食品加工营养手册（英文版）：36659_09

9 Enhancing the nutritional value of meat J. D. Higgs, Food To Fit; and B. Mulvihill 9.1 Introduction The most common dietary problems in developed countries are due mainly to over nutrition. The incidence of overweight, obesity and adult onset-diabetes is increasing steadily. Cancer is now the most common cause of death in many developed countries. The most common cancers are breast, lung, bowel and prostate, which are virtually absent in some developing countries. However, even in our affluent society, we also see signs of nutritional inadequacies. For instance, in the UK nearly half of females aged between 11 and 14 are not getting enough iron in their diet, while more than a third are not getting enough zinc (Gregory et al, 2000). We are living in a society where both signs of over- and under- nutrition occur side by side. To correct for these nutritional paradoxes we as consumers have to get the balance of nutrients, energy and physical activity right. The objective of this chapter is to highlight the nutritional role that meat can play in modern society. The National Food Survey for 1999 (Ministry of Agriculture Fisheries and Food, 1999) included a special analysis on meat and meat products consumption in the UK. It stated that ‘meat, meat products...are important contributors to the intakes of many nutrients in the British diet’. Data from this survey showed that meat and meat products supply: energy 15%, protein 30%, fat 22% (SFA 22%, MUFA 27%, PUFA 15%), vitamin D 19%, B 2 14%, B 6 21%, B 12 22%, vitamin A equivalents 20%, niacin 37%, zinc 30%, iron 14%. Meat has been a major part of the human diet for at least 2 million years. Human genetic make-up and physical features have been adapted over 4.5 million years for a diet containing meat. An example of this adaptation is our present teeth and jaw structure, that has developed to become efficient at chewing and swallowing meat. Meat is a highly nutritious and versatile food. The primary importance of meat as a food lies in the fact that when digested its protein is broken down releasing amino acids, which are assimilated and ultimately used for the repair and growth of cells. Meat is a nutrient dense food, providing valu- able amounts of many essential micronutrients. Meat supplies fatty acids, vita- mins, minerals, energy and water and is involved in the synthesis of protein, fat and membranes in the body. Traditionally meat was considered a highly nutritious food, highly valued and associated with good health and prosperity. As such, western societies gradually increased consumption with increasing affluence. The healthy image of red meat gradually became eroded during the 1980s, when research on the role of lipids in heart disease focused attention on the fat contributed from meat. The British Government’s Committee on Medical Aspects of Food and Nutrition (COMA) report on coronary heart disease (CHD) in 1984 identified meat as a major source of saturated fat, contributing a quarter of UK intakes (Committee on Medical Aspects of Food Policy, 1984). Although the multifactorial nature of CHD risk is now widely acknowledged (British Nutrition Foundation,1996; COMA, 1994), the health image of red meat remains tarnished due to this negative association. More recently, we have seen the publication of two reports on diet and cancer (World Cancer Research Fund, 1997; COMA, 1998). These reports associated red meat consumption with increased incidence of certain cancers, in particular, colorectal cancer (CRC), despite the existence of conflicting evidence. Both of these reports issued guidelines on the limits of red meat one should consume, to reduce the risk of developing CRC, which negatively influenced the image of red meat. The 1990s also saw major publicity on non-nutritional issues including animal health concerns such as bovine spongiform encephalopathy (BSE) and more recently the return of foot and mouth disease (FMD) to Britain. The last 25 years have been the most turbulent regarding issues surrounding meat consumption with much of the publicity being negative thus downplaying meat’s nutritional value. 9.2 Meat consumption trends The negative nutritional image that surrounds red meat is in some way respon- sible for the decrease in expenditure. In 1999, 25.8% of expenditure on home food in Great Britain was spent on meat and meat products (Ministry of Agri- culture Fisheries and Food, 1999). This is a significant drop compared with 32.1% in 1979. During this time period there have been major changes in the type of meat that people are buying in the UK. Expenditures on beef, lamb, pork, bacon and ham each fell, whilst expenditure shares on poultry and on other meats have risen. The major growth area in processed meats and meat products has been frozen convenience meat products, meat based ready meals and other meat prod- ucts such as Chinese and Italian meals containing meat (Ministry of Agriculture 210 The nutrition handbook for food processors Fisheries and Food, 1999). There are many factors responsible for these changes, the tarnished image of red meat being one such. Other influencing factors include changes in lifestyle trends which saw the drive for convenience foods, and the resultant responsiveness of the industry to this has greatly influenced the chang- ing meat-buying habits of consumers. 9.3 Cancer Meat consumption has been implicated in many cancers, as being either protec- tive or causative, depending on the type of cancer. Meat consumption has been shown to protect against cancers of the stomach (Hirayama, 1990; Tuyns et al, 1992; Azevedo et al, 1999), liver and the oesophagus (Zeigler et al, 1981; Tuyns et al, 1987; Nakachi et al, 1988). These are three of the top five cancers globally. On the other hand, meat consumption has been implicated as a cause of colorectal (colon and rectal), breast and prostate cancer, with the main emphasis being on CRC. CRC is the fourth most common cancer in the world, but in Europe and other Western countries it is second in terms of incidence and mortality (after lung cancer in men and breast cancer in women) with 190 000 new cases per year in Europe (Black et al, 1997; Bingham, 1996). There is strong evidence from epi- demiological studies showing that diet plays an important role in most large bowel cancers, implying that it is a potentially preventable disease (Higginson, 1966; COMA, 1998). The precise dietary components that influence CRC risk have not been fully elucidated. However, epidemiological studies suggest that high intakes of fat, meat and alcohol increase risk, whereas vegetables, cereals and non-starch polysaccharides, found in fruit and many other foods, decrease the risk (Bingham, 1996). For many of these dietary factors the evidence is equivo- cal. In the case of meat, the evidence is conflicting, early cross-sectional com- parisons attributed much of the world-wide variation in CRC incidence to fat and animal protein consumption (Armstrong and Doll, 1975). In contrast, subsequent case-control and cohort studies are much less consistent (Hill, 1999a). Meat consumption and CRC became a high profile issue during 1997 and 1998 with the global launch of the World Cancer Research Fund report (WCRF, 1997), timed to coincide with the publication of the British COMA report, both on diet and cancer. The WCRF report was particularly negative towards red meat, which fuelled the launch publicity. This stimulated several critical appraisals of the report, all challenging the conclusions regarding meat (Hill, 1999b). The scien- tific evidence is not sufficiently robust to recommend a maximum of 80 g/day red meat as pronounced by the WCRF and the initial announcement by COMA for a similar recommendation was subsequently revised. Most of the data show- ing an association between meat consumption and CRC are American, whereas several studies conducted outside the US (many in Europe) have shown no such relationship (Hill, 1999a). On final publication, COMA (1998) reassured UK consumers that average consumption levels (90 g/day of cooked red meat) were acceptable. COMA suggests that high consumers, less than 15% of the UK popu- Enhancing the nutritional value of meat 211 lation, eating above 140 g/day might benefit from a reduction. Equally impor- tantly, this report acknowledged that meat and meat products remain a valuable source of a number of nutrients including iron and that for many a moderate intake makes an important contribution to micronutrient status. The potential effect on iron status of further reductions to red meat intakes was subsequently investi- gated, as recommended within the COMA report. Given that a 50% reduction in intake would result in a third of women having low iron intakes (below 8 mg/d), the appropriateness of public health messages concerning meat consumption should be carefully considered prior to reaching the media (Gibson and Ashwell, 2001). Various components of meat (protein, iron, and heterocyclic amines) have been suspected of contributing to the development of CRC. Dietary protein is broken down in the body to amino acids, which are further degraded to ammonia, which may have cancer-initiating effects. The human colon is also rich in amides and amines that are substrates for bacterial nitrosation by nitric oxide (NO) to N- nitroso compounds that are found in human faeces. There is no conclusive evi- dence that protein derived compounds can increase cancer risk in humans. It is hypothesised, but not yet established, that the intake of iron from meat and other iron-rich foods may increase the risk of cancer via the production of free radi- cals in the body. Heterocyclic amines are formed by the Maillard reactions that involve amino acids, sugars and creatine during cooking. They are usually pro- duced on the surface of meat during cooking at very high temperatures, such as in frying, grilling or barbecuing but they are minimal when meat is steamed, microwaved or marinated. The heterocyclic amines are known mutagens in vitro and carcinogens in rodents. The most abundant heterocyclic amine produced in meat is phenylimadazo pyridine (PhIP), which is a relatively weak carcinogen compared to other heterocyclic amines such as IQ and MeIQ. The role of hete- rocyclic amines in causing CRC is not fully elucidated in humans. Truswell summarised the evidence in 2000 and showed that 20 out of 30 case- control studies and 10 out of 14 prospective studies showed no relationship between meat intake and CRC with some of the results of the remaining studies being confused and one prospective study showing an inverse correlation between meat consumption and CRC risk (Hill, 2000). If meat consumption were associ- ated with increased risk for cancer, one would expect mortality from cancer to be much lower among vegetarians. In a recent meta-analysis of five cohort studies, results have shown no significant differences in mortality from cancer in general, and more specifically mortality in stomach, breast, lung, prostate and colorectal cancer between vegetarians and omnivores (Key et al, 1998, 1999). If red meat consumption were associated with increased risk for CRC, one would expect a decrease in the incidence of CRC to occur over time as a result of decreasing meat consumption trends. During the past 30 years, red meat con- sumption in the UK has decreased by approximately 25%, while during the same time the incidence of CRC has increased by about 50% (Hill, 1999b). Similarly, if meat consumption were associated with increased risk for CRC, one would 212 The nutrition handbook for food processors expect the rates of CRC to be higher in countries with high meat consumption and lower in countries with low meat consumption. People in the Mediterranean countries eat more red meat than do, for instance, the inhabitants of the UK, yet these countries have lower CRC rates (Hill, 2000). Such paradoxical findings are further evidence that, at current levels, meat consumption is not a risk factor for CRC incidence. Epidemiological associations between dietary components, specific foods or food groups and chronic disease, such as cancer, can identify risk factors, but are generally insufficient to establish cause and effect relationships. Findings from epidemiological studies must be combined with other types of evidence (e.g. animal experiments, human clinical trials) before a persuasive causal relation- ship can be established. CRC is multi-factorial; it is confounded by diet, smoking, alcohol, physical activity, obesity, aspirin use, age and family history. There are known protective and causative factors. It is well-known that daily consumption of vegetables and meat reduces the risk of cancer at many sites, whereas daily meat consumption with less frequent vegetable consumption increases risk (Hirayama, 1986; Kohlmeier et al, 1995; Cox and Whichelow, 1997). Evidence suggests that it is the reduced intakes of the protective factors such as vegetables and cereals that are the main determinants of CRC risk with meat being coinci- dentally related. There is a need to assess the role of meat when consumed in normal quanti- ties, by normal cooking methods, and within the context of a mixed, balanced, diet. The method of cooking meat and the degree of browning are of particular importance to this whole issue. A major effort by International Meat Industry partners has attempted to raise awareness of the complexities of meat prepara- tion and cooking habits and how these differ between countries. Dietary assess- ment techniques adopted by nutrition scientists currently do not take full account of the diverse differences between meat products world-wide and the consequent influences these may have on the body. For example, it is well recognised that meat is often cooked more evenly through the muscle within Europe, whereas it tends to be ‘blackened’ on the outside whilst remaining rare on the inside in North America. This may be one reason for the greater negative findings in American studies of the role of meat in CRC, compared with European studies. This hith- erto unexplored facet of meat consumption may have far-reaching implications for interpretation of epidemiological data and ultimately for public health rec- ommendations. Certain marinades applied to meat before cooking will reduce the quantity of potential carcinogenic materials present. The application of knowl- edge in this area to the production of processed meat products with all the nutri- tional benefits and none of the potentially harmful components would be pro- gressive indeed. In summary, it is important not only to examine the relationship between meat consumption and CRC alone, but also to look at meat preparation and cooking differences in conjunction with protective factors, such as vegetables and cereals. At a meat and diet workshop, it was stated: Enhancing the nutritional value of meat 213 It is time that the meat CRC story was laid to rest, so that we can get back to recommending that young women of childbearing age eat meat as a ready source of available iron. (Hill, 2000) Nevertheless, it is sensible to consider that there must be an optimal range for meat intakes in order to ensure a balanced diet is achieved whilst optimal weight is maintained. From this practical perspective COMA’s (1998) suggested intake range of 90–140 g cooked meat per day is sensible as a public health message. The overemphasis on reducing meat, however, rather than encouraging greater accompanying plant food intake has served only to confuse the public (Hill, 1999b). Evidence suggests that the risk of cancer will be reduced to a greater extent by increasing intakes of fruit and vegetables than by lowering meat intakes. Once again, the move towards pre-prepared meal solutions provides opportunity for manufacturers to develop recipes with a healthy balance of meat and veg- etable ingredients such that the nutritional profile of the dish is optimised. 9.4 Concerns about fat Regular consumption of red meat is associated epidemiologically with increased risk of coronary heart disease, due to its fat composition. Conversely, a growing bank of evidence is showing that a healthy diet that includes lean red meat can produce positive blood lipid changes (Watts et al, 1988; Scott et al, 1990; Davidson et al, 1999; Beauchesne-Rondeau et al, 1999). Blood cholesterol levels are increased by inclusion of beef fat, not lean beef in an otherwise low-fat diet. Equal amounts of lean beef, chicken, and fish added to low fat, low saturated fat diets, similarly reduce plasma cholesterol and LDL-cholesterol levels in hyper- cholesterolaemic and normocholesterolaemic men and women. Meat is a source of arachidonic acid (20:4n-6), both in the lean and visible fat components (Duo et al, 1998). Assumptions that the 20:4n-6 content of meat was responsible for increasing thrombotic tendencies in Western societies are too sim- plistic. The presence of large amounts of linoleic acid (18:2n-6) in current diets results in plasma increases of linoleic and arachidonic acids only. However, in the absence of linoleic acid, the long chain n-6 and n-3 PUFAs present in lean meat can influence the plasma pool, increasing plasma eicosatrienoic acid (20:3n- 6), 20:4n-6, and eicosapentanoic acid (20:5n-3), and probably reducing throm- botic tendencies. It is the imbalance of n-6: n-3 PUFAs in the diet, brought about by excessive 18:2n-6, that causes high tissue 20:4n-6 levels, so encouraging metabolism to eicosanoids (Sinclair et al, 1994; Mann et al, 1997). Meat contributes between a third and a half of the UK daily cholesterol intake (Chizzolini et al, 1999; British Nutrition Foundation, 1999). Meat’s cholesterol content is, for consumers, another negative influence on meat’s health image, although it is now accepted that dietary intake of cholesterol has little bearing on plasma cholesterol. A review of the cholesterol content of meat indicates sur- prisingly that levels of cholesterol are generally not higher in fatty meat or meat 214 The nutrition handbook for food processors products. The cholesterol content of a meat is related to the number of muscle fibres so tends to be higher the more red the muscle. 9.5 Reductions in the fat content of red meat Twenty years ago red meat and meat products were identified as major contri- butors to fat intake in the UK. Most of the visible (subcutaneous) fat in the meat was consumed. In the early 1980s the red meat industry began to shift produc- tion systems to favour less fat, reflecting more energy-efficient animal husbandry. For many years now there has been emphasis on reducing the fat content of our diets and this continued consumer demand for less fat further prompted the meat industry to consider ways of reducing the fat content of meat. The fat content of the carcase has been reduced in Britain by over 30% for pork, making British pork virtually the leanest in the world, 15% for beef and 10% for lamb, with further reductions anticipated for beef and lamb over the next 5–10 years. The fat content of fully trimmed lamb, beef and pork is now 8%, 5% and 4% respec- tively (Chan et al, 1995). These achievements are due to three factors: selective breeding and feeding practices designed to increase the carcase lean to fat ratio; official carcase clas- sification systems designed to favour leaner production; and modern butchery techniques (seaming out whole muscles, and trimming away all intermuscular fat). It is easier to appreciate the process and extent of fat reduction by looking at the changes over time for a single cut of meat such as a pork chop (Fig. 9.1). The reduction in fat for pig meat is well illustrated by the trend downwards in P 2 fat depth between the 1970s and the 1990s (P 2 is fat depth at the position of the last rib) (Fig. 9.2). Since 1992 it has remained stable at around 11 mm. Although updated compositional figures for British meat were published from 1986 onwards (Royal Society of Chemistry, 1986; 1993; 1996; Meat and Livestock Commission and Royal Society of Chemistry, 1990), it is only since updated supplements to the McCance and Widdowson tables were published in 1995 (Chan et al, 1995 and 1996), that the achievement of the meat industry in reducing the fat content of meat has been more widely acknowledged (Depart- ment Of Health, 1994b; Scottish Office, 1996; Higgs, 2000). A fat audit for the UK, commissioned by the Government’s Ministry of Agri- culture, Fisheries and Food to trace all fat in the human food chain provides a more accurate picture than National Food Survey (NFS) (Ministry of Agriculture, Fisheries and Food, 1981–99) data for identifying principal sources of fat in the diet, between 1982 and 1992 (Ulbricht, 1995). It illustrates that whereas the fat contributed by red meat decreased by nearly a third, that from fats and oils as a group increased by a third to contribute nearly half of our fat intakes (Fig. 9.3). This striking picture is lost in NFS data since vegetable fats (in particular) are consumed within a broad range of end products – from chips (so here they are hidden within the vegetables section) to meat products (so here they artificially inflate the apparent fat contributed by meat). Enhancing the nutritional value of meat 215 216 The nutrition handbook for food processors 30 21.3 19.5 7.9 3.9 3.5 1950s – 1970s 1990s Breed and feed changes Cutting plant and retail trimming Modern butchery Traditional butchery Seam cutting Further cooking loss lean + intermuscular fat only fully trimmed lean only fully trimmed lean only Total back fat trim Trimming, cooking loss and plate waste Fig. 9.1 Change in fat content of pork loin for 100 g of raw edible tissue. (Adapted from Higgs JD and Pratt J, 1998) (McCance and Widdowson, 1940, 1960, 1978; Royal Society of Chemistry, 1995; MLC/RSC report to MAFF, 1990) 1972747678808284868890921994 Year 5 10 15 20 25 P 2 (mm) Fig. 9.2 Average P 2 fat depth of British slaughter pigs 1972–1995. The fat content of meat products can vary considerably, dependent on the pro- portion of lean and fat present and the amount of added non-meat fat (Higgs and Pratt, 1998). Traditional types such as sausages, pastry-covered pies and salami are high in fat (up to 50%) but modern products include ready meals and pre- pared meats that can be low in fat (5%). The trend downwards in fat for red meat is reflected in the reduced fat content of a number of meat products, such as hams and sausages. Some reduced-fat meat products are now available although the potential for product development in this area has not been fully exploited. 9.6 Fatty acids in meat The fatty acid composition of food, including meat, has become increasingly important in recent years because of concerns with the effects they have on human Enhancing the nutritional value of meat 217 24 20 16 12 8 4 0 1982 1992 Year Dietary fat kg Dairy fat Fats and oils Red meat Fish Eggs Chocolate Poultry meat Cereals Nuts Fig. 9.3 Total fat available for consumption (UK) from different food sources. (Ulbricht TLV, 1995) health. Fatty acids play a role in many conditions such as CHD, cancer, obesity, diabetes and arthritis. These roles can be protective, causative or relatively neutral, depending on the disease, the fatty acid, and the opposing effects of other dietary components. Current dietary advice emphasises balancing the intake of the different fatty acids. The Department of Health (COMA, 1994) has recom- mended a reduction in the intake of saturated fat and an increase in the intake of unsaturated fat. Within the unsaturated fatty acids it is recommended to increase the omega-3 (n-3) PUFAs relative to the omega-6 (n-6) PUFAs. 9.6.1 Saturated fatty acids Probably the main misconception about meat fat is that it is assumed to be totally saturated. Meat contains a mixture of fatty acids both saturated and unsaturated and the amount of saturated fat in meat has been reduced in recent years. At the present time, less than half the fat in pork and beef and 51% of the fat in lamb is saturated. The saturated fat contributed to the diet from red meat and meat products has gradually fallen from 24% in 1979 to 19.6% in 1999. Carcase meats now provide 6.7% of total saturated fat intake (Ministry Of Agriculture Fisheries And Food, 1981). In reality, even this figure is an overestimate, since there is a disproportionate wastage in terms of trimming, cooking losses and plate waste (Leeds et al, 1997). The predominant saturated fatty acids in meat are stearic acid (C18:0) and palmitic acid (C16:0). In general terms, saturated fats are known as the ‘bad’ fats as they tend to raise blood cholesterol and cause atherosclerosis. However, not all saturated fats are equal in their effects on blood cholesterol. For instance, stearic acid does not appear to raise blood cholesterol (Bonanome and Grundy, 1988) or other thrombotic risk factors (Kelly et al, 1999, 2001). Stearic acid is a prominent saturated fat in meat, for example; it accounts for approximately one third of the saturated fat in beef. Similarly, palmitic acid, another major saturated fat in meat does not consistently raise blood lipids. On the other hand, myristic acid (C14:0) is the most atherogenic fatty acid, having four times the cholesterol raising potential of palmitic acid (Ulbricht, 1995). Myristic acid is found only in minor quantities in meat. 9.6.2 Monounsaturated fatty acids Meat contains a mixture of unsaturated fatty acids, polyunsaturated fatty acids and monounsaturated fatty acids (MUFAs). MUFAs are the dominant unsaturated fatty acid in meat and they account for approximately 40% of the total fat in meat. It is a neglected fact that meat and meat products are the main contributors to MUFAs in the British diet, supplying 27% of total MUFA intake (Ministry Of Agriculture Fisheries And Food, 1999). MUFAs are considered to be neutral with respect to blood cholesterol levels. The principal MUFA in meat is oleic acid (cis C18:1n-9), which is also found in olive oil and is associated with the healthy Mediterranean diet. 218 The nutrition handbook for food processors 9.6.3 Polyunsaturated fatty acids The PUFAs have a structural role because they are found in the membrane phos- pholipids and they are also involved in eicosanoid synthesis. There are two types of polyunsaturated fatty acids, the omega-3 (n-3) and the omega-6 (n-6). Meat and meat products supply 17% n-6 and 19% n-3 PUFA intake (Gregory et al, 1990). Linoleic acid (C18:2 n-6) and a-linolenic acid (C18:3n-3) are essential fatty acids as we cannot synthesise them ourselves, so we are dependent on diet to provide them. In the body these are further elongated and desaturated to longer chain derivatives, arachidonic acid (C20:4n-6), docosapentaenoic acid (C22:5n- 6), eicosapentaenoic acid (C20:5n-3) and docosahexaenoic acid (C22:6n-3). These are found in useful quantities in meat. Over the past 30 years there has been a major shift in the intakes of the different fatty acids and the saturated fats have been replaced by the unsaturated fats. The increase in the unsaturated fatty acids was mainly due to an increase in n-6 fatty acids as a consequence of replac- ing vegetable oils for animal fat. Today, the usual Western diet contains 10–20 times more n-6 than n-3. For instance, in Britain, the n-6 PUFA intake is now responsible for 87.5% of total PUFA intake, the remainder being the n-3 PUFAs. However, evidence now indicates that it is the n-3 PUFAs which are cardioprotective, in particular, the very long chain n-3 PUFAs, eicosapentaenoic acid (C20:5n-3) and docosahexae- noic acid (C22:6n-3). The GISSI trial showed that 1 g of eicosapentaenoic acid (C20:5n-3) and docosahexaenoic acid (C22:6n-3) daily reduced coronary heart disease deaths by 20% (GISSI, 1999). The exact mechanism for this effect is not clear but they may reduce blood cholesterol. Other beneficial effects of the very long chain n-3 PUFAs include anti-inflammatory and anti-tumourigenic proper- ties. Docosahexaenoic acid (C22:6n-3) also plays a role in neuronal development, cognitive function and visual acuity. It appears that newborn babies have a reduced ability to make the longer chain derivatives and docosahexaenoic acid (C22:6n-3) is an essential fatty acid for the newborn. Meat and fish are the only significant sources of preformed very long chain n-3 PUFAs in the diet. The chief sources of n-3 PUFAs are oily fish and fish oils, however, only one third of the UK population consume oily fish weekly. It is unsurprising, then that in the UK, meat and meat products supply more n-3 PUFAs (19%) than do fish and fish dishes (14%) (Gregory et al, 1990). In a report on n-3 fatty acids the British Nutrition Foundation summarised this fact with the following statement: ‘red meat is likely to rival fish as a source of n-3 PUFAs in many people’s diet’ (BNF, 1999). Animals can convert a–linolenic acid to 20- and 22-carbon n-3 PUFAs but plants cannot, hence, there are no long chain PUFAs in vegan diets. Diets, which exclude meat and fish, such as vegetarian diets, are practically devoid of very long chain n-3 PUFAs. Vegans rely solely on the endogenous synthesis of very long chain n-3 PUFA from a–linolenic acid. This fact is verified by studies that have shown that vegetarians have lower n-3 PUFA intake than their omnivore counterparts. This imbalance may have nutritional consequences for vegans and vegetarians. For instance, results from a recent observation study showed that the Enhancing the nutritional value of meat 219 n-3 :n-6 ratio in plasma phospholipids was significantly lower among ovo lac- tovegetarians and vegans compared with meat eaters and this may be respon- sible for an increased platelet aggregation tendency among vegetarians, which is a risk factor for cardiovascular disease (Li et al, 1999). Meat is already a valuable source of n-3 PUFAs among omnivores, thus any further increase in the n-3 PUFA content of meat will make useful contributions to their overall intakes. Nowadays, researchers are looking at ways to enhance the n-3 PUFA content of meat. Feeding trials of cattle, pigs and sheep have shown dietary modification to be successful in raising n-3 PUFA content of their meats. The n-3 PUFA content of meat can be enhanced by increasing the amount of n- 3 PUFAs in the diet of the animal. For instance, grass is rich in a-linolenic acid (C18:3n-3) and grass-fed meat has a higher n-3 fatty acid content than has grain- fed meat (Enser et al, 1998). Similarly, experiments have shown that including fish oil, marine algae, oils and oilseeds, such as linseed, which are rich sources of n-3 PUFAs, in the animals’ diet can enhance favourably the n-3 content of the resultant meat. Enhancing the n-3 PUFA content of meat is much easier to achieve in monogastrics, such as pigs and poultry, than in ruminants. In the rumen, the dietary unsaturated fatty acids are susceptible to biohydrogenation. Biohydro- genation is a process that occurs in the rumen where the dietary unsaturated fatty acids are hydrogenated by ruminant microorganisms to more saturated end prod- ucts. Evidence indicates that some unsaturated fatty acids appear to be more resis- tant to biohydrogenation than others. Examples include the very long chain n-3 PUFAs. However, more research is required to clarify this issue. Researchers are looking at ways to overcome biohydrogenation in ruminants by protecting the n- 3 PUFA. Altering the fatty acid composition of meat can have negative impacts on the meat quality, its shelf-life, colour and flavour. Therefore animal scientists, food technologists and nutritionists are looking at ways to improve the nutritional quality of meat by enhancing its n-3 PUFA content without causing any adverse sensory qualities or negatively affecting its shelf-life. The Department of Health (1994b) has issued guidelines regarding the rec- ommended intake of saturated and polyunsaturated fats. The current recommen- dation for the polyunsaturated :saturated ratio (P :S ratio) is about 0.4. Pork has a higher P :S ratio whereas the P :S ratios of lamb and beef are lower (Table 9.1), as a consequence of biohydrogenation. The Department of Health (1994b) has also issued an index regarding the ratio of n-6 :n-3 PUFAs. The recommended value for this ratio (n-6 :n-3) is less than 4. The n-6 :n-3 ratios of trimmed beef, lamb and pork are approximately 2.2, 1.3 and 7.5, respectively (Table 9.1). There- fore, both beef and lamb have acceptable n-6 :n-3 ratios whereas that for pork needs to be reduced to reach acceptable values. The high n-6 :n-3 ratio in pork is due to significant amounts of linoleic acid (C18:2 n-6) present in its adipose tissue (Enser et al, 1996). In summary, researchers are focusing on ways of enhancing the n-3 PUFA content of meat and meat products. However, when increasing the n-3 fatty acid composition of ruminant meats such as beef and lamb, they are focusing on ways to increase the P :S ratio whilst retaining the positive n-6 :n-3 ratio. On the other hand, for monogastric meat, such as pork, 220 The nutrition handbook for food processors the n-3 PUFA content should be increased, whilst maintaining its positive P :S ratio. Many of the results to date are promising; for instance, beef and lamb liver from animals raised on grass are particularly good sources of n-3 PUFAs with the n-6 :n-3 being 0.46 (Enser et al, 1998). Such data highlights the potential for carcase meat with improved fatty acid composition as a highly acceptable and effective vehicle for providing optimal fatty acid intake for the consumer. 9.6.4 Conjugated Linoleic Acid (CLA) Another emerging dietary benefit for meat, in particular ruminant meat, is the existence within it of conjugated linoleic acid (CLA). CLA is a fatty acid that occurs naturally in ruminant meats such as beef and lamb. The acronym CLA is a collective term used to describe a mixture of positional (7,9-; 8,10-; 9,11-; 10,12- or 11,13-) and geometrical (c,c-; c,t-; t,t- or t,c-) isomers of linoleic acid (9c,12c-18:2). CLA has the same chain length as linoleic acid (18C), but in CLA the double bonds are conjugated. Conjugated double bonds are separated by only one single carbon bond. The c9-t11-18:2 isomer (rumenic acid) is the predomi- nant isomer of CLA (Kramer et al, 1998). This isomer has been shown to account for at least 60% of total CLA in beef (Shantha et al, 1994; O’Shea et al, 1998). Factors influencing the CLA content of meat include the breed, age and diet of the animal (O’Shea et al, 1998; Mulvihill, 2001). As well as having a high n-3 PUFA content, grass-fed meat also has higher CLA content (Shantha et al, 1994). Since, CLA is formed predominately in the rumen, the CLA content of ruminant meat, beef and lamb, is much higher than non-ruminant meat such as pork, chicken and game (Chin et al, 1992). The best natural dietary sources of CLA are ruminant products such as beef and lamb (Ma et al, 1999). Meat and meat products supply approximately a quarter of dietary CLA in Germany (Fritsche and Steinhart, 1998). Enhancing the nutritional value of meat 221 Table 9.1 Fatty acid ratios related to healthy nutrition Source of meat Sample P:S n-6 :n-3 Beef Muscle 0.11 2.11 Beef Adipose tissue 0.05 2.30 Beef Steak 0.07 2.22 Lamb Muscle 0.15 1.32 Lamb Adipose tissue 0.09 1.37 Lamb Chop 0.09 1.28 Pork Muscle 0.58 7.22 Pork Adipose tissue 0.61 7.64 Pork Chop 0.61 7.57 Values for steaks and chops calculated for whole cut as purchased. Adapted from Enser et al (1996) ‘Fatty acid content and composi- tion of English beef, lamb and pork at retail.’ Meat Science 42(4): 443–56. CLA appears to have a variety of potential health benefits. It has been shown to have tumour reducing (Belury, 1995; Ip and Scimeca, 1997; Ip et al, 1991, 1994, 1999) and atherosclerotic reducing properties (Lee et al, 1994; Nicolosi et al, 1997; Gavino et al, 2000). CLA may also reduce adiposity (Park et al, 1997; West et al, 1998) and delay the onset of diabetes (Houseknecht et al, 1998). The different isomers of CLA appear to be responsible for its differing biologi- cal effects. For instance, the c-9,t-11 isomer may play an anti-carcinogenic role, while the t-10,c-12 isomer appears to play a role in reducing adiposity. So far, most of the research work demonstrating the health benefits of CLA has been conducted in experimental animals or cell culture models. The jury is still out for its effect on human health. The American Dietetic Association has endorsed beef and lamb as functional foods because of the anti-tumourigenic properties of the CLA they contain (ADA, 1999). We are just beginning to understand fully the effect(s) that CLA has on human health and the role that meat plays in its dietary provision. In a review, Mulvihill (2001) raised a number of questions that need to be answered to improve our knowledge about CLA in meat. They include: how is CLA formed in the rumen? can this be regulated? what CLA isomers are in meat? and can meat consumption influence CLA levels in the human body? 9.6.5 Trans-fatty acids Trans-fatty acids raise LDL cholesterol and decrease HDL cholesterol. It is rec- ommended by the Department of Health (1991) that trans-fatty acids contribute less than 2% of total energy. Ruminant meats are a source of trans-fatty acids, contributing around 18% of total intakes. These are formed during biohydro- genation in the rumen. In the British diet the main source of trans-fatty acids are cereals and cereal products and fat spreads which use partially hydrogenated veg- etable and fish oils in their products. Other significant sources include ruminant meat and milk (Gregory et al, 1990). It appears from the analysis of 14 European countries that the fat content of meat does not correlate with the percentage of trans-fatty acid content (Hulshof et al, 1999). Trans-fats have been highlighted as contributing to atherogenesis, although the hydrogenated fats from vegetable sources used in bakery goods and other processed foods appear to be more of a concern than the natural tran-fats found in ruminant meats and milk fat (British Nutrition Foundation, 1995). After assessing the intake of trans-fatty acids in 14 European countries (TRANSFAIR study), the conclusion was that the current intake of TFA in most Western European countries including the United Kingdom does not appear to be a reason for major concern (Hulshof et al, 1999; van de Vijver et al, 2000). In fact, the TRANSFAIR study showed that intakes of trans- fatty acids did not influence LDL and HDL cholesterol and a weak inverse asso- ciation was found in total serum cholesterol (van de Vijver et al, 2000). In the USA, where there is a much greater reliance on processed foods, the consequent higher intakes (6% dietary energy) of non- ruminant trans-fatty acids are causing some concern. 222 The nutrition handbook for food processors 9.6.6 Cholesterol Much research has looked at the effect that individual fatty acids have on blood cholesterol rather than the mixture that we digest. It is now obvious that we should be looking at the effect that diet as a whole has on blood cholesterol. In the United States, the National Cholesterol Education Program (NCEP) recommends dietary guidelines for people with hypercholesterolaemia (raised blood cholesterol). The NCEP dietary guidelines are a first-line therapy for the management of high blood cholesterol. A recent study compared the differing effects of lean red meat (beef, veal and pork) and lean white meat (poultry and fish) in the NCEP diet on blood cholesterol of people with hypercholesterolaemia (Davidson et al, 1999). This study showed that the inclusion of approximately 170 g lean red meat per day, five to seven times per week in the NCEP diet was as effective as lean white meat in reducing both total and LDL cholesterol while simultaneously raising HDL cholesterol. Thus the inclusion of lean red meat in such a diet had a posi- tive impact on blood cholesterol levels. The authors also indicated that the study participants who consumed the lean red meat were more likely to follow their dietary regimen as they had a wider food choice than those on the white meat diet. This study not only highlights the nutritional value of red meat in such a diet but also the practical value, as no diet can possibly work unless it is adhered to! An earlier study conducted in the United Kingdom showed similar results, where mildly hypercholesterolaemic men ate 180 g of lean meat every day, a quantity we would consider high today. This diet was low fat, low saturated fat and high in PUFA and it proved to be effective in lowering total and LDL cho- lesterol (Watts et al, 1988). In Canada, a study was conducted comparing the effects of lipid lowering diets containing lean beef, poultry (without skin) and lean fish on plasma cholesterol levels in men with raised blood cholesterol. The results indicated that when compared to the usual diet, the lean beef and poultry diets significantly reduced both total cholesterol and LDL (‘bad’) cholesterol in men with raised blood cholesterol. Whereas in the fish containing diet, only total cholesterol levels fell significantly when compared to the usual diet (Beauchesne- Rondeau et al, 1999). There is now a wealth of studies showing similar results (Scott et al, 1990; Mann et al, 1997; Davidson et al, 1999), which are not that surprising, as lean red meat is low in fat, low in SFA and contains a mixture of beneficial unsaturated fatty acids, such as linoleic acid, n-3 PUFAs, MUFAs and CLA. 9.7 Protein Protein is the basic building material for making cells and its adequate intake can be of particular benefit for growing young people or in adults where muscle tissue is being rebuilt, such as athletes or those recuperating after surgery. Meat is a good source of protein and it contains all the essential amino acids. In the United Kingdom, meat and meat products supply 30% of dietary protein intakes (Min- Enhancing the nutritional value of meat 223 istry Of Agriculture Fisheries And Food, 1999). Emphasis on a prudent diet for health that recommended just 11E% (National Advisory Committee on Nutrition Education, 1983) from protein has led us to underplay the potential role of high protein foods in the diet. Recent interest in the use of high protein diets (25E%) for weight reduction have utilised the higher satiating properties of protein, important for dietary compliance, and achieved significantly more weight loss over a 6 months dietary intervention compared to lower (12E%) protein. These results were achieved without adverse effects on renal function (Skov et al, 1999a, 1999b). Meat protein has a higher biological value than has plant protein because some of the amino acids are limiting in plant protein. For example, lysine is the limit- ing amino acid in wheat, tryptophan is the limiting amino acid in maize and sulphur-containing amino acids are limiting in soyabean. It is necessary for vegans and vegetarians to eat a wide variety of vegetable protein foods to provide the necessary amounts of each amino acid. Meat is a rich source of taurine. Taurine is considered to be an essential amino acid for newborns, as they seem to have a limited ability to synthesise it. Taurine concentrations in the breast milk of vegans were shown to be considerably lower than in omnivores (Rana and Sanders, 1986). The significance of this finding is unknown. 9.8 The functionality of meat Typical Western omnivorous diets over the last 40 years have been relatively high in protein and fat with insufficient dietary fibre, fruit and vegetables. Meat intake is by definition the key difference between vegetarian and omnivorous diets, thus comparative studies have tended to exaggerate the health benefits of a vegetar- ian diet so reinforcing a negative health image for meat. It has long been recog- nized (Burr, 1988) that although vegetarianism seems to confer some protection against heart disease, it is not clear if this is due to abstinence from meat or high consumption of vegetables. Meat intake has provided a marker for a generally ‘unhealthy’ diet in the past (American Dietetic Association, 1993; COMA, 1991; Sanders and Reddy, 1994; Thorogood, 1994). Furthermore, vegetarians have tended to be more health conscious, they traditionally smoke less, consume less alcohol, tea, and coffee, and tend to exercise more, thus their good health could be attributed to any or a combination of these habits. CHD and cancer are mul- tifactorial; diet is one factor playing a role in these conditions, but diet alone is a very broad term, because within diet there are protective and causative factors. Comparing current omnivorous and vegetarian diets shows that the meat content of the former is not responsible for its higher fat content. Australian research has shown that when the meat component was removed from an omnivore diet, the remaining part of the diet was still significantly higher in total fat, saturated fat and cholesterol than was a vegetarian diet (Li et al, 1999). This suggests that the overall diet rather than the meat is responsible for these diet characteristics. The significance of meat to nutrient intake depends on the importance given 224 The nutrition handbook for food processors to meat in an individual’s, or in a society’s diet and culture. With a limited range of foods available in primitive societies throughout history, meat provided a concentrated source of a wide range of nutrients (Davidson and Passmore, 1969; Sanders, 1999). Considering the diet of modern man, where meat is excluded within traditional vegetarian cultures, the nutrients it provides can be supplied from a combination of other foods and this appears at least adequate, provided the diet is not too restrictive and dependent on nutritionally inferior staples such as maize or cassava (Sanders, 1999). With the range and abundance of foods avail- able to developed societies today, the nutritional significance of any one food is reduced. Traditionally, the vegetarian was likely to consume a wider range of foods than the meat eater. Consequently, vegetarians in Europe and North America his- torically had similar energy intakes to meat eaters and greater intakes of vitamins B 1 , C, E, folic acid, b-carotene, potassium and fibre (Sanders, 1999). Today, veg- etarianism cannot be assumed to provide a favourable fatty acid intake. Com- parative studies of vegetarian and omnivorous children surveyed from 9 to 17 years old found that saturated fat intakes were no lower in the vegetarian chil- dren (Nathan et al, 1994; Nathan et al, 1997; Burgess et al, 2001). There was no significant difference between energy intakes and the percentage energy from fat, or saturated fat intakes between vegetarian and omnivore adolescents in north- west England (Burgess et al, 2001). Vegetarian women have lower zinc intakes and status than their omnivore counterparts (Ball and Ackland, 2000). A recent study in Australia showed vegetarians had a lower intake of beneficial very long chain n-3 PUFAs (Li et al, 1999). A study comparing meat eaters with vegetari- ans has shown that levels of plasma homocysteine, an independent risk factor for heart disease, among vegetarians were significantly higher than their omnivore counterparts, and this was correlated with a lower intake of vitamin B 12 among the vegetarians (Mann et al, 1999; Krajcovicova-Kudlackova et al, 2000; Mann 2001b). Vegans have significantly lower intakes of protein, vitamin D, calcium, and selenium but no difference in energy and iron intakes from those of omni- vores and the vegans have significantly lower vitamin B 12 blood concentration (Larsson and Johansson, 2001). Modern eating habits contribute to erosion of the traditional vegetarian diet in developed countries because there is now a greater dependence on vegetarian convenience foods, coinciding with increased availability and choice. Whilst veg- etarian convenience foods may appear attractive in terms of health as well as for ease and speed of preparation, they are not necessarily of superior nutritional value compared with meat-containing equivalents. There is wide variation in the fat content of vegetarian products, ranging from 2% to 58%, with nearly a third supplying more than 50% of their energy from fat (Reid and Hackett, 2001). Excluding meat whilst paying little attention to selecting appropriate alterna- tive food combinations, to ensure adequate nutrients are supplied, is cause for concern, especially in children and adolescents. Today’s busy lifestyles give rise to more erratic dietary practices making it easier to obtain all nutrients required for health by including meat as a component of the diet. The time spent planning Enhancing the nutritional value of meat 225 and preparing meals is minimal and an increasing proportion of our daily food intake is consumed outside the home as snacks and quick meals. NFS data suggest that in 1998 28% of total expenditure on food and drink was outside the home (MAFF, 1999). Data on the dietary intakes and nutritional status of young people aged between 4 and 18 years in Britain show that energy intakes of young people are now approximately 20% below estimated average requirements (EAR) for age. Growth patterns suggest such intakes are adequate and merely reflect the corresponding lower activity levels of youngsters today, which in itself is a con- cern. Reduced energy intakes must increase the emphasis on a more nutrient dense diet, particularly in growing children. The survey has recorded intakes of iron, zinc and copper below the RNI particularly in older girls (Gregory et al, 2000). It is possible that the recorded lower meat intakes are partly responsible for this. The decision to become vegetarian should be accompanied by adequate nutritional information and education. Despite popular opinion, vegetarianism per se does not guarantee a nutritionally adequate diet. Conversely, using meat as a significant protein source in the diet provides a concentrated nutrient sup- plement, thus ensuring the diet is nutritionally adequate (Department Of Health, 1994a; Millward, 1999). The potential for producing nutritionally superior, con- venience products, that include meat as a functional ingredient, is enormous and deserves more thorough exploitation. 9.9 Meat, Palaeolithic diets and health Humans are omnivores. Evidence such as dentition, gut structure and ecosystem, enzymic range and adaptability and our dependence on both plant and animal sources for our essential nutrients all support this issue. We begin life as omni- vores, because as babies in utero, all the nutrients we receive are of animal origin. During the Ice Age, plants could not grow and so humans had to depend on meat as their main source of nutrition. There is much historical evidence and data from carbon isotopes, gut morphology, brain size, cranio-dental features, tools, wea- pons and rock art depiction of hunting all tracing the evolution of humans as omnivores (Mann, 2001a). There is considerable weight to the argument that our brains evolved because we could eat a variety of foods including meat. As we begin the new Millennium, some experts are looking at the diet of Palaeolithic (stone-age) man in a search for ways to reduce the incidences of ‘modern’ diseases such as obesity, cancer and coronary heart disease. Research from hunter-gatherer societies has indicated that these people were relatively free of many of the chronic and degenerative diseases that plague us today; this is in part attributable to the different dietary practices. Investigation of the dietary habits of modern hunter-gatherer societies, as an approximation of Palaeolithic practices, has shown a high reliance on animal foods compared with plant foods for basic energy requirements (Cordain et al, 2000). It has been estimated that the hunter-gatherers obtained approximately 45–65% of their total energy intake 226 The nutrition handbook for food processors from meat, which was either hunted or fished (Cordain et al, 2000). It is only with the relatively recent rise in agriculture that humans have begun to consume high levels of carbohydrates. This is now recognised as a major contributor to ‘Western lifestyle’ diseases. We have changed from a diet high in meat to a diet where grains and refined foods dominate. The hunter-gatherer diet was high in protein (19–35% E) and low in carbohydrate (22–40% E) whereas today, the opposite prevails – lower in protein (15% E) and much higher in carbohydrates (55% E) (Cordain et al, 2000). The fatty acid profiles of such diets may have dif- fered with higher levels of unsaturated fatty acids in wild animals, compared to domesticated farm animals. Studies have shown that Australian Aborigines have shown significant health improvements, including a reduction in blood cholesterol levels, after returning to their natural diets, where there is a high reliance on animal foods (O’Dea, 1991). Research of macronutrient proportions in the diet of hunter-gatherer popu- lations shows a clear relationship between high protein content and the evolution of insulin resistance, which offered a survival and reproductive advantage (Brand- Miller and Colagiuri, 1994). However, the advent of agriculture saw the rise of a diet higher in carbohydrate; this has meant that people were unprepared for the high glycaemic load which in turn is responsible for the current incidence of non-insulin dependent diabetes mellitus (Brand-Miller and Colagiuri, 1994). However, we must also remember that humans are not carnivores and thus we cannot exist on protein intakes above 35% energy for extended periods of time. ‘A clear role for lean red meat in a healthy balanced diet becomes evident as the diet history of our species is uncovered’ (Mann, 2001a). 9.10 Meat and satiety The prevalence of obesity has increased dramatically in recent years (National Audit Office, 2001). Satiety influences the frequency of meals and snacks, whereas satiation influences the size of meals and snacks. Macronutrients have differing effects on satiety; protein is more satiating than carbohydrates that are more satiating than fat (Hill and Blundell, 1986; Barkeling et al, 1990; Stubbs, 1995). The exact mechanism by which protein exerts its satiating effect is not elucidated, but it may involve changes in the levels and patterns of metabolites and hormones (e.g. amino acids, glucose and insulin), cholecystokinin and amino acid precursors of the neurotransmitters serotonin, noreadenaline and dopamine. A meat-containing meal was shown to have more sustained satiety than a veg- etarian meal (Barkeling et al, 1990). Other studies have shown that different meats have different satiating powers (Uhe et al, 1992). These differences may be related to differences in amino acid profiles or digestibilities. More research on the effects that different meats have on satiety will prove invaluable in assess- ing whether or not meat can, in the future, be promoted as a food that can negatively curb the growing levels of obesity. Enhancing the nutritional value of meat 227 9.11 Meat and micronutrients 9.11.1 Iron in meat Iron deficiency (Schrimshaw, 1991) and iron deficiency anaemia (Walker, 1998) remain the most common nutritional disorders in the world today. Iron deficiency is the only widespread nutrient deficiency occurring in both developed and devel- oping countries. Iron deficiency affects between 20 and 50% of the world’s popu- lation (Beard and Stoltzfus, 2001). There are many causes of iron deficiency, including hook worm infestation, low iron intakes, low bioavailability of dietary iron and increased demand due to physiological requirements. The most common result of iron deficiency is anaemia. Some of the liabilities associated with iron deficiency and anaemia are defective psychomotor development in infants, impaired education performance in schoolchildren, adverse perinatal outcome in pregnancy and diminished work capacity (Cook, 1999). All of the iron in our body comes from our diet, and meat is a rich dietary source. Concern about iron deficiency is one nutritional reason for recommending eating at least some meat (WHO, 1990; COMA, 1998). Food iron can be classified as haem iron or non-haem iron. Haem iron is derived from haemoglobin and myoglobin and its chief food source is meat, whereas non-haem iron is derived mainly from cereals, fruits and vegetables. Meat is distinctive as it contains both types of iron, haem (50–60%) and non- haem. Our bodies readily absorb haem iron (20–30%) as it is not affected by other dietary factors. Meat positively influences the bioavailability of non-haem iron. Bioavailability of iron refers to the proportion of ingested iron that is absorbed and utilised by the body (O’Dell, 1989). Only two dietary factors enhance non- haem iron bioavailability, they are vitamin C (Hallberg et al, 1989) and meat (Cook and Monsen, 1976; Taylor et al, 1986; Hazell et al, 1978; Kapsokefalou and Miller, 1991, 1993, 1995; Mulvihill and Morrissey, 1998a, 1998b; Mulvihill et al, 1998). Absorption of non-haem iron from meat is typically 15–25%, com- pared with 1–7% from plant sources (Fairweather-Tait, 1989). The presence of meat in a meal enhances the bioavailability of non-haem iron contained in the other foods present such as cereals, fruits and vegetables. The enhancing effect of meat on non-haem iron bioavailability is commonly referred to as the ‘meat factor’. The exact mechanism by which the ‘meat factor’ works still remains unknown despite the fact that numerous efforts have con- centrated on this topic. Research indicates that the mechanism of the ‘meat factor’ may not be due solely to a single factor but due to a number of contributing factors which work together promoting non-haem iron bioavailability. These factors include the release of cysteine-rich small molecular weight peptides during the proteolysis of meat; the ability of these peptides to reduce ferric iron to the more soluble ferrous iron; the chelation of soluble non-haem iron by these peptides; and the ability of meat to promote gastric acid secretion and gastrin release better than other food components do (Mulvihill, 1996). Glutathione is a tripeptide containing cysteine, and this is considered to play a role in the ‘meat factor’. However, reduced glutathione represents only 3% of 228 The nutrition handbook for food processors total cysteine in meat and this is considered too low to have such a profound posi- tive influence on non-haem iron bioavailability (Taylor et al, 1986). Elucidation of the mechanism(s) of the ‘meat factor’ is extremely important in the search for more effective ways to improve iron nutrition. Isolation of the ‘meat factor’ will allow the potential to produce stable non-haem iron absorption enhancers which can be added to other foods, thus improving iron bioavailability. Meat and meat products provide 14% of iron intake (MAFF, 1999); within this, carcase meat and meat products supply 12.5% of total iron intakes. This figure grossly underestimates the value of meat for influencing iron status. Meat has an important influence on iron bioavailability and thus iron status due to its enhancing properties and overall greater absorption capacity. Low iron intakes and status are common among certain subgroups of the popu- lation – toddlers (Gregory et al, 1995; Edmond et al, 1996), adolescents (Nelson et al, 1993; Nelson, 1996), pregnant women (Allen, 1997) and the elderly (Finch et al, 1998). Data from the National Diet and Nutrition Survey of children shows that 20% have low iron stores and 8% have iron deficiency anaemia (Gregory et al, 1995). Iron deficiency anaemia among toddlers is often associated with late weaning practices. A Spanish study showed that children who first ate meat before eight months of age showed a better iron status than those who were introduced to meat later than eight months (Requejo et al, 1999). Another study showed that low iron stores in one- and two-year old children is related to a low meat iron intake (Mira et al, 1996). The COMA report on Weaning and the Weaning Diet recommends that foods containing haem iron should be incorporated into the diets of infants by 6–8 months of age. Soft-cooked puréed meat can be introduced. This goes against the modern trend to delay introduction, the basis for which appears to be non-scientific. Adolescents have high demands for iron to allow for muscle development, increased blood volume and the onset of menstruation in females, that makes them vulnerable to iron deficiency. Half the female population living in the UK aged between 15 and 18 years have iron intakes below the recommended level. This is reflected by the fact that 27% of that age group have low iron stores (Gregory et al, 2000). The prevalence of low iron stores among adolescent girls in the UK has been cited to be as high as 43% (Nelson et al, 1993). During pregnancy, more lac- tovegetarians (26%) reported suffering from iron deficiency than omnivores (11%) (Drake et al, 1999). Lyle et al (1992) has demonstrated that meat supplements were more effective than iron tablets in maintaining iron status during exercise in pre- viously sedentary young women. Among the elderly, both low iron intakes and low iron status has been shown to increase with age (Finch et al, 1998). Serum ferritin, the body’s iron store, is strongly correlated with haem iron (Reddy and Sanders, 1990). Bioavailability of iron plays an important role in determining iron status. Studies have shown that despite the fact that vegetarians have either a similar or a higher iron intake than their omnivore counterparts, their iron status is lower (Nathan et al, 1996; Ball and Bartlett, 1999; Wilson and Ball, 1999). Vegetarians should consume iron-rich foods to compensate for the low bioavailability of non-haem iron from the foods they eat. Enhancing the nutritional value of meat 229 The importance of meat in iron nutrition cannot be over-emphasised. The effects of meat and meat products on iron nutrition are three-fold. Firstly, they are a rich source of iron. Secondly, they contain haem iron, which is readily absorbed. Thirdly, they promote the absorption of non-haem in the diet. 9.11.2 Zinc in meat All meats, but in particular beef, are excellent sources of dietary zinc. It takes 41 oz milk, 15 oz tuna or 6 1 / 2 eggs to equal the amount of zinc in an average 4 oz portion of beef (Hammock, 1987). On average, meat and meat products account for a third of total zinc intakes (MAFF, 1999). Zinc absorption is suppressed by inhibitors such as oxalate and phytate which are found in plant foods (Johnson and Walker, 1992; Zheng et al, 1993; Hunt et al, 1995). On the contrary, meat facilitates the absorption of zinc – 20–40% of zinc is absorbed from meat. For instance, one study showed that female omnivores who had a significantly lower zinc intake than their vegetarian counterparts had a higher zinc status (Ball and Ackland, 2000); such data highlights the role that meat plays in providing an assured source of dietary zinc. Because of the low bioavailability of zinc from plant foods, vegetarians should strive to meet or exceed their RDA for zinc to ensure adequate zinc intakes. Zinc is necessary for growth, healing, the immune system, reproduction (Aggett and Comerford, 1995) and cognitive development (Sandstead, 2000). Low zinc intakes are becoming more prevalent, especially among adolescents. An NDNS survey showed that a tenth of 7–10 year old girls and a third of 11–14 year old girls have intakes of zinc below the recommended level (Gregory et al, 2000). Long-term, low zinc intakes leads to zinc deficiencies that may become a public health problem in the future (Sandstead, 1995). Iron and zinc deficiencies can often occur simultaneously, in particular among adolescents (Sandstead, 2000). Adolescents often avoid eating meat, in some incidences meat is provid- ing up to just 25% of total zinc intakes compared to 40% of adult intakes (Gregory et al, 1995; Mills and Tyler, 1992; Gregory et al, 2000). Thus including meat in the diet of adolescents can aid in averting both iron and zinc deficiencies in concert, as these minerals in meat are in easily absorbable forms. Similarly, concern over low zinc status among infants prompted the DoH, in its COMA weaning report, to recommend increasing meat portion sizes for infants at the weaning stage (Department of Health, 1994a). 9.11.3 Selenium in meat Selenium acts as an antioxidant and is considered to protect against coronary heart disease and certain cancers, such as prostate. Meat contains about 10 mg sele- nium per 100 g, which is approximately 25% of our daily requirement. Beef and pork contain more selenium than does lamb, which may be due to the age of the animal as selenium may collect in the meat over time. Bioavailability of sele- nium from plant foods was thought to be greater than that from animal foods, but 230 The nutrition handbook for food processors recent data demonstrate that meat, raw and cooked, provides a highly bioavail- able source (Shi and Spallholz, 1994). 9.11.4 Other minerals in meat Meat also contains phosphorus; a typical serving provides roughly 20–25% of an adult’s requirement. Phosphorus has important biochemical functions in carbo- hydrates, fat and protein metabolism. Meat also provides useful amounts of copper, magnesium, potassium, iodine and chloride. 9.11.5 B vitamins in meat Meat is a significant and an important source of many B vitamins. The B vita- mins in meat are thiamin (vitamin B 1 ), riboflavin (vitamin B 2 ), niacin, pantothenic acid, vitamin B 6 and vitamin B 12 . B vitamins are water-soluble, hence lean meat contains more of these vitamins than does fattier meat. Some losses of B vita- mins occur during cooking; the amount lost depends upon the duration and the temperature of the cooking method. Thiamin and riboflavin are found in useful amounts in meats. Pork and its products including bacon and ham are one of the richest sources of thiamin. Pork contains approximately 5–10 times as much thiamin as do either beef or lamb. Thiamin aids the supply of energy to the body by working as part of a coenzyme that converts fat and carbohydrates into fuel. It also helps to promote a normal appetite and contributes to normal nervous system function. Typical servings of pork provide all the daily requirement of thiamin. Offal meats are good sources of riboflavin, for example, a single portion (100 g) of kidney or liver provides more than the daily requirement. Riboflavin, like thiamin, aids in supplying energy and also promotes healthy skin, eyes and vision. Meat is the richest source of niacin. Half the niacin provided by meat is derived from tryptophan, which is more readily absorbed by the body than that bound to glucose in plant sources. Niacin helps to supply energy to the body as it plays a role in converting carbohydrates and fats into fuel. Meat and meat products supply more than a third of total niacin intakes in Britain (MAFF, 1999). Liver and kidney are rich sources of pantothenic acid. Although most of this vitamin is leached into the drip loss associated with frozen meat, this is unlikely to be of any nutritional consequence as pantothenic acid is universal in all living matter. A 100 g portion of veal liver provides half our daily vitamin B 6 needs and other meats provide around a third. Vitamin B 6 is a necessary cofactor for more than 100 different cellular enzyme reactions including those related to amino acid metabolism and inter-conversion. Vitamin B 12 is exclusively of animal origin as it is a product of bacterial fermentation that occurs in the intestine of ruminant animals such as cattle, sheep and goats. Vitamin B 12 is required to produce red blood cells and acts as a cofactor for many enzyme reactions. Deficiency of vitamin B 12 causes megaloblastic anaemia, neuropathy and gastrointestinal symp- Enhancing the nutritional value of meat 231 toms. Groups at risk of vitamin B 12 deficiency include vegans and strict vegetar- ians, because vitamin B 12 is exclusively of animal origin, and the elderly, because their ability to absorb this vitamin from the diet diminishes with age (Allen and Casterline, 1994; Swain, 1995; Baik and Russell, 1999; Drake et al, 1999a). In the past some vitamin B 12 was provided from the soil of poorly cleaned foods. This may in part explain the apparent absence of deficiency in some vegan groups. Today, with the emphasis on good food hygiene practices, this source can no longer protect against deficiency in vulnerable individuals. Vegans are recom- mended to take vitamin B 12 supplements since the quantity consumed from foods fortified with the vitamin is too low (Jones, 1995; Draper, 1991; Sanders and Reddy, 1994). The RNI for vitamin B 12 among the elderly is 1.5mg/day (Depart- ment of Health, 1991). A 100 g portion of lean trimmed beef contains 2mg vitamin B 12 , thus supplying all their daily needs for this vitamin. In Britain, meat and meat products supply more than a fifth of both vitamin B 6 and B 12 intakes (MAFF, 1999). The need for vitamin B 12 has been a part of the rationale for recommend- ing the consumption of animal foods among all age groups (WHO, 1990). Raised homocysteine, an amino acid metabolite, is an independent risk factor for cardiovascular disease. It is estimated that 67% of the cases of hyperhomo- cysteinemia are attributable to inadequate plasma concentrations of one or more of the B vitamins namely folate, vitamin B 6 and vitamin B 12 . Some enzymes that reduce homocysteine levels require vitamins B 6 and B 12 as cofactors. Vitamin B 6 is a cofactor for two enzyme reactions which catabolise homocysteine to cys- teine via a transulphuration pathway, they are cystathionine b-synthase and cys- tathionase. Meanwhile, vitamin B 12 is a cofactor for the remethylation enzyme, methionine synthase, which converts homocysteine to methionine. Research has shown that low levels of both vitamins B 6 and B 12 independently correlates with raised homocysteine. For instance, ovo-lactovegetarians or vegans who had sig- nificantly lower serum vitamin B 12 levels than meat eaters had significantly higher levels of plasma homocysteine (Mann et al, 1999; Krajcovicova-Kudlackova et al, 2000; Mann, 2001b). Similarly, low doses of vitamin B 6 can effectively lower fasting plasma homocysteine levels (McKinley et al, 2001). The role of meat in regulating homocysteine is intriguing and needs to be addressed further. 9.11.6 Meat and vitamin D In the body vitamin D acts as a hormone, essential for the absorption of dietary calcium. Thus, vitamin D is essential for skeletal development and severe defi- ciency is associated with defective mineralisation of the bone resulting in rickets in children or its adult equivalent, osteomalacia (Fraser, 1995; Dunnigan and Henderson, 1997; De Luca and Zierold, 1998; Department of Health, 1998b). More subtle degrees of insufficiency lead to increased bone loss and osteoporotic fractures. Other functions of vitamin D include its role in the immune system, as well as possible protection against tuberculosis, muscle weakness, diabetes, certain cancers and coronary heart disease (Department of Health, 1998b). 232 The nutrition handbook for food processors It is well established that sunlight exposure on the skin is the main source of vitamin D. However, there are certain subgroups in the population who are more at risk of vitamin D deficiency, and these depend on diet in addition to sunlight in obtaining adequate vitamin D. Such subgroups include infants, toddlers, preg- nant and lactating women, elderly and those who have low sunlight exposure, such as certain ethnic minorities and the housebound (Department of Health, 1998a). The prevalence of vitamin D inadequacies among these groups is wide- spread. For instance, 27% of 2 year old Asian children living in England have low vitamin D status (Lawson and Thomas, 1999), and 99% of elderly people living in institutions are not receiving enough dietary vitamin D (Finch et al, 1998). Vitamin D deficiency among the elderly will become much more appar- ent and a greater public health problem when we consider that we are living in an increasingly ageing population. Liver aside, meat and meat products were considered poor sources of vitamin D. However, new analytical data for the composition of meat indicates that this is not true (Chan et al, 1995). Meat and meat products contain significant amounts of 25-hydroxycholecalciferol, assumed to have a biological activity five times that of cholecalciferol. In fact, the meat group is now recognised as the richest natural dietary source of vitamin D, supplying approximately 21% (Gibson and Ashwell, 1997). Vitamin D is present in both the lean and the fat of meat although its exact function in the animal is not yet known. Since inter- est in the role of meat in supplying vitamin D is a relatively new subject matter, there are certain areas that need to be researched such as the effect of cooking meat on vitamin D levels, the bioavailability of vitamin D from meat and the influence of seasonal variation on the vitamin D content of meat and meat products. Low intakes of meat and meat products emerged as an independent risk factor for Asian rickets and absent intakes of meat and meat products emerged as an independent risk factor for Asian osteomalacia (Dunnigan and Henderson, 1997). It has been hypothesised by this research group that there may be a ‘magic factor’ in meat which is protective against rickets and osteomalacia. In Glasgow, at the beginning of the century, the incidence of rickets was high, whereas, between 1987 and 1991, only one case of rickets was reported. This may be explained by the fact that today infants are weaned onto an omnivorous diet from four months of age and this meat inclusion is offering protection against rickets (Dunnigan and Henderson, 1997). Obviously, much more research is required to improve our knowledge on this subject matter. It is also of interest to note that signs of both iron and vitamin D deficiency can occur simultaneously among toddlers (Lawson and Thomas, 1999). For instance, during the winter, half of the toddlers had both low vitamin D and low iron levels (Lawson and Thomas, 1999). Such evidence highlights the potential protective role that meat inclusion can play in a toddler’s diet. It is important for toddlers and children to eat foods rich in both iron and vitamin D such as meat and meat products as well as playing out of doors to get sunlight. Enhancing the nutritional value of meat 233 9.12 Future trends As we begin the twenty-first century, we look to the future to predict the likely nutritional problems we will need to tackle. The four major nutritional problems today are heart disease, hypertension, obesity and diabetes. These are likely to remain significant public health problems in the future. The demographic struc- ture of the population is changing. Throughout Europe, both birth and death dates are falling, people are living longer and it is estimated that by the year 2030 more than half the population living in the UK will be over 50 years of age. With this knowledge we shall try to ascertain the likely future nutritional role of meat. This chapter clearly outlines ways to reduce the fat content of meat and ma- nipulate its fatty acid composition. The meat that is on sale today has never been leaner. Fortunately, most of the valuable nutrients of meat are located in the lean component, so reducing the visible fat of meat has little bearing on its micronu- trient status. Researchers are focusing on ways of further improving the fatty acid composition of meat, using the knowledge that grass feeding results in high levels of both n-3 PUFAs and CLA content. Both n-3 PUFAs and CLA may have many possible benefits for human health, and in particular may offer protection against predicted future health problems (Cordain et al, 2002). N-3 PUFAs, in parti- cular those that have very long chains, are cardioprotective and have anti- inflammatory and anti-tumourigenic properties. CLA can prevent formation and slow the growth for tumour development (Ip et al, 1994), reduce atherosclerosis development (Lee et al, 1994) and can help normalise blood glucose levels, which may be shown to prevent adult-onset diabetes (Houseknecht et al, 1998). Studies in human subjects are needed before we realise fully the benefits of CLA on human health. The fat and fatty acid story for meat so far is positive and only research and time will tell whether this story will be further improved. The prevalence of overweight and obesity is increasing steadily in many devel- oped countries. In the UK, over a quarter of the population are either overweight or obese. Obesity is a risk factor for many conditions. During a 10-year follow- up study, the incidence of colon cancer, diabetes, heart disease, hypertension, stroke (men only) and gallstones increased in line with the degree of overweight among adults (Field et al, 2001). Thus, reducing the incidence of overweight and obesity is a major public health priority. A positive energy balance is the cause of practically all cases of overweight and obesity. Factors regulating food intake are hunger, appetite, satiation and satiety. Meat-containing meals have higher satiety values than vegetable containing meals (Barkeling et al, 1990). Research needs to be undertaken to determine whether meat can play a role in curtailing obesity, as a result of its high satiety value. Media hype about CLA has concentrated on its ability to reduce body fat and increase lean body mass. Studies have noted that CLA induces a relative decrease in body fat and an increase in lean muscle (Park et al, 1997; West et al, 1998). Trials are currently taking place to confirm whether or not these benefits occur in humans. Lean meat is already low in fat, but other attributes such as its 234 The nutrition handbook for food processors high satiety value and the CLA it contains may be used in the future to market meat as a food that can help to reduce overweight and obesity. Furthermore, the capacity of meat to encourage greater vegetable and salad consumption, due to the way it is eaten, should not be overlooked in this regard. An increase in the incidence of hip fractures is an inevitable consequence of people living longer. Research has shown that an increase in meat protein con- sumption among elderly women correlates with a decrease in the risk of hip frac- ture (French et al, 1997). Decreasing the risk of hip fracture is a public health priority. Vegetarian women tended to have lower spinal bone mineral density than non-vegetarians (Barr et al, 1998). Dunnigan and Henderson (1997) suggested that there may be a ‘magic factor’ in meat protecting against rickets and osteo- malacia. To suggest that meat plays a role in bone health is relatively new and exciting and warrants further investigation. Another emerging benefit for meat is that it supplies selenium. Up to the middle part of the last century the main source of selenium in the diet was from wheat-containing products. Wheat, which was imported mainly from the United States, was high in selenium. Nowadays, there is a much greater reliance on European wheat, which is much lower in selenium. This has resulted in the fact that our intake of selenium has decreased steadily during the past fifty years, but the proportion of selenium we get from meat has increased. Recent studies have found that selenium may reduce the risk of heart disease and certain types of cancer such as prostate and enhance the body’s ability to fight infections. Meat does provide a wide range of valuable nutrients, for example, one study has shown that young women consuming a high meat diet have greater intakes of thiamine, niacin, zinc and iron than those consuming a low meat diet (Ortega et al, 1998). In a review on optimal iron intakes, iron contained in animal foods is far better assimilated than that from vegetarian foods (Cook, 1999). Meat is one of the richest natural sources of glutathione, an important reducing agent providing a major cellular defence against a variety of toxicological and pathological processes. Moderate levels of glutathione are found in fruit and vegetables and low levels are present in dairy and cereal products. Glutathione inhibits formation of mutagens in model systems (Trompeta and O’Brien, 1998). It also maintains ascorbate in a reduced and functional form. Glutathione importance in the defence against chronic disease provides positive potential for meat and merits further research (Bronzetti, 1994; Trompeta and O’Brien, 1998). There has never before been such a wide variety and choice of food on sale in western societies and in the recent past we have seen the development of func- tional foods. A functional food can be loosely described as a food that provides a health benefit beyond its basic nutritional content. In the United States beef and lamb are now described as functional foods (ADA, 1999), because of the CLA they contain. At a Meat Marketing/Communication Workshop, Dr Lynne Cobiac (CSIRO) (Cobiac, 2000) described some nutritive and non-nutritive meat com- ponents that may have potential health-promoting properties. They are sum- marised as follows: Enhancing the nutritional value of meat 235 ? Lipoic acid has antioxidant properties and has been shown to be beneficial in diabetics and in the prevention of cataract development in animal models and cell lines. Organ meats contain higher quantities of lipoic acid than muscle meats. ? Carnosine is a dipeptide composed of alanine and histidine. Carnosine is found in meats and its antioxidant properties may confer some protection against oxidative stress. It’s an anti-inflammatory agent and has anti-tumouri- genic properties in rats and it also plays a role in cellular homeostasis. ? Biogenic amines are naturally formed from bacterial decarboxylation of amino acids or natural decarboxylase activity. They have been linked with improving gut health and cognitive performance. ? Nucleotides are added to enteral feeds to enhance the general immune func- tion. Organ meats are good sources of nucleotides. ? Glutathione is a tripeptide containing the sulphur amino acid cysteine. Glu- tathione may be the ‘meat factor’ which enhances non-haem iron absorption. ? Choline is now termed a nutrient. In the United States, it is an essential nutri- ent and the estimated adequate intake is 550 mg/day for men and 425 mg/day for women. Choline is a precursor of the neurotransmitter acetlycholine, it is necessary for central nervous system development, folate/homocysteine metabolism, it plays a role in the immune system, fat metabolism and improves athletic performance. Beef and in particular liver is one of the richest sources of choline. ? Carnitine is composed of lysine and methionine. Seventy-five percent of car- nitine comes from the diet, mainly from red meat, lamb being a particularly good source. Carnitine carries the long chain fatty acids to the mitochondria for oxidation to give energy and thus can be used to improve athletic perfor- mance. It also has antioxidant capabilities and it may be critical for normal brain development by providing acetyl groups to synthesise acetylcholine, a neurotransmitter. This range of meat components may have the ability to fight against certain cancers, CHD, anaemia and cataracts, enhance immunity and cognition, improve gut and bone health, regulate body weight and may be used in sports nutrition. However, a lot of the evidence indicating beneficial effects of these components comes from animal or cell culture models. Research will have to be conducted in humans to demonstrate their effect on human health. But even glancing at the amount of ‘potential’ components present in meat does indicate a positive and competitive future for meat. However, when looking to the future we must also try and visualise what changes are likely to occur that may influence meat consumption. Traditionally, food purchase was predominantly influenced by price and sustenance. Current and future food choice depends on these values but they lie alongside other factors such as health, food safety, convenience and welfare concerns. Changes in our social patterns, such as moving away from the formal family meat-eating patterns to a ‘grazing’ or ‘snacking’ habit, will become much more apparent. Increasing 236 The nutrition handbook for food processors loss of culinary skills is already evident and is likely to rise. The market will demand more convenience and processed meat products in place of traditional cuts of meats. Eating outside the home will place a greater emphasis on the cater- ing sector as food providers. Availability of ‘exotic’ meats will escalate. Demand for organic meat is expected to rise. Competition from other foods will intensify. The emergence of more functional foods is likely to occur. These are some of the factors that will sculpt the future demand for meat and meat products. Meat must adapt to the changing environment. However, the emphasis between food choice and health was never as great and is likely to become even more important. In the past meat responded to consumer demands by decreasing its fat content. Meat is a versatile food. However, it is time that we banish the misinformation that surrounds the nutritional value of meat. Meat is a relatively low fat nutrient dense food. Meat and meat products are an integral part of the UK diet and for those who choose to consume meat, it makes a valuable contribution to nutritional intakes. (BNF, 1999). 9.13 Conclusion There has been considerable emotive and public health debate over the last two decades on the relative importance of meat in the diet of modern humans. Early dismissive arguments have more recently been revisited and challenged as a result of the continual progress and review of nutritional science. The early focus on fat as the predominant cause of western style diseases of affluence led, na?vely, to meat being blamed for diet related problems. More recently, the focus on the diets of our ancestors has effectively reversed this thinking and lean red meat has been rediscovered as a mainstay of human diet evolution. The serious health con- cerns resulting from the epidemic rise in CHD, obesity, diabetes and cancers require more carefully guided public health advice, based on a holistic approach to diet and lifestyle. Lean meat can be seen as the ultimate natural functional food. Eaten in mod- erate quantities as part of a meal along with sufficient plant foods, it provides a valuable, arguably essential nutrient-dense supplement to the diet with beneficial effects for health, both in the short and long term. As a key ingredient of modern processed pre-prepared meals, meat, when added as a quality ingredient, can enhance the nutritional benefits of the food product and make a significant, pos- itive contribution to our health. It would be na?ve to ignore this potential. 9.14 References aggett p j and comerford j g (1995), ‘Zinc and Human Health’, Nutrition Reviews, 53, S16–S22 Enhancing the nutritional value of meat 237 allen l (1997), ‘Pregnancy and iron deficiency: unresolved issues’, Nutrition Reviews, 55(4), 91–101 allen l h and casterline j (1994), ‘Vitamin B 12 deficiency in elderly individuals: diag- nosis and requirements’, American Journal of Clinical Nutrition, 60, 12–14 american dietetic association (1993), ‘Position of the American Dietetic Association: vegetarian diets’, Journal of The American Dietetic Association, 1317–19 american dietetic association report (1999), ‘Position of the American Dietetic Asso- ciation: functional foods’, Journal of The American Dietetic Association, 99, 1278–85 armstrong b and doll r (1975), ‘Environmental factors and the incidence and mortal- ity from cancer in different countries with special reference to dietary practices’, Inter- national Journal of Cancer, 15, 617–31 azevedo l f, salgueiro l f, claro r, teixeira-pinto a and costa-pereira a (1999), ‘Diet and gastric cancer in Portugal – a multivariate model’, European Journal of Cancer Prevention, 8, 41–8 baik h w and russell r m (1999), ‘Vitamin B 12 deficiency in the elderly’, Annual Reviews of Nutrition, 19, 357–77 ball m and ackland m (2000), ‘Zinc intake and status in Australian vegetarians’, British Journal of Nutrition, 83, 27–33 ball m and bartlett m (1999), ‘Dietary intake and iron status of Australian vegetarian women’, American Journal of Clinical Nutrition, 70, 353–8 barkeling b, rossner s and bjorvell h (1990), ‘Effects of a high protein meal (meat) and a high carbohydrate meal (vegetarian) on satiety measured by automated comput- erized monitoring of subsequent food intake, motivation to eat and food preferences’, International Journal of Obesity, 14, 743–51 barr s i, prior j c, janelle k c and lentle b c (1998), ‘Spinal bone mineral density in premenopausal vegetarian and nonvegetarian women: cross-sectional and prospective comparisons’, Journal of the American Dietetic Association, 98(7), 760–5 beard j and stoltzfus r (2001), ‘Foreward – iron deficiency anaemia: reexamining the nature and magnitude of the public health problem’, Journal of Nutrition, 131, 563S beauchesne-rondeau e, gascon a, bergeron j and jacques h (1999), ‘Lean beef in lipid lowering diet: effects on plasma cholesterol and lipoprotein B in hypercholestero- laemic men’, Canadian Journal of Dietetic Practice and Research, 60, June Supplement belury m a (1995), ‘Conjugated dienoic linoleate: a polyunsaturated fatty acid with unique chemoprotective properties’, Nutrition Reviews, 53, 83–9 bingham s a (1996), ‘Epidemiology and mechanisms relating to risk of colorectal cancer’, Nutrition Research Reviews, 9, 197–239 black et al (1997), ‘Cancer incidence and mortality in the European Union. Cancer reg- istry data and cancer incidence for 1990’, European Journal of Cancer, 33, 1075–107 bonanome a and grundy s m (1988), ‘Effect of dietary stearic acid on plasma choles- terol and lipoprotein levels’, New England Journal of Medicine, 318, 1244–8 brand-miller j and colagiuri s (1994), ‘The carnivore connection: dietary carbohydrate in the evolution of NIDDM’, Diabetologia, 37, 1280–6 british nutrition foundation (1996), Diet and heart disease: a round table of facts, 2ed, M Ashwell (ed), BNF, London british nutrition foundation (1999), Meat in the Diet, Briefing Paper, BNF, London british nutrition foundation’s task force (1995), Trans fatty Acids – the Report of the BNF Task Force, BNF. London bronzetti g (1994), ‘Antimutagens In Food’, Trends in Food Science and Technology, 5 December, 390–5 burgess l, hackett a f, maxwell s and rouncefield m (2001), ‘The nutrient intakes of vegetarian and omnivorous adolescents in North-West England’, Proceedings of the Nutrition Society, 60(4), 69A burr m l (1988), ‘Heart Disease In British Vegetarians’, American Journal of Clinical Nutrition, 48, 30–2 238 The nutrition handbook for food processors chan w, brown j, lee s m and buss d h (1995), ‘Meat, poultry and game’, Supplement to McCance and Widdowson’s ‘The Composition of Foods’, Cambridge Royal Society of Chemistry and London, Ministry of Agriculture, Fisheries and Food, HMSO London chan w, brown j, church s m and buss d h (1996), ‘Meat Products and Dishes’ Sup- plement to McCance and Widdowson’s ‘The Composition Of Foods’, Cambridge Royal Society Of Chemistry and London, Ministry Of Agriculture Fisheries And Foods HMSO London chin s f, liu w, storkson j m, ha y l and pariza m w (1992), ‘Dietary sources of con- jugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens’, Journal of Food Composition and Analysis, 5, 185–97 chizzolini r, zanardi e, dorigoni v and ghidini s (1999), ‘Calorific value and cho- lesterol content of normal and low fat meat and meat products’, Trends in Food Science and Technology, 10, 119–28 cobiac l (2000), ‘Could red meat be a functional food of the future?’ marketing/ communication workshop, July 6–7, 2000, Organised by the International Meat Secretariat and hosted by The Meat and Livestock Commission committee on medical aspects of food policy (1984), Diet and Cardiovascular Disease: Report on Health and Social Subjects, No. 28, Department of Health and Social Security, HMSO London committee on medical aspects of food policy (1991), ‘Dietary Reference Values for Food, Energy and Nutrients for the United Kingdom’, Report of the Panel on Dietary Reference Values, No. 41, HMSO London committee on medical aspects of food policy (1994), ‘Nutritional Aspects of Car- diovascular Disease’, Report of the working group on diet and cancer, No. 46, HMSO London committee on medical aspects of food policy (1998), ‘Nutritional Aspects of the Development of Cancer’, Report of the working group on diet and cancer of the Com- mittee on Medical Aspects of Food and Nutrition Policy’, No 48, HMSO London cook j d (1999), ‘Defining optimal body iron’, Proceedings of the Nutrition Society, 58, 489–95 cook j d and monsen e r (1976), ‘Food iron absorption in human subjects III. Compar- ison of the effect of animal proteins on non-haem iron absorption’, American Journal of Clinical Nutrition, 29, 859–67 cordain l, watkins b a, florant g l, kelher m, rogers l and li y (2002), ‘Fatty acid analysis of wild ruminant tissues: evolutionary implications for reducing diet-related chronic disease’, European Journal of Clinical Nutrition, 56(3) cordain l, brand-miller j, eaton s b, mann n j, holt s h and speth j d (2000), ‘Plant- animal subsistence ratios and macronutrient energy estimations in worldwide hunter- gatherer diets’, American Journal of Clinical Nutrition, 71, 682–92 cox b d and whichelow m j (1997), ‘Frequent consumption of red meat is not a risk factor for cancer’, British Medical Journal, 315, 1018 davidson m h, hunninghake d, maki k c, kwiterovich p o and kafonek s (1999), ‘Comparison of the effects of lean red meat vs lean white meat on serum lipid levels among free-living persons with hypercholesterolaemia’, Archives of Internal Medicine 159, 1331–8 davidson s and passmore r (1969), ‘Human nutrition and dietetics’, London, Churchill Livingstone de luca h f and zierold c (1998), ‘Mechanisms and functions of vitamin D’, Nutrition Reviews, 56(2), S4–S10 department of health (1991), Dietary Reference Values for Food Energy and Nutri- ents for the United Kingdom, Report on Health and social subjects 41, London, HMSO department of health (1994a), Weaning and the Weaning Diet, Report On Health And Social Subjects 45, London, HMSO Enhancing the nutritional value of meat 239 department of health (1994b), Eat Well! an Action Plan from the Nutrition Task Force to Achieve the Health of The Nation Targets on Diet and Nutrition, HMSO, London department of health (1998a), Nutrition and Bone Health, Report On Health And Social Subjects 49, The Stationery Office, London department of health (1998b), Nutrition and Bone Health: with Particular Reference to Calcium and Vitamin D. Committee on the Medical Aspects of Food and Nutrition Policy. Working Group on the Nutritional Status of the Population Subgroup on Bone Health. The Stationery Office, London department of health (1998c), Nutritional Aspects of the Development of Cancer, Report On Health And Social Subjects 48, The Stationery Office, London drake r, reddy s and davies g j (1999a), ‘Dietary and supplement intake of vegetarians during pregnancy’, American Journal of Clinical Nutrition, 70(suppl), 627S drake r, reddy s and davies g j (1999b), ‘Health of vegetarians during pregnancy and pregnancy outcome’, American Journal of Clinical Nutrition, 70(suppl), 628S draper a (1991), ‘The energy and nutrient intakes of different types of vegetarians: a case for supplements’, British Journal of Nutrition, 69, 3–19 dunnigan m g and henderson j b (1997), ‘An epidemiological model of privational rickets and osteomalacia’, Proceedings of the Nutrition Society, 56, 939–56 duo li, ng a, mann n j and sinclair a j (1998), ‘Contribution of meat fat to dietary arachidonic acid’, Lipids, 33(4), 437–40 edmond a m, hawkins n, pennick c, golding j and the alspac children in focus team (1996), ‘Haemoglobin and ferritin concentrations in infants at 8 months of age’, Archives of Disease in Childhood, 74, 36–9 enser m, hallett k, hewitt b, fursey g a j and wood j d (1996), ‘Fatty acid content and composition of English beef, lamb and pork at retail’, Meat Science, 42(4), 443–56 enser m, hallett k g, hewitt b, fursey g a j, wood j d and harrington g (1998), ‘Fatty acid content and composition of UK beef and lamb muscle in relation to pro- duction system and implications for human nutrition’, Meat Science, 49, 329–41 fairweather-tait s j (1989), ‘Iron in foods and its availability’, Acta Paediatrica Scand, Suppl. 361, 12–20 field a e, coakley e h, must a, spadano j l, laird n, dietz w h, rimm e and colditz g a (2001), ‘Impact of overweight on the risk of developing common chronic diseases during a 10-year period’, Archives of Internal Medicine, 161(13), 1581–6 finch s, doyle w, lowe c, bates c j, prentice a, smithers g and clarke p c (1998), ‘National diet and nutrition survey: people aged 60 years and over’, London HMSO fraser d r (1995), ‘Vitamin D’, Lancet, 345, 104–7 french s a, folsom a r, jeffery r w, zheng w, mink p j and baxter j e (1997), ‘Weight variability and incident disease in older women: the Iowa Women’s Health Study’, International Journal of Obesity Related Metabolic Disorders, 21(3), 217–23 fritsche j and steinhart h (1998), ‘Amounts of conjugated linoleic acid (CLA) in German foods and evaluation of daily intake’, Z Lebensm Unters Forsch A, 206, 77–82 gavino v c, gavino g, leblanc m and tuchweber b (2000), ‘An isomeric mixture of conjugated linoleic acids but not pure cis-9, trans-11-octadecadienoic acid affects body weight gain and plasma lipids in hamsters’, Journal of Nutrition, 130, 27–9 gibson s and ashwell m (2001), ‘Implications for reduced red and processed meat con- sumption for iron intakes among British women’, Proceedings of the Nutrition Society, 60(4), 60A gibson s a and ashwell m (1997), ‘New Vitamin D values for meat and their implica- tion for vitamin D intake in British adults’, Proceedings of the Nutrition Society, 56, 116A gissi-prevenzione investigators (1999), ‘Dietary supplementation with n-3 PUFAs and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial’, Lancet, 354, 447–55 240 The nutrition handbook for food processors gregory j, foster k, tyler h and wiseman m (1990), The Dietary and Nutritional Survey of British Adults, London HMSO gregory j, lowe s, bates c j, prentice a, jackson l v, smithers g, wenlock r and farron m (2000), National Diet and Nutrition Survey: Young People aged 4 to 18 years, London, The Stationery Office gregory j r, clarke p c, collins d l, davies p s w and hughes j m (1995), National Diet and Nutrition Survey; Children aged 1 1 / 2 To 4 1 / 2 years, London HMSO hallberg l, brune m and rossander l (1989), ‘Iron absorption in man: ascorbic acid and dose dependent inhibition by phytate’, American Journal of Clinical Nutrition, 49, 140–4 hammock d a (1987), ‘The red meat in our diet – good or bad?’ in: Nutrition 87/88, C C Cook Fuller (ed.) Sushkin Publishing group, Guildford, Conn, 16–18 hazell t, ledward d a and neale r j (1978), ‘Iron availability from meat’, British Journal of Nutrition, 39, 631–8 higginson j (1966), ‘Etiological factors in gastrointestinal cancer in man’, Journal – National Cancer Institute, 37, 527–45 higgs j d (2000), ‘An overview of the compositional changes in red meat over the last 20 years and how these have been achieved’, Food Science and Technology Today, 14(1), 22–6 higgs j d and pratt j (1998), ‘Meat poultry and meat products: Nutritional Value’, Volume 2, 1272–82, in The Encyclopaedia Of Human Nutrition, M J Sadler, J J Strain and B Cabalerro (eds), Academic Press Limited, London hill a j and blundell j e (1986), ‘Macronutrients and satiety: the effects of a high protein or high carbohydrates meal on subjective motivation to eat and food preferences’, Nutri- tion and Behavior, 3, 133–4 hill m j (1999a), ‘Meat and colorectal cancer’, Proceedings of the Nutrition Society, 58, 261–4 hill m j (1999b), ‘Meat and colorectal cancer: a European perspective’, European Journal of Cancer Prevention, 8, 183–5 hill m j (2000), ‘Meeting Report: meat and nutrition’, Hamburg: 17–18 October 2000, European Journal of Cancer Prevention, 9, 465–70 hirayama t (1986), ‘A large scale cohort study on cancer risks by diet – with special ref- erence to the risk reducing effects of green-yellow vegetable consumption’ in T Hayashi et al (eds), Diet Nutrition and Cancer, Tokyo, Japan Sci Soc Press and Utrecht, VNU SCI Press 41–53 hirayama t (1990), Lifestyle and Mortality: a Large scale Census based Study in Japan, Basle, Karger houseknecht k l, vanden heuvel j p, moya-camarena s y, portocarrero c p, peck l w, nickel k p and belury m a (1998), ‘Dietary conjugated linoleic acid normalises impaired glucose tolerance in the Zucker diabetic fatty fa/fa rat’, Biochemical and Biophysical Research Communications, 244, 678–82 hulshof k f, van erp-baart m a, anttolainen m, becker w, church s m, couet c, hermann-kunz e, kesteloot h, leth t, martins i, moreiras o, moschandreas j, pizzoferrato l, rimestad a h, thorgeirsdottir h, van amelsvoort j m, aro a, kafatos a g, lanzmann-petithory d and van poppel g (1999), ‘Intake of fatty acids in western Europe with emphasis on trans fatty acids: the TRANSFAIR Study’, Euro- pean Journal of Clinical Nutrition, 53(2), 143–57 hunt j r, gallagher s k, johnson l k and lykken g i (1995), ‘High- versus low-meat diets: effects on zinc absorption, iron status, and calcium, copper, iron, magnesium, manganese, nitrogen, phosphorus, and zinc balance in postmenopausal women’, American Journal of Clinical Nutrition, 62, 621–32 ip c and scimeca j a (1997), ‘Conjugated linoleic acid and linoleic acid are distinc- tive modulators of mammary carconogenesis’, Nutrition and Cancer, 27(2), 131– 5 Enhancing the nutritional value of meat 241 ip c, chin s f, scimeca j a and pariza m w (1991), ‘Mammary cancer prevention by con- jugated dienoic derivative of linoleic acid’, Cancer Research, 51, 6118–24 ip c, singh m, thompson h j and scimeca j a (1994), ‘Conjugated linoleic acid suppresses mammary carcinogenesis and proliferative activity of the mammary gland in the rat’, Cancer Research, 54, 1212–15 ip m m, masso-welch p a, shoemaker s f, shea-eaton w k and ip c (1999), ‘Conju- gated linoleic acid inhibits proliferation and induces apoptosis of normal rat mammary epithelial cells in primary culture’, Experimental Cell Research, 250, 22–34 johnson j m and walker p m (1992), ‘Zinc and iron utilization in young women con- suming a beef-based diet’, Journal of the American Dietetic Association, 12, 1474–8 jones d p (1995), ‘Glutathione distribution in natural products’, Methods in Enzymology, 252, 3–13 kapsokefalou m and miller d d (1991), ‘Effects of meat and selected food components on the valence of non-haem iron during in vitro digestion’, Journal of Food Science, 56, 352–8 kapsokefalou m and miller d d (1993), ‘Lean beef and beef fat interact to enhance non- haem iron absorption in rats’, Journal of Nutrition, 123, 1429–34 kapsokefalou m and miller d d (1995), ‘Iron speciation in intestinal contents of rats fed meals composed of meat and non-meat sources of protein and fat’, Food Chemistry, 52, 47–56 kelly f d, mann n j, turner a h and sinclair a j (1999), ‘Stearic acid-rich diets do not increase thrombotic risk factors in healthy males’, Lipids, 34, S199 kelly f d, sinclair a j, mann n j, turner a h, abedin l and li d (2001), ‘A stearic acid-rich diet improves thrombogenic and atherogenic risk factor profiles in healthy males’, European Journal of Clinical Nutrition, 55, 88–96 key t j, fraser g e, davey g k, thorogood m, appleby p n, beral v, reeves g, burr m l, chang-claude j, frentzel-beyne r, kuzma j w, mann j and mcpherson k (1998), ‘Mortality in vegetarians and non-vegetarians: a collaborative analysis of 8300 deaths among 76 000 men and women in five prospective studies’, Public Health Nutri- tion, 1(1), 33–41 key t j, fraser g e, thorogood m, appleby p n, beral v, reeves g, burr m l, chang- claude j, frentzel-beyme r, kuzma j w, mann j and mcpherson k (1999), ‘Mortality in vegetarians and non-vegetarians: detailed findings from a collaborative analysis of 5 prospective studies’, American Journal of Clinical Nutrition, 70(suppl), 516S–524S key t j, davey g k and appleby p n (1999), ‘Health benefits of a vegetarian diet’ in Meat or Wheat for the Next Millennium? Proceedings of the Nutrition Society, 58(2), 271–5 kohlmeier l, simmansen n and mottins k (1995), ‘Dietary modifiers of carcinogene- sis’, Environmental Health Perspectives, 103 Supplement 8, 180–4 krajcovicova-kudlackova m, blazicek p, kopcova j, bederova a and babinska k (2000), ‘Homocysteine levels in vegetarians versus omnivores’, Annual Nutrition Metabolism, 44, 135–8 kramer j k g, parodi p w, jensen r g, mossoba m m, yurawecz m p and adlof r o (1998), ‘Rumenic acid: a proposed common name for the major conjugated linoleic acid isomer found in natural products’, Lipids, 33, 835 larsson c l and johansson g (2001), ‘Dietary intake and nutritional status of young vegans and omnivores in Sweden’, Proceedings of the Nutrition Society, 60(4), 69A lawson m and thomas m (1999), ‘Vitamin D concentrations in Asian children aged 2 years living in England: population survey’, British Medical Journal, 318, 28–9 lee k n, kritchevsky d and pariza m w (1994), ‘Conjugated linoleic acid and athero- sclerosis in rabbits’, Atherosclerosis, 108, 19–25 leeds a r, randle a and matthews k r (1997), ‘A study into the practice of trimming fat from meat at the table, and the development of new study methods’, Journal of Human Nutrition and Dietetics, 10, 245–51 242 The nutrition handbook for food processors li d, sinclair a, mann n, turner a, ball m, kelly f, abedin l and wilson a (1999), ‘The association of diet and thrombotic risk factors in healthy male vegetarians and meat-eaters’, European Journal of Clinical Nutrition, 53, 612–19 lyle r m, weaver c m, sedlock d a, rajaram s, martin b and melby c l (1992), ‘Iron status in exercising women: the effect of oral iron therapy vs increased consumption of muscle foods’, American Journal of Clinical Nutrition, 56(6), 1049–55 ma d w l, wierzbicki a a, field c j and clandinin m t (1999), ‘Conjugated linoleic acid in Canadian dairy and beef products’, Journal of Agricultural and Food Chem- istry, 47(5), 1956–60 mann n j (2001a), ‘The evidence for high meat intake during the evolution of hominids’, Proceedings of the Nutrition Society, 60, 61A mann n j (2001b), ‘Effect of vitamin B 12 status on homocysteine levels in healthy male subjects’, Proceedings of the Nutrition Society, 60, 58A mann n j, sinclair a j, pille m, johnson l, warrick g, reder e and lorenz r (1997), ‘The effect of short term diets rich in fish, red meat or white meat on thromboxane and prostacyclin synthesis in humans’, Lipids, 32(6), 635–43 mann n j, li d, sinclair a j, dudman n p, guo x w, elsworth g r, wilson a k and kelly f d (1999), ‘The effect of diet on plasma homocysteine concentrations in healthy male subjects’, European Journal of Clinical Nutrition, 53(11), 895–9 mckinley m c, mcnulty h, mcpartlin j, strain j j, pentieva k, ward m, weir d g and scott j m (2001), ‘Low dose vitamin B 6 effectively lowers fasting plasma homocys- teine in healthy elderly persons who are folate and riboflavin replete’, American Journal of Clinical Nutrition, 73, 759–64 meat and livestock commission and royal society of chemistry (1990), The Chem- ical Composition Of Pig Meat. Report to the Ministry Of Agriculture, Fisheries and Food on the Trial to Determine the Chemical Composition of Fresh and Cured Pork from British Pigs of Different Breed Types, Sexes and Origins. Milton Keynes, Meat And Livestock Commission mills a and tyler h (1992), Food and Nutrient Intakes of British Infants aged 6–12 months, Ministry of Agriculture Fisheries and Food, HMSO, London millward d j (1999), ‘Meat or Wheat for the next millennium?’, Proceedings of the Nutri- tion Society, 58(2), 209–10 ministry of agriculture fisheries and food (1981), Household Food Consumption And Expenditure: 1979 National Food Survey Committee, London, HMSO ministry of agriculture fisheries and food (1999), National Food Survey 1999, London, The Stationery Office ministry of agriculture fisheries and food, food safety directorate (1992, 1993, 1995, 1998) National Food Survey – Household Consumption for 1991, 1992, 1994, 1997, London, MAFF mira m, alperstein g, karr m, ranmuthugala g, causer j, niec a and lilburne a m (1996), ‘Haem iron intake in 12–36 month old children depleted in iron: case-control study’, British Medical Journal, 312, 881–3 mulvihill b (1996), The Effect of Meat Systems on the Bioavailability of Non-haem Iron, PhD Thesis, University College Cork, Republic of Ireland mulvihill b (2001), ‘Ruminant meat as a source of conjugated linoleic acid (CLA)’, Nutrition Bulletin, 26(4), 295–300 mulvihill b and morrissey p a (1998a), ‘Influence of the sulphydryl content of animal proteins on in vitro bioavailability of non-haem iron’, Food Chemistry, 61(1–2), 1–7 mulvihill b and morrissey p a (1998b), ‘An investigation of factors influencing the bioavailability of non-haem iron from meat systems’, Irish Journal of Agricultural and Food Research, 37(2), 219–26 mulvihill b, kirwan f m, morrissey p a and flynn a (1998), ‘Effect of myofibrillar proteins on the in vitro bioavailability of non-haem iron’, International Journal of Food Science and Technology, 49, 187–92 Enhancing the nutritional value of meat 243 nakachi k, imai k, hoshiyama y and sasaba t (1988), ‘The joint effects of two factors in the aetiology of oesphageal cancer in Japan’, Journal of Epidemiology and Commu- nity Health, 42, 755–61 nathan i, hackett i f and kirby s (1994), ‘Vegetarianism and health: is a vegetarian diet adequate for the growing child?’, Food Science and Technology Today, 8(1), 13–15 nathan i, hackett a f and kirby s (1996), ‘The dietary intake of a group of vegetarian children aged 7–11 years compared with matched omnivores’, British Journal of Nutri- tion, 75(4), 533–44 nathan i, hackett i f and kirby s p (1997), ‘A longitudinal study of the growth of matched pairs of vegetarian and omnivorous children aged 7–11 years in the north-west of England’, European Journal of Clinical Nutrition, 51, 20–5 national advisory committee on nutrition education (1983), Proposals For Nutri- tional Guidelines for Health Education in Britain, London, Health Education Council national audit office report (2001), ‘Tackling Obesity in England’, London, The Stationery Office nelson m (1996), ‘Anaemia in adolescent girls: effects on cognitive function and activ- ity’, Proceedings of the Nutrition Society, 55, 359–67 nelson m, white j and rhodes c (1993), ‘Haemoglobin, ferritin, and iron intakes in British children aged 12–14 years: a preliminary investigation’, British Journal of Nutrition, 70, 147–55 nicolosi r j, rogers e j, kritchevsky d, scimeca j a and hith p j (1997), ‘Dietary con- jugated linoleic acid reduces plasma lipoproteins and early aortic atherosclerosis in hypercholesterolemic hamsters’, Artery, 22(5), 266–77 o’dea k (1991), Traditional diet and food preferences of Australian aboriginal hunter- gatherers’, Philosophical Transactions of the Royal Society of London, B Biological Sciences, 334, 233–41 o’dell b l (1989), ‘Bioavailability of trace elements’, Nutrition Reviews, 42, 301–8 ortega r, lopez-sobaler a, requejo a, quintas m, gaspar m, andres p and navia b (1998), ‘The influence of meat consumption on dietary data, iron status and serum lipid parameters in young women’, International Journal for Vitamin and Nutrition Research 68, 255–62 o’shea m, lawless f, stanton c and devery r (1998), ‘Conjugated linoleic acid in bovine milk fat: a food-based approach to cancer chemoprevention’, Trends in Food Science and Technology, 9, 192–6 park y, albright k j, liu w, storkson j m, cook m e and pariza m w (1997), ‘Effect of conjugated linoleic acid on body composition in mice’, Lipids, 32, 853–8 rana s k and sanders t a b (1986), ‘Taurine concentrations in the diet, plasma, urine and breast milk of vegans compared with omnivores’, British Journal of Nutrition, 56, 17–27 reddy s and sanders t a b (1990), ‘Haemotological studies on pre-menstrual Indian and caucasian omnivores’, British Journal of Nutrition, 64, 331–8 reid r l and hackett a f (2001), ‘A database of vegetarian convenience foods’, Proceedings of the Nutrition Society, 60(4), 4A requejo a m, navia b, ortega r m, lopez-sobaler a m, quintas e, gaspar m j and osorio o (1999), ‘The age at which meat is first included in the diet affects the inci- dence of iron deficiency and ferropenic anaemia in a group of pre-school children from Madrid’, International Journal for Vitamin and Nutrition Research, 69(2), 127–31 royal society of chemistry (1986), ‘Nitrogen factors for pork’, Analyst, 111(8), 969–73 royal society of chemistry (1993), ‘Nitrogen factors for beef; a reassessment’, Analyst, 118(9), 1217–26 royal society of chemistry (1996), ‘Nitrogen factors for sheep meat’, Analyst, 121(7), 889–96 sanders t a b (1999), ‘The nutritional adequacy of plant based diets’ in ‘Meat or wheat for the next millennium?’ Proceedings of The Nutrition Society, 58(2), 265–9 244 The nutrition handbook for food processors sanders t a b and reddy s (1994), ‘Vegetarian diets and children’, American Journal of Clinical Nutrition, Supplement 59 120(4), 1176S–81S sandstead h h (1995), ‘Is zinc deficiency a public health problem?’ Nutrition, 11, 87–92 sandstead h h (2000), ‘Causes of iron and zinc deficiencies and their effects on brain’, Journal of Nutrition, 130(2S Suppl), 347S–9S scott l e, kimball k t, wittels e h, dunn j k, brauchi d j, pownall h j, herd j a, savell j w and papadopoulous l s (1990), ‘The effect of lean beef, chicken and fish on lipoprotein profile’, in 63rd Scientific Sessions of the American Heart Association, Nov 12–15, Dallas, Texas scottish office department of health (1996), ‘Eating for health – a diet action plan for Scotland’, Edinburgh, HMSO schrimshaw n s (1991), ‘Iron deficiency’, Scientific American, October, 24–30 shantha n c, crum a d and decker e a (1994), ‘Evaluation of conjugated linoleic acid concentrations in cooked beef’, Journal of Agricultural and Food Chemistry, 42, 1757–60 shi b and spallholz j e (1994), ‘Selenium peroxidase is highly available as assessed by liver glutathione peroxidase activity and tissue selenium’, British Journal of Nutrition, 72(6), 873–81 sinclair a j, johnson l, o’dea k and holman t (1994), ‘Diets rich in lean beef increase the arachidonic acid and long chain n-3 PUFA levels in plasma phospholipids’, Lipids, 29(5), 337–43 skov a r, toubro s, ronn b, holm l and astrup a (1999a) ‘Randomisd trial on protein vs carbohydrate in ad Libitum fat reduced diet for the treatment of obesity’, Interna- tional Journal of Obesity, 23, 528–36 skov a r, toubro s, bulow j, krabbe k, parving h-h and astrup a (1999b) ‘Changes in renal function during weight loss induced by high vs low-protein diets in overweight subjects’, International Journal of Obesity, 23, 1170–7 stubbs r j (1995), ‘Macronutrient effects on appetite’, International Journal of Obesity, 19, S11–19 swain r (1995), ‘An update on vitamin B 12 metabolism and deficiency states’, The Journal of Family Practice, 41(6), 595–600 taylor p g, martinez-torres c, romano e l and layrisse m (1986), ‘The effect of cys- teine-containing peptides released during meat digestion on iron absorption in humans’, American Journal of Clinical Nutrition, 43, 68–71 thorogood m, mann j, appleby p and mcpherson k (1994), ‘Risk of death from cancer and ischaemic heart disease in meat and non-meat eaters’, British Medical Journal, 308, 1667–71 trompeta v and o’brien j (1998), ‘Inhibition of mutagen formation by organosulphur compounds’, Journal of Agricultural and Food Chemistry, 46, 4318–23 tuyns a j, riboli e, doornbos g and peguinot g (1987), ‘Diet and esophageal cancer in Calvados (France)’, Nutrition and Cancer, 9, 81–92 tuyns a j et al (1992), ‘Diet and gastric cancer. A case-control study in Belgium’, Inter- national Journal of Cancer, Apr 22, 51(1), 1–6 uhe a m, collier g r and o’dea k (1992), ‘A comparison of the effects of beef, chicken and fish protein on satiety and amino acid profiles’, Journal of Nutrition, 122, 467– 72 ulbricht t l v (1995), Fat in the Food Chain, A Report to The Ministry of Agriculture Fisheries and Food, April 1995, London, MAFF ulbricht t l v and southgate d a t (1991), ‘Coronary heart disease: seven dietary factors’, Lancet, 338, 985–92 van de vijver l p l, kardinaal a f m, couet c, aro a, kafatos a, steingrimsdoit- tir l, amorim cruz j a, moreiras o, becker w, van amelsvoort j m m, vidal-jessel s, salminen i, moschandreas j, sigfusson n, martins i, carbajal, a, ytterfors a and van poppel g (2000), ‘Association between trans fatty acid intake and cardiovas- Enhancing the nutritional value of meat 245 cular risk factors in Europe: the TRANSFAIR study’, European Journal of Clinical Nutrition, 54, 126–35 walker a r p (1998), ‘The remedying of iron deficiency: what priority should it have?’ British Journal of Nutrition, 79, 227–35 watts g, ahmed w, quiney j, houlston r, jackson p, iles c and lewis b (1988) ‘Effec- tive lipid lowering diets including lean meat’, British Medical Journal (Clin Res Ed), 296(6617), 235–7 west d b, delany j p, camet p m, blohm f, truett a a and scimeca j (1998), ‘Effect of conjugated linoleic acid on body fat and energy metabolism in the mouse’, American Journal of Physiology, 44, R667–72 who (1990), Diet, Nutrition and the prevention of chronic diseases, Report of a WHO Study Group, WHO Technical Series 797, World Health Organisation, Geneva, Switzerland wilson a and ball m (1999), ‘Nutrient intake and iron status of Australian male vege- tarians’, European Journal of Clinical Nutrition, 53, 189–94 world cancer research fund (1997), ‘Food nutrition and the prevention of cancer: a global perspective’, Washington DC, American Institute Of Cancer Research zeigler r g, morris l e, blot w j, pottern l m, hoover r and fraumeni j f j (1981), ‘Esophageal cancer among black men in Washington DC. II Role of nutrition’, Journal – National Cancer Institute, 67, 1199–206 zheng j j, mason j b, rosenberg i h and wood r j (1993), ‘Measurement of zinc bioavail- ability from beef and a ready-to-eat high-fiber breakfast cereal in humans: application of a whole-gut lavage technique’, American Journal of Clinical Nutrition, 58, 902–7 246 The nutrition handbook for food processors