Health effects of vegetarian and vegan diets

Proceedings of the Nutrition Society (2006), 65, 35–41 Health effects of vegetarian and vegan diets Timothy J. Key*, Paul N. Appleby and Magdalena S. Rosell Cancer Research UK Epidemiology Unit, University of Oxford, Richard Doll Building, Roosevelt Drive, Vegetarian diets do not contain meat, poultry or fish; vegan diets further exclude dairy productsand eggs. Vegetarian and vegan diets can vary widely, but the empirical evidence largelyrelates to the nutritional content and health effects of the average diet of well-educated vege-tarians living in Western countries, together with some information on vegetarians in non-Western countries. In general, vegetarian diets provide relatively large amounts of cereals,pulses, nuts, fruits and vegetables. In terms of nutrients, vegetarian diets are usually rich incarbohydrates, n-6 fatty acids, dietary fibre, carotenoids, folic acid, vitamin C, vitamin E andMg, and relatively low in protein, saturated fat, long-chain n-3 fatty acids, retinol, vitamin B12and Zn; vegans may have particularly low intakes of vitamin B12 and low intakes of Ca. Cross-sectional studies of vegetarians and vegans have shown that on average they have a relativelylow BMI and a low plasma cholesterol concentration; recent studies have also shown higherplasma homocysteine concentrations than in non-vegetarians. Cohort studies of vegetarianshave shown a moderate reduction in mortality from IHD but little difference in other majorcauses of death or all-cause mortality in comparison with health-conscious non-vegetariansfrom the same population. Studies of cancer have not shown clear differences in cancer ratesbetween vegetarians and non-vegetarians. More data are needed, particularly on the healthof vegans and on the possible impacts on health of low intakes of long-chain n-3 fatty acidsand vitamin B12. Overall, the data suggest that the health of Western vegetarians is good andsimilar to that of comparable non-vegetarians.
A large number of individuals around the world follow with a very large increase in East Asia from only 8.7 in vegetarian diets, but in most countries vegetarians com- 1964–6 to 58.5 in 2030 (World Health Organization, prise only a small proportion of the population. India is 2003). Steinfeld (2004) has estimated that world total meat a notable exception because a substantial proportion of production ( · 106 tonnes/year) increased from about 92 the population, perhaps approximately 35 %, follows a in 1967–9 to 218 in 1997–9 and will increase further to traditional vegetarian diet and has done so for many 376 in 2030, a fourfold increase in 60 years.
generations (International Vegetarian Union, 2005; Refsum Understanding of the health effects of vegetarian and et al. 2001). The numbers of vegetarians in Western vegan diets is quite good but many uncertainties remain countries are unknown, with estimates based on rather (Fraser, 1999; Key et al. 1999a; Sanders, 1999a; Willett, small samples; for example, in a survey of 2251 indivi- 2003). The purpose of the present brief overview is to duals throughout the UK (Henderson et al. 2002) 5 % summarize current knowledge on the health effects of reported being vegetarian or vegan. While the number of vegetarian and vegan diets with an emphasis on recent vegetarians may be increasing in some of the most affluent findings and results from large studies, including the work countries, there is an opposite picture for other countries of the authors’ group on the European Prospective Investi- around the world, in that meat consumption is increasing gation of Cancer and Nutrition (EPIC)-Oxford cohort greatly in many countries that until recently had a low (Davey et al. 2003). Most of the discussion is related intake of meat. Per capita meat consumption (kg/year) is to vegetarians in affluent Western countries; the health of predicted to increase from 24.2 in 1964–6 to 45.3 in 2030, vegetarians and individuals with a very low meat intake in Abbreviation: EPIC, European Prospective Investigation of Cancer and Nutrition.
*Corresponding author: Professor Tim Key, fax + 44 1865 289 610, email tim.key@ceu.ox.ac.uk poorer countries is a very important topic and there is some close to or above the recommended intakes, where appli- information available, but proper consideration of this cable (Davey et al. 2003), and these nutrients are not dis- topic is outside the scope of the present brief overview.
cussed further in the present review. For n-3 fatty acids andvitamin B12, however, there is substantial recent researchrelevant to the status of vegetarians in relation to these Dietary characteristics of vegetarian diets nutrients and this aspect will be discussed further, togetherwith Fe status.
Vegetarians are defined as individuals who do not eatany meat, poultry or fish. Vegetarians are sub-classified aslacto-ovo vegetarians who eat dairy products and/or eggs and vegans who do not eat any animal products. Since Plant foods can provide a-linolenic acid but are devoid vegetarian diets are defined by what they do not contain, of the long-chain n-3 fatty acids EPA and DHA (marine the actual composition of vegetarian diets can vary widely.
algae can provide EPA and DHA and are acceptable to For the purpose of the present review the discussion is vegetarians but are not considered here as a plant food); largely based on the observed average diet of vegetarians eggs and to a lesser extent dairy products contain low as described in published reports, and mostly for indi- levels of EPA and DHA that vary according to the feeding viduals living in affluent Western countries.
of the animal. Studies of plasma levels of n-3 fatty acidshave consistently shown that vegetarians have lower levelsof EPA and DHA than meat-eaters, with lower levels in vegans than in lacto-ovo-vegetarians (Sanders et al. 1978a;Sanders, 1999b). Recently, it has been shown that plasma levels of EPA and DHA in vegans are not related to the Reviews by expert groups such as the American Dietetic duration of adherence to the diet over periods of £20 Association and Dietitians of Canada (2003) have con- years, suggesting that the endogenous production of these cluded that a well-planned vegetarian diet is adequate for fatty acids in vegetarians and vegans may result in low all stages of the life cycle including infancy, childhood and but stable plasma concentrations (Rosell et al. 2005c).
adolescence. Comparisons of the food intakes of vege- Studies using labelled a-linolenic acid have shown that tarians and non-vegetarians show that vegetarian diets conversion of this fatty acid to EPA and DHA can occur in generally provide relatively large amounts of cereals, human subjects but that the rate of conversion is low in pulses, nuts, fruits and vegetables. Together with the differ- females and very low in males (Williams & Burdge, 2006).
ences in intakes of animal foods, these differences in food Vegetarian diets are usually rich in linoleic acid, which intake result in several characteristic differences in nutrient may reduce the conversion of a-linolenic acid to EPA intake. Vegetarian diets are usually rich in carbohydrates, and DHA (Davis & Kris-Etherton, 2003), but there is no n-6 fatty acids, dietary fibre, carotenoids, folic acid, vita- direct evidence that plasma levels of EPA and DHA in min C, vitamin E and Mg, and relatively low in protein, vegetarians can be substantially increased by following a saturated fat, long-chain n-3 fatty acids, retinol, vitamin diet low in linoleic acid and high in a-linolenic acid.
B12 and Zn; vegans can have particularly low intakes of It is unknown whether the low levels of EPA and DHA vitamin B12 and low intakes of Ca (e.g. data from EPIC- in the plasma of vegetarians have effects on health. In a small uncontrolled trial in which supplements of EPA and These differences in nutrient intake might have favour- DHA were given to ten vegetarians Mezzano et al. (2000) able or unfavourable effects on the nutritional status and observed an increase in the plasma levels of these fatty health of vegetarians. Current knowledge of nutrition sug- acids and a reduction in platelet aggregation, a possible gests that the relatively high intakes of dietary fibre, folic risk factor for CVD, but more research is needed to explore acid, vitamin C, vitamin E and Mg and low intake of saturated fat might all have benefits. In particular, vege-tarians are more likely than non-vegetarians to reach the UK Department of Health (1991) targets for fruit and vegetables and the dietary reference values for saturated Food plants do not contain vitamin B12; therefore, the only fatty acids of 10 % total energy and NSP of 18 g/d. For reliable sources of vitamin B12 for vegetarians are dairy example, mean saturated fat intakes expressed as percen- products and eggs, fortified foods and dietary supplements tage energy are estimated as 10.7 and 10.4 in male and (Herbert, 1988; Dagnelie et al. 1991). It has been claimed female meat-eaters, 9.4 and 9.3 in male and female vege- that some plant foods such as seaweed and tempeh might tarians and 5.0 and 5.1 in male and female vegans (Davey provide true vitamin B12, but this claim has not been et al. 2003). For NSP, mean intakes (g/d) are 18.7 and 18.9 established and much or all the material in these foods in male and female meat-eaters, 22.7 and 21.8 in male and that is detected by assays for vitamin B12 may be vitamin female vegetarians, and 27.7 and 26.4 in male and female B12 analogues that are either inactive or may antagonize true vitamin B12 (Dagnelie et al. 1991; Dagnelie, 1997).
The impact on health of the relatively high intakes Early studies of vitamin B12 status in vegetarians have of carbohydrates and n-6 fatty acids and relatively low shown that, as would be expected, dietary intake and intakes of protein, retinol and Zn in vegetarians is unclear; plasma concentrations are lower than those in meat-eaters mean intakes of these nutrients in vegetarians are probably (Armstrong et al. 1974; Sanders et al. 1978b). Clinical evidence of vitamin B12 deficiency has been reported in some vegans but is apparently uncommon (Antony, 2003).
Studies of Western vegetarians have consistently reported Recent research using more sensitive indicators of vitamin that vegetarians have a lower BMI than comparable B12 status (plasma methylmalonic acid, homocysteine and holotranscobalamin II) has shown that substantial propor- about 1 kg/m2 (Key et al. 1999b); the proportion of tions of vegans and even of vegetarians have suboptimal vegetarians who are obese is correspondingly lower than vitamin B12 status according to these criteria, both among that among non-vegetarians (Key & Davey, 1996). The affluent Western vegetarians and in other countries reasons for this difference are not well understood, but including India, China and Taiwan (Mann et al. 1999; may include differences in the composition of the diet such Refsum et al. 2001; Hung et al. 2002; Kwok et al. 2002; as a higher fibre intake and a lower protein intake (Spencer Herrmann et al. 2003; Koebnick et al. 2004). Dietary et al. 2003). Follow-up of body weight among 21 966 vitamin B12 deficiency is also now recognized to be a individuals in EPIC-Oxford shows a mean body-weight serious problem in non-vegetarian populations with a low increase of approximately 400 g/year overall, with signifi- intake of meat because of poverty (Stabler & Allen, 2004).
cantly lower weight gain in vegans, but not in vegetarians, Recent work shows that vegetarians must be careful to than in meat-eaters (Rosell et al. 2005b).
ensure that they do consume adequate amounts of vitamin B12 (Herrmann & Geisel, 2002; Antony, 2003; Stabler & BMI between vegetarians and non-vegetarians, obesity is Allen, 2004). The current UK dietary reference values for common among some populations that follow largely vitamin B12 (1.5 mg/d in adults; Department of Health, vegetarian diets, such as Indians living in the UK (Jebb 1991) were derived partly from studies of vegetarians and et al. 2004) and in India (Shetty, 2002).
vegans that have suggested that intakes of vitamin B12 ofapproximately 0.3 mg/d are sufficient to prevent anaemiaand macrocytosis. However, intakes of 0.3 mg/d may be probably associated with moderate elevation in homo- cysteine that might be detrimental to health.
Studies have consistently reported that total plasmacholesterol is lower in vegetarians than in non-vegetarians, e.g. by 0.61 mmol/l in the Health Food ShoppersStudy, 0.43 mmol/l in the Oxford Vegetarian Study and The Fe content of vegetarian diets is typically quite similar 0.39 mmol/l and 0.35 mmol/l in men and women respec- to that of non-vegetarian diets, but the bioavailability of tively in EPIC-Oxford (Key et al. 1999b). The effect of a the Fe is lower because of the absence of haem-Fe. Vegan vegetarian diet on plasma cholesterol is dependent on the diets are usually higher in Fe than lacto-vegetarian diets exact composition of the diet, particularly in relation to because dairy products are low in Fe. For example, in saturated and unsaturated fatty acids, and Jenkins et al.
EPIC-Oxford estimated Fe intakes among 43 582 women (2003) have shown that a vegetarian diet including a are 12.6, 12.8, 12.6 and 14.1 mg/d for meat-eaters, fish- portfolio of cholesterol-lowering foods such as soyabean eaters, lacto-vegetarians and vegans respectively (Davey and nuts reduces serum LDL-cholesterol substantially et al. 2003). Studies of Fe status (for example, see more than a control vegetarian diet.
Waldmann et al. 2004) have consistently shown that serumferritin is lower in vegetarians than in non-vegetarians and that Hb levels are similar or slightly lower in vegetariansthan in non-vegetarians. Low Fe status is not common in The main diet-related determinants of hypertension are men, but is moderately common among premenopausal high salt intake, obesity and excess alcohol consumption women throughout the world, and young female vegetar- (Scientific Advisory Committee on Nutrition, 2003). Some ians need to ensure that their diet includes good sources of early studies have suggested that vegetarians have a lower Fe with vitamin C to help absorption and that they take blood pressure than similar non-vegetarians, with differ- ences of 2–10 mmHg in systolic or diastolic pressure(Beilin et al. 1988). However, analyses of blood pressureamong 11 004 men and women in EPIC-Oxford indicatevery little difference in blood pressure between vegetarians and meat-eaters (£1 mmHg); blood pressure was observedto be 2–3 mmHg lower in vegans than in meat-eaters, A well-planned vegetarian diet is considered to be ade- largely associated with the lower BMI of the vegans quate for all stages of the life cycle including infancy, (Appleby et al. 2002). In this study the very small differ- childhood and adolescence (American Dietetic Association ences in blood pressure between the dietary groups would and Dietitians of Canada, 2003), but epidemiological data not be expected to cause a detectable difference in rates on growth and development in vegetarians are still sparse.
Recent data on 390 lifelong vegetarians in EPIC-Oxford(Rosell et al. 2005a) show no significant differences in height in men or women, or in age at menarche in women,between lifelong vegetarians and those who became Collaborative re-analysis of five prospective studies, each including a large proportion of vegetarians, has shown the mortality from IHD to be 24 (95 % CI 6, 38) % lower in vegetarians than in non-vegetarians (Key et al. 1999b).
Most of the epidemiology of breast cancer can be Results published subsequently are similar; a death rate explained by hormonal factors, and the only definite ratio of 0.75 (95 % CI 0.4, 1.37) in the first analysis of dietary effects on risk are obesity in post-menopausal EPIC-Oxford (Key et al. 2003) and 0.70 (95 % CI 0.41, women and alcohol. Endogenous oestrogen levels are 1.18) in the extended follow-up of the cohort in Germany clearly associated with breast cancer risk in post- (Chang-Claude et al. 2005). In a case–control study among menopausal women (Key et al. 2002), and there is some Indians in Bangalore the risk for myocardial infarction evidence that high levels of insulin-like growth factor-I in vegetarians compared with non-vegetarians has been may also increase risk (Renehan et al. 2004). Although reported to be 0.81 (95 % CI 0.46, 1.43; Pais et al. 1996).
studies of hormone levels in vegetarians have shown that Law et al. (1994) have estimated that a reduction in total plasma oestrogen levels are not different from those of serum cholesterol of 0.6 mmol/l would reduce mortality non-vegetarians (Thomas et al. 1999), they have shown from IHD by 27 %; therefore, the observed differences that vegans have lower plasma levels of insulin-like growth in cholesterol between vegetarians and non-vegetarians of factor-I than either meat-eaters or lacto-vegetarians (Allen approximately 0.4 mmol/l would be expected to reduce et al. 2002). Vegetarians, and especially vegans, often mortality from IHD by approximately 20 %. The observed consume substantial amounts of soyabeans or foods made difference in mortality of about 24 % is therefore of the from soyabeans; soya foods are rich in phyto-oestrogens, magnitude that might be predicted from the difference in which have been hypothesized to reduce breast cancer risk serum cholesterol. The lower BMI of vegetarians would but research on this topic has so far been inconclusive also be expected to cause a small reduction in mortality Studies of breast cancer incidence or mortality have not demonstrated any difference between lacto-vegetariansand non-vegetarians (Mills et al. 1989a; Rao et al. 1994; Key et al. 1999b; Dos Santos Silva et al. 2002).
The main known risk factor for stroke is high bloodpressure. The only data on stroke mortality in vegetarianscomes from the five prospective studies, pooled analysis of which shows a death rate ratio for stroke in vegetarians Hormones are thought to be important determinants of compared with non-vegetarians of 0.93 (95 % CI 0.74, prostate cancer risk, but understanding of these relation- ships is still poor. There is some evidence that high levelsof active androgens and of insulin-like growth factor-I mayincrease prostate cancer risk (Eaton et al. 1999; Renehan et al. 2004). No differences in androgens have been foundbetween vegetarians and non-vegetarians but, as in women, There are few data on cancer rates in vegetarians but vegan men have lower plasma levels of insulin-like growth some information is available, particularly for colo-rectal, factor-I than either meat-eaters or lacto-vegetarians (Allen Studies of prostate cancer incidence or mortality have not demonstrated any difference between lacto-vegetarians and non-vegetarians (Mills et al. 1989b; Key et al. 1999b).
The causes of colo-rectal cancer are not well understoodbut researchers agree that diet is important, and there issubstantial, although not conclusive, evidence that diets high in red and processed meat are associated with amoderate increase in colo-rectal cancer risk (Key et al.
The bone health of vegetarians has been a topic of interest 2004; Norat et al. 2005). As well as the absence of meat for many years but few data are available. Ca intake in from their diet, some putative risk factors for colo-rectal lacto-vegetarians is similar to that in non-vegetarians, cancer are more favourable in vegetarians than in non- whereas vegans usually have a substantially lower Ca vegetarians; for example, vegetarians have a lower intake unless they consume a lot of Ca-rich plant foods proportion of secondary bile acids in their faeces (Reddy such as dark-green vegetables. It has been suggested that et al. 1998) and are less likely to have infrequent bowel the absence of meat might be beneficial for bone health movements (Sanjoaquin et al. 2004a). Studies of colo- because of a reduced ‘acid load’, but whether this factor rectal cancer in vegetarians have suggested that the inci- is important is controversial and overall it is not clear dence may be lower than in non-vegetarians (Fraser, 1999; whether the bone health of vegetarians is better or worse Sanjoaquin et al. 2004b), but the pooled analysis of than that of comparable non-vegetarians (New, 2004).
mortality among vegetarians and non-vegetarians in five Early results from EPIC-Oxford show no difference in cohorts shows no difference between the dietary groups fracture rates between vegetarians and non-vegetarians, but (Key et al. 1999b; some of the cases in this analysis do show the importance of adequate Ca intake in reducing of mortality are the same individuals as in the studies of fracture risk (TJ Key, PN Appleby, EA Spencer, AW incidence of Fraser (1999) and Sanjoaquin et al. (2004b).
Roddam and NE Allen, unpublished results).
prostate, but there are no data on the risk for these cancersin vegans; the only data on cancer risk are for vegetarians, The question of whether vegetarianism is associated with mostly lacto-vegetarians, who do not have reduced levels beneficial or detrimental effects on athletic performance of insulin-like growth factor-I. Vegetarians have low levels has been investigated in some observational studies and of long-chain n-3 fatty acids and often have low levels of a few small trials (Nieman, 1999; Barr & Rideout, 2004).
In general, there is little evidence that athletic performance research on the health effects of these differences is differs much between vegetarians and non-vegetarians, needed. Overall, the health of vegetarians appears to be as long as the diet is nutritionally adequate, but more data good, but as with all dietary patterns care is needed to are needed. Particular care needs to be taken to ensure ensure that the diet is as nutritious and well-balanced as adequate Fe status, and there is some evidence that the possible according to current understanding.
lower muscle creatine concentration in vegetarians mayreduce supramaximal exercise performance (Barr &Rideout, 2004).
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