Abstract:
Vegetarian diets that exclude meat, fish and poultry and/or egg and dairy products, are based on grains, fruits, vegetables, legumes and seeds. Vegetarian diets are often varied in composition, involving a wide range of dietary practices and individual dietary restrictions. Vegetarian dietary patterns have been reported to be associated with several favorable health outcomes in epidemiological studies. There is good evidence for the protective effects of a vegetarian diet on lipid profile, blood pressure, fasting blood sugar, blood insulin and C-reactive protein (CRP). Vegetarian diets typically contain large amounts of antioxidant micronutrients (such as vitamins C and E, phytochemicals and fiber) which may improve inflammatory processes and decrease circulatory levels of inflammatory biomarkers, thereby reduce the risk of chronic diseases. Few comprehensive reviews have addressed the effect of a vegetarian diet on preventing diet-related diseases and its nutrients adequacy for all life stages. Therefore, this review aimed to explore the impact of a vegetarian diet on health outcomes. Additionally, the adequacy of the nutrients of these vegetarian diets (energy, protein, ω-3 fatty acids, iron, zinc, calcium, vitamin D and vitamin B12) in different stages of the life-cycle was also discussed.
INTRODUCTION
DEFINITIONS AND TYPES OF VEGETARIAN DIETS
There are numerous variations of a plant-based diet; vegetarian diets are completely devoid of red or white meat1. Some vegetarian diets are restricted to plant products (plant-based) only such as a vegan diet that omits all animal products from the diet; fruitarian that includes processed or cooked foods but in minimum quantity and raw vegan which includes vegetables, fruit, nuts, seeds, legumes and sprouted grains1. Other vegetarian diets include eggs and/or dairy products or both are classified as ovo vegetarian who does not eat meat or dairy products but eats eggs2, lacto-vegetarian who does not eat eggs but eats dairy products2, while lacto-ovo vegetarian diet excludes all meat but includes eggs and dairy products. Lacto-ovo-vegetarian diet includes dairy and egg products, it is a less restrictive diet with more food choices than a vegan diet and more calorie-dense, so it is considered as the best diet for optimal child growth3.
Macrobiotic diet excludes all meat, poultry, dairy products and eggs but at initial levels may include fish1. Pescetarian diet excludes red meat and poultry but includes fish (although factory-farmed fish are usually avoided)1. “Flexitarian” or “Semi-vegetarian” is a newly introduced term for those who mostly eat a vegetarian diet but occasionally eat meat; they have given up red meat due to health problems and only eat free-range or organic animals and animal products1.
REASONS FOR FOLLOWING VEGETARIAN DIETS
A vegetarian diet may be adopted for various reasons such as distaste of eating flesh4, food beliefs and peer and/or family influences5. Some vegetarians avoid meat to derive certain health benefits or to lose weight6,7, while some vegetarians do not eat meat for ethical reasons, they believe that it is morally wrong to kill animals for food8. Environmental and ecological impacts are other reasons for avoiding meat and animal products9 and some people are allergic to both dairy products and lactose10.
Abstinence from the consumption of meat and animal products is one of some religious practices including Buddhism and Seventh Day Adventism11. In many cultures, diet is perceived as essential to good health and longevity, while poor diet is associated with lower levels of health and even specific diseases4. People who followed a vegetarian diet and healthy lifestyle claim that a plant-based diet is a cheap, healthy and safe approach for the prevention and possible management of modern lifestyle diseases12.
PREVALENCE OF VEGETARIANISM
Vegetarianism and veganism are increasingly acquiring popularity in the western world13. The prevalence of vegetarianism varies widely around the world14. India has the highest proportion of vegetarians as compared to other countries with about 30% of the population adopting a vegetarian diet14. About 4.3 to 10% of the population in Germany is estimated to be vegetarians, whereas the number of vegans is estimated at 1.6%13. Switzerland, Italy, Austria and the United Kingdom show a similar number of vegetarians as Germany at 9-11%13. About 3% of American adults are vegetarians or vegans according to a nationwide poll15.
HEALTH IMPLICATIONS OF VEGETARIAN DIETS
In the last 50 years, the health effects of vegetarian diets have been studied with a more scientific view16. Early studies often focused on examining vegetarians for possible nutrients deficiencies and the focus has been expanded to evaluate possible health benefits of these long-standing real-world dietary patterns16.
Obesity and overweight: In observational studies, people who follow a plant-based diet show lower body weight compared to persons following other dietary patterns17, suggesting that a plant-based diet may be useful for preventing or treating weight problems17. A healthy body weight is associated with improved cardiovascular function and insulin sensitivity18, as well as reducing the risk of other chronic diseases2. Plant-based dietary patterns were found to be associated with lower BMI2. In the Adventist Health Study-2, average BMI was highest (28.8 kg m–2) in non-vegetarians and lowest in those who avoided all animal products (23.6 kg m–2)19. Research indicates that the therapeutic use of a vegetarian diet is effective for treating overweight and may perform better than an alternative non-vegetarian diet for the same purpose2.
Non-communicable diet-related diseases: In developed and some developing countries such as middle-eastern countries, the epidemiologic transition is characterized by an increase in non-communicable diseases (NCD), such as cardiovascular diseases (CVD), diabetes mellitus and obesity. Vegetarians consume smaller amounts of total fat and saturated fat and larger amounts of unsaturated fats and fiber than non-vegetarians10. There is convincing evidence that vegetarians have lower rates of coronary heart disease (largely explained by low LDL cholesterol), hypertension and diabetes mellitus and lower prevalence of obesity20. Additionally, cancer rates among vegetarians appear to be moderately lower than others living in the same communities and life expectancy appears to be greater20.
The consumption of a vegetarian diet is believed to decrease the risk of CVD20. In the Adventist Health Study-2 of 73,308 Seventh-day Adventists, researchers found that vegetarians had a 13 and 19% decreased risk for developing CVD and ischemic heart Disease16. A case-control study conducted in Jordan showed consumption of some fruit and vegetable could be considered as a protective factor against developing CVD21. Additionally, a vegetarian diet improves several modifiable heart disease risk factors, including abdominal obesity22, blood pressure23, serum lipid profile24 and blood glucose25. A case-control study has been performed by Tayyem et al.26 to detect the association between dietary patterns and metabolic syndrome. The authors reported a protective effect of the Mediterranean diet (which is loaded with fruits, vegetables and legumes) against the development of metabolic syndrome. Vegetarian diet also decreases markers of inflammation such as C-reactive protein, reduces oxidative stress and protects against atherosclerotic plaque formation27. Consequently, vegetarians have reduced the risk of developing and dying from ischemic heart disease16,28.
Epidemiologic studies have consistently shown that a regular consumption of fruit, vegetables, legumes, or whole grains is associated with a reduced risk of certain cancers2,29,30. A vast array of phytochemicals, such as sulforaphane, ferulic acid, genistein, indole-3-carbinol, curcumin, epigallocatechin- 3-gallate, diallyl disulfide, resveratrol, lycopene and quercetin found in vegetables, legumes, fruits, spices and whole grains may protect against cancer31. These phytochemicals are known to interfere with several cellular processes involved in the progression of cancer32.
Vegetarian diet is associated with several factors that promote bone health, including high intakes of vegetables and fruits; an abundant supply of magnesium, potassium, vitamin K, vitamin C and a relatively low acid load33. Conversely, they can compromise bone health when their component is low in calcium, vitamin D, vitamin B12 and protein33. EPIC-Oxford reported a 30% increase in fractured risk of vegans as a group but no increase in fracture risk in lacto-ovo-vegetarians compared to non-vegetarians33. Inadequate intakes of vitamins D and B12 have been linked to low bone mineral density, increased fracture risk and developing osteoporosis33. To achieve and maintain excellent bone health, vegetarians and vegans are well-advised to meet the RDA of all nutrients, particularly calcium, vitamin D, vitamin B12 and protein and to consume generous servings of vegetables and fruits33.
Fasting blood glucose and vegetarian diet: Vegetarian diets have been studied over the past few decades for their preventative and therapeutic effects on diabetes that might be more beneficial than medication for diabetes management34. Additionally, interventional studies have shown that following a vegetarian diet is an effective method in glycemic control and that this diet control plasma glucose to a greater level than do control diet, including diets traditionally recommended for patients with diabetes (e.g., diets based on carbohydrate counting)35. Studies indicate that a vegetarian diet can be universally used in type 2 diabetes prevention and as a way to improve blood glucose management35.
Lipid profile and vegetarian diet: Plasma total cholesterol is lower in vegetarians as compared to non-vegetarians, primarily due to a reduction in LDL cholesterol, with little difference in HDL cholesterol36. This difference in plasma cholesterol is likely to be largely due to differences in animal fat intake since meat is a rich source of saturated fatty acid whereas some plant foods such as vegetable oils, nuts and seeds are rich sources of polyunsaturated fatty acid37.
Serum vitamin B12 and vegetarian diet: Individuals who follow a vegetarian diet are at risk of developing vitamin B12 deficiency due to suboptimal intake of this vital vitamin38. Vitamin B12 is essential for the synthesis of nucleic acids, erythrocytes and in the maintenance of myelin38. De ciency may result in a variety of symptoms some of them may be severe while others may be irreversible38. Reduced consumption of cobalamin from food or impaired intestinal absorption leads to severe deficiency when tissue stores of the vitamin are depleted39.
Early symptoms of a severe B12 deficiency are unusual fatigue, tingling in the fingers or toes, poor cognition, poor digestion and failure to thrive in small children38. Additionally, subclinical B12 deficiency may result in elevated homocysteine. If folic acid intake is high, hematological symptoms of vitamin B12 deficiency may be masked and go undetected until neurological symptoms are manifested40. Laboratory tests, that are used if there are concerns about vitamin B12 status, include serum methylmalonic acid, serum or plasma B12 and serum holo-transcobalamin (Holo-TC or Holo-TCII)41.
Inflammatory biomarkers and vegetarian diet: The vegetarian diet contains different anti-inflammatory components. Lower serum concentrations of inflammatory biomarkers among vegetarians compared to non-vegetarians have been reported by Haghighatdoost et al.42. The authors declared that a vegetarian diet substantially can alter fecal ora which may play an important role in the inflammatory response42.
Fruits and vegetables are known as dietary sources of salicylic acid which is considered an active ingredient of anti-inflammatory medications42. Further, fruits and vegetables may modulate gut microbiota via dietary fiber42. The ratio of the anti-inflammatory bacterium, Faecalibacterium prausnitzii, is higher in vegetarian diets43. The cytokines and C-reactive protein are biomarkers with pro-inflammatory or anti-inflammatory properties, or both44. Inflammatory biomarkers are influenced by genetic, environmental and/or lifestyle factors, among which diet is thought to be particularly influential44.
A vegetarian diet generally contains higher amounts of foods that are thought to be anti-inflammatory such as those of plant origin and somewhat lower amounts of inflammation-related foods such as fried foods, white bread and meats which are abundant in Western diets44. The relationship between C-reactive protein (CRP) and vegetarian diet depends on the particular population and study design45. Most of the available evidence regarding vegetarianism and chronic inflammation comes from observational studies and their results are conflicting42. While Haghighatdoost et al.42 reported lower levels of inflammation in vegetarians, Lee et al.46 did not find any significant difference between groups and reported greater levels of inflammatory markers (e.g. IL-6 and hs-CRP) in vegetarians.
NUTRIENTS CONSIDERATIONS FOR VEGETARIANS
In the Dietary Guidelines for Americans (2015-2020), vegetarian diets are recommended as one of three healthful dietary patterns and meal plans are provided for those who follow lacto-ovo-vegetarian and vegan diets47. The nutrients of concern in the diet of vegetarians include vitamin B12, vitamin D, ω-3 fatty acids, calcium, iron and zinc; although a vegetarian diet can meet current recommendations for all of these nutrients, the use of supplements and fortified foods provide a useful shield against nutrientdeficiency3.
Energy intake: Previously various studies have indicated differences in nutrients intake in vegetarians and vegans as compared to non-vegetarians48,49. Nevertheless, total energy intake does not seem to differ significantly but the contribution of proteins (total energy intake) was lower in the non-meat-eating diet groups48. Total fat intake, expressed as a percentage of total energy, was lowest in vegans and highest in non-vegetarians48.
Protein intake: A variety of plant foods supplies protein and essential amino acids and meet the energy and nutrients need2.The consistent and regular use of legumes and soy products could ensure an adequate protein intake for the vegetarian, as well as providing other essential nutrients2,49. Protein needs at all ages, including those for athletes, can be well achieved by balanced vegetarian diets2.
ω-3 fatty acids intake: Craig and Mangels10 reported that n-6 fatty acids are high in vegetarian diets. However, ω-3 fatty acids are low in vegetarian diets. Diets that do not include fish, eggs, or generous amounts of algae are generally low in eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), fatty acids are important for cardiovascular health as well as eye and brain development10. Intake of linolenic acid (ALA) is similar in vegetarians and non-vegetarians, dietary intakes of the long-chain ω-3 fatty acids, EPA and DHA are lower in vegetarians and typically absent in vegans compared with non-vegetarians50. Additionally, blood and tissue had lower levels of EPA and DHA15. The clinical relation of reduced EPA and DHA status among vegetarians and vegans is unknown50.
Iron intake: Iron intake among vegetarians is often slightly higher than those of the non-vegetarians2. Despite having similar iron intakes, the iron stores among vegetarians are typically lower those of non-vegetarians2. Non-heme iron absorption depends on physiological needs and is regulated in part by iron stores. Its absorption varies greatly, depending on both the meal composition and the iron status of the individual. Bioavailability of non-heme iron is impacted by the ratio of inhibitors, such as phytates and polyphenolics and enhancers, such as vitamin C, citric acid and other organic acids2. Although vegetarian adults have lower iron stores than non-vegetarians, their serum ferritin levels are usually within the normal range2.
Zinc intake: Because phytate binds zinc and animal protein enhance zinc absorption, total zinc bioavailability appears to be lower in vegetarian diets2. Compared with non-vegetarian control groups, Foster et al.51 showed that adult vegetarians have similar or somewhat lower dietary zinc intakes and serum zinc concentrations that were lower but within the normal range. Food preparation techniques, such as soaking and sprouting beans, grains, nuts and seeds, as well as leavening bread, can reduce the binding of zinc by phytic acid and increase zinc bioavailability52. Acids, such as citric acid, also can enhance zinc absorption to some extent52.
Calcium intake: Calcium intake for lacto-ovo vegetarians typically meet or exceed recommended value while calcium intakes of vegans vary widely and sometimes fall below the recommendations2. Bioavailability of calcium from plant foods, which is related to the oxalate content of foods and a lesser degree, phytate and fiber, is an important consideration53. Oxalates present in some foods can greatly reduce calcium absorption, so vegetables such as spinach, beet greens and Swiss chard that are very high in these compounds, are not good sources of usable calcium despite their high calcium content. Phytate may also inhibit calcium absorption. However, some foods with high contents of both phytate and oxalate, such as soy foods, still provide well-absorbed calcium54.
Vitamin D intake: Vitamin D not only maintain the bone health but also plays an important role in immune function, the reduction of inflammation and reducing the risk of chronic diseases40. Many genes encoding proteins that regulate cell proliferation, differentiation and apoptosis are modulated in part by vitamin D55. Adequate vitamin D intake is essential since all tissues in the body have a vitamin D receptor and respond to its active form, (1,25-dihydroxyvitamin D3)55. Vitamin D status depends on sunlight exposure and intake of vitamin D fortified foods or supplements55. The production of vitamin Dis dependent on several factors such as the time of day, season, latitude, air pollution, skin pigmentation, sunscreen use, amount of clothing covering the skin and age33,55.
Low intake of vitamin D and plasma or serum 25-hydroxy vitamin D levels has been reported in some vegan vegetarians, especially when the blood was collected in the winter or spring and especially in those living at high latitudes33. Dietary and supplemental sources of vitamin D are commonly needed to meet the nutrient requirements2. Cow’s milk, some non-dairy milks, fruit juices, breakfast cereals and margarines are fortified with vitamin D. Eggs also provide some vitamin D33. Both vitamin D2 and vitamin D3 are used in supplements and to fortify foods. Vitamin D3 (cholecalciferol) may be of plant or animal origin, while vitamin D2 (ergocalciferol) is produced from the ultraviolet irradiation of ergosterol from yeast33. At low doses, vitamin D2 and vitamin D3 appear to be equally effective but at higher doses, vitamin D2 appears to be less effective than vitamin D333. If sun exposure and intake of fortified foods are insufficient, vitamin D supplements are recommended, especially for older adults33,55.
Vitamin B12 intake: Vitamin B12 is found naturally in meat and animal products38. It contains a corrin ring with mineral cobalt38. Physiologic functions of vitamin B12 include erythropoiesis, the synthesis and maintenance of the myelin sheath and the synthesis of nucleic acid (DNA)38. Lacto-ovo-vegetarians can obtain adequate amount of vitamin B12 from1 dairy foods, eggs, fortified foods and supplements if regularly consumed10. The vegans should eat foods high in vitamin B12, such as fortified soy and rice beverages, some breakfast cereals and meat analogs, or Red Star Vegetarian Support Formula nutritional yeast; otherwise, a daily vitamin B12 supplement is needed10. Unfortified plant food doesn’t contain significant amount of vitamin B1210. Fermented soy products cannot be considered as a reliable source of active B1210.
B12 are absorbed via an active process that requires an intrinsic factor. Because the intrinsic factor becomes saturated at about half the RDA, B12 absorption requires 4-6 h2. Hence, One of the best ways to get enough vitamin B12 is to eat fortified foods at least twice a day2. A second absorption mechanism is a passive diffusion at a rate of 1%, allowing less frequent consumption of large supplemental doses2.
Recommendations based on large doses have been made (eg, 500 to 1,000 mg cyanocobalamin several times per week)2. There are four forms of B12 (Adenosylcobalamin, Cyanocobalamin, Hydroxocobalamin and Methylcobalamin). Cyanocobalamin is the form of B12 that is the most commonly used in fortified foods and supplements because of its stability. Methylcobalamin and adenosylcobalamin are forms used in the body’s enzymatic reactions; these are available in the form of supplements which are no more effective than cyanocobalamin and may require higher doses than the RDA. Hydroxocobalamin is used effectively in injections form56. Many individuals who adhere to vegetarian diets and do not use vitamin B12 supplements can develop vitamin B12 deficiency; regardless of the type of vegetarian diet, they consume57.
VEGETARIAN DIETS THROUGHOUT LIFE CYCLE
Health professionals do not have complete and exhaustive knowledge about vegetarian diets and lack information on health outcomes and the adoption of a vegetarian diet throughout the different life cycles and nutrients58. Nutritional deficiencies may cause serious and irreversible health issues which creates difference of opinion about the appropriateness of vegetarian diets during all phases of an individual’s life59.
The American Dietetic Association and the Academy of Nutrition and Dietetics stated that well-planned vegetarian diets are nutritionally sufficient and meet the nutrients requirements and promote normal growth in all stages of the life cycle, including pregnancy and lactation, infancy, childhood, adolescence and older adulthood60. In contrast, the German Nutrition Society and the European Society for Pediatric Gastroenterology Hepatology and Nutrition advised that such dietary patterns could be catastrophic for child growth61,62.
Pregnancy and lactation: Pregnancy is a delicate time in a woman’s life. Appropriate maternal energy intake is important to prevent poor pregnancy outcomes and for physiological growth of the fetus. In recent years, this factor has been tied to birth weight, which is an indicator of the infant health status and predicts future health of infants63.
During pregnancy, the woman should take all the required macronutrients and micronutrients to meet her energy needs and for fetal health59. Therefore, if the pregnant woman wants to adopt a plant-based diet, she must be aware of the possible risks of nutrientsdeficiencies59. There is increased risk of nutrients deficiency, such as iron, zinc, vitamin D, vitamin B12, iodine, proteins and ω-3 fatty acids, if the pregnant mother consumes only vegetarian diet58. The vegetarian diet is not appropriately planned and balanced. This issue has been underlined by several scientific societies, particularly with regard to the promotion of children's neuropsychomotor development59.
Vitamin B12 deficiency can lead to anemia and neurological disorders. Vitamin B12 deficiency have been reported in infants of vegan mothers who strictly adopt vegetarian diet and/or with limited access to foods of animal origin59. A previous study showed that where food access is adequate, pregnancy outcomes of vegetarian mothers, such as birth weight and pregnancy duration, were similar to those in non-vegetarian pregnant mothers64. Melina et al.2 reported that the use of a vegetarian diet in the first trimester resulted in a lower risk of excessive gestational weight gain. A maternal diet high in plant-derived foods may decrease the risk of pregnancy complications, such as gestational diabetes65. The American Dietetic Association60 stated that appropriately planned vegan, lacto-vegetarian and lacto-ovo-vegetarian diets may result in positive maternal and infant health outcomes. However, in practice, balancing of diet without necessary experience or nutritional knowledge is very difficult. The main difference in the composition of vegetarian mothers' milk compared to non-vegetarians' is the lower content of docosahexaenoic acid and higher content of Linoleic and α-Linolenic acid66.
Infancy and childhood: The European Society for Paediatric Gastroenterology Hepatology and Nutrition (ESPGHAN) recommends a careful evaluation of potential B12 deficiency. The lack of adequate nutritional intake or supplement of B12 is found to be associated with severe neurological consequences62. Many vegetarians are young parents who decide to share their dietary patterns with their children58. People are not adequately educated and they do not know the negative effects of inappropriate diets and thus they follow a diet because of fashion or ethical issues related to animal welfare58.
Health professionals who look after pregnant women, newborns and children should provide the proper nutritional education to their patients to avoid nutritional imbalances67. A previous study reported that vitamin B12 deficient mothers gave birth to an infant with neurological defect68. Vitamin B12 deficiency has also been linked to long-term neurological disturbances such as an increased risk of adulthood depression in babies born to vegan or vegetarian mothers69. These outcomes show the significant nexus between maternal nutrition during pregnancy and fetal programming69. Exclusive breastfeeding is recommended for the first 6 months70. If breastfeeding is not possible, commercial infant formula milk should be used as the primary beverage for the first year2. Complementary foods should be rich in energy, protein, iron and zinc and may include hummus, tofu, well-cooked legumes and mashed avocado2. Full-fat, fortified soy milk or dairy milk can be started as early as one year of age for toddlers who are growing normally and eating a variety of foods71.
Average protein intake of children who consume vegetarian diet generally may meet or exceed its recommended level2. Need of protein for vegan children may be slightly higher than those of non-vegan children because of differences in protein digestibility and amino acid composition2.
Elderly: The nutritional profiles of older adults consuming vegetarian diets is reviewed and specific recommendations are made for their diets72. Generally, the results of following vegetarian diet in older adults go in track of those in younger vegetarians. Though, following the vegetarian diet presents many favorable nutritional characteristics, concerns regarding the potential weaknesses in certain vegetarian diets still remain, especially vitamin B12, calcium, protein and zinc72. Caloric needs generally decrease while some nutrients need increase with age; thus, all older people must choose nutrient-dense diets72.
Protein is used less efficiently in older adults and need to increase its intake to maintain muscle mass and strength and bone health72. Older adult vegetarians and vegans need to include protein-rich foods such as legumes and soy foods in their diets. Meat analogs contained a good supply of protein2. Older people synthesize vitamin D less efficiently and are recommended to consume its supplements. Older adults can meet their nutritional requirements more easily from fortified foods such as fortified plant-milks and cereals2. Also, the requirement for vitamin B-6 increases with aging and may be higher than the current RDAs for older people2. Atrophic gastritis is common among older adults and can result in decreased absorption of vitamin B12 from animal products. Therefore, older people require vitamin B12 supplements2.
CONCLUSION
Vegetarian diets are usually low in fat, particularly saturated fat and high in fiber. They are also likely to include more legumes, whole grains, nuts and fruits and vegetables and lack of most types of meat, which may provide many benefits for the prevention and treatment of obesity and chronic health problems, including diabetes and cardiovascular disease. Although a well-planned vegetarian diet can meet all the nutritional needs of an individual. Additionally, the vegetarian diet and plant-based eating pattern exert a beneficial effect on lipid profile, blood glucose and other biochemical parameters.
SUGGESTIONS FOR FUTURE RESEARCH
A cohort study is warranted to investigate the effect of a vegetarian diet on health in the long-term among the developing countries. Cultural and socioeconomic differences among vegetarian populations should be studied to assess nutrients adequacy and their effects in reducing the risk of developing chronic diseases related to diet.