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Quinoa (pronounced ‘keen-wah’) is a tiny grain native to the Andes Mountains of South America where it’s been a staple for more than 5,000 years. The Incas prized it as the ‘mother grain’ and used it to supplement their predominantly vegetarian diet of potatoes and corn.
Despite its size, quinoa is a nutrition powerhouse. It’s a complete source of protein as it contains all nine essential amino acids including lysine, which is essential for tissue repair and growth – 100g uncooked quinoa provides roughly the same amount of protein as 2 small eggs and more than a quarter of our daily needs!
It’s high in fibre, too, and has good amounts of vitamins and minerals. In particular, it’s rich in iron – 100g uncooked quinoa provides more than half our daily needs for this nutrient. Add this to its high protein content and quinoa is a great choice for people who follow a vegetarian or vegan diet. Plus, it’s gluten and wheat free, making it a good alternative to pasta and bread for people with coeliac disease.
Quinoa grains come in various colours, from white or pale yellow to red, purple brown and black. You can also buy it as flakes (a good alternative to breadcrumbs) and flour (good for making gluten-free pastry).
It’s easy to prepare. First, rinse the grains in water, then drain. Simmer in a pan of water, stock or milk (one part quinoa to three parts liquid) for 10–15 min. To really bring out the flavour, you can toast the quinoa before simmering. Or you can cook quinoa in the microwave: put the same ratio of quinoa to liquid in a large microwavable bowl, cover and cook on high for 7 min. Allow to stand for 7 min or until the liquid is absorbed.
The delicate texture of quinoa works in soups, stews, salads, breads and sweets. In fact, there’s no end to its versatility!
For a taste of the wonders of this nutritious ingredient, try HFG recipe consultant Phil Mundy’s festive recipe …
Quinoa, dried cranberry and pine nut stuffing
Prep 10 min
Cook 40 min
Serves 12
Cooking oil spray
200g quinoa
1½tsp gluten-free reduced-salt veg stock powder
1 large onion, finely chopped
2 garlic cloves, crushed
50g dried cranberries, roughly chopped
35g pine nuts, lightly toasted
2tbsp chopped thyme
Juice of ½ orange
1 Preheat the oven to 190°C/fan 170°C/gas 5 and lightly spray a 1 litre ovenproof dish with oil.
2 Put the quinoa in a medium pan with the stock powder and 500ml boiling water. Bring to the boil, then reduce the heat to low, cover and simmer for 15–18 min until the water is absorbed and the grains are tender.
3Meanwhile, spray a non-stick frying pan with a little oil and put over a medium heat. Add the onion and cook, stirring occasionally, for 5 min or until softened. Add the garlic and stir for 1 min more, then remove from the heat.
4 Transfer the quinoa and onion mixture to a large mixing bowl, then stir through the remaining ingredients and season with ground black pepper. Spoon the mixture into the prepared dish, then bake for 20 min.
Vilhjalmur Stefansson was an Artic explorer known for his observations on the traditional living Inuit-Eskimo, which he lived together with in the winter of 1906-1907 in the Mackenzie Delta of Canada. Stefansson asserted that during this time he subsisted on traditional Inuit fare, based almost exclusively on flesh. In part based on less than extensive observations of the health of the Inuit, Stefansson hypothesized that a number of chronic and degenerative diseases, including cancer are diseases of civilization which can be prevented by adherence to a pre-modern diet and lifestyle. However, Stefansson did not suggest that only flesh based dietary patterns, such as that consumed by the traditional living Inuit, but also primarily vegetarian diets, such as that consumed by the Hunza may protect against such diseases.1
The term diseases of civilization, which Stefansson has contributed to the popularization of is frequently referred to by proponents of Low-Carb, Paleo, Primal and Weston A. Price Foundation type diets. Many of these proponents have extrapolated limited suggestive evidence that obesity, type 2 diabetes, coronary heart disease, certain cancers, and a number of other chronic and degenerative diseases were uncommon during the Paleolithic period to suggesting that foods derived from naturally raised, grass-fed animals, as was consumed by Paleolithic humans must therefore somehow provide protection against these so-called diseases of civilization. Many of these proponents have also claimed that a vast number of scientific studies that have been used as evidence to conclude that animal foods increase the risk of such diseases have been complicated by confounding of other unhealthy foods and lifestyle factors, or by the use of unnaturally raised animal foods. This series of posts will examine the evidence to help determine whether these claimed confounding variables can actually explain the evidence linking animal foods with certain chronic and degenerative diseases, often referred to as diseases of civilization, but also as western diseases, lifestyle diseases and diseases of affluence.
In 1928, Stefansson and his colleague Karsten Anderson participated in a monitored experiment partly funded by the meat industry in which they consumed a flesh exclusive diet for the period of one year. Although the researchers concluded that these two men were in good health throughout the experiment, Anderson experienced a severe elevation in blood cholesterol, with measurements as high as 800 mg/dl on one occasion, which returned to pre-experiment levels after resuming a higher carbohydrate diet.2 A glucose tolerance test carried out immediately after the termination of the meat based experiment showed a marked rise in blood sugar in both men compared to a subsequent test carried out after resuming a higher carbohydrate diet. Glucose was detected in the urine of Anderson in the test following the meat based experiment, a marker of untreated diabetes. This abnormality was not detected in the subsequent test after resuming a higher carbohydrate diet.3
Short-term experiments such as this cannot provide adequate insight into the long-term consequences of following such a diet, as it can take many decades for diseases caused by exposure to harmful substances to become clinically significant. For example, the greatest risk of excess death from radiation-related solid cancers among the atomic bomb survivors of Hiroshima and Nagasaki was more than half a century after exposure.4 Furthermore, other flesh based experiments have resulted in considerably more unfavorable outcomes. For example, in 1906, Russell noted an even earlier experiment:
A recent instance occurred in South Africa, where about twenty natives out of some hundreds who were supplied with a large amount of flesh, as an experiment, by mine-owners, died, and many others were ill.5
Cardiovascular Disease in Ancient Civilizations
The traditional living Inuit's were certainly not immune from atherosclerosis
If a diet rich in naturally raised animal foods provides protection against cardiovascular disease as many proponents of Low-Carb type diets claim, it would be expected that traditional living populations consuming such a diet, particularly those living prior to the rapid westernization of the globe would demonstrate evidence of superior cardiovascular health compared to those populations who subsisted primarily on starchy staples, including grains, legumes and tubers. Populations who have inhabited the arctic, where scant plant matter is available throughout most parts of the year, such as the Inuit and Aleut were forced to subsist almost exclusively on hunted marine animals for extensive periods of time.16 This should make these populations suitable to study the hypothesis that naturally raised animal foods protect against cardiovascular disease.
Contrary to claims of the traditional living Inuit being immune from cardiovascular disease, evidence of severe atherosclerosis has been identified in several frozen mummies of Alaskan Inuit dating back to 400 CE and 1520 CE, both instances predating European contact.78 Atherosclerosis has also previously been identified in several artificially prepared mummies of Aleut-Unangan hunter gatherers who lived in the 18th century in the Aleutian Islands in Alaska.910 Recently the HORUS study, which examined an additional five recovered mummies of Unangan hunter gatherers who lived in the mid and late 19th century found definite evidence of atherosclerosis in several major arteries in all three who were over the age of 25.11
When considering the findings from all of these Alaskan Inuit and Aleut mummies it becomes evident that these Alaskan natives likely experienced a greater incidence of atherosclerosis, especially given the young mean age compared to the three other ancient populations studied in the HORUS study. Unlike the Alaskan natives, these other three populations, which were the ancient Egyptians, ancient Peruvians and Ancestral Puebloans practiced agriculture and consumed grains.
In addition to evidence of atherosclerosis from native Alaskan mummies, reports from medical officers provide further evidence of unfavorable rates of cardiovascular disease among the Inuit before the rapid transition to the western diet. In 1940, based on decades of clinical practice and reviewing reports of medical officers dating all the way back 175 years ago, Bertelsen, who is considered the father of Greenland epidemiology stated in regards to the mortality patterns among the Greenland Inuit that:
...arteriosclerosis and degeneration of the myocardium are quite common conditions among the Inuit, in particular considering the low mean age of the population.12
Bjerregaard and colleagues performed a literature review for studies addressing the incidence of atherosclerosis and cardiovascular disease among the Inuit of Alaska, Canada and Greenland spanning from the 1930s to more recent decades. The researchers found that the incidence of atherosclerosis was generally similar to that of other western populations that suffered from high rates of cardiovascular disease. Mortality from stroke was found to be even higher, and mortality from all cardiovascular diseases combined was found to be similar or even higher among the Inuit. The researchers also found that mortality from coronary heart disease among the Inuit was not significantly different after adjusting for ill-defined causes of cardiovascular death, suggesting that the substantial proportion of cardiovascular deaths being classified as ‘garbage codes’, particularly in Greenland may have hidden a significant portion of deaths from coronary heart disease. The researchers concluded:
The mortality from all cardiovascular diseases combined is not lower among the Inuit than in white comparison populations. If the mortality from IHD [ischemic heart disease] is low, it seems not to be associated with a low prevalence of general atherosclerosis. A decreasing trend in mortality from IHD in Inuit populations undergoing rapid westernization supports the need for a critical rethinking of cardiovascular epidemiology among the Inuit and the role of a marine diet in this population.12
A similar phenomenon to the misclassification of deaths from coronary heart disease among the Inuit populations has also been observed in France, which may largely explain the so-called French Paradox. Data from the World Health Organization MONICA Project suggests that the official mortality statistics for France significantly underreport deaths from cardiovascular disease compared to other countries, with deaths from coronary heart disease being underestimated by 75%. Other reports suggest that this is likely explained by a much higher rate of French doctors classifying deaths as due to ‘other causes’ than in other countries.1314
It has been observed that among the Alaskan Inuit a higher intake of saturated fat is associated with elevated blood pressure, insulin resistance, glucose intolerance and carotid atherosclerosis, suggesting that the traditional Inuit foods relatively rich in saturated fat were likely to have been detrimental to the cardiovascular health of the Inuit.151617 It has also been observed that among Alaskan Inuit elevated LDL cholesterol is associated with a greater than fourfold increased risk of cardiovascular disease.18 Furthermore, rheumatic disorders that have been linked to cardiovascular disease, such as gout and rheumatoid arthritis have been found to be just as, or even more common among the Eskimo populations compared to that of the general North American population.1920 Established risk factors, a number of which are likely adversely affected by the traditional Inuit diet can probably in part explain the evidence of severe atherosclerosis and unfavorable rates of cardiovascular disease observed among the traditional living Inuit and Aleut populations.
In the HORUS study it was found that two of the four Ancestral Puebloan who lived in southwestern United States dating between 1500 BCE and 500 CE exhibited probable evidence of atherosclerosis, the two other both being under the age of 30. These Ancestral Puebloans were identified as being from a time when they were transitioning from hunter-gatherers to farmer-foragers, and were likely to have relied on hunted animal foods to supply at least a modest portion of their diet. An additional Ancestral Puebloan mummy aged 18-22 found from a later period after a greater transition towards agriculture did not exhibit any evidence of atherosclerosis.11
In the HORUS study the ancient Egyptian mummies exhibited the next greatest frequency of atherosclerosis, with 29 (38%) of the 76 of the mummies exhibiting at least probable evidence of atherosclerosis.11 In their book Protein Power, Michael and Mary Eades assert that the ‘diet of the average [ancient] Egyptian consisted primarily of carbohydrates’, which they suggest was ‘a veritable nutritionist’s nirvana… rich in all the foods believed to promote health and almost devoid of saturated fat and cholesterol'. These authors go on to suggesting that the carbohydrate rich diet of the ‘average Egyptian’ which they describe as being based on whole-grain wheat and barley supplemented by a variety of fruits, vegetables, legumes, nuts and some goats milk is responsible for the atherosclerosis and obesity exhibited by the ancient Egyptian mummies.21
The authors of Protein Power suggest that complex carbohydrates, such as wheat made the ancient Egyptians obese
There is much evidence that casts doubt on these authors description of the diets of the ancient Egyptian mummies. For example, Macko and colleagues have shown that isotope analyses of the amino-acid composition of hair from the ancient Egyptian mummies far more closely resemble that of modern westerners following an omnivorous diet than a vegetarian, and especially vegan diet.22 In addition, David and colleagues showed that evidence from hieroglyphic inscriptions on ancient Egyptian temples suggest that the elites of ancient Egyptian society, being those who were primarily mummified consumed a diet rich in flesh and saturated animal fat. These researchers addressed the confusion surrounding the diet and atherosclerosis of the ancient Egyptian mummies, asserting:
It is important to point out that there was a marked difference between the mainly vegetarian diet most Egyptians ate and that of royalty and priests and their family members whose daily intake would have included these high levels of saturated fat. Mummification was practised by the elite groups in society, ensuring that their remains have survived to provide clear indications of atherosclerosis; by contrast, there is a lack of evidence that the condition existed among the less well-preserved remains of the [mainly vegetarian] lower classes.23
The findings of a lower incidence of atherosclerosis among the lower classes of ancient Egypt who subsisted primarily on a carbohydrate-rich vegetarian diet are consistent with observations in Egypt in the early 20th century. In 1934, Rosenthal asserted:
Of interest is the report of Ismail in Egypt, who has communicated that among his private patients, whose diet is similar to that of the Europeans, the incidence of atherosclerosis is high, while in his hospital practice, composed mainly of natives, who subsist largely on a carbohydrate diet, the incidence of atherosclerosis is low.24
It is clear that the authors of Protein Power have confused the diet of the elites of the ancient Egyptian society, who certainly cannot be considered as the 'average Egyptian' with the largely vegetarian diet of the of the lower classes who exhibit a lack of atherosclerosis, and which scant evidence suggests were obese. The findings from ancient Egyptian mummies do not support the claimed benefits of a low carbohydrate, high saturated fat diet promoted by these authors.
In the HORUS study, despite having the highest mean age, nearly 10 years older than that of the Unangan and Ancestral Puebloans mummies, the ancient Peruvians exhibited the lowest incidence of atherosclerosis, being evident in 13 (25%) of 51 of the mummies. Compared to these other studied ancient populations, the Peruvians likely relied more on staple plant foods, such as corn, beans and tubers, although did consume some domesticated and hunted animals.11
The researchers of the HORUS study suggested that exposure to smoke from fire used for cooking and25 heating may help explain some of the degree of atherosclerosis identified in these ancient populations. However, the description of the use of fire for cooking in ancient Egypt provided by these researchers would apply primarily to the lower classes of ancient Egypt which exhibit a lack of atherosclerosis, rather than the mummified elites that these researchers examined who would typically have had servants to cook for them.
Gout was known to be common among
the Mongols of the Golden Horde
In regards to the traditional living Inuit and Aleut, it has been suggested that the extensive exposure to seal oil lamps may help explain the relatively severe degree of atherosclerosis in these populations. These findings should however be considered in light of evidence of atherosclerosis in other populations which have high exposure to hazardous smoke but consume contrasting diets. For example, it has been observed that the Papua New Guinean highlanders have a smoking prevalence of greater than 70% for males and 20% for females while also being exposed to smoke for up to twelve hours a day due to the use of centrally placed open wood fires in their houses which lack both ventilation and chimneys. Despite such a high exposure to hazardous smoke it has been observed that the Papua New Guinean highlanders have among the lowest age-adjusted incidence of atherosclerosis of any studied population. However, unlike the Inuit, the Papua New Guinean highlanders traditionally consumed a plant based diet with carbohydrate supplying more than 90% of total energy intake, predominantly derived from sweet potatoes.2627
Another population that have historically been documented to subsist almost exclusively on a diet derived from grass-fed, free-ranging animals are the largely nomadic Mongolians. John of Plano Carpini who visited the Mongols in the mid-13th century noted:
[The Mongols] have neither bread nor herbs nor vegetables nor anything else, nothing but meat… They drink mare’s milk in very great quantities if they have it; they also drink the milk of ewes, cows, goats and even camels.28
Smith reviewed the literature regarding the health of the Mongols from the 13th century and noted that a number of unfavorable cardiovascular risk factors, including obesity and gout were both common disorders. Smith went on to state:
Cardio-vascular problems, although not then subject to diagnosis, may be suspected as well.29
In 1925, Kuczynski reported on the nomadic pastoralists of the Kirghiz and Dzungarian Steppes in Central Asia and northern China that were of Mongolian descent. Similar to the observations of the diet of the nomadic Mongols of the 13th century, Kuczynski observed that these nomadic pastoralists subsisted almost exclusively on enormous quantities of meat and milk from grass-fed, free-ranging animals. Other authors have also come to the same conclusions regarding the composition of the diet of the nomadic pastoralists of the Central Asian Steppes. For example, Tayzhanov asserted:
…the people [of the steppe] lived exclusively on meat, fat and sour milk. Bread was added only later and even then some households did not adopt or consume this food.30
Similarly, Barfield asserted:
In good legendary style, the pure Central Asian nomads eat only meat, marrow, and milk products {preferably ferments}. They despise farmers, farming, and grain…31
These findings suggest that the diet of these nomadic pastoralists of the Central Asian Steppes was almost exclusively animal based, virtually devoid of grains, legumes and refined carbohydrates. This should make these populations also suitable to study the hypothesis that naturally raised animal foods protect against cardiovascular disease. However, not only did Kuczynski observe that these nomadic pastoralists suffered from high rates of obesity and gout similar to the Mongols of the 13th century, Kuczynski's observations further extended to the diagnosis of cardiovascular disease and other dietary related disorders. Kuczynski asserted:
They get arteriosclerosis in an intense degree and often at an early age as shown by cardiac symptoms, nervous disordes, typical changes of the peripheral vessels, nephrosclerosis and, finally, apoplectic attacks. Even in men thirty-two years old I frequently observed arcus senilis.32
It was also observed that in the 1960s the prevalence of coronary heart disease among the nomadic pastoralists in Xinjiang in northern China who consumed large quantities of animal fat from grass-fed, free-ranging animals was more than seven times higher than that of other populations both within Xinjiang and throughout China which consumed significantly less animal fat.33 These observations support the suggestion that cardiovascular disease was common among the Mongols of the 13th century who subsisted almost exclusively on a diet based on grass-fed, free-ranging animals.
Dispelling Grass-Fed Fairy Tales
These findings from populations living before the 20th century suggest that similar to the findings from people studied in more modern times, a greater intake of minimally refined plant foods strongly predicts a lower prevalence of atherosclerosis and cardiovascular disease. These findings cast doubt on the hypothesis that foods from organic, naturally raised animals protect against cardiovascular disease compared to staple plant foods. Furthermore, these findings suggest that the traditional living populations that relied predominantly on naturally raised animal based foods suffered from complications related to cardiovascular disease at a relatively young age and are poor role models for health.
Future posts in this series will further address how naturally raised animal foods influence cardiovascular disease, as well as other so-called diseases of civilization.
Recently two meta-analysis papers were published addressing the findings from population studies of the association between egg intake and the risk of cardiovascular disease.12 Unfortunately the authors of these two review papers reached contradictory conclusions regarding the dangers of egg intake which is likely to lead to unnecessary public confusion. The authors of the most recent meta-analysis paper reviewed studies on coronary heart disease, heart failure, diabetes and all cardiovascular diseases (CVD) combined and concluded:
Our study suggests that there is a dose-response positive association between egg consumption and the risk of CVD and diabetes.
In contrast to this conclusion, the authors of the earlier meta-analysis paper limited their review to studies that specifically addressed coronary heart disease and stroke and concluded:
Higher consumption of eggs (up to one egg per day) is not associated with increased risk of coronary heart disease or stroke. The increased risk of coronary heart disease among diabetic patients and reduced risk of hemorrhagic stroke associated with higher egg consumption in subgroup analyses warrant further studies.
The second meta-analysis paper is problematic in part because the authors failed to consider the relevant findings from dozens of rigorously controlled feeding experiments on humans and thousands of experiments on animals, including nonhuman primates that strongly support the recommendations to limit the intake of eggs and cholesterol [reviewed previously]. This paper is also problematic in part because the authors failed to consider many other relevant findings from prospective cohort studies which suggest that egg and cholesterol intake increases the risk of coronary heart disease, diabetes, heart failure, cardiovascular disease and all-cause mortality.
Firstly, the association between egg intake and the risk of cardiovascular disease is meaningless without considering suitable substitutes for eggs. As a lower intake of eggs implies a higher intake of other foods in order to maintain caloric balance, the effect that egg intake has on coronary heart disease depends on which foods eggs are substituted for. For example, data from the Nurses’ Health Study, one of the largest studies included in these meta-analyses suggested that replacing one serving of nuts, but not red meat and dairy with one serving of eggs per day is associated with a significantly increased risk of coronary heart disease.3 The authors of both meta-analyses failed to address this factor despite the fact that the importance of evaluating suitable food alternatives has been strongly emphasized by many prominent diet-heart researchers.4 The findings from these meta-analyses should therefore be interpreted with caution as eggs may have been primarily compared to processed foods and other animal foods which make up the majority of caloric intake in developed nations.45
Eggs, Cholesterol and Diabetics
The authors of the most recent meta-analysis paper found that among diabetics, frequent egg intake was associated with a 83% increased risk of cardiovascular disease, whereas the authors of the earlier meta-analysis paper found that frequent intake was associated with a 54% increased risk of coronary heart disease. The authors of the most recent meta-analysis paper excluded one, while the authors of the earlier meta-analysis paper excluded two additional cohort studies that found that among diabetics, high compared to low intake of eggs was associated with an approximately five-fold increased risk of cardiovascular disease.67 These additional studies had they been addressed by these authors would have potentially strengthened the association between egg intake and an increased risk of cardiovascular disease in diabetics.
The authors of the most recent meta-analysis found that frequent egg intake was associated with a 68% increased risk of type II diabetes, a major risk factor for cardiovascular disease. However, the authors of the earlier meta-analysis largely failed to address this evidence. A literature search I performed produced papers from 5 separate prospective cohort studies addressing egg intake and the risk of developing type II diabetes, including two additional studies that were not addressed in both meta-analyses papers.891011 In addition, I also found one additional cohort study addressing egg intake and the risk of developing gestational diabetes.12 All except one smaller cohort found a statistically significant association after adjusting for potential confounders. These cohorts also found suggestive evidence that the increased risk persisted regardless of whether eggs were consumed in the presence of a higher or lower carbohydrate diet, and that the association was even stronger when repeated measurements of egg intake were considered.9 In addition, these cohorts also found suggestive evidence that the increased risk could partly be explained by the dietary cholesterol and protein content of eggs, and that substituting eggs with carbohydrate-rich foods, especially fiber-rich bread and cereals significantly decreases the risk of developing type II diabetes.891112
In the one cohort that did not find a statistically significant association, average egg intake was relatively low and there was suggestive evidence of an increased risk when a follow-up measurement of egg intake was used to update exposure overtime.10 In addition to these findings, a paper from the Health Professionals Follow-Up Study also found suggestive evidence that egg intake is associated with an increased risk of type II diabetes.13 Furthermore, papers from an additional 5 cohort studies found that dietary cholesterol was associated with a significantly increased risk of developing either type II diabetes or gestational diabetes.141516
Overall findings from 12 prospective cohort studies with 265,675 participants and 14,497 cases of type II diabetes and gestational diabetes strongly implies that egg and cholesterol intake are significant risk factors in the development of diabetes. In addition to the findings from cohort studies, 4 cross-sectional studies found that egg or cholesterol intake was associated with between a nearly two-fold and greater than four-fold increased risk of developing type II diabetes and gestational diabetes.12171819 Also consistent with these findings, in the Adventist Health Study 2 it was observed that vegans had a lower risk of developing type II diabetes compared to lacto-ovo vegetarians, and especially non-vegetarians.20
One cohort included in these meta-analyses that used repeated egg intake measurements to update exposure over time found that in diabetics, intake of at least 7 eggs compared to less than 1 egg per week was associated with a two-fold increased risk of all-cause mortality, whereas another cohort that did not use repeated measurements found suggestive evidence of a 30% increased risk of all-cause mortality.2122 The authors of the first study stated:
…among male physicians with diabetes, any egg consumption is associated with a greater risk of all-cause mortality, and there was suggestive evidence for a greater risk of MI [heart attack] and stroke.
An additional study found that in diabetics, an increment of one egg per day was associated with a greater than three-fold increased risk of all-cause mortality.6
According to the International Diabetes Federation, globally approximately 183 million people, or half of those who have diabetes have not been diagnosed. Even in high-income countries about one-third of people with diabetes have not been diagnosed.23 Given this data and the data that egg and cholesterol intake is associated with a significantly increased risk of developing diabetes, and that in diabetics egg intake is associated with a significantly increased risk of coronary heart disease, cardiovascular disease and all-cause mortality, there is likely a significantly greater number of people at risk than suggested by the authors of these recent meta-analyses.
Eggs, Cholesterol and Non-Diabetics
The Nurses’ Health Study found that an increment of cholesterol equivalent to one medium size egg per day was associated with a 17% increased risk of all-cause mortality, consistent with the findings from several other studies.242526 Another study included in these meta-analyses found that in non-diabetics, intake of at least 7 eggs compared to less than 1 egg per week was associated with a 22% increased risk of all-cause mortality.21 Also, another cohort from Japan found that frequent egg intake was associated with an increased risk of all-cause mortality in women, consistent with the findings from the Adventists Mortality Study.2728 In addition, a cohort of elderly found suggestive evidence that egg intake was associated with a significantly increased risk of all-cause mortality, and that substituting eggs with fruits, vegetables and grains significantly decreases risk.29
The authors of the most recent meta-analysis paper found that in largely non-diabetic populations that frequent egg intake was associated with 19% increased risk of cardiovascular disease compared to all other sources of calories combined, which is predominantly processed foods and other animal foods. The authors of the earlier meta-analysis that did not reach this conclusion suggested that their findings are relevant for total cardiovascular disease but failed to address the findings from prospective cohort studies regarding the risk for heart failure. For example, two cohort studies which were included in the most recent meta-analyses found that intake of at least 7 eggs compared to less than 1 egg per week was associated with an approximately 30% increased risk of heart failure.3031
Another potential important finding that has contributed to the knowledge of the dangers of eggs are the results from studies that were carried out on populations with a low habitual cholesterol intake, such as vegetarian populations. The authors of the most recent meta-analysis paper excluded one, while the authors of the earlier meta-analysis paper excluded two cohort studies that were carried out on largely vegetarian populations. Frequent consumption of eggs was associated with a more than 2.5 increased risk of fatal coronary heart disease in the Oxford Vegetarian Study and also an increased risk in females in the Adventists Mortality Study.2832 The characteristics of the participants in these studies differ from that of most other studies, not only because of the their lower habitual intake of dietary cholesterol, but also because of their lower rates of obesity and typically healthier overall diet. Therefore separately analyzing egg intake in this subgroup of the population may be of significant importance. The authors of a paper from the Nurses’ Health Study and the Health Professionals Follow-Up Study cited in these meta-analyses described the potential importance of addressing egg intake in people with very low habitual cholesterol intake and how their study may have been inadequate to test this hypothesis: 33
One potential alternative explanation for the null finding is that background dietary cholesterol may be so high in the usual Western diet that adding somewhat more has little further effect on blood cholesterol. In a randomized trial, Sacks et al found that adding 1 egg per day to the usual diet of 17 lactovegetarians whose habitual cholesterol intake was very low (97 mg/d) significantly increased LDL cholesterol level by 12%. In our analyses, differences in non-egg cholesterol intake did not appear to be an explanation for the null association between egg consumption and risk of CHD. However, we cannot exclude the possibility that egg consumption may increase the risk among participants with very low background cholesterol intake.
As it is well documented that cholesterol intake has a much greater effect of raising serum cholesterol when baseline intake is very low, this may in part explain why egg and cholesterol intake was more strongly associated with coronary heart disease in studies on largely vegetarian populations.3435 Another explanation for a possibly stronger association in vegetarian populations is that egg intake may have a greater effect in leaner people, and it has been well documented that vegetarians are generally leaner than their omnivorous counterparts [reviewed previously]. This hypothesis is supported by several dietary experiments which found that dietary cholesterol had a greater effect of raising serum cholesterol among leaner compared to overweight participants.3637 This hypothesis is also supported by the findings from the Chicago Western Electric Study which found that while dietary cholesterol was associated with a significantly increased risk of coronary heart disease in lean men over and above the adverse effects it has on serum cholesterol, increased intake had little appreciable effect on men with a greater BMI and body fatness.38 Another explanation for these findings is that vegetarians may choose healthier substitutes for eggs, such as nuts which was associated with a significantly lower risk of coronary heart disease compared to eggs in the Nurses’ Health Study.3
It was found in a sub-analysis based on 4 cohorts included in the earlier meta-analyses that egg intake was associated with an 18% non-significant increased risk of fatal coronary heart disease. The addition of the mortality findings from the two largely vegetarian cohorts that were excluded from this meta-analysis would have likely strengthened this association.2832 This suggests that similar to saturated fat intake, egg intake may increase the risk of fatal coronary heart disease more than non-fatal coronary heart disease [reviewed previously]. The lack of a significant association likely reflects the fact that eggs were not compared to healthy foods, and also likely due to misclassification of participants into ranges of usual dietary intake as the result of measurement error [reviewed previously].
In the video below Dr. Michael Gregor addresses recent research on choline when consumed from eggs and other animal foods and the risk of cardiovascular disease and cancer.
Carnitine, Choline, Cancer and Cholesterol: The TMAO Connection
Egg Intake and Stroke
In regards to a sub-group analysis of 5 cohort studies, the authors of the earlier meta-analysis suggested that egg intake was associated with a lower risk of hemorrhagic stroke. The authors suggested that the inverse association between egg intake and hemorrhagic stroke is supported by findings of an inverse association between serum cholesterol and hemorrhagic stroke in several cohort studies. However, in the largest cohort study the authors cited, the inverse association was confined to participants with elevated blood pressure.39 A similar interaction between blood pressure and serum cholesterol and hemorrhagic stroke was observed in much larger cohort studies in both Asian and Western populations that the authors of this meta-analysis conveniently failed to cite.4041 In a meta-analysis of 61 cohort studies it was found that among participants with near optimal systolic blood pressure (<125 mmHg), lower serum cholesterol was actually associated with a significantly lower risk of hemorrhagic, ischemic and total stroke mortality [reviewed previously]. Furthermore, most mammalian species have very low LDL levels (mean value of 42 mg/dl in 18 species), and there is very scant evidence that these animals are at high risk of having a stroke.42
This data demonstrates that continued emphasis should be placed on lowering both LDL cholesterol and blood pressure which have been proven in hundreds of randomized controlled trials to lower not only the risk of cardiovascular disease, but also all-cause mortality.4344 Increasing the intake of eggs after achieving a near optimal blood pressure is unlikely to reduce the risk of hemorrhagic stroke and will likely increase the risk of dying of any cause.
Unwarranted Mediocre Health Recommendations
The conclusions of the earlier meta-analysis are misleading and inconsistent with the body of literature. What is more concerning is that these findings will likely be used in marketing campaigns to confuse the general population, of which the great majority are already at risk of cardiovascular disease. The most recent meta-analysis paper while being overall informative and more clearly demonstrating the dangers of eggs for both diabetics and non-diabetics, the authors still failed to address many important findings that have been addressed in this series of posts. A greater emphasis on the effects of replacing eggs with other suitable foods is required, and the available evidence suggests a significant benefit of replacing eggs with whole plant foods, including fruits, vegetables, whole grains and nuts.31129 As Spence and colleagues pointed out in regards to recent controversy surrounding dietary cholesterol and eggs:45
…the only ones who could eat egg yolk regularly with impunity would be those who expect to die prematurely from nonvascular causes.
A recent publication from the EPIC-Oxford cohort with 15,000 vegetarians and 30,000 non-vegetarians found that the vegetarians had a 32% lower risk of hospitalization or death from coronary heart disease.1 These findings are consistent with a previous meta-analysis of 5 cohort studies with 48,000 non-vegetarians and 28,000 vegetarians which found that lacto-ovo vegetarians had a 34% lower risk of fatal coronary heart disease compared to regular meat eaters.2 These findings remained significant even after adjusting for non-dietary factors and alcohol intake. In addition, in each of these 6 cohort studies, vegetarians and non-vegetarians shared a similar interest in healthy lifestyles or were of a similar religious background, therefore limiting the number of potential confounders that could have obscured these findings.
This review will focus on the evidence from randomized controlled trials and long-term prospective cohort studies addressing the influence of vegetarian dietary patterns on the risk of coronary heart disease, and how these findings have contributed to the current understanding of the diet-heart hypothesis. This review will also consider the question as to whether the simple definition of a vegetarian diet is meaningful in the context of a healthy diet to reduce the risk of coronary heart disease. Regarding cohort studies, this review will primarily consider the influence of lacto-ovo vegetarian diets on the risk of coronary heart disease due to limited evidence from these studies addressing the long-term adherence to other types of vegetarian diets. A more informative analysis maybe possible after a longer follow-up of the on-going and largest cohort of vegetarians, the Adventist Health Study 2, which has observed more favorable cardiovascular risk factors within different vegetarian subgroups, particularly vegans.3
Skeptics of the diet-heart hypothesis often suggest that there are no plausible mechanisms in which a vegetarian dietary pattern can lower the risk of coronary heart disease, and often ascribe the observed benefits of vegetarianism to factors other than the avoidance of animal foods. Typically either ignored or downplayed by these skeptics is the convincing evidence that vegetarian dietary patterns can lower LDL cholesterol, which is an established risk factor for coronary heart disease.456
Establishing Causation
In the 6 cohorts described, a sizable portion of the non-vegetarians consumed significantly less meat than the general population. For example, in the EPIC-Oxford cohort, most participants were either occasional meat eaters, or affiliated with vegetarians or with vegetarian societies. Also, a potential problem in these cohorts is that measurement error of usual dietary intake of meat may have resulted in misclassifying a sizable portion of non-vegetarians as vegetarians. For example, in the Health Food Shoppers Study included among these cohorts, a validity assessment of the survey used to classify the participants vegetarian status suggested that 34% of the participants classified as vegetarians actually consumed meat. This data strongly suggests a much smaller than otherwise expected difference in dietary intake between the groups classified as vegetarians and non-vegetarians, potentially masking a stronger protective effect of a vegetarian dietary pattern.7
Another potential problem in these cohorts is the possibility that a sizable portion of participants classified as vegetarians stopped consuming meat or other animal foods in response to deteriorating health or unfavorable risk factors that would ultimately become life-threatening. This has been referred to as the ‘sick quitter effect’, which is known to mask the protective effect of smoking cessation in studies due to participants quitting in response to deteriorating health.8 In regards to diet, it has been documented that people tend to lower intake of saturated fat and cholesterol in response to unfavorable serum cholesterol levels, which has actually been shown to bias the association between diet and serum cholesterol in the opposite direction than expected [reviewed previously]. This bias is known as reverse causation, and may explain why in the Adventist studies that participants with short-term adherence (less than 5 years) to a vegetarian diet experienced an increased risk of mortality, while participants with long-term adherence (more than 17 years) to a vegetarian diet experienced a significantly lower risk of mortality compared to non-vegetarians (Fig. 1).8
Figure 1. Life expediencies for long-term vegetarians and short-term vegetarians in the Adventist Health Study and Adventist Mortality Study*
These factors should be taken into account when testing for causality as failing to do so may mask a protective effect of a vegetarian dietary pattern. One of the most important factors in order to establish causality is to address whether the association is biologically plausible, which in this case requires examining how vegetarian dietary patterns can influence cardiovascular risk factors.
Serum Lipids
In 1922, de Langen published what was perhaps the first study that provided strong evidence that a vegetarian dietary pattern favorably effects serum cholesterol when he placed five native Indonesians consuming a rice-based vegetarian diet into a metabolic ward and shifted the diet to one rich in meat, butter and egg fats, resulting in significant elevations in serum cholesterol [reviewed previously]. In 1954, Hardinge and Stare published what was perhaps the first observational study comparing the serum lipids of vegetarians to non-vegetarians in an affluent population. Lacto-ovo vegetarians and especially vegans had significantly lower serum cholesterol concentrations despite relatively high intakes of saturated fat.910 In 2009, Ferdowsian and Barnard published a systematic review of 27 randomized controlled trials and observational studies on either vegetarian or predominantly plant-based diets, and found that certain plant-based dietary patterns can lower LDL cholesterol by up to 35%, independent of changes to body weight (Figs 2, 3).4
Figure 2. Effects of plant-based diets in normolipidemic individuals: Randomized controlled trials*
Figure 3. Effects of plant-based diets in hyperlipidemic individuals: randomized controlled trials*
In the Lifestyle Heart Trial lead by Dr. Dean Ornish, intensive lifestyle changes including a vegetarian diet that allowed a small amount of non-fat dairy foods successfully reduced LDL by 37.2%, angina episodes by 91% and regressed coronary atherosclerosis in the experimental group after 1 year. In both the experimental and control group LDL and total cholesterol was correlated with changes in coronary atherosclerosis.11
A recent meta-analysis of statin based randomized controlled trials found that lowering LDL cholesterol to less than 100 mg/dl was associated with regression of coronary atherosclerosis in participants with coronary heart disease.12 Similarly, a recent mendelian randomization study of over 100,000 individuals found that genetically-predicted higher LDL cholesterol was associated with greater carotid atherosclerosis, but there was no causal association for HDL cholesterol and triglycerides.13 Consistent with these lines of evidence, it has been consistently demonstrated in experiments on non-human primates that coronary atherosclerosis induced by feeding of dietary cholesterol and saturated fat can be reversed by a cholesterol lowering diet [reviewed previously]. Therefore the preponderance of evidence strongly suggests that the findings from the Lifestyle Heart Trial of a correlation between lower LDL cholesterol and regression of coronary atherosclerosis was causal, and can at least partly be explained by the intervention of a cholesterol lowering vegetarian diet. In the meta-analysis of 5 cohorts it was found that in a sample of participants from 3 of the cohorts that serum cholesterol ranged from between 13 mg/dl to 23 mg/dl lower in the vegetarians compared to non-vegetarians. The researchers suggested that the difference in serum cholesterol could have largely explained the difference in fatal coronary heart disease between these groups.2 In the EPIC-Oxford cohort, serum lipids and blood cholesterol were measured in a sample of the participants. Non-HDL cholesterol was 17 mg/dl lower and systolic blood pressure was 3.3 mmHg lower in the vegetarians compared to the non-vegetarians. The researchers calculated that the differences between these two risk factors alone would expect to lower the risk of coronary heart disease by 24%, which is less than the observed 32% lower risk.1
The researchers from the EPIC-Oxford cohort suggested that the high ratio of polyunsaturated fat to saturated fat largely explained the difference in non-HDL cholesterol between groups, but failed to mention that a number of other plant based nutrients may have also contributed to this difference.1 It has been repeatedly demonstrated in randomized controlled trials that intake of plant protein, particularly from soy, plant sterols, and dietary fiber can also lower LDL cholesterol.141516 In fact in many of the interventions with the greatest diet induced decrease in LDL cholesterol, the decrease could not be explained by changes in dietary fat and cholesterol intake alone, but also likely due to the additive effects of a number of plant based nutrients.171819
It is clear that the LDL cholesterol levels of the vegetarians in these cohort studies far exceeded optimal levels, likely due to a diet deficient in whole plant foods and still relatively rich in animal foods. If these vegetarians had adhered to a much more phytonutrient rich cholesterol lowering diet such as that used in the aggressive dietary experiments, an even significantly lower risk of coronary heart disease may have been observed.Plant Positive recently referred to this informative statement made by Michael Brown and Joseph Goldstein the year before they were awarded the Nobel Prize for their research on the LDL-receptor:20
If the LDL-receptor hypothesis is correct, the human receptor system is designed to function in the presence of an exceedingly low LDL level. The kind of diet necessary to maintain such a level would be markedly different from the customary diet in Western industrial countries (and much more stringent than moderate low-cholesterol diets of the kind recommended by the American Heart Association). It would call for the total elimination of dairy products as well as eggs, and for a severely limited intake of meat and other sources of saturated fat.
Evidence from over one hundred randomized controlled trials has proven beyond plausible doubt that changing from a diet rich in animal foods to a dieter richer in certain whole plant foods significantly lowers LDL cholesterol.41415162122 Similarly, evidence from over one hundred randomized controlled trials has proven beyond plausible doubt that lowering LDL cholesterol decreases the risk of coronary heart disease and all-cause mortality.56 Therefore consistent with the diet-heart hypothesis, there is convincing evidence that an appropriately designed vegetarian diet would reduce the risk of coronary heart disease, and that this reduction can at least be partly explained by lower LDL cholesterol.
Beyond Cholesterol
There are likely a number of dietary related factors that contribute to the lower risk of coronary heart disease observed in people with vegetarian dietary patterns that cannot entirely be explained by lower LDL cholesterol. For example, it has been shown in randomized controlled trials that a number of plant based nutrients can lower blood pressure, which may explain the lower blood pressure observed in vegetarians in a number of observation and intervention studies [reviewed previously]. Furthermore, appropriately designed vegetarian diets likely reduce the risk of being overweight and developing type II diabetes.2324252627 Other factors such as reduced oxidation of LDL and changes in blood clotting have also been suggested as explanations for the lower risk of coronary heart disease observed in vegetarians.2829
Perhaps the main concern with an inappropriately designed vegetarian diet is that it may result in elevated homocysteine due to an inadequate intake of vitamin B12, suggested to be a risk factor for coronary heart disease. Although deficiency of vitamin B12 is rarely observed in some populations in the developed world consuming a predominantly plant based diet, perhaps due to regular contact with vitamin B12 producing bacteria, health authorities strongly recommended that vegetarians diets be supplemented regularly with a bioavailable source of vitamin B12.3031 Jack Norris, RD regularly posts informative reviews on the latest research on vitamin B12 intake and homocysteine, and updates his recommendations for vitamin B12 supplementation in response to new findings.
In all of the cohort studies, and perhaps most intervention studies carried out on vegetarians, there is little doubt that only very few vegetarians were actually consuming a diet predominantly based on whole plant foods, and as expected although these vegetarians experienced a significantly lower risk of coronary heart disease than their omnivorous counterparts, they still experienced a substantial residual risk of coronary heart disease.32 In Dr. Caldwell Esselstyn’s more recent decade long study (pending publication) of around 200 patients that were advised to consume a whole foods, plant-based diet, it was found that recurrent cardiac events only occurred in 0.5% of adherent participants. This is an approximately 40 fold lower risk than achieved in other dietary or statin based trials, strongly suggesting that these results can only partially be explained by the use of LDL cholesterol lowering medication [reviewed previously]. This is an excellent example of how a whole foods, plant-based diet can confer significant benefit over-and-above favorable changes to traditional risk factors.
Caldwell Esselstyn on making heart attacks history
The definition of a vegetarian diet typically only defines which type of animal foods are restricted and not the quantity and quality of plant foods consumed. As all vegetarian diets are not created equal, studies on vegetarians may only provide limited information of the influence a more nutrient dense vegetarian dietary pattern on the risk of coronary heart disease.33 The restriction of certain animal foods however may encourage at least a modest increase of intake of high quality plant matter, including fruits, vegetables, whole grains, legumes and nuts in order to make up for calories and certain nutrients otherwise consumed from animal foods. Nevertheless, even the studies examining less than optimal vegetarian diets may contribute more to the knowledge of optimal dietary patterns than many studies on homogenous populations due to greater differences in intake of specific foods and nutrients. Vegetarian diets should be designed according to not only which animal foods are restrict, but also the quality of plant foods consumed in order to minimize and preferably eliminate the risk of developing coronary heart disease. There is very strong evidence that such a diet would also lower the risk of numerous other chronic and degenerative diseases.
