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The Vegetarian Athlete
Chapter 33 The Vegetarian Athlete JACQUELINE R. BERNING Introduction All athletes at some time in their career look at alternative ways of eating to reach their athletic potential. While some athletes take pills, powders or potions in the belief that these will enhance their performance, others have changed their eating styles to a vegetarian diet to gain advantages in training and performance. Unfortunately, after many years of research, the effects of elimination of animal products from the diet on athletic performance are still unclear. Some data do exist on elite athletes who consume a vegetarian diet, but studies that include Olympic-calibre athletes are limited. In addition, most of the research on vegetarianism in the past decade has been focused on the health aspects of a vegetarian diet, rather than on human performance issues. There is certainly a lack of information regarding vegetarianism and its relationship to athletic performance. However, an athlete who consumes a poorly planned vegetarian diet may be at risk of multiple nutritional deficiencies as well as poor physical performance. Early meat eaters It well known that ancient Greek athletes consumed large amounts of meats and many of them believed that their performances were dependent upon animal protein. As an example, Milo of Croton, the legendary Greek wrestler, consumed huge amounts of animal protein and trained by carrying animals across his shoulders. 442 As the animals grew, so did his strength. While Milo’s diet would be viewed today as containing excessive amounts of protein, he was never brought to his knees in the course of the five Olympiads in which he competed (Ryan 1981; Whorton 1982). This concept of the need for large amounts of animal protein was promoted in the early 1800s by Liebig, the pre-eminent physiological chemist of the time (Whorton 1982). He believed that protein was the main substrate for the exercising muscle. While Liebig’s hypothesis was disproved by Atwater in the mid-1800s, his philosophy of consuming large amounts of protein continues to have influence even into the modern day. Today, many athletes still believe that, by consuming large amounts of protein, they will become stronger and gain lean body mass (Berning et al. 1991). Early vegetarians While many ancient Greeks were consuming large amounts of animal protein for athletic prowess, the founder of the philosophical vegetarian movement was also Greek. Pythagoras, the Greek mathematician, is the father of vegetarianism, and until the middle of the 19th century, vegetarians referred to themselves as ‘Pythagoreans’ (Dombrowski 1984). Many of the vegetarians in the mid- to late 1800s were determined to prove that their diet was superior to that of meat eaters. As a result, the London Vegetarian Society formed an athletic and cycling club in the late 1800s to compete the vegetarian athlete against their carnivorous counterparts and in most cases outperformed them in athletic competition (Nieman 1988). Due to their success, many other vegetarian athletes joined the movement. One such competition was the 1893 race from Berlin to Vienna, a 599-km course in which the first two competitors to finish were vegetarian (Whorton 1982). Over the next 10–20 years many other vegetarian athletes performed well in endurance performances around Europe. Because of the success of vegetarian athletes, a few researchers in the early part of the 20th century were interested in measuring their physical capabilities, and Fischer (1907) conducted experiments on Yale student athletes. The subjects were exposed to a wide variety of foods including meat and meatless choices and performed a variety of endurance tests. Those athletes who gravitated toward the meatless diet were classified as vegetarians and were compared with athletes who ate meat. Each subject was tested to determine the maximum length of time that they could hold their arms out horizontally and the number of maximum deep knee bends and leg raises they could perform. Fischer noted that the vegetarians scored better than their meat-eating counterparts. Wishart (1934) reported on a 48-year-old Olympic cyclist who had been a vegetarian for 23 years. The subject was submitted to four different meatless meals with different levels of protein during the 4-week experimental period. The exercise protocol involved riding a cycle ergometer for 8.5 h on four occasions after stabilizing on a different level of dietary protein. During the ride, measurements were made of external work and total energy expenditure. Higher speeds were recorded on the cycle ergometer after consuming the diets with a higher protein content, especially after 4 h of riding. The improved performance was attributed to an increased supply of energy coming from the meatless protein foods. While the energy content of each of the four different meatless meals varied by about 840 kJ (200 kcal), the amount of carbohydrate was not calculated and the increase in protein content for each of the 443 four experimental diets came from dairy products which contain a significant amount of carbohydrates. Modern-day vegetarian athletes The recent literature contains few publications dealing with vegetarianism and athletic performance. However, Cotes et al. (1970) studied the effect of a vegan diet on physiological responses to submaximal exercise in 14 females who had consumed a vegetarian diet for an average of more than 11 years. They compared the vegetarians with two different controls, one that included 66 females of comparable social background and a second group of 20 office cleaners who had a comparable level of activity to that of the vegetarians. All subjects performed a submaximal test on a cycle ergometer in which they cycled for 3 min at 30 and 60 W. Ventilation and cardiac frequency were obtained as well as width of the muscles in the thigh. Their results showed that the sedentary controls had a significantly higher cardiac frequency while having a significantly lower grade of activity (P > 0.02). No statistical differences exist between the groups for thigh circumference or anterior skinfold thickness. The authors concluded that the data do not support the hypothesis that a low dietary intake of animal protein impairs the physiological response to submaximal exercise. Few data exist on the relationship between athleticism and vegetarian diets even today, in spite of the popular belief that a vegetarian diet may be beneficial to some athletes. However, anecdotal reports abound. The Tarahumara, a Ute-Aztecan tribe inhabiting the Sierra Madre Occidental Mountains in the north central state of Chihuahua, Mexico, have been reported to be capable of extraordinary physical fitness and endurance as long-distance runners (Balke & Snow 1965), while consuming a vegetarian diet. Their diet contains very little food from animal sources and they have reportedly run distances up to 320 km in ‘kickball’ races which often last several days (Balka & Snow 1965). Cerqueira and associates (1979) investigated the Tarahumaras’ 444 special considerations food intake and nutrient composition and reported that most of their daily energy and nutrients come from corn, beans and squash. About 94% of their daily protein intake is from vegetable sources and only 6% from animal sources. Since most of the fat in their diet (9–12%) was derived from corn, beans and squash, their diets are rich in linoleic acid and plant sterols. The Tarahumara diet is extremely low in cholesterol (71 mg · day–1) since their primary source of cholesterol is eggs, of which they consume about two or three per week. Other sources of fat and cholesterol in the Tarahumara diet come from small, infrequent servings of meat, fish, poultry and dairy products and lard. Even though the diet of the Tarahumara Indians is a simple one consisting mainly of plant foods, it is of high nutritional quality and is nutritionally sound, resulting in little chronic deficiencies and no widespread undernutrition (Cerqueira et al. 1979). Hanne et al. (1986) investigated various fitness parameters of vegetarian athletes and compared them with non-vegetarians. Forty-nine athletes (29 men and 20 women) who had been either lacto-ovo- or lactovegetarian for at least 2 years were compared with 49 controls (29 men and 20 women). Subject ages ranged from 17 to 60 years of age, with the majority of the subjects in the age range of 17–35 years. Fitness parameters included anthropometric measurements, pulmonary function, aerobic and anaerobic capacity and blood chemistries. The authors found no significant differences in body mass between the two groups, although the female vegetarians had a significantly (P > 0.01) high percentage body fat than their non-vegetarian counterparts. No differences were found in pulmonary function, heart rate, blood pressure or in the electrocardiogram. No differences were found between the two groups of subjects in aerobic capacity or anaerobic capacity as determined from a submaximal test and a Wingate test, respectively. Results from the blood examination found that non-vegetarian controls had lower uric acid levels than the vegetarian males, but the nonvegetarian group were within the normal range. Vegetarian women had lower haematocrit values than controls, but haemoglobin, total protein, and glucose were similar in both groups. While no differences were found between the two groups, it is always difficult to find significant differences, because vegetarianism does not embrace a single, well-defined diet, and the influence of other lifestyle factors, including habitual physical activity levels, may obscure possible effects of the diet itself. Herein may lie part of the problem, as past research on vegetarianism and athletic performance did not clearly define the type of diet being followed by groups of individuals studied. Many athletes may call themselves vegetarian when in fact they simply eliminate from their diet a food group or a certain class of foods. Information on the diet of vegetarian athletes would be helpful in defining limiting or beneficial factors. Classifications of vegetarian diets Vegetarian diets range from the vegan diet, which excludes all animal proteins, to the semivegetarian diet, which may include some animal proteins (Table 33.1). Whatever the term an individual uses, it appears that vegetarianism is a continuum of eating styles, which range from the sole consumption of plant foods to a diet restricting certain kinds of animal proteins or limiting the frequency of animal protein consumption (Ratzin 1995). Because of the variety of vegetarian eating styles among practitioners, it is difficult to define the variables that will influence human performance, but relationships have been found between vegetarianism and a reduction in specific health risks. Health implications of vegetarian diets There is increasing tendency among researchers to conclude that the reduced disease risk observed among vegetarians is not explained so much by the absence of meat from the diet, but by the fact that they eat more plant foods. Results the vegetarian athlete 445 Table 33.1 Classifications of various types of vegetarian diets. From Rudd (1989), with permission. Diet Description Semivegetarian Some but not all groups of animal-derived products, such as meat, poultry, fish, seafood, eggs, milk and milk products may be included in this diet New vegetarian Plant-food diet supplemented with some groups of animal products, but emphasis is placed on foods that are ‘organic, natural and unprocessed or unrefined’ Pescovegetarian Excludes red meats, but consumes fish as well as plant foods Lacto-ovovegetarian Milk and milk products and eggs included in this diet, but meat, poultry, fish, seafood and eggs excluded Ovovegetarians Eggs are included in this diet, but milk and milk products, meat, poultry, fish and seafood are excluded Strict vegetarian/vegan All animal-derived foods, including meat, poultry, fish, seafood, eggs, milk and milk products are excluded from this diet Macrobiotic Avoids all animal foods. Uses only unprocessed, unrefined, natural and organic foods. In some types there is fluid restriction. Tamari, miso and various seaweeds are used Fruitarian This diet consists of raw or dried fruits, nuts, seeds, honey and vegetable oil of epidemiological research are traditionally expressed in terms of relative risk, a difficult concept for the athletic and consumer population to grasp. In a recent re-examination of data from the Adventist Health Study (Fraser et al. 1995), novel statistical calculations show how certain effects may delay or advance the first expression of disease. The Adventist Health Study is a cohort investigation of approximately 34 000 Californian, non-Hispanic, white subjects living in Seventh Day Adventist households who were followed for 6 years. Some of the findings from this study are as follows. 1 Non-vegetarians develop coronary disease 1.77 years earlier than vegetarians. 2 Among males, non-vegetarians have a remaining lifetime risk of developing coronary disease that is 11.9% higher (P < 0.05) than that of vegetarians. 3 Non-vegetarian females have a remaining lifetime risk of developing coronary disease that is 0.26 percentage points lower than that of female vegetarians. 4 Those who rarely consume nuts develop coronary disease 2.6 years earlier and have a remaining lifetime risk 11.9 percentage points greater (P < 0.05) than persons who eat nuts at least five times per week. While Seventh Day Adventists show a reduced risk of several chronic diseases, many of them also abstain from smoking and alcohol, and they are more physically active than non-vegetarians, which also affects the prevalence of chronic diseases. To date, no one has followed a vegetarian athletic population to see if they show the same health benefits. Nutritional adequacy of vegetarian diets Protein quality A nutritionally sound vegetarian diet is possible if adequate amounts of a wide variety of foods are consumed (Grandjean 1989; Harding et al. 1996), but there are certain nutrients that vegetarians must be aware of and plan for to ensure the presence of adequate amounts in their diets. The most obvious nutrient of concern is protein. Lacto-ovovegetarians and ovovegetarians receive high-quality complete proteins and are unlikely to incur protein deficiencies. Vege- 446 special considerations tarians who consume only plant proteins could become protein deficient unless they balance their amino acids. Plant proteins are incomplete and lack one or more essential amino acid. While it was once thought that all the amino acids must be consumed in one meal, it is now agreed that timing of the amino acid intake is less critical and that amino acid intake must be balanced over days rather than hours. Research now shows that the liver monitors the amino acid composition of proteins consumed in a meal: if the meal is low in an essential amino acid, the liver can break down its own proteins to supply it. When the amino acid is once again plentiful, the liver will replenish its protein source. Because individual plant foods do not contain all the essential amino acids, it is recommended that vegetarians complement their proteins. For example, cereals are very low in the essential amino acid lysine, while legumes are slightly deficient in the sulphur-containing amino acids. By combining these two groups of foods (i.e. refried beans and corn tortillas), a vegetarian could provide a mixture of amino acids similar to that of a complete or high-quality protein food. Figure 33.1 illustrates different combinations of incomplete proteins to make a complete protein as well as demonstrating the fact that when an animal protein is combined with an incomplete Milk products Rice with sesame seeds Pe Ri ce an an ut d bu be tte an rs ca an dw sse ich ro le Protein requirements for vegetarian athletes A major concern for vegetarian athletes is to make sure that they have consumed enough food so that their protein requirement will be met. The total protein intake of athletes consuming a vegetarian diet may have to be increased slightly to take account of the lower digestibility, lower energy density and lower protein quality of plant foods consumed. This may lead to problems with the volume of food to be consumed, because athletes with high energy requirements may find it difficult to consume sufficient volume of foods to maintain energy balance on a purely vegetarian diet. Generally, if vegetarian athletes consume between 0.8 and 1.7 g protein · kg–1 body mass · day–1 and maintain energy balance, they should meet their protein requirement for exercise and health. Vitamin B12 Another nutrient that may be low in a vegetarian diet is vitamin B12, especially for those individuals on a strict plant-based diet (vegans). Rauma et al. (1995) studied the vitamin B12 status of long- Nuts and seeds Sunflower seed and peanuts Macaroni and cheese cereal with milk Grains protein, the result is a complete, high-quality protein. Milk in legume soups Legumes Fig. 33.1 The concept of mutual supplementation, which is the strategy of combining two incomplete sources of protein so that the amino acids in each food make up for those lacking in other foods. Such protein combinations are sometimes called complementary proteins. the vegetarian athlete term adherents to a strict uncooked vegan diet called the ‘living food diet’ (LFD). Most food items in this diet are fermented or sprouted. Serum B12 concentrations and the dietary intakes of 21 long-term adherents of the LFD were compared with those of 21 omnivorous controls. In a longitudinal study, the LFD diet resulted in a decrease in serum vitamin B12 in six of nine subjects. The cross-sectional study revealed significantly lower serum vitamin B12 in the LFD adherents than in their matched omnivorous controls. Those following the LFD who consumed nori or chinerilla seaweeds had somewhat better B12 status than those who did not, but B12 levels fell over time in all but one subject. While lower levels of vitamin B12 have been found in strict vegans, few cases of clinical deficiency have been found. Helman and DarntonHill (1987) found the mean serum vitamin B12 levels of vegetarians to be significantly lower (350 pg · ml–1) than those of omnivores (490 pg · ml–1), while 16% of the vegetarians had values less than 200 pg · ml–1. Vitamin B12 deficiency is rare among lacto-ovovegetarians because milk and eggs contain sufficient quantities of this nutrient. Vegans should be encouraged to use soybean milk fortified with vitamin B12 or a vitamin B12 supplement. Analogues of the vitamin found in algae, spirulina, nori or fermented soy products do not have vitamin activity for humans. Individuals with low serum B12 may manifest paraesthesia (numbness and tingling in the hands and legs), weakness, fatigue, loss of vibration and position sense, and a range of psychiatric disorders including disorientation, depression and memory loss. The use of alcohol, tobacco and drugs such as antacids, neomycin, colchicine and aminosalicylic acid may contribute to the problem by causing B12 malabsorption in both omnivores and vegetarians. less risk of iron deficiency anaemia. In absolute amounts, red meat contains only an average amount of iron, but the bioavailabilty of iron from red meat is superior to that derived from plant sources. There are two forms of iron in the diet: haem iron and non-haem iron. Haem iron found in meats, fish and poultry is better absorbed than non-haem iron, which is found in grains, vegetables and fruits. The fractional absorption of haem and non-haem iron varies between 3% and 35%, depending on the presence of dietary enhancing factors such as ascorbic acid, consumption of sources of haem iron and on the body stores of iron. Table 33.2 lists the ranges of intestinal absorption of iron from haem and non-haem food sources which is dependent upon body stores of iron. Iron is classified as an essential nutrient and is required for the formation of haemoglobin and myoglobin, as well as the cytochromes, which are components of the electron transport chain in the mitochondria. Iron is also a cofactor for a number of enzymatic reactions, including those involved in the synthesis of collagen and of various neurotransmitters. In addition, iron is needed for proper immune function and plays a role in the drug detoxification pathways (Wardlaw & Insel 1995). Since iron plays a critical role in oxidative energy metabolism, it is essential for athletes to have adequate iron stores. There are some differences of opinion about the prevalence of iron deficiency among athletes. A number of studies have used serum ferritin as a measure of iron deficiency anaemia, while other studies have used haemoglobin and haematocrit as determinants of iron deficiency anaemia. The number Table 33.2 Absorption rate (as % of intake) of haem and non-haem iron in relation to body stores of iron. Haem (%) Non-haem (%) Low stores of iron 35 20 Normal stores of iron 15 Iron availability in vegetarian diets While both vegetarian and non-vegetarians may have difficulty in meeting the dietary requirements for iron, athletes who eat red meat are at 447 2–3 448 special considerations of athletes suffering from true iron deficiency anaemia is therefore difficult to establish (Eichner 1988). Further debates have been sparked by the fact that many athletes with low iron stores eat little haem iron and yet have no performance decrements (Dallongeville et al. 1989; Snyder et al. 1989; Lyle et al. 1992; Pate et al. 1993; Williford et al. 1993). It is, however, important to monitor iron status among athletes, especially female athletes. The Sports Medicine and Science Division of the United States Olympic Committee recommend screening for haemoglobin and haematocrit twice yearly. Other tests of iron stores are recommended based on menstruation records. Snyder et al. (1989) investigated the iron intake and iron stores in female athletes who either were consuming a mixed diet or were classified as a modified vegetarian. The subjects were matched for age, body mass, aerobic capacity, training load and number of pregnancies. The modified vegetarians (n = 9) consumed less than 100 g of red meat per week while the subjects on the mixed diet (n = 9) included red meat in their diet. Both groups consumed the same amount of iron (14 mg · day–1), but serum ferritin and total iron-binding capacity were significantly lower in the modified vegetarian group (P < 0.05). The authors also found that the bioavailability of the iron consumed by the two groups was different. Iron consumed by the modified vegetarian group was significantly less available than the iron consumed by the mixed-diet group. These data suggest that in female runners non-haem iron may not be as readily available as haem iron. These findings have also been confirmed in the non-athletic population. In 1995 Shaw et al. (1995) investigated the iron status of young Chinese Buddhist vegetarians (23 men and 32 women) and compared them with non-vegetarian students (20 men and 39 women). Dietary assessment of iron intake and haematological measurements of biochemical indices, including haemoglobin, plasma iron, transferrin saturation and plasma ferritin, were made. A characteristic of the vegetarian diets was that most of the protein was coming from soybean products, which have limited bioavailable iron. Daily iron intake was similar in both vegetarian and nonvegetarian men, but iron intake was significantly higher in female vegetarians than nonvegetarians. Results from the haematological measurements showed that for both sexes, the median plasma ferritin concentration of the vegetarians was about half that of the nonvegetarians. There was also a greater prevalence of low ferritin levels and anaemia in the vegetarian group, especially among the vegetarian women. food strategies for increasing iron in a vegetarian diet Because animal foods are the best and most absorbable source of iron, this presents a potential problem to the vegetarian who eats no red meat. Lacto-ovovegetarians also have a problem consuming enough iron, as milk and dairy products are poor sources of iron. Vegetarians can incorporate leafy green vegetables such as spinach and legumes as well as fortified and enriched whole grains into their diets. Dried fruit can also provide iron in the vegetarian diet. Dietary iron may also be derived from iron cooking utensils. When acidic foods are cooked in iron cookware, some of the iron is taken up with the food. Zinc status among athletes Since the best food sources of zinc are meats, dairy products and seafood (especially oysters), zinc nutriture is of concern for vegetarians. Whole-grain cereals and cereal products are the primary sources of zinc in many vegetarian diets, but the phytate and fibre content of these products reduces the bioavailability of zinc (Reinhold et al. 1976). Zinc is found in almost every tissue in the body and is a cofactor for over 100 enzymes, of which several are important in the pathways for energy metabolism. Zinc is also needed for protein synthesis and is a part of the insulin molecule. Several studies have demonstrated that the vegetarian athlete exercise increases zinc loss from the body (Dressendorfer & Socklov 1980; Haralambie 1981; Singh et al. 1990; Clarkson & Haymes 1994) and that levels may be low in athletes. Possible explanations for the reduced level of zinc stores include inadequate intake of zinc, low bioavailability, increased zinc loss during exercise, dilution of zinc by expansion of plasma volume, and redistribution of zinc in the body. Contrary to these reports, Lukaski (1989; Lukaski et al. 1990) has found that zinc status is not affected by physical training as long as dietary intakes of zinc are adequate. Lukaski et al. (1990) studied 16 female and 13 male swimmers and 13 female and 15 male non-swimming controls. Plasma zinc values were within the normal range for all subjects and did not change throughout the swimming season. In addition to Lukaski’s studies, Duester et al. (1989) investigated the effects of endurance training on zinc status in 13 highly trained women and compared them with 10 untrained controls. Three-day dietary records were evaluated for zinc intake while blood and 24 h urine samples were taken before and after a 25-mg oral zinc load. Mean daily zinc intakes did not differ and were below the recommended dietary allowance set for zinc for both groups. The authors reported no differences between fasting concentrations of plasma zinc, serum albumin, a-2-macroglobulin, and erythrocyte zinc content among the two groups. However, the trained women had significantly (P < 0.05) higher urinary zinc excretion and reduced responses to the oral zinc load than did the untrained women. The authors concluded that the increase in zinc excretion in the highly trained women may reflect higher rates of skeletal muscle turnover. zinc and the vegetarian In addition to these studies of athletes, several studies confirm lower zinc status among vegetarians (Freeland-Graves et al. 1980; Gibson 1994; Kadrabova et al. 1995). Janelle and Barr (1995) recently reported a study comparing nutrient intakes between 449 female vegetarians and non-vegetarians with similar health practices and found that vegans and lactovegetarians had lower zinc intakes (8.5 and 8.2 mg · day–1, respectively) than the recommended dietary allowance of 15 mg · day–1. Similar results were found in a study conducted by Donovan and Gibson (1995), who found that 33% of semivegetarians, 24% of lacto-ovovegetarians and 18% of omnivores had serum zinc levels below 10.7 nmol · l–1. They also reported that the phytate to zinc ratio in the diet was negatively associated with the serum zinc concentration (P < 0.05). The authors concluded that the suboptimal zinc status was the result of low intakes of poorly available zinc in all dietary groups. food strategies for increasing zinc in a vegetarian diet Foods for the vegetarian that have the highest zinc content are oysters, crab, shrimp, wheat germ and legumes. Incorporating other good sources of zinc into a vegetarian diet will also help meet the dietary recommendations: nuts, beans and whole grains can all contribute. Zinc is not part of the enrichment process, so refined flours are not a good source. Calcium requirements of vegetarians The diets of strict vegetarians or vegans tend to be low in calcium unless adequate amounts of milk and dairy products or dark leafy greens are consumed daily. As with iron and zinc, the absorption of calcium may be reduced by phytates, oxalates, fibre and tannins (James et al. 1978; Weaver et al. 1996). Phytic acid is found in oatmeal and other whole-grain cereals, while oxalates are commonly found in beets, spinach and leafy greens. These binders seem to depress absorption of calcium present in some calciumcontaining foods but not in others. That is why strict vegans who obtain most of their dietary calcium from leafy greens and whole-grain products are at a greater risk of an inadequate calcium availability than milk-drinking vegetarians. A 450 special considerations purely vegan diet may also be low in vitamin D, which will further impair calcium absorption and utilization. In an interesting anthropological study of prehispanic burials from the Canary Islands, Gonzalez-Reimers and Arnay-de-la-Rosa (1992) found a high prevalance of osteoporosis among the 117 skeletons analysed for trace elements. Bone trace element analysis showed that low concentrations of iron, zinc and copper were found in skeletons with a reduced trabecular bone mass. The authors state that during this prehispanic period many of the residents of the Canary Islands existed in a relative proteinenergy malnutrition state which consisted mainly of a vegetarian diet which may have predisposed these individuals to osteoporosis. It has been suggested that vegetarians who restrict their intake of dairy products should provide calcium-rich foods or supplements by consuming calcium-fortified soy products as well as consuming dark leafy green vegetables on a daily basis. food strategies for increasing calcium in a vegetarian diet Foods with the highest nutrient density for calcium are leafy greens, such as spinach and broccoli, non-fat milk, romano cheese, swiss cheese, sardines and canned salmon. The calcium found in some leafy greens is not well absorbed because of the presence of oxalic acid, but this effect is not as strong for kale, collard, turnip, and mustard greens. Overall, nonfat milk is the most nutrient-dense source of calcium because of its high bioavailability and low energy value. The new calcium-fortified orange juices and other beverages offer an alternative to the individual who is a strict vegetarian; other calcium-fortified foods include bread, breakfast cereal, breakfast bars, and snacks. Another good source for the vegetarian is soybean curd (tofu) if it is made with calcium carbonate (check the food label). While there are concerns about the potential lack of some nutrients in a vegetarian diet, many of these concerns can be overcome by using a wide variety of foods and planning meals so that they complement proteins and include nutrientdense foods. Table 33.3 summarizes the nutrients that may be lacking in a vegetarian diet and gives some examples of foods that could be included in a vegetarian diet to overcome these inadequacies. Hormonal alterations as a result of a vegetarian diet There is evidence that nutritional status and diet can affect the reproductive system. Hill et al. (1984) found that Caucasian women (n = 16), who normally ate meat had a significantly (P < 0.01) shorter follicular phase of their second menstrual cycle when they ate a vegetarian diet for two cycles. The vegetarian diet decreased (P < 0.01) the pituitary response to releasing luteinizing hormone and decreased (P < 0.05) the episodic release of luteinizing hormone. The experiment also included supplementing nine vegetarian Black South African women with daily meat product: an increased length of the follicular phase was observed (P < 0.01). The authors concluded that a lower episodic release of gonadotrophins and a shorter duration of the follicular phase, when omnivorous women ate no animal protein, implies that a vegetarian diet plays a role in the control of ovulation through the hypothalamic axis of the central nervous system. In a similar study, Pirke et al. (1986) investigated the influence of a vegetarian diet on the menstrual cycles of 18 healthy normal weight women aged 17–27 years. Plasma levels of oestradiol, progesterone and luteinizing hormone were measured on Monday, Wednesday and Friday throughout the 6-week diet period. Nine women followed a vegetarian diet while nine followed an omnivorous diet. Both groups lost weight during the experimental period (1 kg body weight · week–1). Seven of the nine vegetarian women became anovulatory and had significantly decreased luteinizing hormone during the mid-cycle and luteal phase. Oestrogen and progesterone levels were also signifi- the vegetarian athlete 451 Table 33.3 Nutrients that are of concern in a vegetarian diet and strategies to lower nutritional deficiencies. From Rudd (1990). Nutrient RDA Physiological function Vegetarian food sources Protein 0.8 g ◊ kg-1 BW Build and repair tissues; major component of antibodies, enzymes, hormones; responsible for transport of nutrients and fluid balance Eggs, fish, legumes, peanut butter, milk, brown rice, peanuts, soybeans Vitamin B12 2.0 mg ◊ day-1 Promotes growth; cofactor for several enzymes; maintains the sheath around nerve fibres; helps folate in preventing anaemia Eggs, dairy products, clams, oysters, some seafood Iron Males, 10 mg ◊ day-1; females, 15 mg ◊ day-1 Constituent of haemoglobin and myoglobin; carrier of O2 and CO2 Clams, whole grains, enriched cereals, green leafy vegetables, dried fruits, tofu, legumes Calcium Teens, 1200 mg ◊ day-1; adults, 800 mg ◊ day-1 Major component of hydroxyapatite for bones and teeth; regulation of muscle contraction, heart beat, clotting of blood, and transmission of nerve impulses; blood pressure Dairy products, leafy green vegetables, fish and shellfish, tofu, legumes Zinc Males, 15 mg ◊ day-1; females, 12 mg ◊ day-1 Part of over 100 enzymes; associated with insulin; involved in making DNA and RNA; involved with the immune system; transport of vitamin A; wound healing and normal development of the fetus Fish, oysters, dairy products, black beans, kidney beans, tofu, beets, peas, whole-grain breads, bran flakes Vitamin D 400 IU ◊ day-1 Promotes normal bone and teeth formation; aids body’s absorption, transportation and deposition of calcium and phosphorus Fortified dairy products, egg yolk, shrimp, sunlight cantly decreased in the vegetarian group. In comparison, seven of nine women in the omnivorous group maintained ovulatory cycles and had no change in cycle length or in the length of the follicular phase. In both of these studies a vegetarian diet appears to be involved in the incidence of menstrual irregularities, but the underlying pathophysiology remains unclear. Vegetarian diets and oestrogen levels Adlercreutz et al. (1986a, 1986b, 1995) have provided some possible reasons why a vegetarian diet may play a role in menstrual-cycle regularity. Dietary constituents such as fibre and a vege- tarian eating pattern have been shown to alter oestrogen levels in humans by influencing oestrogen synthesis, availability, excretion metabolism and action. Currently there is a great deal of interest in plant-derived lignans and isoflavonic phyto-oestrogens, as they have been found in human urine and appear to exhibit, both in vitro and in vivo, weak oestrogenic and sometimes anti-oestrogenic activities. Plant lignans and isoflavonoids, glycosides from soybean products as well as whole grains, seeds and nuts are converted by intestinal microflora to hormone-like compounds. These compounds bind, with low affinity, to oestrogen receptors, and preliminary results suggest that they may 452 special considerations induce production of sex hormone-binding globulin in the liver and in this way influence sex hormone metabolism and biological effects. Indeed, Gorbach and Goldin (1987) measured urinary, faecal and plasma levels of oestrogens in pre- and postmenopausal women eating different diets. Premenopausal US women consuming a ‘Western’ diet composed of 40% fat and low fibre were compared with age-matched vegetarians eating 30% of their energy intake as fat and a high-fibre diet. The researchers found that the vegetarian women excreted threefold more oestrogen in their faeces, had lower urinary oestrogen excretion, and had 15–20% lower plasma oestrogen than the omnivorous women. When pre- and postmenopausal women eating a Western diet were compared with Asian immigrants eating a very low fat diet (20–25% of total energy from fat), similar results were found, except that the plasma oestrogen levels were 30% lower among the Orientals than in the Western omnivore group. Correlation analysis of dietary components and plasma oestrogen showed that plasma oestrogen was positively associated with fat intake and negatively associated with dietary fibre. The authors concluded that diets high in fibre, like a vegetarian diet, can alter the route of excretion of oestrogen by influencing the enterohepatic circulation and thus influence plasma levels of oestrogen. In a similar study, Pedersen et al. (1991) examined the effect of different nutritional patterns on menstrual regularity in premenopausal women. Forty-one non-vegetarian and 34 vegetarian women were recruited and completed a questionnaire regarding menstrual history and a 3-day dietary record. The reported incidence of menstrual irregularity was 4.9% among the non-vegetarians and 26.5% among the vegetarians. The vegetarian group consumed significantly more polyunsaturated fatty acids, carbohydrates, vitamin B6 and dietary fibre, whereas the non-vegetarians consumed significantly more caffeine, cholesterol, saturated fatty acids and alcohol. Logistic regression analysis showed that the probability of menstrual regularity among all subjects was positively correlated with increasing protein and cholesterol intakes. The probability of developing menstrual irregularities was negatively correlated with increasing dietary fibre and increasing amounts of magnesium in the diet. This study is consistent with the notion that premenopausal vegetarian women as a group have decreased circulating oestrogen concentrations. Additional data from Adlercreutz et al. (1986a) have also found that vegetarians may be excreting more oestrogen than omnivores: they investigated the possible effects of variations in dietary fibre intake on oestrogen metabolism in young Finnish women through one winter and one summer. Eleven of the subjects were lactovegetarians, while 12 were omnivorous. Within the groups there was a seasonal variation in fibre intake. The vegetarian group consumed more fibre (P < 0.02), more grains (P < 0.02) and more vegetables (P < 0.02) during the winter than during the summer. The excretion of oestrogens was remarkably constant in the omnivorous group, while the vegetarian group had a significant seasonal variation of total and individual catecho-oestrogens and estrone (P < 0.05–0.005). There were no differences between the groups in excretion of total or individual urinary oestrogens in any season or between mean values for both seasons, but a significant negative correlation was found between dietary intake of total grain fibre per kilogram of body weight and the excretion of individual oestrogens were found. These studies are consistent with the notion that menstrual regularity can be influenced by specific dietary nutrients that may have a direct effect on oestrogen. Hormonal responses of a vegetarian lifestyle on males Most of the data collected on diet and hormone relationships among vegetarians is on women, and information on males is sparse. Howie and Shultz (1985) studied the relationship between dietary nutrients and plama testosterone, 5-adihydrotestosterone, oestradiol-17-b, luteinizing hormone, and prolactin levels in 12 Seventh Day Adventist vegetarian, 10 Seventh Day Adventist the vegetarian athlete non-vegetarian and 8 non-Seventh Day Adventist, non-vegetarian males. Fasting blood samples and 3-day dietary intakes were obtained from all subjects. The Seventh Day Adventist vegetarians consumed significantly more crude and dietary fibre than the other non-vegetarian subjects. Plasma levels of testosterone and oestradiol-17-b were significantly lower in the Seventh Day Adventist vegetarians than in the ominvores. Additionally, plasma levels of testosterone and oestradiol-17-b of all subjects were negatively correlated with dietary fibre intake. The authors concluded that a vegetarian eating style may lead to decreased plasma concentrations of androgens and oestrogens in men. In contrast, Naik and Snyder (1997) examined the independent effects of diet and endurance training on basal serum testosterone concentration by comparing endurance-trained cyclists with vegetarian individuals who had abstained from eating red meat and poultry for 1 year. The aerobic ability of the endurance athletes was significantly greater than that of the sedentary vegetarians. Nutrient intake, however, was similar in both groups, except for dietary fibre intake, which was higher in the vegetarian group. Serum total and free testosterone concentrations were not different for either main effect (i.e. diet and exercise). Perhaps the lack of difference in sex hormones could be attributed to the fact that the diets were very similar in both groups. Implications of vegetarian diets for athletes Vegetarian diets have been associated with a low incidence of cancers of the breast, endometrium and prostate. However, lowered plasma levels and increased urinary excretion of oestrogen can lead to menstrual abnormalities which may in turn lead to irregular menstrual cycles and compromised bone health in vegetarians. Brooks et al. (1984) noted that most female athletes with amenorrhoea were vegetarian. They compared the diets of amenorrhoeic runners (82% vegetarian) with regularly menstruating runners (13% vegetarian) and found that the runners with 453 regular menstrual cycles ate five times more meat and significantly (P < 0.05) more fat than amenorrhoeic runners. Kaiserauer et al. (1989) also found that amenorrhoeic runners consumed significantly less fat, red meat and total energy than did regularly menstruating runners. Slavin et al. (1984) found that there was a high incidence of vegetarianism among amenorrhoeic athletes and speculated that trace elements or plant hormones may affect menstruation. While it appears that vegetarianism may influence menstrual function, the real importance of menstrual irregularities in female athletes is related to bone health. In a landmark study on bone health and athletic amenorrhoea, Drinkwater et al. (1984) studied 28 female athletes, 14 of whom were amenorrhoeic. When compared with the regularly menstruating runners, the amenorrhoeic runners had significantly lower lumbar vertebral bone mineral densities. The mean age of the amenorrhoeic athletes was 25 years, but their average bone mineral density was equivalent to that of a 51-year-old. While there is a clear relationship between athletic amenorrhoea and bone health, there is a limited amount of information on the possible effects of a vegetarian lifestyle. Hunt et al. (1989) investigated the relationship of bone mineral content/bone width in elderly, independently living Methodist omnivores and Seventh Day Adventist vegetarians. Bone mass was measured by single photon absorptiometry and dietary intakes were assessed by 24-h dietary recall and food frequency methods. Bone mineral/bone width was not different in omnivores compared to vegetarians and no significant relationships were found to exist between current or early dietary intakes and bone mineral/bone width. Lloyd et al. (1991) also found no significant differences in bone density between vegetarian and non-vegetarian women despite a significantly higher prevalence of menstrual irregularities among the vegetarian subjects. These studies support the concept that, despite the differences in dietary practices, vegetarian and non-vegetarian women do not appear to differ in bone health. Caution must be taken, 454 special considerations however, when dealing with an athlete who is a vegetarian. Bone mineral densitiy should be measured and adequate amounts of calcium should be consumed to ward off the potential harmful effects of low oestrogen on bone. While vegetarianism is not a risk factor for the Female Athlete Triad, it may become a factor if an athlete is amenorrhoeic due to her vegetarian eating pattern. Conclusions and recommendations Currently most information on vegetarianism relates to nutritional adequacy and the implications for lifestyle diseases such as heart disease and cancer. Little is known about the relationship between vegetarianism and athletic performance. What is clearly understood is that the vegetarian athlete must plan his or her diet carefully to avoid the risk of nutritional deficiencies and an adverse effect on performance. There are advantages to the athlete of consuming a vegetarian diet. Vegetarian athletes usually consume a higher proportion of energy in the form of carbohydrates. It is well documented that athletes, especially endurance athletes, should be consuming a higher proportion of carbohydrates in their diets to maximize muscle glycogen concentration. Prolonged strenuous exercise can deplete most of the glycogen stored in the muscles and the athlete can become chronically fatigued. Increasing dietary carbohydrates will be beneficial to the athlete involved in heavy training. More research is needed to answer some of the current concerns of vegetarian athletes, especially with regard to hormonal alterations and their impact on bone health as well as the questions on protein-energy requirements for strict vegetarians who consume no animal protein. If athletes adopt a vegetarian lifestyle, they must become aware of the limitations of the diet and make sure that their nutritional requirements are met so as not to influence performance. Vegan diets should not be attempted by any athlete without previous experience or without consultation with a dietitian or health care provider. Young growing athletes should be dis- couraged from such a strict diet due to its possible limitations on growth and performance. Vegan diets should only be considered if an athlete is willing to devote time and effort to understanding the proper combinations and amounts of foods necessary to achieve a nutritionally balanced diet. In planning vegetarian diets of any type, athletes should choose a wide variety of foods and ensure that the energy intake is adequate to meet their needs. Additionally, the American Dietetic Association (1993) gives the following recommendations for individuals who are vegetarian or thinking of becoming vegetarian. • Keep the intake of foods with a low nutrient density, such as sweets and fatty foods, to a minimum. • Choose whole or unrefined grain products, instead of refined products, whenever possible, or use fortified or enriched cereal products. • Use a variety of fruits and vegetables, including a good food source of vitamin C. • If milk or dairy products are consumed, use low-fat or non-fat varieties. • Limit egg intake to three or four per week. • Vegans should have a reliable source of vitamin B12, such as some fortified commercial breakfast cereals, fortified soy beverage or a cyanocobalamin supplement. 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