fibre and large amounts of the above (Bracco 1994). During digestion, lipases hydrolyse the bonds at
listed fat was recommended. This is not a recommendation that the sn-1 and sn-3 position, resulting in a monoglyceride and two
is in any current medical guideline. Yet several pieces of evidence free FA, and the monoglycerides are taken up more efficiently.
show that it is valid. First, infants take in no fibre, so amount of However, this preference is only likely to affect monoglycerides
fibre is not a variable. Animal fats in the formula result in stools of stearic acid (Bracco 1994), since >99% of all the other FA
that are softer, larger, and that are easier to pass than plant fats are taken up irrespective of the sn-x position that they occur in.
(Forsyth et al. 1999), and babies also grow better when the source These monoglycerides preferentially form the backbones for new
of the fat is from animal rather than plant sources (López-López TAG in the host (Zock et al. 1996). Plant oils tend to have more
et al. 2001). The exact reasons for these effects are not known, but PUFA in the sn-2 position than animal fat (Hunter 2001), which
these effects are thought to be due partly to the characteristic would then result in PUFA being preferentially incorporated into
stereoisomeric structure of animal fats compared with plant fats reformed TAG in the individual. Given the discussion on a high
842 Animal Production Science W. Barendse

OMR and reactive oxygen species (see above and below) this addition, measurements on Western volunteers of both sexes
may have unfortunate effects on stored and structural lipid in the show the generation of ketone bodies a few hours after moderate
individual. Stereoisomeric modifications of palmitic acid in a to high fat meals if no snacks are taken (Marinou et al. 2011).
normal diet in adults appeared to make no significant difference to As blood glucose and insulin levels gradually decline after a
the HDL-C or LDL-C concentrations in the blood (Zock et al. meal, levels of NEFA increase in the circulation, and the
1995). However, in a review of the literature on interesterification, ketone bodies acetoacetate and b-hydroxybutyrate start to rise
(Hayes and Pronczuk 2010) report that a large amount of stearic (Cahill 2006; Hodson et al. 2008; Marinou et al. 2011). The
acid in the sn-2 position had negative effects on the relative HDL- metabolism of ketone bodies requires less oxygen to generate
C and LDL-C profile. As stearic acid is generally not found at high the same physiological output and generates fewer free radicals
frequency in the sn-2 position in natural fats, and is usually (Sato et al. 1995), so is less damaging to tissues (Halliwell
considered as hypocholesterolemic (see above), they considered 2006), than the metabolism of serum glucose. In the presence
this a concern for manufactured fats. Furthermore, they report of both serum glucose and ketone bodies, less glucose is used
that interesterified fats alter the HDL-C and LDL-C ratios and (Kashiwaya et al. 1994) suggesting that the body will protect
concentrations in the serum of both infants and piglets away from its glucose sources in the presence of ketone bodies. In these
the pattern seen when they are fed their mother’s milk (Hayes and mild ketotic states, the amount of acetocarnitine and ubiquinone-
Pronczuk 2010), which generally has SFA at the sn-2 position 10 (Coenzyme Q10), the latter through its obligate relationship to
(Hunter 2001). This is a concern given the known improvement the uncoupling proteins, are increased in tissues including the
in growth of infants on animal versus plant fats (López-López liver, heart, brain, and skeletal muscle (Pearson and Tubbs 1967;
et al. 2001). Finally, the overall structure of a fat may affect McGarry et al. 1975; Echtay et al. 2000; Sullivan et al. 2004).
its digestion. For example, butter is a water-in-oil emulsion, These are two important anti-oxidants in the body whose levels
compared with the lipid contents of the gut, which after appear to decline with age and are associated with the decline of
secretion of bile, becomes an oil-in-water emulsion. This has function of mitochondria due to age-related oxidative damage
been hypothesised to explain the result of a shorter period of (Shigenaga et al. 1994; Hiatt 2001).
elevated lipemia after a meal using butter compared with olive High fat low carbohydrate low to moderate protein diets, often
or sunflower oils, with an increased number of chylomicrons called ketogenic diets, have been shown to reverse the metabolic
and faster processing of chylomicron remnants, a positive syndrome and non-alcoholic fatty liver disease without
physiological result (Mekki et al. 2002). The alternative medication and address a range of other biological indicators
explanation is that the cholesterol and SFA in butter increased (Hite et al. 2011; Peréz-Guisado and Munoz-Serrano 2011a,
the expression of apoE (see above), resulting in more 2011b). These diets have not only led to weight loss without
chylomicrons that were processed more efficiently by the direct calorie restriction they have resulted in improvement in
body. Animal fats as a constituent of adipose or muscle tissue the risk factors associated with CVD when animal and other
or dairy products and plant fats or oils in the form of nuts, seeds or fats are used (Foster et al. 2003; Volek et al. 2003; Herron et al.
oily fruits are absorbed slowly compared with refined cooking 2004; Sharman and Volek 2004; Volek and Sharman 2004;
oils or fats added to food, due to the structures and digestibility of Yancy et al. 2004, 2010; Brinkworth et al. 2009; Sacks et al.
the items (Berry et al. 2008; Damasceno et al. 2011; Michalski 2009). Moreover, trials of ketogenic diets in the treatment of
et al. 2013; Garcia et al. 2014). final stage cancer patients and in experimental systems (Tisdale
Where lipids are the overwhelming energy source then there et al. 1987; Breitkreutz et al. 2005; Zuccoli et al. 2010; Ho et al.
is substantial generation of ketone bodies, and there are 2011; Klement and Kaemmerer 2011; Schmidt et al. 2011; Chang
some benefits to be had from the metabolism of ketone bodies et al. 2013) have occurred, with some interesting results of
(Veech et al. 2001; Volek et al. 2008). The ketone bodies reduction in tumour size, reduction of cachexia, or delay of
b-hydroxybutyrate and acetoacetate are deliberately generated initiation of cancer. Ketogenic diets continue to be used to
from FA and are not a consequence of incomplete glucose treat some classes of epilepsy (Freeman et al. 1998; Kossoff
metabolism via the tricarboxylic acid cycle (Krebs 1966; et al. 2006; Neal et al. 2008), and have been suggested for other
Krebs et al. 1971). These are a form of energy from fat that is mental disorders or dementias including Alzheimer’s disease
directly soluble in aqueous solution rather than either being and Parkinson’s disease (VanItallie and Nufert 2003; Kim
carried as NEFA attached to albumin or TAG carried via et al. 2007; Kossoff and Hartman 2012). A random controlled
serum cholesterol or chylomicrons, and are the only metabolite trial of an additive to the normal diet, AC-1202, consisting of
from FA that can be directly metabolised by the brain (Cahill short- and medium-chain TAG derived from coconut oil and
2006). In a further parallel to serum glucose, levels of ketone that are metabolised to ketone bodies, has shown some
bodies are regulated by insulin, so that a pulse of higher levels improvement in Alzheimer’s disease sufferers from ketone
of ketone bodies increases insulin thereby reducing release of body production (Henderson et al. 2009). Therapeutic doses
lipid from adipocytes (Hawkins et al. 1971). It is thought that were 20 g per day, which generated similar levels of ketone
ancestral human diets would have generated ketone bodies for bodies to a low carbohydrate diet. Butter fat consists of >10% of
parts of the day or for days (Krebs et al. 1971; Veech et al. 2001; short-chain FA and a further 15% of the medium-chain SFA
Volek et al. 2008), because they are metabolites associated with of C12:0 and C14:0, which are rapidly oxidised in the liver
starvation (Cahill 2006). Although levels of serum ketone bodies (Bach and Babayan 1982; MacDougall et al. 1996; DeLany
have not been measured in traditional hunter-gatherers, there is et al. 2000) and would therefore generate increased levels of
evidence from contemporary study of some hunter-gatherers of ketone bodies in a high fat but not necessarily low carbohydrate
absence of food for days (Stefansson 1912; Marlowe 2005). In diet.
Animal fats back on the table Animal Production Science 843

Finally, at the opposite extreme, consumption of large combinations of fish meal. Some research suggests that farmed
amounts of sugar, refined carbohydrate and food fish such as salmon have the ability to generate their own long-
overconsumption in general can lead to obesity, high serum chain n-3 PUFA when the diet is limiting (Sanden et al. 2011).
glucose and hyperinsulinaemia. The effects of high serum Approximately 35–45% of chicken and other poultry fat is
glucose and hyperinsulinaemia, hall marks of type 2 diabetes, MUFA, between 22 and 27% of the fat is CISFA, 13–26% of
are well known and are associated with a wide range of chronic fat is PUFA depending on species and method of rearing, but there
diseases of Western civilisation (Kuusisto et al. 1997; Xu et al. can be large changes in long-chain n-3 PUFA if the ration contains
2004; Friberg et al. 2007; Xue and Michels 2007; Johnson et al. higher levels of a-linolenic acid (Chartrin et al. 2006; Jia et al.
2009; Orgel and Mittelman 2013). High serum glucose is 2010; Givens et al. 2011). In pigs there are smaller changes in
functionally related to the glycosylation of protein, which stearic acid, MUFA and PUFA with different rations and
increases the rate of aging of tissues. High serum glucose is genotypes than in chickens but CISFA are ~27% of the fat and
also functionally related to the increased glycosylation of small can as low as 21% for free-range pigs (Rodríguez-Sánchez et al.
dense LDL-C and subsequent damage to apoB-100 molecules 2010; Razmaite et al. 2011; Barea et al. 2013). The value of the
within the blood stream (Younis et al. 2013), contributing OMR is dependent on the food source. Interestingly, genetic
to atherosclerosis. Serum glucose is needed for cancer cell modification of pigs with the nematode delta-3 desaturase results
growth, as cancerous cells are switched to obtaining energy in animals with a lower OMR even if fed diets high in n-6 PUFA
from aerobic glycolysis, the Warburg effect. Cancerous cells (Ren et al. 2011). This has not yet been reported in other food
use the intermediates of the glycolytic pathway to generate animal species.
FA and other biosynthetic intermediates within the cell so as Ruminants have low levels of PUFA in their fat due to bio-
to generate cell membranes and organelles and thereby allow cell hydrogenation of dietary PUFA (Doreau and Ferlay 1994)
growth and division, and this is what most of the glucose is although there are differences in ruminants in the amount of
used for (Warburg 1956; Wang et al. 2012). Paradoxically, these oleate depending on genetics and feed source (Yang et al. 1999a).
cells do not derive much energy from either ketone bodies or One of the major effects on ruminant fat is the ratio of stearate to
b-oxidation of FA, irrespective of the circulating level of oleate, which depends on the location of the fat within the body:
FA. Carbohydrate sources vary in their ability to maintain high the closer to the surface the higher the oleate and the lower the
serum glucose and promote insulin resistance, with recent stearate (Meng et al. 1969; West and Shaw 1975; Morin 2007;
research showing that fructose, and by association sucrose, Staerfl et al. 2011). Despite the difference in total SFA between
have a much higher ability to promote insulin insensitivity free-range chicken, pig and ruminant fat, they contain very similar
and, consequently, a prolonged elevation in serum glucose levels of CISFA, in a range ~25%. Although the level of PUFA in
than glucose itself (Stanhope et al. 2009). Individuals respond ruminant fat is much lower than in monogastric fat, the OMR is
differently to these two factors, leading to correlations between still dependent on the ration or type of feed, with lower OMR
disorders. For example, diabetic individuals are more likely achievable on feed if higher levels of n-3 fats are used (Bobe et al.
to have CVD, or a cancer, or either vascular dementia or 2007). Changing the OMR in ruminant feed will affect the OMR
Alzheimer’s disease (Stamler et al. 1993; Luchsinger et al. of PUFA available for human consumption, and this would be a
2001). Non-diabetic individuals with Alzheimer’s disease are benefit. Whether the feeding of cattle in feedlots will grow or
more likely to have high serum glucose and hyperinsulinaemia, decline in the future will be affected by a range of factors including
even though BMI is not associated to Alzheimer’s disease. Some amount of methane produced per kilogram meat produced, the
of these disorders have historically been blamed on high fat cost of feedlot rations compared with the cost and requirement
consumption using evidence from ecological comparisons, but for biodiesel and other fuels, and the availability of rangeland for
the evidence from high fat ketogenic diets (cf. above) suggests pasture for ruminants.
instead that these disorders are due to food overconsumption The palatability of animal foods is affected by the amount and
rather than fat overconsumption. Obviously, animal fat is not a composition of its fat, but at present, in Western countries like
panacea for all ills, but avoidance of animal fat is no panacea Australia, a lot of emphasis is placed on reducing the amount of
either. fat in livestock. Palatability and eating quality of meat is related
to increased fat content, as reported in tests of consumers, but
consumers in many Western countries actively select leaner cuts
Recommendations for animal industries when meat is presented raw (Wood et al. 1999; Thompson 2004;
If humans are to consume animal fat then the best quality fat Dransfield et al. 2005; Polkinghorne and Thompson 2010; Utrilla
should be produced (Kelly et al. 2001; Tume 2004; Givens 2005; et al. 2010). Although it is suggested that this reduction in meat fat
Shingfield et al. 2013). This review suggests that this results in will improve human health, as this review has shown, this claim is
some clear selection and production/nutrition goals for animals. dubious. This demand for leaner meat has led to some distortions
These goals are that where possible animals should be produced in selection and production goals. From poultry to cattle, animals
with a low OMR, that long-chain n-3 PUFA should be increased, are selected for more meat and less fat (Abasht et al. 2006;
that higher levels of oleate or stearate and lower levels of palmitate Lagarrigue et al. 2006; Givens et al. 2011), and meat is presented
should be encouraged, but that increased n-6 PUFA content need with more fat trimmed from the cuts. This has led to fat being
not be encouraged. discarded and, in some cases, excess animal fat burned for fuel
The composition of the fat of monogastric animals is changed (Fairlie 2010), which is wasted production. Selecting animals
by the feed they eat. Farmed fish are known to have lower levels of for more meat, greater efficiency, greater productivity, and less
long-chain n-3 PUFA and many of the most valuable fish are fed fat has occasionally resulted in negative consequences for the
844 Animal Production Science W. Barendse

animals themselves, such as reductions in fertility and fecundity, Albrink MJ, Man EB (1959) Serum triglycerides in coronary artery disease.
dystocia, porcine stress syndrome, Rendement Napole, or skeletal Archives of Internal Medicine 103, 4–8. doi:10.1001/archinte.1959.
problems (Carlson et al. 1980; Hanset et al. 1982; Enfält et al. 00270010010002
1997; Grobet et al. 1997; Pitchford 2004). Changing the selection Aldai N, Dugan MER, Kramer JKG, Martinez A, Lopez-Campos O,
Mantecon AR, Osoro K (2011) Length of concentrate finishing affects
goal of more meat and less fat may well be intractable, however, as
the fatty acid composition of grass-fed and genetically lean beef: an
it is partly a response to consumer preference, and consumer
emphasis on trans-18:1 and conjugated linoleic acid profiles. Animal 5,
preference can take decades to change. 1643–1652. doi:10.1017/S1751731111000607
Nevertheless, it is not impossible for consumer sentiment to Alexander DD, Morimoto LM, Mink PJ, Lowe KA (2010) Summary
change, a newspaper article titled ‘Butter crisis spreads in and meta-analysis of prospective studies of animal fat intake and breast
Norway’ (Anonymous 2011) reported that due to a high fat cancer. Nutrition Research Reviews 23, 169–179. doi:10.1017/S0954422
low carbohydrate diet craze Norway ran out of butter in the 41000003X
lead in to the Christmas period. New formulations of products, Anderson KE (2011) Comparison of fatty acid, cholesterol, and vitamin A
such as Christmas Puddings and Chicken Liver Pate, are and E composition in eggs from hens housed in conventional cage and
appearing on Australian supermarket shelves with ingredients range production facilities. Poultry Science 90, 1600–1608. doi:10.3382/
including animal fats and margarines made from edible animal ps.2010-01289
tallow (change observed between December 2012 and April Anonymous (2011) Butter crisis spreads in Norway. The Australian 15
November 2011, 10.
2013) that previously had potato starch as stabiliser or
Antar MA, Hodges RE, Ohlson MA (1964) Changes in retail market food
vegetable shortening only. Prominent medical professionals supplies in the United States in the last seventy years in relation to the
are starting to say that it is better to control sugar, especially incidence of Coronary Heart Disease, with special reference to dietary
fructose and thereby sucrose (Lustig et al. 2012), and that carbohydrates and essential fatty acids. The American Journal of Clinical
controlling dietary saturated fat is irrelevant, so it may be that Nutrition 14, 169–178.
the wheel has started to turn. Animal industries should be aware of Appel LJ (2008) Dietary patterns and longevity: expanding the Blue Zones.
these trends and need to take advantage of them when they arise, Circulation 118, 214–215. doi:10.1161/CIRCULATIONAHA.108.
because changing selection goals or production practises does not 788497
occur overnight. More emphasis should be placed on healthy fat Arai Y, Hirose N, Yamamura K, Shimizu K, Takayama M, Ebihara Y, Osono
from animals, not just from fish, but also from livestock of all Y (2001) Serum insulin-like growth factor-1 in centenarians: implications
kinds. of IGF-1 as a rapid turnover protein. Gerontology Series A 56, M79–M82.
Archer SY, Meng SF, Shei A, Hodin RA (1998) p21(WAF1) is required
for butyrate-mediated growth inhibition of human colon cancer cells.
Acknowledgements Proceedings of the National Academy of Sciences, USA 95, 6791–6796.
I thank J. Henshall, D. Topping, and A. Yang for critically reading the doi:10.1073/pnas.95.12.6791
manuscript. Although the author has been supported by funds from Meat Aune D, Chan DSM, Vieira AR, Rosenblatt DAN, Vieira R, Greenwood DC,
& Livestock Australia, Dairy Australia, and the Beef Cooperative Research Kampman E, Norat T (2013) Red and processed meat intake and
Centre in the past, no meat or dairy industry body commissioned, funded or risk of colorectal adenomas: a systematic review and meta-analysis of
had any part in this review. Any discussion of the role of animal food in human epidemiological studies. Cancer Causes & Control 24, 611–627.
nutrition these days needs a declaration of biases: the author was raised a strict doi:10.1007/s10552-012-0139-z
whole-food ovo-lacto vegetarian and occasionally relapses to that state; this Austin MA, Breslow JL, Hennekens CH, Buring JE, Willett WC, Krauss RM
review is a response to the author’s question of his own research, ‘Why are we (1988) Low density lipoprotein subclass patterns and risk of myocardial
trying to increase intramuscular fat if animal fat is so bad for us?’ infarction. Journal of the American Medical Association 260, 1917–1921.
doi:10.1001/jama.1988.03410130125037
Bach AC, Babayan VK (1982) Medium chain triglycerides – an update. The
References American Journal of Clinical Nutrition 36, 950–962.
Abasht B, Dekkers JCM, Lamont SJ (2006) Review of quantitative trait loci Barea R, Isabel B, Nieto R, Lopez-Bote C, Aguilera JF (2013) Evolution of
identified in the chicken. Poultry Science 85, 2079–2096. doi:10.1093/ps/ the fatty acid profile of subcutaneous back-fat adipose tissue in
85.12.2079 growing Iberian and Landrace · Large White pigs. Animal 7, 688–698.
Abbey M, Belling GB, Noakes M, Hirata F, Nestel PJ (1993) Oxidation doi:10.1017/S175173111200184X
of low-density liproteins – intraindividual variability and the effect of Barrows BR, Parks EJ (2006) Contributions of different fatty acid sources to
dietary linoleate supplementation. The American Journal of Clinical very low-density lipoprotein-triacylglycerol in the fasted and fed states.
Nutrition 57, 391–398. The Journal of Clinical Endocrinology and Metabolism 91, 1446–1452.
Abrams JJ, Grundy SM, Ginsberg H (1981) Metabolism of plasma doi:10.1210/jc.2005-1709
triglycerides in hypothyroidism and hyperthyroidism in man. Journal Basu S, Yoffe P, Hills N, Lustig RH (2013) The relationship of sugar to
of Lipid Research 22, 307–322. population-level diabetes prevalence: an econometric analysis of repeated
Acheson KJ, Schutz Y, Bessard T, Anantharaman K, Flatt JP, Jequier E (1988) cross-sectional data. PLoS ONE 8, e57873. doi:10.1371/journal.pone.
Glycogen storage capacity and de novo lipogenesis during massive 0057873
carbohydrate overfeeding in man. The American Journal of Clinical Berry SEE, Tydeman EA, Lewis HB, Phalora R, Roxborough J, Picout DR,
Nutrition 48, 240–247. Ellis PR (2008) Manipulation of lipid bioavailability of almond seeds
Ackman RG, Sebedio J-L (1981) Fatty acids and sterols in oils from canola influences postprandial lipemia in health human subjects. The American
screenings. Journal of the American Oil Chemists’ Society 58, 594–598. Journal of Clinical Nutrition 88, 922–929.
doi:10.1007/BF02672372 Beulens JWJ, Van der A DL, Grobbee DE, Sluijs I, Spijkerman AMW, van der
Ahrens EH Jr, Hirsch J, Insull W Jr, Tsaltas TT, Blomstrand R, Peterson ML Schouw YT (2010) Dietary phylloquinone and menaquinones intakes and
(1957) The influence of dietary fats on serum-lipid levels in man. Lancet risk of type 2 diabetes. Diabetes Care 33, 1699–1705. doi:10.2337/dc09-
269, 943–953. doi:10.1016/S0140-6736(57)91280-1 2302
Animal fats back on the table Animal Production Science 845

Bézard J, Bugaut M, Clement G (1971) Triglyceride composition of low density lipoprotein subclasses. Journal of Lipid Research 36,
coconut oil. Journal of the American Oil Chemists’ Society 48, 462–472.
134–139. doi:10.1007/BF02545736 Carlson JP, Christian LL, Kuhlers DL, Rasmusen BA (1980) Influence of
Bézard J, Blond JP, Bernard A, Clouet P (1994) The metabolism and the porcine stress syndrome on production and carcass traits. Journal
availability of essential fatty acids in animal and human tissues. of Animal Science 50, 21–28.
Reproduction, Nutrition, Development 34, 539–568. doi:10.1051/ Carlson JJ, Eisenmann JC, Norman GJ, Ortiz KA, Young PC (2011)
rnd:19940603 Dietary fiber and nutrient density are inversely associated with the
Blaxter KL, Webster AJF (1991) Animal production and food: real problems metabolic syndrome in US adolescents. Journal of the American
and paranoia. Animal Production 53, 261–269. doi:10.1017/S000335 Dietetic Association 111, 1688–1695. doi:10.1016/j.jada.2011.08.008
6100020250 Carluccio A, Contaldo G (2012) ‘Two greedy Italians eat Italy.’ (Quadrille
Bobe G, Zimmerman S, Hammond EG, Freeman AE, Porter PA, Luhman Publishing: London)
CM, Beitz DC (2007) Butter composition and texture from cows with Carro E, Torres-Aleman I (2006) Serum insulin-like growth factor I in
different milk fatty acid compositions fed fish oil or roasted soybeans. brain function. The Keio Journal of Medicine 55, 59–63. doi:10.2302/
Journal of Dairy Science 90, 2596–2603. doi:10.3168/jds.2006-875 kjm.55.59
Bocuse P (1988) ‘The cuisine of Paul Bocuse.’ (Grafton Books: London) Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum
Boerwinkle E, Brown S, Sharrett AR, Heiss G, Patsch W (1994) insulin-like growth factor I regulates brain amyloid-levels. Nature
Apolipoprotein E polymorphism influences postprandial retinyl Medicine 8, 1390–1397. doi:10.1038/nm1202-793
palmitate but not triglyceride concentrations. American Journal of Castelli WP (1986) The triglyceride issue – a view from Framingham.
Human Genetics 54, 341–360. American Heart Journal 112, 432–437. doi:10.1016/0002-8703(86)
Bonanome A, Grundy SM (1988) Effect of dietary stearic acid on plasma 90296-6
cholesterol and lipoprotein levels. The New England Journal of Medicine Castelli WP (1992) Concerning the possibility of a nut. Archives of Internal
318, 1244–1248. doi:10.1056/NEJM198805123181905 Medicine 152, 1371–1372. doi:10.1001/archinte.1992.00400190013003
Bousser MG, Amarenco P, Chamorro A, Fisher M, Ford I, Fox KM, Hennerici Castelli WP, Garrison RJ, Wilson PWF, Abbott RD, Kalousdian S, Kannel
MG, Mattle HP, Rothwell PM, de Cordoue A, Fratacci MD, Investigators WB (1986) Incidence of coronary heart disease and lipoprotein
PS (2011) Terutroban versus aspirin in patients with cerebral ischaemic cholesterol levels – the Framingham study. Journal of the American
events (PERFORM): a randomised, double-blind, parallel-group trial. Medical Association 256, 2835–2838. doi:10.1001/jama.1986.03380
Lancet 377, 2013–2022. doi:10.1016/S0140-6736(11)60600-4 200073024
Bracco U (1994) Effect of triglyceride structure on fat absorption. The Chajes V, Torres-Mejia G, Biessy C, Ortega-Olvera C, Angeles-Llerenas A,
American Journal of Clinical Nutrition 60, 1002S–1009S. Ferrari P, Lazcano-Ponce E, Romieu I (2012) Omega-3 and omega-6
Breitkreutz R, Tesdal K, Jentschura D, Haas O, Leweling H, Holm E (2005) polyunsaturated fatty acid intakes and the risk of breast cancer in Mexican
Effects of a high-fat diet on body composition in cancer patients receiving women: impact of obesity status. Cancer Epidemiology, Biomarkers &
chemotherapy: a randomized controlled study. Wiener Klinische Prevention 21, 319–326. doi:10.1158/1055-9965.EPI-11-0896
Wochenschrift 117, 685–692. doi:10.1007/s00508-005-0455-3 Chang HT, Olson LK, Schwartz KA (2013) Ketolytic and glycolytic
Brenna JT (2002) Efficiency of conversion of alpha-linolenic acid to long enzymatic expression profiles in malignant gliomas: implication for
chain n-3 fatty acids in man. Current Opinion in Clinical Nutrition and ketogenic diet therapy. Nutrition & Metabolism 10, 47. doi:10.1186/
Metabolic Care 5, 127–132. doi:10.1097/00075197-200203000-00002 1743-7075-10-47
Brennan SF, Cantwell MM, Cardwell CR, Velentzis LS, Woodside JV (2010) Chapman MJ, Ginsberg HN, Amarenco P, Andreotti F, Boren J, Catapano AL,
Dietary patterns and breast cancer risk: a systematic review and meta- Descamps OS, Fisher E, Kovanen PT, Kuivenhoven JA, Lesnik P, Masana
analysis. The American Journal of Clinical Nutrition 91, 1294–1302. L, Nordestgaard BG, Ray KK, Reiner Z, Taskinen MR, Tokgozoglu L,
doi:10.3945/ajcn.2009.28796 Tybjaerg-Hansen A, Watts GF Soc European Atherosclerosis (2011)
Brinkworth GD, Noakes M, Buckley JD, Keogh JB, Clifton PM (2009) Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol
Long-term effects of a very-low-carbohydrate weight loss diet compared in patients at high risk of cardiovascular disease: evidence and guidance
with an isocaloric low-fat diet after 12 mo. The American Journal of for management. European Heart Journal 32, 1345–1361. doi:10.1093/
Clinical Nutrition 90, 23–32. doi:10.3945/ajcn.2008.27326 eurheartj/ehr112
Brown MS, Goldstein JL (1983) Lipoprotein metabolism in the macrophage: Chartrin P, Bernadet MD, Guy G, Mourot J, Duclos MJ, Baeza E (2006)
implications for cholesterol deposition in atherosclerosis. Annual Review The effects of genotype and overfeeding on fat level and composition of
of Biochemistry 52, 223–261. doi:10.1146/annurev.bi.52.070183.001255 adipose and muscle tissues in ducks. Animal Research 55, 231–244.
Buffa R, Floris G, Lodde M, Cotza M, Marini E (2010) Nutritional status in doi:10.1051/animres:2006011
the healthy longeval population from Sardinia (Italy). The Journal of Cleave TL (1974) ‘The saccharine disease.’ (John Wright & Sons: Bristol)
Nutrition, Health & Aging 14, 97–102. doi:10.1007/s12603-010-0018-9 Connolly BS, Barnett C, Vogt KN, Li T, Stone J, Boyd NF (2002) A
Burdge GC, Calder PC (2005) Conversion of alpha-linolenic acid to longer- meta-analysis of published literature on waist-to-hip ratio and risk
chain polyunsaturated fatty acids in human adults. Reproduction, of breast cancer. Nutrition and Cancer 44, 127–138. doi:10.1207/
Nutrition, Development 45, 581–597. doi:10.1051/rnd:2005047 S15327914NC4402_02
Burkitt DP (1973) Some diseases characteristic of modern western Corbo RM, Scacchi R (1999) Apolipoprotein E (APOE) allele distribution in
civilization. British Medical Journal 1, 274–278. doi:10.1136/bmj. the world. Is APOE*4 a ‘thrifty’ allele? Annals of Human Genetics 63,
1.5848.274 301–310. doi:10.1046/j.1469-1809.1999.6340301.x
Cachaldora P, Garcia-Rebollar P, Alvarez C, Mendez J, De Blas JC (2008) Cordain L, Eaton SB, Miller JB, Mann N, Hill K (2002a) The paradoxical
Double enrichment of chicken eggs with conjugated linoleic acid and n-3 nature of hunter-gatherer diets: meat-based, yet non-atherogenic.
fatty acids through dietary fat supplementation. Animal Feed Science and European Journal of Clinical Nutrition 56, S42–S52. doi:10.1038/
Technology 144, 315–326. doi:10.1016/j.anifeedsci.2007.10.010 sj.ejcn.1601353
Cahill GF (2006) Fuel metabolism in starvation. Annual Review of Nutrition Cordain L, Watkins BA, Florant GL, Kelher M, Rogers L, Li Y (2002b)
26, 1–22. Fatty acid analysis of wild ruminant tissues: evolutionary implications
Campos H, Dreon DM, Krauss RM (1995) Associations of hepatic and for reducing diet-related chronic disease. European Journal of Clinical
lipoprotein lipase activities with changes in dietary composition and Nutrition 56, 181–191. doi:10.1038/sj.ejcn.1601307
846 Animal Production Science W. Barendse

Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, Watkins BA, Cancer Research and Treatment 127, 23–31. doi:10.1007/s10549-011-
O’Keefe JH, Brand-Miller J (2005) Origins and evolution of the Western 1467-5
diet: health implications for the 21st century. The American Journal of Doreau M, Ferlay A (1994) Digestion and utilization of fatty-acids
Clinical Nutrition 81, 341–354. by ruminants. Animal Feed Science and Technology 45, 379–396.
Costello C, Ovando D, Hilborn R, Gaines SD, Deschenes O, Lester SE (2012) doi:10.1016/0377-8401(94)90039-6
Status and solutions for the world’s unassessed fisheries. Science 338, Dorfman SE, Lichtenstein AH (2006) Dietary fatty acids differentially
517–520. doi:10.1126/science.1223389 modulate messenger RNA abundance of low-density lipoprotein
Couvreur S, Hurtaud C, Lopez C, Delaby L, Peyraud JL (2006) The linear receptor, 3-hydroxy-3-methylglutaryl coenzyme A reductase, and
relationship between the proportion of fresh grass in the cow diet, milk microsomal triglyceride transfer protein in Golden-Syrian hamsters.
fatty acid composition, and butter properties. Journal of Dairy Science 89, Metabolism: Clinical and Experimental 55, 635–641. doi:10.1016/
1956–1969. doi:10.3168/jds.S0022-0302(06)72263-9 j.metabol.2005.12.005
Curtin F, Morabia A, Bernstein M, Dederding J-P (1998) A population survey Dorfman SE, Laurent D, Gounarides JS, Li X, Mullarkey TL, Rocheford EC,
of bowel habits in urban Swiss men. European Journal of Public Health Sari-Sarraf F, Hirsch EA, Hughes TE, Commerford SR (2009) Metabolic
8, 170–175. doi:10.1093/eurpub/8.2.170 implications of dietary trans-fatty acids. Obesity 17, 1200–1207.
Daley CA, Abbott A, Doyle PS, Nader GA, Larson S (2010) A review of doi:10.1038/oby.2009.144
fatty acid profiles and antioxidant content in grass-fed and grain-fed Dougherty RM, Allman MA, Iacono JM (1995) Effects of diets containing
beef. Nutrition Journal 9, 10. doi:10.1186/1475-2891-9-10 high and low amounts of stearic acid on plasma lipoprotein fractions
Damasceno NRT, Perez-Heras A, Serra M, Cofan M, Sala-Vila A, Salas- and fecal fatty acid excretion of men. The American Journal of Clinical
Salvado J, Ros E (2011) Crossover study of diets enriched with virgin Nutrition 61, 1120–1128.
olive oil, walnuts or almonds. Effects on lipids and other cardiovascular Dransfield E, Ngapo TM, Nielsen NA, Bredahl L, Sjoden PO, Magnusson M,
risk markers. Nutrition, Metabolism, and Cardiovascular Diseases 21, Campo MM, Nute GR (2005) Consumer choice and suggested price for
S14–S20. doi:10.1016/j.numecd.2010.12.006 pork as influenced by its appearance, taste and information concerning
de Hollander EL, Bemelmans WJE, Boshuizen HC, Friedrich N, country of origin and organic pig production. Meat Science 69, 61–70.
Wallaschofski H, Guallar-Castillon P, Walter S, Zillikens MC, doi:10.1016/j.meatsci.2004.06.006
Rosengren A, Lissner L, Bassett JK, Giles GG, Orsini N, Heim N, Dreon DM, Fernstrom HA, Miller B, Krauss RM (1995) Apolipoprotein E
Visser M, de Groot L, Collaborators WCE (2012) The association isoform phenotype and LDL subclass response to a reduced fat diet.
between waist circumference and risk of mortality considering body Arteriosclerosis, Thrombosis, and Vascular Biology 15, 105–111.
mass index in 65- to 74-year-olds: a meta-analysis of 29 cohorts doi:10.1161/01.ATV.15.1.105
involving more than 58 000 elderly persons. International Journal of Dreon DM, Fernstrom HA, Campos H, Blanche P, Williams PT, Krauss RM
Epidemiology 41, 805–817. doi:10.1093/ije/dys008 (1998) Change in dietary saturated fat intake is correlated with change in
de Lorgeril M, Renaud S, Mamelle N, Salen P, Martin J-L, Monjaud I, mass of large low-density-lipoprotein particles in men. The American
Guidollet J, Touboul P, Delaye J (1994) Mediterranean alpha-linolenic Journal of Clinical Nutrition 67, 828–836.
acid-rich diet in secondary prevention of coronary heart disease. Lancet Dreon DM, Fernstrom HA, Williams PT, Krauss RM (1999) A very-low-fat
343, 1454–1459. doi:10.1016/S0140-6736(94)92580-1 diet is not associated with improved lipoprotein profiles in men with a
de Lorgeril M, Salen P, Martin J-L, Monjaud I, Delaye J, Mamelle N (1999) predominance of large, low-density lipoproteins. The American Journal
Mediterranean diet, traditional risk factors, and the rate of cardiovascular of Clinical Nutrition 69, 411–418.
complications after myocardial infarction: Final report of the Lyon Diet Duron E, Funalot B, Brunel N, Coste J, Quinquis L, Viollet C, Belmin J,
Heart Study. Circulation 99, 779–785. doi:10.1161/01.CIR.99.6.779 Jouanny P, Pasquier F, Treluyer JM, Epelbaum J, le Bouc Y, Hanon O
de Lorgeril M, Salen P, Martin JL, Boucher F, Paillard F, de Leiris J (2002) (2012) Insulin-like growth factor-I and insulin-like growth factor binding
Wine drinking and risks of cardiovascular complications after recent protein-3 in Alzheimer’s disease. The Journal of Clinical Endocrinology
acute myocardial infarction. Circulation 106, 1465–1469. doi:10.1161/ and Metabolism 97, 4673–4681. doi:10.1210/jc.2012-2063
01.CIR.0000029745.63708.E9 Echtay KS, Winkler E, Klingenberg M (2000) Coenzyme Q is an obligatory
de Roos NM, Schouten EG, Katan MB (2001) Consumption of a solid fat cofactor for uncoupling protein function. Nature 408, 609–613.
rich in lauric acid results in a more favorable serum lipid profile in healthy doi:10.1038/35046114
men and women than consumption of a solid fat rich in trans-fatty acids. Egeberg R, Olsen A, Christensen J, Halkjaer J, Jakobsen MU, Overvad K,
The Journal of Nutrition 131, 242–245. Tjonneland A (2013) Associations between red meat and risks for colon
DeLany JP, Windhauser MM, Champagne CM, Bray GA (2000) Differential and rectal cancer depend on the type of red meat consumed. The Journal
oxidation of individual dietary fatty acids in humans. The American of Nutrition 143, 464–472. doi:10.3945/jn.112.168799
Journal of Clinical Nutrition 72, 905–911. Egert S, Rimbach G, Huebbe P (2012) ApoE genotype: from geographic
Dent J, El-Serag HB, Wallander MA, Johansson S (2005) Epidemiology of distribution to function and responsiveness to dietary factors. The
gastrooesophageal reflux disease: a systematic review. Gut 54, 710–717. Proceedings of the Nutrition Society 71, 410–424. doi:10.1017/
doi:10.1136/gut.2004.051821 S0029665112000249
Di Vincenzo D, Maranz S, Serraiocco A, Vito R, Wiesman Z, Bianchi G Eisenmann JC (2003) Secular trends in variables associated with the
(2005) Regional variation in shea butter lipid and triterpene composition metabolic syndrome of North American children and adolescents: a
in four African countries. Journal of Agricultural and Food Chemistry review and synthesis. American Journal of Human Biology 15,
53, 7473–7479. doi:10.1021/jf0509759 786–794. doi:10.1002/ajhb.10214
Dilzer A, Park Y (2012) Implication of conjugated linoleic acid (CLA) in Elam MB, von Wronski MA, Cagen L, Thorngate F, Kumar P, Heimberg M,
human health. Critical Reviews in Food Science and Nutrition 52, Wilcox HG (1999) Apolipoprotein B mRNA editing and apolipoprotein
488–513. doi:10.1080/10408398.2010.501409 gene expression in the liver of hyperinsulinemic fatty Zucker rats:
Dickson Wright C (2011) ‘A history of English food.’ (Random House Books: relationship to very low density lipoprotein composition. Lipids 34,
UK) 809–816. doi:10.1007/s11745-999-0427-z
Dong JY, Zhang LJ, He K, Qin LQ (2011) Dairy consumption and risk of Elwood PC, Pickering JE, Givens DI, Gallacher JE (2010) The consumption
breast cancer: a meta-analysis of prospective cohort studies. Breast of milk and dairy foods and the incidence of vascular disease and
Animal fats back on the table Animal Production Science 847

diabetes: an overview of the evidence. Lipids 45, 925–939. doi:10.1007/ Fontana L, Partridge L, Longo VD (2010) Extending healthy life span – from
s11745-010-3412-5 yeast to humans. Science 328, 321–326. doi:10.1126/science.1172539
Enfält AC, Lundstrom K, Hansson I, Johansen S, Nystrom PE (1997) Ford ES, Ajani UA, Croft JB, Critchley JA, Labarthe DR, Kottke TE, Giles
Comparison of non-carriers and heterozygous carriers of the RN(–) WH, Capewell S (2007) Explaining the decrease in US deaths
allele for carcass composition, muscle distribution and technological from coronary disease, 1980–2000. The New England Journal of
meat quality in Hampshire-sired pigs. Livestock Production Science Medicine 356, 2388–2398. doi:10.1056/NEJMsa053935
47, 221–229. doi:10.1016/S0301-6226(96)01409-1 Forsyth JS, Varma S, Colvin M (1999) A randomised controlled study of the
Enig MG, Munn RJ, Keeney M (1978) Dietary fat and cancer trends – effect of long chain polyunsaturated fatty acid supplementation on stool
critique. Federation Proceedings 37, 2215–2220. hardness during formula feeding. Archives of Disease in Childhood 81,
Enser M, Richardson RI, Wood JD, Gill BP, Sheard PR (2000) Feeding 253–256. doi:10.1136/adc.81.3.253
linseed to increase the n-3 PUFA of pork: fatty acid composition of Foster GD, Wyatt HR, Hill JO, McGuckin BG, Brill C, Mohammed BS,
muscle, adipose tissue, liver and sausages. Meat Science 55, 201–212. Szapary PO, Rader DJ, Edman JS, Klein S (2003) A randomized trial of a
doi:10.1016/S0309-1740(99)00144-8 low-carbohydrate diet for obesity. The New England Journal of Medicine
Escoffier A (1921) ‘The complete guide to the art of modern cookery.’ 348, 2082–2090. doi:10.1056/NEJMoa022207
(Heinemann: London) Fraser GE, Shavlik DJ (2001) Ten years of life is it a matter of choice?
Esterbauer H, Gebicki J, Puhl H, Jurgens G (1992) The role of lipid Archives of Internal Medicine 161, 1645–1652. doi:10.1001/archinte.
peroxidation and antioxidants in oxidative modification of LDL. Free 161.13.1645
Radical Biology & Medicine 13, 341–390. doi:10.1016/0891-5849(92) Freedman LS, Kipnis V, Schatzkin A, Potischman N (2008) Methods of
90181-F epidemiology: evaluating the fat-breast cancer hypothesis – comparing
Evans A (2011) The French paradox and other ecological fallacies. dietary instruments and other developments. Cancer Journal (Sudbury,
International Journal of Epidemiology 40, 1486–1489. doi:10.1093/ Mass.) 14, 69–74. doi:10.1097/PPO.0b013e31816a5e02
ije/dyr138 Freeman JM, Vining EPG, Pillas DJ, Pyzik PL, Casey JC, Kelly MT (1998)
Evans AE, Ruidavets JB, McCrum EE, Cambou JP, McClean R, Dousteblazy The efficacy of the ketogenic diet – 1998: a prospective evaluation of
P, McMaster D, Bingham A, Patterson CC, Richard JL, Mathewson ZM, intervention in 150 children. Pediatrics 102, 1358–1363. doi:10.1542/
Cambien F (1995) Autre pays, autre coeurs? Dietary patterns, risk peds.102.6.1358
factors and ischaemic heart disease in Belfast and Toulouse. QJM: An Friberg E, Orsini N, Mantzoros CS, Wolk A (2007) Diabetes mellitus and risk
International Journal of Medicine 88, 469–477. of endometrial cancer: a meta-analysis. Diabetologia 50, 1365–1374.
Everitt AV, LeCouteur DG (2007) Life extension by calorie restriction in doi:10.1007/s00125-007-0681-5
humans. Annals of the New York Academy of Sciences 1114, 428–433. Fullerton SM, Clark AG, Weiss KM, Nickerson DA, Taylor SL, Stengard JH,
doi:10.1196/annals.1396.005 Salomaa V, Vartiainen E, Perola M, Boerwinkle E, Sing CF (2000)
Fairlie S (2010) ‘Meat: a benign extravagance.’ (Permanent Publications: Apolipoprotein E variation at the sequence haplotype level:
East Meon, UK) implications for the origin and maintenance of a major human
Féart C, Samieri C, Rondeau V, Amieva H, Portet F, Dartigues J-F, Scarmeas polymorphism. American Journal of Human Genetics 67, 881–900.
N, Barberger-Gateau P (2009) Adherence to a Mediterranean diet, doi:10.1086/303070
cognitive decline, and risk of dementia. Journal of the American Garcia C, Antona C, Robert B, Lopez C, Armand M (2014) The size and
Medical Association 302, 638–648. doi:10.1001/jama.2009.1146 interfacial composition of milk fat globules are key factors controlling
Fernandez ML, McNamara DJ (1989) Dietary fat mediated changes in hepatic triglycerides bioavailability in simulated human gastro-duodenal
apoprotein B/E receptor in the guinea pig – effect of polyunsaturated, digestion. Food Hydrocolloids 35, 494–504. doi:10.1016/j.foodhyd.
monounsaturated, and saturated fat. Metabolism: Clinical and 2013.07.005
Experimental 38, 1094–1102. doi:10.1016/0026-0495(89)90046-2 Gardner CD, Fortmann SP, Krauss RM (1996) Association of small low-
Fielding CJ, Fielding PE (1995) Molecular physiology of reverse cholesterol density lipoprotein particles with the incidence of coronary artery disease
transport. Journal of Lipid Research 36, 211–228. in men and women. Journal of the American Medical Association 276,
Flore R, Ponziano FR, Di Rienzo TA, Zocco MA, Flex A, Gerardino L, 875–881. doi:10.1001/jama.1996.03540110029028
Lupascu A, Santoro L, Santoliquido A, Di Stasio E, Chierici E, Lanti A, Gilsing AMJ, Weijenberg MP, Goldbohm RA, van den Brandt PA, Schouten
Tondi P, Gasbarrini A (2013) Something more to say about LJ (2011) Consumption of dietary fat and meat and risk of ovarian cancer
calcium homeostasis: the role of vitamin K2 in vascular calcification in the Netherlands cohort study. The American Journal of Clinical
and osteoporosis. European Review for Medical and Pharmacological Nutrition 93, 118–126. doi:10.3945/ajcn.2010.29888
Sciences 17, 2433–2440. Givens DI (2005) The role of animal nutrition in improving the nutritive
Fogerty AC, Ford GL, Svoronos D (1988) Octadeca-9,11-dienoic acid in value of animal-derived foods in relation to chronic disease. The
foodstuffs and in the lipids of human blood and breast milk. Nutrition Proceedings of the Nutrition Society 64, 395–402. doi:10.1079/
Reports International 38, 937–943. PNS2005448
Fontana L, Meyer TE, Klein S, Holloszy JO (2004) Long-term calorie Givens DI (2010) Milk and meat in our diet: good or bad for health? Animal
restriction is highly effective in reducing the risk for atherosclerosis in 4, 1941–1952. doi:10.1017/S1751731110001503
humans. Proceedings of the National Academy of Sciences, USA 101, Givens DI, Gibbs RA, Rymer C, Brown RH (2011) Effect of intensive vs
6659–6663. doi:10.1073/pnas.0308291101 free range production on the fat and fatty acid composition of whole birds
Fontana L, Villareal DT, Weiss EP, Racette SB, Steger-May K, Klein S, and edible portions of retail chickens in the UK. Food Chemistry 127,
Holloszy JO, Washington U (2007) Calorie restriction or exercise: effects 1549–1554. doi:10.1016/j.foodchem.2011.02.016
on coronary heart disease risk factors. A randomized, controlled trial. Glavind J, Hartmann S, Clemmesen J, Jessen KE, Dam H (1952) Studies
American Journal of Physiology. Endocrinology and Metabolism 293, on the role of lipoperoxides in human pathology II. The presence of
E197–E202. doi:10.1152/ajpendo.00102.2007 peroxidized lipids in the atherosclerotic aorta. Acta Pathologica et
Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO (2008) Long-term Microbiologica Scandinavica 30, 1–6. doi:10.1111/j.1699-0463.1952.
effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 tb00157.x
concentration in humans. Aging Cell 7, 681–687. doi:10.1111/j.1474- Godley PA, Campbell MK, Gallagher P, Martinson FEA, Mohler JL, Sandler
9726.2008.00417.x RS (1996) Biomarkers of essential fatty acid consumption and risk of
848 Animal Production Science W. Barendse

prostatic carcinoma. Cancer Epidemiology, Biomarkers & Prevention 5, Harvei S, Bjerve KS, Tretli S, Jellum E, Robsahm TE, Vatten L (1997)
889–895. Prediagnostic level of fatty acids in serum phospholipids: omega-3 and
Gogos CA, Ginopoulos P, Salsa B, Apostolidou E, Zoumbos NC, omega-6 fatty acids and the risk of prostate cancer. International Journal
Kalfarentzos F (1998) Dietary omega-3 polyunsaturated fatty acids of Cancer 71, 545–551. doi:10.1002/(SICI)1097-0215(19970516)
plus vitamin E restore immunodeficiency and prolong survival for 71:4<545::AID-IJC7>3.0.CO;2-U
severely ill patients with generalized malignancy – a randomized Havel RJ (1957a) Early effects of fasting and of carbohydrate ingestion on
control trial. Cancer 82, 395–402. doi:10.1002/(SICI)1097-0142 lipids and lipoproteins of serum in man. The Journal of Clinical
(19980115)82:2<403::AID-CNCR21>3.0.CO;2-1 Investigation 36, 855–859. doi:10.1172/JCI103492
Gouda HN, Critchley J, Powles J, Capewell S (2012) Why choice of metric Havel RJ (1957b) Early effects of fat ingestion on lipids and lipoproteins
matters in public health analyses: a case study of the attribution of credit of serum in man. The Journal of Clinical Investigation 36, 848–854.
for the decline in coronary heart disease mortality in the US and other doi:10.1172/JCI103491
populations. BMC Public Health 12, 88. doi:10.1186/1471-2458-12-88 Havel RJ, Eder HA, Bragdon JH (1955) Distribution and chemical
Grande F, Anderson JT, Keys A (1970) Comparison of effects of palmitic composition of ultracentrifugally separated lipoproteins in human
and stearic acids in diet on serum cholesterol in man. The American serum. The Journal of Clinical Investigation 34, 1345–1353.
Journal of Clinical Nutrition 23, 1184–1193. doi:10.1172/JCI103182
Grau K, Hansen T, Holst C, Astrup A, Saris WHM, Arner P, Rossner S, Hawkins RA, Alberti KGM, Houghton CR, Williams DH, Krebs HA (1971)
Macdonald I, Polak J, Oppert JM, Langin D, Martinez JA, Pedersen O, Effect of acetoacetate on plasma insulin concentration. Biochemical
Sorensen TIA (2009) Macronutrient-specific effect of FTO rs9939609 in Journal 125, 541.
response to a 10-week randomized hypo-energetic diet among obese Hayes KC, Pronczuk A (2010) Replacing trans fat: the argument for palm
Europeans. International Journal of Obesity 33, 1227–1234. doi:10.1038/ oil with a cautionary note on interesterification. Journal of the American
ijo.2009.159 College of Nutrition 29, 253S–284S. doi:10.1080/07315724.2010.
Griinari JM, Bauman DE (1999) Biosynthesis of conjugated linoleic acid 10719842
and its incorporation into meat and milk in ruminants. In ‘Advances Henderson ST, Vogel JL, Barr LJ, Garvin F, Jones JJ, Costantini LC (2009)
in conjugated linoleic acid research. Vol. 1’. (Eds MP Yurawecz, MM Study of the ketogenic agent AC-1202 in mild to moderate Alzheimer’s
Mossoba, JKG Kramer, MW Pariza, GJ Nelson) pp. 180–200. (American disease: a randomized, double-blind, placebo-controlled, multicenter trial.
Oil Chemists Society: Champaign, IL)
Nutrition & Metabolism 6, 31. doi:10.1186/1743-7075-6-31
Grobet L, Martin LJR, Poncelet D, Pirottin D, Brouwers B, Riquet J,
Herron KL, Lofgren IE, Sharman M, Volek JS, Fernandez ML (2004) High
Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R,
intake of cholesterol results in less atherogenic low-density lipoprotein
Hanset R, Georges M (1997) A deletion in the bovine myostatin gene
particles in men and women independent of response classification.
causes the double-muscled phenotype in cattle. Nature Genetics 17,
Metabolism: Clinical and Experimental 53, 823–830. doi:10.1016/
71–74. doi:10.1038/ng0997-71
j.metabol.2003.12.030
Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, Wei M, Madia
Hertog MGL, Feskens EJM, Hollman PCH, Katan MB, Kromhout D (1993)
F, Cheng CW, Hwang D, Martin-Montalvo A, Saavedra J, Ingles S,
Dietary antioxidant flavonoids and risk of coronary heart disease: the
de Cabo R, Cohen P, Longo VD (2011) Growth hormone receptor
Zutphen elderly study. Lancet 342, 1007–1011. doi:10.1016/0140-6736
deficiency is associated with a major reduction in pro-aging signaling,
(93)92876-U
cancer, and diabetes in humans. Science Translational Medicine 3,
Hiatt WR (2001) Medical treatment of peripheral arterial disease and
70ra13. doi:10.1126/scitranslmed.3001845
claudication. The New England Journal of Medicine 344, 1608–1621.
Ha YL, Grimm NK, Pariza MW (1987) Anticarcinogens from fried ground-
beef: heat-altered derivatives of linoleic acid. Carcinogenesis 8, doi:10.1056/NEJM200105243442108
Hite AH, Berkowitz VG, Berkowitz K (2011) Low-carbohydrate diet
1881–1887. doi:10.1093/carcin/8.12.1881
Halliwell B (2006) Oxidative stress and neurodegeneration: where are we review: shifting the paradigm. Nutrition in Clinical Practice 26,
now? Journal of Neurochemistry 97, 1634–1658. doi:10.1111/j.1471- 300–308. doi:10.1177/0884533611405791
4159.2006.03907.x Ho VW, Leung K, Hsu A, Luk B, Lai J, Shen SY, Minchinton AI, Waterhouse
Halpern BS, Longo C, Hardy D, McLeod KL, Samhouri JF, Katona SK, D, Bally MB, Lin W, Nelson BH, Sly LM, Krystal G (2011) A low
Kleisner K, Lester SE, O’Leary J, Ranelletti M, Rosenberg AA, carbohydrate, high protein diet slows tumor growth and prevents cancer
Scarborough C, Selig ER, Best BD, Brumbaugh DR, Chapin FS, initiation. Cancer Research 71, 4484–4493. doi:10.1158/0008-5472.
Crowder LB, Daly KL, Doney SC, Elfes C, Fogarty MJ, Gaines SD, CAN-10-3973
Jacobsen KI, Karrer LB, Leslie HM, Neeley E, Pauly D, Polasky S, Ris B, Hodson L, Skeaff CM, Fielding BA (2008) Fatty acid composition of
St Martin K, Stone GS, Sumaila UR, Zeller D (2012) An index to assess adipose tissue and blood in humans and its use as a biomarker of
the health and benefits of the global ocean. Nature 488, 615–620. dietary intake. Progress in Lipid Research 47, 348–380. doi:10.1016/
doi:10.1038/nature11397 j.plipres.2008.03.003
Hanlon CS, Rubinsztein DC (1995) Arginine residues at codon 112 and Hoenselaar R (2012) Saturated fat and cardiovascular disease: the
codon 158 in the apolipoprotein E gene correspond to the ancestral state discrepancy between the scientific literature and dietary advice.
in humans. Atherosclerosis 112, 85–90. doi:10.1016/0021-9150(94) Nutrition 28, 118–123. doi:10.1016/j.nut.2011.08.017
05402-5 Holick MF (2007) Vitamin D deficiency. The New England Journal of
Hanset R, Michaux C, Dessy-Doize C, Burtonboy G (1982) Studies on the Medicine 357, 266–281. doi:10.1056/NEJMra070553
7th rib cut in double muscled and conventional cattle. Anatomical, Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu YQ,
histological and biochemical aspects. In ‘Muscle hypertrophy of Narra K, Hoehn KL, Knotts TA, Siesky A, Nelson DH, Karathanasis SK,
genetic origin and its use to improve beef production’. (Eds JWB Fontenot GK, Birnbaum MJ, Summers SA (2007) Inhibition of
King, F Menissier) pp. 341–349. (Martinus Nijhoff Publishers: The ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and
Hague, The Netherlands) obesity-induced insulin resistance. Cell Metabolism 5, 167–179.
Harper CR, Edwards MJ, DeFilipis AP, Jacobson TA (2006) Flaxseed oil doi:10.1016/j.cmet.2007.01.002
increases the plasma concentrations of cardioprotective (n-3) fatty acids Hooper L, Summerbell CD, Thompson R, Sills D, Roberts FG, Moore H,
in humans. The Journal of Nutrition 136, 83–87. Smith GD (2011) Reduced or modified dietary fat for preventing
Animal fats back on the table Animal Production Science 849

cardiovascular disease. Cochrane Database of Systematic Reviews (Issue Keys A, Kimura N (1970) Diets of middled-aged farmers in Japan. The
5), CD002137. American Journal of Clinical Nutrition 23, 212–223.
Hu FB, Stampfer MJ, Manson JE, Rimm E, Colditz GA, Rosner BA, Keys A, Anderson JT, Grande F (1957) Prediction of serum-cholesterol
Hennekens CH, Willett WC (1997) Dietary fat intake and the risk of response of man to changes in fats in the diet. Lancet 270, 959–966.
coronary heart disease in women. The New England Journal of Medicine doi:10.1016/S0140-6736(57)91998-0
337, 1491–1499. doi:10.1056/NEJM199711203372102 Keys A, Karvonen MJ, Fidanza F (1958) Serum-cholesterol studies in
Hunink MGM, Goldman L, Tosteson ANA, Mittleman MA, Goldman PA, Finland. Lancet 272, 175–178. doi:10.1016/S0140-6736(58)91524-1
Williams LW, Tsevat J, Weinstein MC (1997) The recent decline in Keys A, Anderson JT, Grande F (1965) Serum cholesterol response to changes
mortality from coronary heart disease, 1980–1990. The effect of secular in the diet. IV. Particular saturated fatty acids in the diet. Metabolism:
trends in risk factors and treatment. Journal of the American Medical Clinical and Experimental 14, 776–787. doi:10.1016/0026-0495(65)
Association 277, 535–542. doi:10.1001/jama.1997.03540310033031 90004-1
Hunter JE (2001) Studies on effects of dietary fatty acids as related to their Keys A, Blackburn H, Menotti A, Buzina R, Mohacek I, Karvonen MJ, Punsar
position on triglycerides. Lipids 36, 655–668. doi:10.1007/s11745-001- S, Aravanis C, Corcondilas A, Dontas AS, Lekos D, Fidanza F, Puddu V,
0770-0 Taylor HL, Monti M, Kimura N, van Buchem FSP, Djordjevic BS,
Hursting SD, Smith SM, Lashinger LM, Harvey AE, Perkins SN (2010) Strasser T, Anderson JT, den Hartog C, Pekkarinen M, Roine P, Sdrin
Calories and carcinogenesis: lessons learned from 30 years of calorie H (1970) Coronary heart disease in 7 countries. Circulation 41(Suppl. I),
restriction research. Carcinogenesis 31, 83–89. doi:10.1093/carcin/ I1–I209.
bgp280 Keys A, Grande F, Anderson JT (1974) Bias and misrepresentation revisited –
Hutchison R (1936) Treatment of chronic constipation. British Medical perspective on saturated fat. The American Journal of Clinical Nutrition
Journal I, 374–375. doi:10.1136/bmj.1.3920.374 27, 188–212.
Ishibashi S, Herz J, Maeda N, Goldstein JL, Brown MS (1994) The Keys A, Aravanis C, Blackburn H, Buzina R, Djordjevic BS, Dontas AS,
two-receptor model of lipoprotein clearance: tests of the hypothesis Fidanza F, Karvonen MJ, Kimura N, Menotti A, Mohacek I, Nedeljkovic
in ‘knockout’ mice lacking the low density lipoprotein receptor, S, Puddu V, Punsar S, Taylor HL, van Buchem FSP (1980) ‘Seven
apolipoprotein E, or both proteins. Proceedings of the National Countries: a multivariate analysis of death and coronary heart disease.’
Academy of Sciences, USA 91, 4431–4435. doi:10.1073/pnas.91.10.4431 (Harvard University Press: Cambridge, MA)
Jha P, Flather M, Lonn E, Farkouh M, Yusuf S (1995) The antioxidant Kim DY, Davis LM, Sullivan PG, Maalouf M, Simeone TA, van Brederode J,
vitamins and cardiovascular disease: a critical review of epidemiological Rho JM (2007) Ketone bodies are protective against oxidative stress
and clinical trial data. Annals of Internal Medicine 123, 860–872. in neocortical neurons. Journal of Neurochemistry 101, 1316–1326.
doi:10.7326/0003-4819-123-11-199512010-00009
doi:10.1111/j.1471-4159.2007.04483.x
Jia W, Rogiewicz A, Bruce HL, Slominski BA (2010) Feeding flaxseed
Klement RJ, Kaemmerer U (2011) Is there a role for carbohydrate restriction
enhances deposition of omega-3 fatty acids in broiler meat portions in
in the treatment and prevention of cancer? Nutrition & Metabolism 8, 75.
different manner. Canadian Journal of Animal Science 90, 203–206.
doi:10.1186/1743-7075-8-75
doi:10.4141/CJAS09106
Knekt P, Ritz J, Pereira MA, O’Reilly EJ, Augustsson K, Fraser GE,
Johnson RK, Appel LJ, Brands M, Howard BV, Lefevre M, Lustig RH, Sacks
Goldbourt U, Heitmann BL, Hallmans G, Liu SM, Spiegelman D,
F, Steffen LM, Wylie-Rosett J Council Nutr Phys Activity Metab, Council
Stevens J, Virtamo J, Willett WC, Rimm EB, Ascherio A (2004)
Epidemiology Prevention(2009) Dietary sugars intake and cardiovascular
Antioxidant vitamins and coronary heart disease risk: a pooled analysis
health: a scientific statement from the American Heart Association.
of 9 cohorts. The American Journal of Clinical Nutrition 80, 1508–1520.
Circulation 120, 1011–1020. doi:10.1161/CIRCULATIONAHA.109.
Kobayashi N, Barnard RJ, Henning SM, Elashoff D, Reddy ST, Cohen P,
192627
Leung P, Hong-Gonzalez J, Freedland SJ, Said J, Gui D, Seeram NP,
Karvonen MJ, Orma E, Punsar S, Kallio V, Arstila M, Luomanmaki K,
Popoviciu LM, Bagga D, Heber D, Glaspy JA, Aronson WJ (2006)
Takkunen J (1970) VI. Five-year experience in Finland. Circulation
Effect of altering dietary omega-6/omega-3 fatty acid ratios on prostate
41(Suppl. 1), I-52–I-62. doi:10.1161/01.CIR.41.4S1.I-52
Kashiwaya Y, Sato K, Tsuchiya N, Thomas S, Fell DA, Veech RL, cancer membrane composition, cyclooxygenase-2, and prostaglandin
Passonneau JV (1994) Control of glucose utilization in working E-2. Clinical Cancer Research 12, 4662–4670. doi:10.1158/1078-
perfused rat heart. The Journal of Biological Chemistry 269, 0432.CCR-06-0459
25 502–25 514. Kontush A, Chantepie S, Chapman MJ (2003) Small, dense HDL particles
Kelly MJ, Tume RK, Newman SA, Thompson JM (2001) Environmental exert potent protection of atherogenic LDL against oxidative stress.
effects on the fatty acid composition of subcutaneous beef fat. Australian Arteriosclerosis, Thrombosis, and Vascular Biology 23, 1881–1888.
Journal of Experimental Agriculture 41, 1023–1031. doi:10.1071/ doi:10.1161/01.ATV.0000091338.93223.E8
EA00025 Kossoff EH, Hartman AL (2012) Ketogenic diets: new advances for
Key T, Schatzkin A, Willett WC, Allen NE, Spencer EA, Travis RC (2004) metabolism-based therapies. Current Opinion in Neurology 25,
Diet, nutrition and the prevention of cancer. Public Health Nutrition 7, 173–178. doi:10.1097/WCO.0b013e3283515e4a
187–200. doi:10.1079/PHN2003588 Kossoff EH, McGrogan JR, Bluml RM, Pillas DJ, Rubenstein JE, Vining EP
Keys A (1950) The residues of malnutrition and starvation. Science 112, (2006) A modified Atkins diet is effective for the treatment of intractable
371–373. pediatric epilepsy. Epilepsia 47, 421–424. doi:10.1111/j.1528-1167.
Keys A (1953) Atherosclerosis: a problem in newer public health. Journal 2006.00438.x
of the Mount Sinai Hospital, New York 20, 118–139. Kratz M, Cullen P, Kannenberg F, Kassner A, Fobker M, Abuja PM, Assmann
Keys A (1971) Sucrose in the diet and coronary heart disease. Atherosclerosis G, Wahrburg U (2002) Effects of dietary fatty acids on the composition
14, 193–202. doi:10.1016/0021-9150(71)90049-9 and oxidizability of low-density lipoprotein. European Journal of Clinical
Keys A (1980) Wine, garlic, and CHD in seven countries. Lancet 315, Nutrition 56, 72–81. doi:10.1038/sj.ejcn.1601288
145–146. doi:10.1016/S0140-6736(80)90620-0 Krauss RM, Dreon DM (1995) Low density lipoprotein subclasses and
Keys A (1995) Mediterranean diet and public health: personal reflections. response to a low fat diet in healthy men. The American Journal of
The American Journal of Clinical Nutrition 61, S1321–S1323. Clinical Nutrition 62, S478–S487.
850 Animal Production Science W. Barendse

Krebs HA (1966) The regulation of the release of ketone bodies by the liver. Luchsinger JA, Tang M-X, Stern Y, Shea S, Mayeux R (2001) Diabetes
Advances in Enzyme Regulation 4, 339–353. doi:10.1016/0065-2571(66) mellitus and risk of Alzheimer’s disease and dementia with stroke in a
90027-6 multiethnic cohort. American Journal of Epidemiology 154, 635–641.
Krebs HA, Williamson DH, Bates MW, Page MA, Hawkins RA (1971) doi:10.1093/aje/154.7.635
The role of ketone bodies in caloric homeostasis. Advances in Enzyme Lustig RH, Schmidt LA, Brindis CD (2012) The toxic truth about sugar.
Regulation 9, 387–409. doi:10.1016/S0065-2571(71)80055-9 Nature 482, 27–29. doi:10.1038/482027a
Kritchevsky D (1976) Diet and atherosclerosis. American Journal of MacDougall DE, Jones PJH, Kitts DD, Phang PT (1996) Effect of butter
Pathology 84, 615–632. compared with tallow consumption on postprandial oxidation of myristic
Kuo PT, Carson JC (1959) Dietary fats and the diurnal serum triglyceride and palmitic acids. The American Journal of Clinical Nutrition 63,
levels in man. The Journal of Clinical Investigation 38, 1384–1393. 918–924.
doi:10.1172/JCI103914 MacLean CH, Newberry SJ, Mojica WA, Khanna P, Issa AM, Suttorp MJ,
Kuusisto J, Koivisto K, Mykkanen L, Helkala EL, Vanhanen M, Hanninen T, Lim YW, Traina SB, Hilton L, Garland R, Morton SC (2006) Effects of
Kervinen K, Kesaniemi YA, Riekkinen PJ, Laakso M (1997) Association omega-3 fatty acids on cancer risk – a systematic review. Journal of the
between features of the insulin resistance syndrome and Alzheimer’s American Medical Association 295, 403–415. doi:10.1001/jama.295.
disease independently of apolipoprotein E4 phenotype: cross sectional 4.403
population based study. British Medical Journal 315, 1045–1049. Macquart-Moulin G, Riboli E, Cornee J, Kaaks R, Berthezene P (1987)
doi:10.1136/bmj.315.7115.1045 Colorectal polyps and diet – a case control study in Marseilles.
Lagarrigue S, Pitel F, Carre W, Abasht B, Le Roy P, Neau A, Amigues Y, International Journal of Cancer 40, 179–188. doi:10.1002/ijc.
Sourdioux M, Simon J, Cogburn L, Aggrey S, Leclercq B, Vignal A, 2910400209
Douaire M (2006) Mapping quantitative trait loci affecting fatness Man EB, Gildea EF (1932) The effect of the ingestion of a large amount of
and breast muscle weight in meat-type chicken lines divergently fat and of a balanced meal on the blood lipids of normal man. The Journal
selected on abdominal fatness. Genetics, Selection, Evolution 38, of Biological Chemistry 99, 61–69.
85–97. doi:10.1186/1297-9686-38-1-85 Mandell IB, Buchanan Smith JG, Holub BJ, Campbell CP (1997) Effects
Lamarche B, Tchernof A, Moorjani S, Cantin B, Dagenais GR, Lupien PJ, of fish meal in beef diets on growth performance, carcass characteristics,
Despres JP (1997) Small, dense low-density lipoprotein particles as a and fatty acid composition of longissimus muscle. Journal of Animal
predictor of the risk of ischemic heart disease in men – prospective results Science 75, 910–919.
from the Quebec Cardiovascular Study. Circulation 95, 69–75. Marinou K, Adiels M, Hodsen L, Frayn KN, Karpe F, Fielding BA (2011)
doi:10.1161/01.CIR.95.1.69 Young women partition fatty acids towards ketone body production rather
Lande KE, Sperry WM (1936) Human atherosclerosis in relation to the
than VLDL–TAG synthesis, compared with young men. The British
cholesterol content of the blood serum. Archives of Pathology 22,
Journal of Nutrition 105, 857–865. doi:10.1017/S0007114510004472
301–312.
Marlowe FW (2005) Hunter-gatherers and human evolution. Evolutionary
Lappalainen T, Salmela E, Andersen PM, Dahlman-Wright K, Sistonen P,
Anthropology 14, 54–67. doi:10.1002/evan.20046
Savontaus ML, Schreiber S, Lahermo P, Kere J (2010) Genomic landscape
Marmot MG, Bosma H, Hemingway H, Brunner E, Stansfield S (1997)
of positive natural selection in northern European populations. European
Contribution of job control and other risk factors to social variations in
Journal of Human Genetics 18, 471–478. doi:10.1038/ejhg.2009.184
coronary heart disease incidence. Lancet 350, 235–239. doi:10.1016/
Lehninger AL (1982) ‘Principles of biochemistry.’ (Worth Publishers: New
S0140-6736(97)04244-X
York)
Mathers JC, Movahedi M, Macrae F, Mecklin JP, Moeslein G, Olschwang S,
Lindeberg S (2009) Modern human physiology with respect to evolutionary
Eccles D, Evans G, Maher ER, Bertario L, Bisgaard ML, Dunlop M, Ho
adaptations that relate to diet in the past. In ‘Evolution of hominin diets’.
JWC, Hodgson S, Lindblom A, Lubinski J, Morrison PJ, Murday V,
(Eds JJ Hublin, MP Richard) pp. 43–57. (Springer: Dordrecht, The
Ramesar R, Side L, Scott RJ, Thomas HJW, Vasen H, Gerdes AM, Barker
Netherlands)
Lipp M, Simoneau C, Ulberth F, Anklam E, Crews C, Brereton P, de Greyt W, G, Crawford G, Elliott F, Pylvanainen K, Wijnen J, Fodde R, Lynch H,
Schwack W, Wiedmaier C (2001) Composition of genuine cocoa butter Bishop DT, Burn J, Investigators C (2012) Long-term effect of resistant
and cocoa butter equivalents. Journal of Food Composition and Analysis starch on cancer risk in carriers of hereditary colorectal cancer: an analysis
14, 399–408. doi:10.1006/jfca.2000.0984 from the CAPP2 randomised controlled trial. The Lancet Oncology 13,
Liu L, Zhuang W, Wang R-Q, Mukherjee R, Xiao S-M, Chen X, We X-T, 1242–1249. doi:10.1016/S1470-2045(12)70475-8
Zhou Y, Zhang H-Y (2011) Is dietary fat associated with the risk of Matthan NR, Welty FK, Barrett PHR, Harausz C, Dolnikowski GG, Parks JS,
colorectal cancer? A meta-analysis of 13 prospective cohort studies. Eckel RH, Schaefer EJ, Lichtenstein AH (2004) Dietary hydrogenated
European Journal of Nutrition 50, 173–184. doi:10.1007/s00394-010- fat increases high-density lipoprotein apoA-I catabolism and decreases
0128-5 low-density lipoprotein apoB-100 catabolism in hypercholesterolemic
Livingstone KM, Lovegrove JA, Cockcroft JR, Elwood PC, Pickering JE, women. Arteriosclerosis, Thrombosis, and Vascular Biology 24,
Givens DI (2013) Does dairy food intake predict arterial stiffness and 1092–1097. doi:10.1161/01.ATV.0000128410.23161.be
blood pressure in men? Evidence from the Caerphilly prospective study. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL,
Hypertension 61, 42–47. doi:10.1161/HYPERTENSIONAHA.111. Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W,
00026 Ingram DK, De Cabo R (2012) Impact of caloric restriction on health
Longo VD, Finch CE (2003) Evolutionary medicine: from dwarf model and survival in rhesus monkeys from the NIA study. Nature 489, 318–321.
systems to healthy centenarians? Science 299, 1342–1346. doi:10.1126/ doi:10.1038/nature11432
science.1077991 McClellan WS, Du Bois EF (1930) Clinical calorimetry. XLV. Prolonged
López-López A, Castellote-Bargallo AI, Campoy-Folgoso C, Rivero-Urgell meat diets with a study of kidney function and ketosis. The Journal of
M, Tormo-Carnice R, Infante-Pina D, López-Sabater MC (2001) The Biological Chemistry 87, 651–668.
influence of dietary palmitic acid triacylglyceride position on the fatty McDevitt RM, Bott SJ, Harding M, Coward WA, Bluck LJ, Prentice AM
acid, calcium and magnesium contents of at term newborn faeces. (2001) De novo lipogenesis during controlled overfeeding with sucrose
Early Human Development 65, S83–S94. doi:10.1016/S0378-3782(01) or glucose in lean and obese women. The American Journal of Clinical
00210-9 Nutrition 74, 737–746.
Animal fats back on the table Animal Production Science 851

McGarry JD, Robles-Valdes C, Foster DW (1975) Role of carnitine in hepatic Murff HJ, Shu XO, Li HL, Yang G, Wu XY, Cai H, Wen WQ, Gao YT, Zheng
ketogenesis. Proceedings of the National Academy of Sciences, USA 72, W (2011) Dietary polyunsaturated fatty acids and breast cancer risk in
4385–4388. doi:10.1073/pnas.72.11.4385 Chinese women: a prospective cohort study. International Journal of
McGee DL Diverse Populations Collaboration (2005) Body mass index and Cancer 128, 1434–1441. doi:10.1002/ijc.25703
mortality: a meta-analysis based on person-level data from twenty-six Mushtaq S, Mangiapane EH, Hunter KA (2010) Estimation of cis-9, trans-11
observational studies. Annals of Epidemiology 15, 87–97. doi:10.1016/ conjugated linoleic acid content in UK foods and assessment of dietary
j.annepidem.2004.05.012 intake in a cohort of healthy adults. The British Journal of Nutrition 103,
McMichael AJ, Potter JD, Hetzel BS (1979) Time trends in colo-rectal cancer 1366–1374. doi:10.1017/S000711450999328X
mortality in relation to food and alcohol consumption: United States, Neal EG, Chaffe H, Schwartz RH, Lawson MS, Edwards N, Fitzsimmons G,
United Kingdom, Australia and New Zealand. International Journal of Whitney A, Cross JH (2008) The ketogenic diet for the treatment of
Epidemiology 8, 295–303. doi:10.1093/ije/8.4.295 childhood epilepsy: a randomised controlled trial. Lancet Neurology 7,
Mekki N, Charbonnier M, Borel P, Leonardi J, Juhel C, Portugal H, Lairon D 500–506. doi:10.1016/S1474-4422(08)70092-9
(2002) Butter differs from olive oil and sunflower oil in its effects on Nelson RL, Persky V, Turyk M (1999) Determination of factors responsible
postprandial lipemia and triacylglycerol-rich lipoproteins after single for the declining incidence of colorectal cancer. Diseases of the Colon and
mixed meals in healthy young men. The Journal of Nutrition 132, Rectum 42, 741–752. doi:10.1007/BF02236929
3642–3649. Nestel P, Noakes M, Belling B, McArthur R, Clifton P, Janus E, Abbey M
Meng MS, West GC, Irving L (1969) Fatty acid composition of caribou (1992) Plasma lipoprotein lipid and Lp[a] changes with substitution of
bone marrow. Comparative Biochemistry and Physiology 30, 187–191. elaidic for oleic acid in the diet. Journal of Lipid Research 33, 1029–1036.
doi:10.1016/0010-406X(69)91314-0 Nicholson T, Khademi H, Moghadasian MH (2013) The role of marine n-3
Mensink RP, Zock PL, Kester ADM, Katan MB (2003) Effects of dietary fatty acids in improving cardiovascular health: a review. Food & Function
fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol 4, 357–365. doi:10.1039/c2fo30235g
and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled Nikkilä EA, Kekki M (1972) Plasma triglyceride metabolism in thyroid
trials. The American Journal of Clinical Nutrition 77, 1146–1155. disease. The Journal of Clinical Investigation 51, 2103–2114.
Menzel HJ, Kladetzky RG, Assmann G (1983) Apolipoprotein E doi:10.1172/JCI107017
polymorphism and coronary artery disease. Arteriosclerosis 3, Nishina PM, Johnson JP, Naggert JK, Krauss RM (1992) Linkage of
310–315. doi:10.1161/01.ATV.3.4.310 atherogenic lipoprotein phenotype to the low density lipoprotein
Micha R, Mozaffarian D (2010) Saturated fat and cardiometabolic risk receptor locus on the short arm of chromosome 19. Proceedings of the
factors, coronary heart disease, stroke, and diabetes: a fresh look at the National Academy of Sciences, USA 89, 708–712. doi:10.1073/pnas.
evidence. Lipids 45, 893–905. doi:10.1007/s11745-010-3393-4 89.2.708
Michalski MC, Genot C, Gayet C, Lopez C, Fine F, Joffre F, Vendeuvre JL, Nuernberg K, Dannenberger D, Nuernberg G, Ender K, Voigt J, Scollan ND,
Bouvier J, Chardigny JM, Raynal-Ljutovac K , for the Steering Committee Wood JD, Nute GR, Richardson RI (2005a) Effect of a grass-based and
of RMT LISTRAL (2013) Multiscale structures of lipids in foods as a concentrate feeding system on meat quality characteristics and fatty acid
parameters affecting fatty acid bioavailability and lipid metabolism. composition of longissimus muscle in different cattle breeds. Livestock
Progress in Lipid Research 52, 354–373. doi:10.1016/j.plipres.2013. Production Science 94, 137–147. doi:10.1016/j.livprodsci.2004.11.036
04.004 Nuernberg K, Nuernberg G, Ender K, Dannenberger D, Schabbel W,
Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN, Grumbach S, Zupp W, Steinhart H (2005b) Effect of grass vs.
Goldberg AC, Howard WJ, Jacobson MS, Kris-Etherton PM, Lennie TA, concentrate feeding on the fatty acid profile of different fat depots in
Levi M, Mazzone T, Pennathur S (2011) Triglycerides and cardiovascular lambs. European Journal of Lipid Science and Technology 107,
disease: a scientific statement from the American Heart Association. 737–745. doi:10.1002/ejlt.200501141
Circulation 123, 2292–2333. doi:10.1161/CIR.0b013e3182160726 Oddy DJ, Yudkin J (1969) An evaluation of English diets of the 1860s.
Mooijaart SP, Berbee JFP, van Heemst D, Havekes LM, de Craen AJM, The Proceedings of the Nutrition Society 28, A13–A14.
Slagboom PE, Rensen PCN, Westendorp RGJ (2006) ApoE plasma levels Orgel E, Mittelman SD (2013) The links between insulin resistance, diabetes,
and risk of cardiovascular mortality in old age. PLoS Medicine 3, e76. and cancer. Current Diabetes Reports 13, 213–222. doi:10.1007/s11892-
doi:10.1371/journal.pmed.0030176 012-0356-6
Moreno JA, Perez-Jimenez F, Moreno-Luna R, Perez-Martinez P, Fuentes- Ornish D, Scherwitz LW, Billings JH, Gould KL, Merritt TA, Sparler S,
Jimenez F, Marin C, Portugal H, Lairon D, Lopez-Miranda J (2009) Armstrong WT, Ports TA, Kirkeeide RL, Hogeboom C, Brand RJ (1998)
The effect of apoE genotype and sex on ApoE plasma concentration is Intensive lifestyle changes for reversal of coronary heart disease. Journal
determined by dietary fat in healthy subjects. The British Journal of of the American Medical Association 280, 2001–2007. doi:10.1001/
Nutrition 101, 1745–1752. doi:10.1017/S0007114508111515 jama.280.23.2001
Morin E (2007) Fat composition and Nunamiut decision-making: a new look Owen RW, Weisgerber UM, Carr J, Harrison MH (1995) Analysis of
at the marrow and bone grease indices. Journal of Archaeological calcium–lipid complexes in faeces. European Journal of Cancer
Science 34, 69–82. doi:10.1016/j.jas.2006.03.015 Prevention 4, 247–255. doi:10.1097/00008469-199506000-00006
Mozaffarian D, Rimm EB (2006) Fish intake, contaminants, and human Paolisso G, Ammendola S, DelBuono A, Gambardella A, Riondino M,
health – evaluating the risks and the benefits. Journal of the American Tagliamonte MR, Rizzo MR, Carella C, Varricchio M (1997) Serum
Medical Association 296, 1885–1899. doi:10.1001/jama.296.15.1885 levels of insulin-like growth factor-I (IGF-I) and IGF-binding protein-3
Mozaffarian D, Aro A, Willett WC (2009) Health effects of trans-fatty acids: in healthy centenarians: relationship with plasma leptin and lipid
experimental and observational evidence. European Journal of Clinical concentrations, insulin action, and cognitive function. The Journal of
Nutrition 63, S5–S21. doi:10.1038/sj.ejcn.1602973 Clinical Endocrinology and Metabolism 82, 2204–2209. doi:10.1210/
Multiple Risk Factor Intervention Trial Research Group (1982) Multiple jcem.82.7.4087
risk factor intervention trial risk factor changes and mortality results. Pariza MW, Park Y, Cook ME (2001) The biologically active isomers of
Journal of the American Medical Association 248, 1465–1477. conjugated linoleic acid. Progress in Lipid Research 40, 283–298.
doi:10.1001/jama.1982.03330120023025 doi:10.1016/S0163-7827(01)00008-X
Murdock GP (1967) Ethnographic atlas – a summary. Ethnology 6, 109–236. Parodi PW (1997) Cows’ milk fat components as potential anticarcinogenic
doi:10.2307/3772751 agents. The Journal of Nutrition 127, 1055–1060.
852 Animal Production Science W. Barendse

Parodi PW (2004) Milk fat in human nutrition. Australian Journal of Dairy Rand WM, Pellett PL, Young VR (2003) Meta-analysis of nitrogen balance
Technology 59, 3–59. studies for estimating protein requirements in healthy adults. The
Pasquet P, Brigant L, Froment A, Koppert GA, Bard D, Degarine I, Apfelbaum American Journal of Clinical Nutrition 77, 109–127.
M (1992) Massive overfeeding and energy balance in men – the Guru- Razmaite V, Svirmickas GJ, Siukscius A, Sveistiene R (2011) Comparative
Walla model. The American Journal of Clinical Nutrition 56, 483–490. characterization of fatty acid profiles in intramuscular lipids from
Pearson DJ, Tubbs PK (1967) Carnitine and derivatives in rat tissues. different domestic and wild monogastric animal species. Veterinarija
Biochemical Journal 105, 953–963. Ir Zootechnika 53, 45–50.
Peréz-Guisado J, Munoz-Serrano A (2011a) The effect of the Spanish Reaven PD, Grasse BJ, Tribble DL (1994) Effects of linoleate enriched and
ketogenic Mediterranean diet on nonalcoholic fatty liver disease: a oleate enriched diets in combination with alpha-tocopherol on the
pilot study. Journal of Medicinal Food 14, 677–680. doi:10.1089/ susceptibility of LDL and LDL subfractions to oxidative modification
jmf.2011.0075 in humans. Arteriosclerosis and Thrombosis 14, 557–566. doi:10.1161/
Peréz-Guisado J, Munoz-Serrano A (2011b) A pilot study of the Spanish 01.ATV.14.4.557
ketogenic Mediterranean diet: an effective therapy for the metabolic Reboul E, Borel P (2011) Proteins involved in uptake, intracellular transport
syndrome. Journal of Medicinal Food 14, 681–687. doi:10.1089/ and basolateral secretion of fat-soluble vitamins and carotenoids by
jmf.2010.0137 mammalian enterocytes. Progress in Lipid Research 50, 388–402.
Pes GM, Tolu F, Poulain M, Errigo A, Masala S, Pietrobelli A, Battistini NC, doi:10.1016/j.plipres.2011.07.001
Maioli M (2013) Lifestyle and nutrition related to male longevity in Ren HY, Zheng XM, Chen HX, Li K (2011) Transgenic pigs carrying a
Sardinia: an ecological study. Nutrition, Metabolism, and Cardiovascular synthesized fatty acid desaturase gene yield high level of omega-3 PUFAs.
Diseases 23, 212–219. doi:10.1016/j.numecd.2011.05.004 Agricultural Sciences in China 10, 1603–1608. doi:10.1016/S1671-2927
Phinney SD (2004) Ketogenic diets and physical performance. Nutrition & (11)60157-0
Metabolism 1, 2. doi:10.1186/1743-7075-1-2 Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M (2008) Body-mass
Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K, index and incidence of cancer: a systematic review and meta-analysis of
van der Schouw YT, Spencer E, Moons KGM, Tjonneland A, Halkjaer J, prospective observational studies. Lancet 371, 569–578. doi:10.1016/
Jensen MK, Stegger J, Clavel-Chapelon F, Boutron-Ruault MC, Chajes V, S0140-6736(08)60269-X
Linseisen J, Kaaks R, Trichopoulou A, Trichopoulos D, Bamia C, Sieri S, Richards MP, Trinkaus E (2009) Isotopic evidence for the diets of European
Palli D, Tumino R, Vineis P, Panico S, Peeters PHM, May AM, Bueno- Neanderthals and early modern humans. Proceedings of the National
Academy of Sciences, USA 106, 16 034–16 039. doi:10.1073/pnas.
De-Mesquita HB, van Duijnhoven FJB, Hallmans G, Weinehall L, Manjer
0903821106
J, Hedblad B, Lund E, Agudo A, Arriola L, Barricarte A, Navarro C,
Rimm EB, Stampfer MJ, Ascherso A, Giovannucci E, Colditz GA, Willett
Martinez C, Quiros JR, Key T, Bingham S, Khaw KT, Boffetta P, Jenab M,
WC (1993) Vitamin E consumption and the risk of coronary heart
Ferrari P, Riboli E (2008) General and abdominal adiposity and risk
disease in men. The New England Journal of Medicine 328,
of death in Europe. The New England Journal of Medicine 359,
1450–1456. doi:10.1056/NEJM199305203282004
2105–2120. doi:10.1056/NEJMoa0801891
Roberts R, Bickerton AS, Fielding BA, Blaak EE, Wagenmakers AJ, Chong
Pitchford WS (2004) Genetic improvement of feed efficiency of beef cattle:
MFF, Gilbert M, Karpe F, Frayn KN (2008) Reduced oxidation of
what lessons can be learnt from other species? Australian Journal of
dietary fat after a short term high-carbohydrate diet. The American
Experimental Agriculture 44, 371–382. doi:10.1071/EA02111
Journal of Clinical Nutrition 87, 824–831.
Polidori MC, Mariani E, Baggio G, Deiana L, Carru C, Pes GM, Cecchetti R,
Robinson WS (1950) Ecological correlations and the behaviour of
Franceschi C, Senin U, Mecocci P (2007) Different antioxidant profiles
individuals. American Sociological Review 15:351–357, reprinted in
in Italian centenarians: the Sardinian peculiarity. European Journal of International. Journal of Epidemiology 38, 337–341. doi:10.1093/ije/
Clinical Nutrition 61, 922–924. doi:10.1038/sj.ejcn.1602596 dyn357
Polkinghorne RJ, Thompson JM (2010) Meat standards and grading: a world Rodríguez-Sánchez JA, Ripoll G, Latorre MA (2010) The influence of age
view. Meat Science 86, 227–235. doi:10.1016/j.meatsci.2010.05.010 at the beginning of Montanera period on meat characteristics and fat
Pollak MN, Schernhammer ES, Hankinson SE (2004) Insulin-like growth quality of outdoor Iberian pigs. Animal 4, 289–294. doi:10.1017/
factors and neoplasia. Nature Reviews. Cancer 4, 505–518. doi:10.1038/ S1751731109991029
nrc1387 Roine P, Pekkarinen M, Karvonen MJ, Kihlberg J (1958) Diet and
Potter JD (1999) Colorectal cancer: molecules and populations. Journal of cardiovascular disease in Finland. Lancet 2, 173–175. doi:10.1016/
the National Cancer Institute 91, 916–932. doi:10.1093/jnci/91.11.916 S0140-6736(58)91523-X
Poulain M, Pes GM, Grasland C, Carru C, Ferrucci L, Baggio G, Franceschi C, Rouja PM, Dewailly É, Blanchet C Bardi Community (2003) Fat, fishing
Deiana L (2004) Identification of a geographic area characterized by patterns, and health among the Bardi people of north western Australia.
extreme longevity in the Sardinia island: the AKEA study. Experimental Lipids 38, 399–405. doi:10.1007/s11745-003-1075-z
Gerontology 39, 1423–1429. doi:10.1016/j.exger.2004.06.016 Sacks FM, Bray GA, Carey VJ, Smith SR, Ryan DH, Anton SD, McManus K,
Psaltopoulou T, Kosti RI, Haidopoulos D, Dimopoulos M, Panagiotakos DB Champagne CM, Bishop LM, Laranjo N, Leboff MS, Rood JC, de Jonge
(2011) Olive oil intake is inversely related to cancer prevalence: a L, Greenway FL, Loria CM, Obarzanek E, Williamson DA (2009)
systematic review and a meta-analysis of 13 800 patients and 23340 Comparison of weight-loss diets with different compositions of fat,
controls in 19 observational studies. Lipids in Health and Disease 10, protein, and carbohydrates. The New England Journal of Medicine
127. doi:10.1186/1476-511X-10-127 360, 859–873. doi:10.1056/NEJMoa0804748
Rajpathak SN, Liu YH, Ben-David O, Reddy S, Atzmon G, Crandall J, Sanden M, Stubhaug I, Berntssen MHG, Lie Ø, Torstensen BE (2011)
Barzilai N (2011) Lifestyle factors of people with exceptional longevity. Atlantic salmon (Salmo salar L.) as a net producer of long-chain
Journal of the American Geriatrics Society 59, 1509–1512. doi:10.1111/ marine omega-3 fatty acids. Journal of Agricultural and Food
j.1532-5415.2011.03498.x Chemistry 59, 12697–12706. doi:10.1021/jf203289s
Rajpathak SN, He MA, Sun Q, Kaplan RC, Muzumdar R, Rohan TE, Gunter Sandker GW, Kromhout D, Aravanis C, Bloemberg BPM, Mensink RP,
MJ, Pollak M, Kim M, Pessin JE, Beasley J, Wylie-Rosett J, Hu FB, Karalias N, Katan MB (1993) Serum cholesteryl ester fatty acids and their
Strickler HD (2012) Insulin-like growth factor axis and risk of type 2 relation with serum lipids in elderly men in Crete and The Netherlands.
diabetes in women. Diabetes 61, 2248–2254. doi:10.2337/db11-1488 European Journal of Clinical Nutrition 47, 201–208.
Animal fats back on the table Animal Production Science 853

Sato K, Kashiwaya Y, Keon CA, Tsuchiya N, King MT, Radda GK, Chance B, Sofi F, Abbate R, Gensini GF, Casini A, Trichopoulou A, Bamia C (2012)
Clarke K, Veech RL (1995) Insulin, ketone bodies, and mitochondrial Identification of change-points in the relationship between food groups in
energy transduction. The FASEB Journal 9, 651–658. the Mediterranean diet and overall mortality: an ‘a posteriori’ approach.
Scarmeas N, Stern Y, Tang M-X, Mayeux R, Luchsinger JA (2006) European Journal of Nutrition 51, 167–172. doi:10.1007/s00394-011-
Mediterranean diet and risk for Alzheimer’s disease. Annals of 0202-7
Neurology 59, 912–921. doi:10.1002/ana.20854 Song YQ, Stampfer MJ, Liu SM (2004) Meta-analysis: apolipoprotein E
Schaafsma A, Muskiet FAJ, Storm H, Hofstede GJH, Pakan I, Van der Veer E genotypes and risk for coronary heart disease. Annals of Internal Medicine
(2000) Vitamin D3 and vitamin K1 supplementation of Dutch 141, 137–147. doi:10.7326/0003-4819-141-2-200407200-00013
postmenopausal women with normal and low bone mineral densities: Sponheimer M, Dufour DL (2009) Increased dietary breadth in early
effect on serum 25-hydroxyvitamin D and carboxylated osteocalcin. hominin evolution: revisiting arguments and evidence with a focus on
European Journal of Clinical Nutrition 54, 626–631. doi:10.1038/sj. biogeochemical contributions. In ‘Evolution of hominin diets’. (Eds JJ
ejcn.1601065 Hublin, MP Richard) pp. 229–240. (Springer: Dordrecht, The
Scheppach W (1994) Effects of short chain fatty acids on gut morphology and Netherlands)
function. Gut 35, S35–S38. doi:10.1136/gut.35.1_Suppl.S35 Sprecher H (2002) The roles of anabolic and catabolic reactions in the
Schmidt M, Pfetzer N, Schwab M, Strauss I, Kammerer U (2011) Effects of a synthesis and recycling of polyunsaturated fatty acids. Prostaglandins,
ketogenic diet on the quality of life in 16 patients with advanced cancer: Leukotrienes, and Essential Fatty Acids 67, 79–83. doi:10.1054/
a pilot trial. Nutrition & Metabolism 8, 54. doi:10.1186/1743-7075-8-54 plef.2002.0402
Schmitz G, Ecker J (2008) The opposing effects of n-3 and n-6 fatty acids. Srivastava RAK (1996) Regulation of the apolipoprotein E by dietary lipids
Progress in Lipid Research 47, 147–155. doi:10.1016/j.plipres.2007. occurs by transcriptional and post-transcriptional mechanisms. Molecular
12.004 and Cellular Biochemistry 155, 153–162. doi:10.1007/BF00229312
Sharman MJ, Volek JS (2004) Weight loss leads to reductions in inflammatory Srivastava RAK, Bhasin N, Srivastava N (1996) Apolipoprotein E gene
biomarkers after a very-low-carbohydrate diet and a low-fat diet in expression in various tissues of mouse and regulation by estrogen.
overweight men. Clinical Science 107, 365–369. doi:10.1042/ Biochemistry and Molecular Biology International 38, 91–101.
CS20040111 Staerfl SM, Soliva CR, Leiber F, Kreuzer M (2011) Fatty acid profile and
Shigenaga MK, Hagen TM, Ames BN (1994) Oxidative damage and oxidative stability of the perirenal fat of bulls fattened on grass silage and
mitochondrial decay in aging. Proceedings of the National Academy of
maize silage supplemented with tannins, garlic, maca and lupines. Meat
Sciences, USA 91, 10771–10778. doi:10.1073/pnas.91.23.10771
Science 89, 98–104. doi:10.1016/j.meatsci.2011.04.006
Shingfield KJ, Bonnet M, Scollan ND (2013) Recent developments in
Stamler J, Vaccaro O, Neaton JD, Wentworth D (1993) Diabetes, other risk
altering the fatty acid composition of ruminant-derived foods. Animal
factors, and 12-yr cardiovascular mortaility for mean screened in the
7(Suppl. 1), 132–162. doi:10.1017/S1751731112001681
multiple risk factor intervention trial. Diabetes Care 16, 434–444.
Simonsen N, van’t Veer P, Strain JJ, Martin-Moreno JM, Huttunen JK,
doi:10.2337/diacare.16.2.434
Navajas JFC, Martin BC, Thamm M, Kardinaal AFM, Kok FJ,
Stampfer MJ, Krauss RM, Ma J, Blanche PJ, Holl LG, Sacks FM, Hennekens
Kohlmeier L (1998) Adipose tissue omega-3 and omega-6 fatty acid
CH (1996) A prospective study of triglyceride level, low-density
content and breast cancer in the EURAMIC study. American Journal of
lipoprotein particle diameter, and risk of myocardial infarction.
Epidemiology 147, 342–352. doi:10.1093/oxfordjournals.aje.a009456
Journal of the American Medical Association 276, 882–888.
Simopoulos AP (1991) Omega-3 fatty acids in health and disease and in
doi:10.1001/jama.1996.03540110036029
growth and development. The American Journal of Clinical Nutrition 54,
Stanhope KL, Schwarz JM, Keim NL, Griffen SC, Bremer AA, Graham JL,
438–463.
Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid Hatcher B, Cox CL, Dyachenko A, Zhang W, McGahan JP, Seibert A,
ratio in cardiovascular disease and other chronic diseases. Experimental Krauss RM, Chiu S, Schaefer EJ, Ai M, Otokozawa S, Nakajima K,
Biology and Medicine 233, 674–688. doi:10.3181/0711-MR-311 Nakano T, Beysen C, Hellerstein MK, Berglund L, Havel PJ (2009)
Sinclair LA (2007) Nutritional manipulation of the fatty acid composition of Consuming fructose-sweetened, not glucose-sweetened, beverages
sheep meat: a review. The Journal of Agricultural Science 145, 419–434. increases visceral adiposity and lipids and decreases insulin sensitivity
doi:10.1017/S0021859607007186 in overweight/obese humans. The Journal of Clinical Investigation 119,
Sinclair AJ, Barone S, Stobaus T, Tume R, Beilken S, Mueller W, 1322–1334. doi:10.1172/JCI37385
Cunningham J, Barnes JA, Greenfield H (2010) Lipid composition of Stefansson V (1912) ‘My life with the Eskimo.’ (Harper and Brothers,
Australian pork cuts 2005/2006. Food Chemistry 121, 672–681. Norwood Press: Norwood, MA)
doi:10.1016/j.foodchem.2009.12.096 Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL (1989)
Singh PP, Singh M, Mastana SS (2006) APOE distribution in world Beyond cholesterol modifications of low-density lipoprotein that
populations with new data from India and the UK. Annals of Human increase its atherogenicity. The New England Journal of Medicine 320,
Biology 33, 279–308. doi:10.1080/03014460600594513 915–924.
Siri-Tarino PW, Sun Q, Hu FB, Krauss RM (2010) Meta-analysis of Steinmetz KA, Potter JD (1991) Vegetables, fruit, and cancer. II. Mechanisms.
prospective cohort studies evaluating the association of saturated fat Cancer Causes & Control 2, 427–442. doi:10.1007/BF00054304
with cardiovascular disease. The American Journal of Clinical Stengard JH, Zerba KE, Pekkanen J, Ehnholm C, Nissinen A, Sing CF (1995)
Nutrition 91, 535–546. doi:10.3945/ajcn.2009.27725 Apolipoprotein-E polymorphism predicts death from coronary heart
Smit M, Deknijff P, Rosseneu M, Bury J, Klasen E, Frants R, Havekes L disease in a longitudinal study of elderly Finnish men. Circulation 91,
(1988) Apolipoprotein E polymorphism in the Netherlands and its 265–269. doi:10.1161/01.CIR.91.2.265
effect on plasma lipid and apolipoprotein levels. Human Genetics 80, Stiner MC, Munro ND (2011) On the evolution of diet and landscape during
287–292. doi:10.1007/BF01790099 the Upper Paleolithic through Mesolithic at Franchthi Cave (Peloponnese,
Sniderman AD, Islam S, Yusuf S, McQueen MJ (2012) Discordance Greece). Journal of Human Evolution 60, 618–636. doi:10.1016/j.jhevol.
analysis of apolipoprotein B and non-high density lipoprotein 2010.12.005
cholesterol as markers of cardiovascular risk in the INTERHEART Stocker R, Keaney JF (2004) Role of oxidative modifications in
study. Atherosclerosis 225, 444–449. doi:10.1016/j.atherosclerosis.2012. atherosclerosis. Physiological Reviews 84, 1381–1478. doi:10.1152/
08.039 physrev.00047.2003
854 Animal Production Science W. Barendse

Sullivan PG, Rippy NA, Dorenbos K, Concepcion RC, Agarwal AK, Rho JM Thompson JM (2004) The effects of marbling on flavour and juiciness scores
(2004) The ketogenic diet increases mitochondrial uncoupling protein of cooked beef, after adjusting to a constant tenderness. Australian
levels and activity. Annals of Neurology 55, 576–580. doi:10.1002/ Journal of Experimental Agriculture 44, 645–652. doi:10.1071/EA02171
ana.20062 Tisdale MJ, Brennan RA, Fearon KC (1987) Reduction of weight loss and
Tanaka T, Shen J, Abecasis GR, Kisialiou A, Ordovas JM, Guralnik JM, tumor size in a cachexia model by a high fat diet. British Journal of Cancer
Singleton A, Bandinelli S, Cherubini A, Arnett D, Tsai MY, Ferrucci L 56, 39–43. doi:10.1038/bjc.1987.149
(2009) Genome-wide association study of plasma polyunsaturated fatty Topping DL, Clifton PM (2001) Short-chain fatty acids and human colonic
acids in the InCHIANTI study. PLOS Genetics 5, e1000338. doi:10.1371/ function: roles of resistant starch and nonstarch polysaccharides.
journal.pgen.1000338 Physiological Reviews 81, 1031–1064.
Taubes G (2001) The soft science of dietary fat. Science 291, 2536–2545. Trejo JL, Carro E, Nunez A, Torres-Aleman I (2002) Sedentary life impairs
doi:10.1126/science.291.5513.2536 self-reparative processes in the brain: the role of serum insulin-like growth
Taubes G (2007) ‘Good calories, bad calories: challenging the conventional factor-I. Reviews in the Neurosciences 13, 365–374. doi:10.1515/
wisdom on diet, weight control, and disease.’ (A.A. Knopf: New York) REVNEURO.2002.13.4.365
Taylor HL, Keys A (1950) Adaptation to caloric restriction. Science 112, Tribble DL, Holl LG, Wood PD, Krauss RM (1992) Variations in oxidative
215–218. doi:10.1126/science.112.2904.215 susceptibility among 6 low density lipoprotein subfractions of differing
Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, density and particle size. Atherosclerosis 93, 189–199. doi:10.1016/0021-
Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, Johansen CT, 9150(92)90255-F
Fouchier SW, Isaacs A, Peloso GM, Barbalic M, Ricketts SL, Bis JC, Trichopoulou A, Costacou T, Bamia C, Trichopoulou D (2003) Adherence to
Aulchenko YS, Thorleifsson G, Feitosa MF, Chambers J, Orho-Melander a Mediterranean diet and survival in a Greek population. The New England
M, Melander O, Johnson T, Li XH, Guo XQ, Li MY, Cho YS, Go MJ, Kim Journal of Medicine 348, 2599–2608. doi:10.1056/NEJMoa025039
YJ, Lee JY, Park T, Kim K, Sim X, Ong RTH, Croteau-Chonka DC, Lange Tsai CJ, Leitzmann MF, Willett WC, Giovannucci EL (2005) Dietary
LA, Smith JD, Song K, Zhao JH, Yuan X, Luan JA, Lamina C, Ziegler A,
carbohydrates and glycaemic load and the incidence of symptomatic
Zhang W, Zee RYL, Wright AF, Witteman JCM, Wilson JF, Willemsen
gall stone disease in men. Gut 54, 823–828. doi:10.1136/gut.2003.031435
G, Wichmann HE, Whitfield JB, Waterworth DM, Wareham NJ, Waeber
Tume RK (2004) The effects of environmental factors on fatty acid
G, Vollenweider P, Voight BF, Vitart V, Uitterlinden AG, Uda M,
composition and the assessment of marbling in beef cattle: a review.
Tuomilehto J, Thompson JR, Tanaka T, Surakka I, Stringham HM,
Australian Journal of Experimental Agriculture 44, 663–668.
Spector TD, Soranzo N, Smit JH, Sinisalo J, Silander K, Sijbrands
doi:10.1071/EA02152
EJG, Scuteri A, Scott J, Schlessinger D, Sanna S, Salomaa V,
Ungar PS, Sponheimer M (2011) The diets of early hominins. Science 334,
Saharinen J, Sabatti C, Ruokonen A, Rudan I, Rose LM, Roberts R,
190–193. doi:10.1126/science.1207701
Rieder M, Psaty BM, Pramstaller PP, Pichler I, Perola M, Penninx B,
Uotila U, Raekallio J, Ehrnrooth W (1958) Goitre and atherosclerosis. Lancet
Pedersen NL, Pattaro C, Parker AN, Pare G, Oostra BA, O’Donnell CJ,
2, 171–173. doi:10.1016/S0140-6736(58)91522-8
Nieminen MS, Nickerson DA, Montgomery GW, Meitinger T,
Usydus Z, Szlifder-Richert J, Adamczyk M (2012) Variation in proximate
McPherson R, McCarthy MI, McArdle W, Masson D, Martin NG,
composition and fatty acid profiles of Baltic sprat (Sprattus sprattus
Marroni F, Mangino M, Magnusson PKE, Lucas G, Luben R, Loos
balticus). Food Chemistry 130, 97–103. doi:10.1016/j.foodchem.2011.
RJF, Lokki ML, Lettre G, Langenberg C, Launer LJ, Lakatta EG,
07.003
Laaksonen R, Kyvik KO, Kronenberg F, Konig IR, Khaw KT, Kaprio
Utermann G (1988) Apolipoprotein polymorphism and multifactorial
J, Kaplan LM, Johansson A, Jarvelin MR, Janssens A, Ingelsson E, Igi W,
hyperlipemia. Journal of Inherited Metabolic Disease 11, 74–86.
Hovingh GK, Hottenga JJ, Hofman A, Hicks AA, Hengstenberg C, Heid
IM, Hayward C, Havulinna AS, Hastie ND, Harris TB, Haritunians T, Hall doi:10.1007/BF01800572
Utermann G, Pruin N, Steinmetz A (1979) Polymorphism of apolipoprotein
AS, Gyllensten U, Guiducci C, Groop LC, Gonzalez E, Gieger C, Freimer
NB, Ferrucci L, Erdmann J, Elliott P, Ejebe KG, Doering A, Dominiczak E. III. Effect of a single polymorphic gene locus on plasma lipid levels
AF, Demissie S, Deloukas P, de Geus EJC, de Faire U, Crawford G, in man. Clinical Genetics 15, 63–72. doi:10.1111/j.1399-0004.1979.
Collins FS, Chen YDI, Caulfield MJ, Campbell H, Burtt NP, Bonnycastle tb02028.x
LL, Boomsma DI, Boekholdt SM, Bergman RN, Barroso I, Bandinelli S, Utrilla MC, Soriano A, Ruiz AG (2010) Quality attributes of pork loin with
Ballantyne CM, Assimes TL, Quertermous T, Altshuler D, Seielstad M, different levels of marbling from Duroc and Iberian cross. Journal of Food
Wong TY, Tai ES, Feranil AB, Kuzawa CW, Adair LS, Taylor HA, Quality 33, 802–820. doi:10.1111/j.1745-4557.2010.00352.x
Borecki IB, Gabriel SB, Wilson JG, Holm H, Thorsteinsdottir U, Van Niekerk PJ, Burger AEC (1985) The estimation of the composition of
Gudnason V, Krauss RM, Mohlke KL, Ordovas JM, Munroe PB, edible oil mixtures. Journal of the American Oil Chemists’ Society 62,
Kooner JS, Tall AR, Hegele RA, Kastelein JJP, Schadt EE, Rotter JI, 531–538. doi:10.1007/BF02542327
Boerwinkle E, Strachan DP, Mooser V, Stefansson K, Reilly MP, Samani VanItallie TB, Nufert TH (2003) Ketones: metabolism’s ugly duckling.
NJ, Schunkert H, Cupples LA, Sandhu MS, Ridker PM, Rader DJ, van Nutrition Reviews 61, 327–341. doi:10.1301/nr.2003.oct.327-341
Duijn CM, Peltonen L, Abecasis GR, Boehnke M, Kathiresan S (2010) Van Munster IP, Tangerman A, Nagengast FM (1994) Effect of resistant
Biological, clinical and population relevance of 95 loci for blood lipids. starch on colonic fermentation, bile acid metabolism, and mucosal
Nature 466, 707–713. doi:10.1038/nature09270 proliferation. Digestive Diseases and Sciences 39, 834–842.
Thissen JP, Ketelslegers JM, Underwood LE (1994) Nutrional regulation of doi:10.1007/BF02087431
the insulin-like growth factors. Endocrine Reviews 15, 80–101. Veech RL, Chance B, Kashiwaya Y, Lardy HA, Cahill GR Jr (2001)
Tholstrup T, Marckmann P, Jespersen J, Sandstrom B (1994a) Fat high in Ketone bodies, potential therapeutic uses. IUBMB Life 51, 241–247.
stearic acid favorably affects blood lipids and factor VII coagulation doi:10.1080/152165401753311780
activity in comparison with fats high in palmitic acid or high in myristic Veniant MM, Kim E, McCormick S, Boren J, Nielsen LB, Raabe M, Young
and lauric acids. The American Journal of Clinical Nutrition 59, 371–377. SG (1999) Insights into apolipoprotein B biology from transgenic and
Tholstrup T, Marckmann P, Jespersen J, Vessby B, Jart A, Sandstrom B gene-targeted mice. The Journal of Nutrition 129, 451S–455S.
(1994b) Effect on blood lipids, coagulation, and fibrinolysis of a fat high in Volek JS, Sharman MJ (2004) Cardiovascular and hormonal aspects of
myristic acid and a fat high in palmitic acid. The American Journal of very-low-carbohydrate ketogenic diets. Obesity Research 12,
Clinical Nutrition 60, 919–925. 115S–123S. doi:10.1038/oby.2004.276
Animal fats back on the table Animal Production Science 855

Volek JS, Sharman MJ, Gomez AL, Scheett TP, Kraemer WJ (2003) Yancy WS, Olsen MK, Guyton JR, Bakst RP, Westman EC (2004) A low-
An isoenergetic very low carbohydrate diet improves serum HDL carbohydrate, ketogenic diet versus a low-fat diet to treat obesity and
cholesterol and triacylglycerol concentrations, the total cholesterol to hyperlipidemia – a randomized, controlled trial. Annals of Internal
HDL cholesterol ratio and postprandial lipemic responses compared with Medicine 140, 769–777. doi:10.7326/0003-4819-140-10-200405180-
a low fat diet in normal weight, normolipidemic women. The Journal of 00006
Nutrition 133, 2756–2761. Yancy WS, Westman EC, McDuffie JR, Grambow SC, Jeffreys AS, Bolton J,
Volek JS, Fernandez ML, Feinman RD, Phinney SD (2008) Dietary Chalecki A, Oddone EZ (2010) A randomized trial of a low-carbohydrate
carbohydrate restriction induces a unique metabolic state positively diet vs Orlistat Plus a low-fat diet for weight loss. Archives of Internal
affecting atherogenic dyslipidemia, fatty acid partitioning, and Medicine 170, 136–145. doi:10.1001/archinternmed.2009.492
metabolic syndrome. Progress in Lipid Research 47, 307–318. Yang A, Larsen TW, Powell VH, Tume RK (1999a) A comparison of fat
doi:10.1016/j.plipres.2008.02.003 composition of Japanese and long-term grain-fed Australian steers. Meat
Vuorio AF, Turtola H, Piilahti K-M, Repo P, Kanninen T, Kontula K (1997) Science 51, 1–9. doi:10.1016/S0309-1740(98)00065-5
Familial hypercholesterolemia in the Finnish North Karelia. Yang A, Larsen TW, Smith SB, Tume RK (1999b) Delta(9) desaturase
Arteriosclerosis, Thrombosis, and Vascular Biology 17, 3127–3138. activity in bovine subcutaneous adipose tissue of different fatty acid
doi:10.1161/01.ATV.17.11.3127 composition. Lipids 34, 971–978. doi:10.1007/s11745-999-0447-8
Wang ZX, Jeon HY, Rigo F, Bennett CF, Krainer AR (2012) Manipulation Yang YJ, Lee SH, Hong SJ, Chung BC (1999c) Comparison of fatty acid
of PK-M mutually exclusive alternative splicing by antisense profiles in the serum of patients with prostate cancer and benign prostatic
oligonucleotides. Open Biology 2, 120133. doi:10.1098/rsob.120133 hyperplasia. Clinical Biochemistry 32, 405–409. doi:10.1016/S0009-
Warburg O (1956) On the origin of cancer cells. Science 123, 309–314. 9120(99)00036-3
doi:10.1126/science.123.3191.309 Yerushalmy J, Hilleboe HE (1957) Fat in the diet and mortality from heart
Welch AA, Shrestha SS, Lentjes MAH, Wareham NJ, Khaw KT (2010) disease a methodological note. New York State Journal of Medicine 57,
Dietary intake and status of n-3 polyunsaturated fatty acids in a population 2343–2354.
of fish-eating and non-fish-eating meat-eaters, vegetarians, and vegans Younis NN, Soran H, Pemberton P, Charlton-Menys V, Elseweidy MM,
and the precursor-product ratio of alpha-linolenic acid to long-chain n-3 Durrington PN (2013) Small dense LDL is more susceptible to glycation
polyunsaturated fatty acids results from the EPIC-Norfolk cohort. The than more buoyant LDL in Type 2 diabetes. Clinical Science 124,
American Journal of Clinical Nutrition 92, 1040–1051. doi:10.3945/ 343–349. doi:10.1042/CS20120304
ajcn.2010.29457 Yu-Poth S, Yin DZ, Kris-Etherton PM, Zhao GX, Etherton TD (2005)
West GC, Shaw DL (1975) Fatty acid composition of Dall sheep bone Long-chain polyunsaturated fatty acids upregulate LDL receptor
marrow. Comparative Biochemistry and Physiology. Part B, protein expression in fibroblasts and HepG2 cells. The Journal of
Biochemistry & Molecular Biology 50, 599–601. doi:10.1016/0305- Nutrition 135, 2541–2545.
0491(75)90096-6 Yudkin J (1957) Diet and coronary thrombosis hypothesis and fact. Lancet
Willcox BJ, Willcox DC, Todoriki H, Fujiyoshi A, Yano K, He Q, Curb JD, 2, 155–162. doi:10.1016/S0140-6736(57)90614-1
Suzuki M (2007) Caloric restriction, the traditional Okinawan diet, and Yudkin J (1964) Dietary fat and dietary sugar in relation to ischaemic
healthy aging. Annals of the New York Academy of Sciences 1114, heart-disease and diabetes. Lancet 2, 4–5. doi:10.1016/S0140-6736(64)
434–455. doi:10.1196/annals.1396.037 90002-9
Willcox DC, Willcox BJ, Todoriki H, Suzuki M (2009) The Okinawan diet: Zhu H, Tucker HM, Grear KE, Simpson JF, Manning AK, Cupples LA,
health implications of a low-calorie, nutrient-dense, antioxidant-rich Estus S (2007) A common polymorphism decreases low-density
dietary pattern low in glycemic load. Journal of the American College lipoprotein receptor exon 12 splicing efficiency and associates with
of Nutrition 28, 500S–516S. doi:10.1080/07315724.2009.10718117 increased cholesterol. Human Molecular Genetics 16, 1765–1772.
Willett WC, Stampfer MJ, Manson JE, Colditz GA, Speizer FE, Rosner BA, doi:10.1093/hmg/ddm124
Sampson LA, Hennekens CH (1993) Intake of trans fatty acids and risk of Zock PL, Katan MB (1998) Linoleic acid intake and cancer risk: a review
coronary heart disease among women. Lancet 341, 581–585. doi:10.1016/ and meta-analysis. The American Journal of Clinical Nutrition 68,
0140-6736(93)90350-P 142–153.
Wood JD, Enser M, Fisher AV, Nute GR, Richardson RI, Sheard PR (1999) Zock PL, de Vries JHM, de Fouw NJ, Katan MB (1995) Positional distribution
Manipulating meat quality and composition. The Proceedings of the of fatty acids in dietary triglycerides: effects on fasting blood lipoprotein
Nutrition Society 58, 363–370. doi:10.1017/S0029665199000488 concentrations in humans. The American Journal of Clinical Nutrition 61,
Wright SH, Snape JW Jr, Battle W, Cohen S, London RL (1980) Effect of 48–55.
dietary components on gastrocolonic response. The American Journal of Zock PL, Gerritsen J, Katan MB (1996) Partial conservation of the sn-2
Physiology 238, G228–G232. position of dietary triglycerides in fasting plasma lipids in humans.
Xia SH, Wang JD, Kang JX (2005) Decreased n-6/n-3 fatty acid ratio reduces European Journal of Clinical Investigation 26, 141–150. doi:10.1046/
the invasive potential of human lung cancer cells by downregulation j.1365-2362.1996.t01-1-105263.x
of cell adhesion/invasion-related genes. Carcinogenesis 26, 779–784. Zock PL, Mensink RP, Harryvan J, de Vries JHM, Katan MB (1997) Fatty
doi:10.1093/carcin/bgi019 acids in serum cholesteryl esters as quantitative biomarkers of dietary
Xu WL, Qiu CX, Wahlin A, Winblad B, Fratiglioni L (2004) Diabetes intake in humans. American Journal of Epidemiology 145, 1114–1122.
mellitus and risk of dementia in the Kungsholmen project – a 6-year doi:10.1093/oxfordjournals.aje.a009074
follow-up study. Neurology 63, 1181–1186. doi:10.1212/01.WNL. Zuccoli G, Marcello N, Pisanello A, Servadei F, Vaccaro S, Mukherjee P,
0000140291.86406.D1 Seyfried TN (2010) Metabolic management of glioblastoma multiforme
Xue F, Michels KB (2007) Diabetes, metabolic syndrome, and breast cancer: using standard therapy together with a restricted ketogenic diet: case
a review of the current evidence. The American Journal of Clinical report. Nutrition & Metabolism 7, 33. doi:10.1186/1743-7075-7-33
Nutrition 86, 823S–835S.

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