Vegetarian and vegan diets

Definition

Strict vegetarianism eliminates the intake of animal products, such as meat, poultry, game, fish, shellfish or crustacea, or slaughter by-products such as gelatine or animal fats.  The term vegan is explicitly used to define individuals who do not use any animal products, therefore also excluding eggs and milk and other dairy products; the latter being a prime source of calcium in the diet.

Types of vegetarian diets

• Lacto-ovo-vegetarian. Eats both dairy products and eggs.  There is less likelihood of nutritional deficiencies.
• Lacto-vegetarian. Eats dairy products but not eggs.
• Vegan. Does not eat dairy products, eggs, or any other animal product.  Calcium and vitamin B12 are especially a concern.

• Macrobiotic. A diet followed for spiritual and philosophical reasons. Aims to maintain a balance between foods seen as ying (positive) or yang (negative). The diet progresses through ten levels, becoming increasingly restrictive. Not all levels are vegetarian, though each level gradually eliminates animal products. The highest levels eliminate fruit and vegetables, eventually reaching the level of a brown rice diet.

The term vegetarianism therefore encompasses a wide range of dietary practices with potentially differing implications for health.  Due to the variability of dietary practices among vegetarians, the individual assessment of dietary intakes is required.

Dietary considerations

Protein

Iron

Vitamin B12

Calcium

Nutrient deficiencies, due to malabsorption, are common in patients with coeliac disease, both at diagnosis and after commencing a gluten-free diet.  Common nutrient deficiencies include iron, calcium, folate, and vitamin B12.  Similarly these nutrients may be a concern for vegetarians.  Combining any dietary regimens, e.g. a gluten free and vegetarian diet, can increase the risk of nutritional deficiencies and both coeliac disease and vegetarianism have similar nutritional risks in that both diets could potentially pre-dispose to osteoporosis due to poor calcium intake and malabsorption (in the case of coeliac disease). Some of the complex dietary interactions are considered below.

Protein 

Vegetarians

• Plant protein can meet requirements when a variety of plant foods is consumed and energy needs are met.  In more restrictive diets, where variety and energy intake is limited, greater attention must be given to providing an adequate protein intake, especially in pregnant women, infants, growing children, and the elderly. 
• A vegetarian diet, including milk and eggs, provides all essential amino acids.
• Research indicates that an assortment of plant foods eaten over the course of the day can provide all essential amino acids, therefore complementary proteins do not need to be consumed in the same meal (1). Lysine is the limiting amino acid in cereal grains and methionine is the limiting amino acid in legumes.
• The quality of plant protein varies, and in general plant proteins in their natural form are less digestible than animal protein sources.  Isolated soya protein can meet protein needs as effectively as animal protein and has been shown to be as digestible as egg protein (2).  The consumption of dietary protein from a variety of sources should be encouraged.
• A slightly lower protein intake may in fact be beneficial for some individuals with or prone to osteoporosis, as evidence suggests that a high animal protein intake may increase loss of calcium through urinary calcium excretion (3).

Vegans

• Vegetarians whose dietary protein sources are mainly those that are less well digested, such as some cereals, may have greater dietary protein requirements.  It has been suggested that protein requirements of vegans may be increased by 30-35% for infants up to the age of two years, and 20-30% for 2-6 years olds, and 15-20% for those 6 years and older in comparison with those of non-vegetarians (4).
• The consumption of dietary protein from a variety of sources should be encouraged.
• It is essential to seek the advice of a dietitian if bringing up a child on a gluten-free and vegan diet, as children have special nutritional requirements for growth and development.

Iron 

• Plant foods contain only non-haem iron, which is less available than haem iron from animal sources, additionally plant foods contain a variety of substances known to reduce iron availability.
• Anaemia is a common presentation of coeliac disease and as many as 50% of coeliacs have evidence of anaemia at presentation (5).  Iron deficiency anaemia is the commonest, while folate and B12 deficiency is less common.  The more restricted the diet the greater the risk of iron-deficiency anaemia.  The iron status of vegetarians with coeliac disease may therefore be questionable and must be monitored regularly.
• The absorption of non-haem iron in plant foods (and eggs) is enhanced by vitamin C and citric acid and inhibited by phytates (found in wheat bran and legumes), oxalates (found in spinach), tannins (found in tea) and other polyphenols (found in coffee and cocoa) in the diet (6). To ensure a good intake of iron vegans and vegetarians should be encouraged to include legumes, eggs, fortified gluten free products, dried apricots, and green leafy vegetables daily in their diet.
• To maximize the absorption of iron, vitamin C-containing foods should be consumed with meals, while drinking tea, containing tannins, with meals should be discouraged due to the interference with iron absorption. 
• Some food preparation techniques such as soaking and sprouting beans, grains, and seeds, can hydrolyse phytate and may improve iron absorption (7)
• Vegans and vegetarians may carry a greater risk of developing iron deficiency anaemia if iron requirements are increased (e.g. during infancy, pregnancy, blood loss).                                 

Table 1. Vegetarian sources of iron 

Vitamin B12

• Vitamin B12 deficiency may not typically be expected in coeliacs as absorption is co-factor dependent and occurs in the often unaffected terminal ileum, however B12 levels are statistically lower in people with coeliac disease compared with controls. The haematological symptoms of vitamin B12 deficiency may be masked by good intakes of folic acid.  
• The only reliable unfortified sources of vitamin B12 are meat, dairy products and eggs.  The current nutritional consensus is that no plant foods can be relied on as a safe source of vitamin B12.  Foods such as sea vegetables, spirulina, or fermented soya products are not reliable sources of vitamin B12.  Vitamin B12 is therefore a nutrition concern for vegans (8)
• Good sources of vitamin B12 for vegetarians are dairy products and eggs.
• Vegans are recommended to ensure their diet includes foods fortified with vitamin B12, such as fortified yeast extracts or vegetable stock, fortified soya milk, fortified textured vegetable protein, and fortified margarines.  Not all vegan foods fortified with vitamin B12 will be gluten free.  Supplementation with vitamin B12 may be indicated; cyanocobalamin is its most bioavailable form.
  

Calcium

Adequate calcium and vitamin D intakes are important to ensure optimal bone status. Coeliac disease is a risk factor for osteoporosis.  Milk and milk products are prime sources of calcium in the diet, therefore eliminating dairy foods from the diet can severely restrict calcium intake.  Lactose intolerance is not uncommon in patients with coeliac disease and may be a reason for restricting calcium intake in lacto-ovo vegetarians (9).

Calcium intakes of lacto-vegetarians are comparable to or higher than those of non-vegetarians, while calcium intake in vegans tends to be less than lacto-vegetarians or non-vegetarians (10). Vegans may therefore require attention to ensure appropriate intake, especially during periods of growth. 

Dietary factors affecting calcium absorption:

• Oxalates present in some foods can greatly reduce calcium absorption, therefore high-oxalate vegetables such as spinach and Swiss chard are not good sources of calcium despite their high calcium content.  In contrast kale, broccoli, Chinese cabbage, and mustard and turnip greens provide substantial amounts of available calcium. 
• Phytates may also inhibit calcium absorption.
• A consistently lower intake of animal protein, as often seem amongst vegetarians, may decrease calcium requirements.  However, it has been suggested that the characteristically increased consumption by particularly vegans of oxalate- and phytate-containing foods may offset the benefits of their lower intake of protein.
• A high intake of sodium increases calcium excretion
• Vitamin D enhances calcium absorption

For adults in the general population (19 years and over), the recommended amount of calcium to aim for is 700mg per day.

For adults with coeliac disease, the recommended target is 1000mg of calcium per day. For post menopausal women and men over the age of 55 years, an increased requirement of 1200mg is recommended (11).

The use of supplements should be decided on an individual basis. 

There are no guidelines that recommend a higher requirement for calcium in children with coeliac disease. Following a calcium rich gluten-free diet is recommended, using Reference Nutrient Intake (RNI) values as a guide (see below) depending on the individual case.

1-3 years 350 mg
4-6 years 450 mg
7-10 years 550 mg
11-18 years (female) 800 mg
11-18 years (male) 1000 mg

There are no specific recommendations for lactating mothers who have coeliac disease. An additional 550mg/day are recommended for all women while breastfeeding, so appropriate adjustments for those with coeliac disease should be made on an individual basis.

Calcium sources suitable for vegans include tofu, baked beans, fresh or dried figs, sesame seeds and nuts e.g. almonds. 

Table 2. Calcium Content of Vegetarian Foods

Vitamin D

• Adequate calcium and vitamin D intakes are important to ensure optimal bone status.  Low vitamin D levels have been observed in some vegan populations at northern latitudes who did not use supplements or fortified foods (12).  
• Vitamin D3 (cholecalciferol) is of animal origin, whereas vitamin D2 (ergocalciferol) is a form acceptable to vegans, and is found in some fortified vegan margarines, soya milks and soya cheeses.  Supplementation with vitamin D may be required if sun exposure and intake of fortified foods are insufficient to meet requirements.
• Dietary sources of vitamin D are limited to animal foods (egg yolk, oily fish, liver) and fortified foods such as margarine, soya milk and breakfast cereal. 

References:
 
1 Young VR, Pellett PL (1994)  Plant proteins in relation to human protein and amino acid nutrition.  Am J Clin Nutr 59:1203S-1212S.
 
2 Young VR, Fajardo I, Murray E, Rand WM, Scrimshaw NS (1975)  Protein requirements of man: comparative nitrogen balance response within the submaintenance to maintenance range of intakes of wheat and beef protein.  J Nutr 105:534-542.

3 Kerstetter JE, Allen LH (1990)  Dietary protein increases urinary calcium.  J Nutr 120: 134-136.

4 Messina V, Mangels AR (2001)  Considerations in planning vegan diets: Children.  J Am Diet Assoc 101: 661-669).

5 Bode S, Gudmand-Hoyer E (1996)  Symptoms and haematologic features of consecutive adult coeliac patients.  Scand J Gastroenterol 32(1): 54-60). 

6 British Nutrition Foundation (1995)  Iron.  Task Force Report.  London. 

7 Sandberg AS, Brune M, Carlsson NG, Hallberg L, Skoglung  E, Rossander-Hulthen L (1999)  Inositol phosphates with different numbers of phosphate groups influence iron absorption in humans.  Am J Clin Nutr 70: 240-246.

8 Donaldson MS (2000)  Metabolic vitamin B12 status on a mostly raw vegan diet with follow-up using tables, nutritional yeast, or probiotic supplements.  Ann Nutr Metab 44: 229-234.            

9 Ojetti V, Nucera G, Migneco et al (2005)  High prevalence of Celiac Disease in Patients with Lactose Intolerance.  Digestion 71: 106-110.

10 Tear R, Notelovitiz M, Shim E, Dauwell G, Brown J (1992)  Axial and peripheral bone density and nutrient intakes of postmenopausal vegetarian and omnivorous women.  Am J Clin Nutr 56: 699-704.

11. Lewis NR, Scott BB for the British Society of Gastroenterology (2007)  Guidelines for osteoporosis in coeliac disease and inflammatory bowel disease.  Accessed at www.bsg.org.uk

12  Fonseca V, Agnew JE, Nag D, Dandona P (1988)  Bone density and cortical thickness in nutritional vitamin D deficiency:  effect of secondary hyperparathyroidism.  Ann Clin Biochem 25: 271-274