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Trends in Food Science & Technology 18 (2007) 567e578

Review

Healthier lipid formulation approaches in meatbased functional foods. Technological options for replacement of meat fats by non-meat fats
Francisco Jimenez-Colmenero*
Instituto del Fro (CSIC), Ciudad Universitaria, C/Jose Antonio Novais, 10, 28040-Madrid, Spain (Tel.: D34 91 549 23 00; fax: D34 91 549 36 27; e-mail: fjimenez@if.csic.es)
Healthier lipid formulation based on processing strategies is one of the most important current approaches to the development of potential meat-based functional foods. This article discusses the partial replacement of meat fats with various non-meat fats (of plant and marine origin) which are added to different meat products (fresh, cooked and fermented), using a variety of available technological options. It analyses factors associated with the composition and physicochemical properties of the new lipid materials used in meat processing. And it further discusses the consequences of changes in the composition of meat products as they relate to the potential contribution to fatty acid intake goals and lipid oxidation stability.

Introduction Recent advances in food and nutrition sciences have highlighted the possibility of modulating some specic
* Corresponding author.
0924-2244/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tifs.2007.05.006

physiological functions in the organism through food intake. This means that it is possible to help optimize certain physiological functions through the diet and/or dietary components in order to improve health status and wellbeing and/or reduce the risk of disease. This is the context in which we are seeing the emergence of so-called functional foods, which are currently an expanding market and one of the chief factors driving the development of new products. Like other food-related sectors, the meat industry is undergoing major transformations, driven among other things by changes in consumer demands. One of the main trends shaping developments in the consumption of meat derivatives is consumer interest in the possibilities of improving health through diet. Meat-based functional foods are seen as an opportunity to improve their image and address the needs of consumers, as well as to update nutrient dietary goals. Because of their importance, lipids are among the bioactive components (functional ingredients) that have received most attention, particularly (in quantitative and qualitative terms) with respect to the development of healthier meat products (Anandh, Lakshmanan, & Anjaneluyu, 2003; Arhiara, 2006; Fernandez-Gines, Fernandez-Lopez, Sayas Barbera, & Perez-Alvarez, 2005; Jimenez-Colmenero, Carballo, & Cofrades, 2001; Jimenez-Colmenero, Reig, & Toldra, 2006; Muguerza, Gimeno, Ansorena, & Astiasaran, 2004). There is growing evidence that dietary fat may play a role in the prevention of and therapy for a number of chronic disorders, particularly coronary heart disease. Recommendations for optimal intake of total and unsaturated fatty acids have been proposed by a number of scientic authorities and nutritional organizations including the World Health Organisation (WHO, 2003). Dietary fat intake should ideally account for between 15% and 30% of total diet energy. According to dietary recommendations for the intake of specic fatty acids as a proportion of total diet energy, no more than 10% of calorie intake should be from saturated fatty acids (SFAs), 6e10% should be from polyunsaturated fatty acids (PUFAs) (n-6, 5e8%; n-3, 1e2%), around 10e15% should be from monounsaturated fatty acids (MUFAs), and less than 1% should be from trans fatty acids. It is also recommended to limit cholesterol intake to 300 mg/ day (WHO, 2003). There is abundant evidence to suggest that regular consumption of and/or dietary supplementation with long chain n-3 PUFAs (eicosapentaenoic e EPA, 20:5 and docosahexaenoic e DHA C22:6 acids) confers a number

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of health benets (Garg, Wood, Singh, & Moughan, 2006; Simopoulos, 2002). Since the health implications of fat consumption are determined by the proportions between fatty acids, some recommendations are still made on the basis of specic fatty acid ratios. Accordingly, the recommended ratio of PUFA to SFA is between 0.4 and 1.0, and the n-6/n-3 PUFA ratio should not exceed 4 (Enser, 2000; Wood et al., 2003). Excessive amounts of n-6 PUFAs and very high n-6/n-3 PUFA ratios promote pathogenesis of many kinds, including cardiovascular disease (CVD), cancer and inammatory and autoimmune diseases, whereas increased levels of n-3 PUFAs (and low n-6/n-3 PUFA ratios) exert suppressive effects (Simopoulos, 2002). It was recently demonstrated that the greatest risk factor for arteriosclerosis and ischaemic heart disease is not hypercholesterolaemia or high cholesterol intake but a high n-6/n-3 PUFA ratio (Okuyama & Ikemoto, 1999). So, although it is frequently asserted that less fat in the diet is better, qualitative aspects of fat need to be taken into account, including the fact that some fatty acids are essential in our diet. Saturated, monounsaturated and n-6 polyunsaturated fatty acids make up most of the fatty acid present in human diet. Of the n-3 PUFAs, a-linolenic acid (ALNA, C18:3) is present in large quantities in plant products such as oils (maize, soy, cotton, canola, linseed, walnut, etc.), while other long chain fatty acids (EPA, docosapentaenoic acid e DPA C22:5 and DHA) are found largely in seafood (sh and algal oils). Depending on the different recommendations and on physical activity, a reasonable estimate of optimal intake would be 0.8e1.4 g (or even more) for EPA and DHA, or 3e5.5 g for total n-3 PUFAs per day (Kolanowski, Swiderski, & Berger, 1999). Western diets are decient in n-3 PUFAs (especially long chain) and contain excessive amounts of n-6 PUFAs, with an n-6/n-3 PUFA ratio of 15e20 as opposed to the recommended range of 1e4 (Simopoulos, 2002). Moreover, consumption trends for food containing n-3 PUFAs are currently static or declining (Lee, Faustman, Djordjevic, Faraji, & Decker, 2006). Therefore, in order to improve the health status of the population, health agencies and professional organizations have issued recommendations to increase the consumption of food rich in n-3 PUFAs (especially for certain sectors of the population), as a means of promoting a reduction in the n-6/n-3 PUFA ratio (Garg et al., 2006; Kolanowski et al., 1999; Simopoulos, 2002). Similarly, diets rich in monounsaturated fat have been associated with positive health benets (Mattson & Grundy, 1985), and it is therefore recommended that the majority of fatty acids be derived from monounsaturates (Simopoulos, 2002). The recommendations cited in fact refer to the overall diet; however, given that meat and meat products are some of the most important sources of dietary fat (Givens, Khem, & Gibbs, 2006; Valsta, Tapanainen, & Mannisto, 2005) and the PUFA/SFA and n-6/n-3 PUFA ratios of some meats are naturally somewhat removed from the

recommended values (Wood et al., 2003), changes in the amounts and the lipid proles of such products could help to improve the nutritional quality of the Western diet (Anandh et al., 2003; Arhiara, 2006; Fernandez-Gines nez-Colmenero et al., 2001, 2006). et al., 2005; Jime Although meat, particularly red meat, is already an important dietary source of long chain n-3 PUFAs, in which DPA predominates, further enrichment of meat with these PUFAs may be a practical means of increasing population intakes of n-3 PUFAs (Howe, Meyer, Record, & Baghurst, 2006). The unwillingness of consumers to change dietary habits suggests that there is a considerable potential market for frequently consumed foods such as meats which have been reformulated to incorporate health benets. At the same time, the diversication of products with health-promoting ingredients offers added possibilities of augmenting their presence in the diet and thus coming closer to recommended intakes. In response to these considerations, numerous researchers are endeavouring to optimize the amounts of lipids and the fatty acid proles of various meat products in order to achieve a more convenient composition related to nutrient intake goals. Lipids have been cited as functional ingredients in some reviews dealing with the development of designer meat foods (Anandh et al., 2003; Arhiara, 2006; Fernandez-Gines et al., 2005; JimenezColmenero et al., 2001, 2006), but there have been no reports of research that specically analyses non-meat lipid sources, technological options for replacement of animal fat, or problems and consequences of use in the formulation of different meat products. This paper reviews processing strategies for the development of healthier lipid meat products, looking at the different non-meat fats (of plant and marine origin) added to various meat products as partial meat fat replacers, and also the various technological options available for that purpose. This aspect is particularly important given the differences in the composition, physicochemical properties and stability of the new lipid materials being used in meat processing. It also discusses the consequences of composition changes as regards their potential contribution to fatty acid intake goals. Processing strategies to develop healthier lipid formulation in meat products In the development of healthier meat and meat derivatives, a number of different strategies have been described for modulating the presence of numerous compounds (endogenous and exogenous) that have various different potential effects on the organism. Hitherto, qualitative and/or quantitative changes in the lipids present in meat and meat derivatives have mainly been achieved by means of animal production practices and processing strategies (Jimenez-Colmenero et al., 2001, 2006). Genetic and dietary approaches have been reported as means of altering fatty acid contents and/or proles of the meat. Recent reviews describe the opportunities that these offer (Givens et al., 2006; Jimenez-Colmenero et al.,

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2006; Raes, De Smet, & Demeyer, 2004; Scollan et al., 2006; Wood et al., 2003). Leaving aside approaches involving animal feeds (not discussed in this paper), there have been many studies involving the alteration of lipid contents and proles of processed meats by means of processing strategies, which offer more opportunities and are more versatile. Reformulation of meat derivatives is one of the strategies that has been studied in order to develop meat-based functional foods. Where the lipid fraction is concerned, reformulation is generally based on the replacement (to a greater or lesser extent) of the animal fat normally present in the product with another fat whose characteristics are more in line with health recommendations: i.e., with smaller proportions of SFAs and larger proportions of MUFAs or PUFAs, better n-6/n-3 PUFA and PUFA/SFA ratios, and if possible cholesterol-free. There are various plant and marine lipid sources that can help supply such nutritional and functional benets to varying degrees. Non-meat fats used to formulate healthier meat products Meat product fatty acid composition can be modied by the formulation approach through the ingredients employed: meat raw material and non-meat ingredients. A variety of non-meat fats of plant and marine origin (Tables 1e3) have been added to different meat products as partial substitutes for meat fats (mainly from pork or beef). The type of vegetable oil affects the fatty acid composition of a reformulated meat product. Vegetable oils are rich sources of MUFAs and PUFAs and are cholesterol-free. In order to improve their nutritional quality, various meat products have been made using oils from olive, high-oleic acid
Table 1. Fresh meat products formulated with different non-meat fats Products Ground beef patties Oil Corn Cottonseed Palm Peanut Soybean Palm Soybean Palm mid-fraction Palm super-olein Palm stearin Rened Groundnut Maize Algal Algal Incorporation Solid form: Solid form: Solid form: Solid form: Solid form: Solid Liquid Solid Liquid Solid PHa PH PH PH PH

sunower, linseed (axseed), soybean, peanut, palm, etc. While some of these oils have been used to promote MUFA content, others are used essentially for their PUFA, or more specically n-3 PUFA, contents. Besides providing a source of various health-promoting fatty acids, vegetable oils have been used because they contain a wide range of other bioactive compounds, some of them antioxidant. Of vegetable oils, olive is the one that has received most attention, chiey as a source of MUFAs. Olive oil is the most monounsaturated vegetable oil and has a high biological value, attributed to a high ratio of vitamin E to polyunsaturated fatty acids. It has a lower ratio of saturated to monounsaturated fatty acids than any other vegetable oil and contains antioxidant substances in optimum concentrations (Bloukas, Paneras, & Fournitzis, 1997). Olive oil intake is associated with a lessened risk of heart disease and breast cancer, and it has positive effects on colon cancer. Also, it has benecial effects on postprandial lipid metabolism and thrombosis and inhibits LDL oxidation (Luruena-Martinez, Vivar-Quintana, & Revilla, 2004). Partial substitution (in various percentages) of pork backfat by olive oil has been tried in various cooked and cured meat products, adding between 1 and 10 g of olive oil per 100 g of product (Tables 2 and 3). In the case of meat-based gel/emulsion products, the purpose of substitution has been essentially to produce low-fat formulations (Table 2), but it has also been tried in fermented products with normal-fat formulations (Table 3). Olive oil increases MUFAs in meat products without signicantly altering the n-6/n-3 PUFA ratio (Ansorena & Astiasaran, 2004; Muguerza, Fista, Ansorena, Astiasaran, & Bloukas, 2002). Substantial amounts of MUFAs have also been

Fat content (g/100 g) 9.6 9.9 9.6 9.6 9.6 14e45 14e45 14e45 14e45 15 17 18 3 21 2 20 e 15

Oil content (g/100 g) 5 5 5 5 5 5e40 5e40 5e40 5e40 15 14 15 1.1 1.1 1.1 1.1 <15

n-3 PUFA g/100 g e e e e e e e e e e e e 0.400 0.400 0.402 0.397 0.402 e

Source 1

Ground beef patties

Beef burgers Ground beef patties

3 4

Ground turkey patties Fresh pork sausages Ground turkey patties Fresh pork sausages Restructured hams Beef burgers

Liquid Liquid Oil-in-water emulsioneWPIa Oil-in-water emulsioneWPI

5 6

Palm

Solid

1. Liu et al., 1991; 2. Shiota et al., 1995; 3. Babji et al., 1998; 4. Dzudie et al., 2004; 5. Lee, Faustman, et al., 2006; 6. Lee, Hernandez, et al., 2006; 7. Wan Rosli, Babji, Aminah, Foo, & Abd Malik, 2006. a PH, partially hydrogenated; WPI, whey protein isolate.

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Table 2. Cooked meat products formulated with different non-meat fats Products Oil Incorporation Fat content (g/100 g) 17 15 12e29 11e28 15 11 10 10 10 10 22 22e30 22 22 22 10 10 10 10 9 5e7 21e22 18e19 18e21 31 12 25 25 Oil content (g/100 g) 7.5e13.1 5 7.2e17.4 6e24 10 7 6.7 6.7 6.7 6.7 19.5 19.5e27.5 19.5 19.5 19.5 4 4 4 4 2.7e5.4 4e6 6e10 6e10 6e10 1.2e5 5 10e20 10e20 % of Cholesterol reductionb e e 17e35 e e e e e e e e e e e e e 59 52 56 e e e e e e e e e n-3 PUFA g/100 g e e e e e e 0.05c 0.03c 0.02c 0.44c e e e e e e 0.10c 0.06c 0.15c e e e e e e e e e MUFA g/100 g 12.2c e e e e e 6.8c 3.1c 2.9c 2.5c e e e e e e 4.0c 4.0c 5.0c e e e e e e e e e n-6/n-3 PUFA e e e e e e 14.8 132 215 7.7 e e e e e e 24 31 10 e e 8.6e10.0 6.5 9.3e10.7 e e e e MUFA/ SFA 5.0e6.2 e e 2.6e3.8 e e 2.9 1.5 1.4 1.2 e e e e e e 1.1 1.0 1.3 e e 0.78e1.1 0.69e0.98 1.27e1.18 e e e e PUFA/SFA Source

Frankfurter Frankfurter Frankfurter Bologna Frankfurter Frankfurter

High-oleic acid sunower Deodorized sh Peanut High-oleic acid sunower Corn Virgin olive Olive (O) Corn Sunower Soybean (S) Soyseed Sunower Cottonseed (C) Corn seed Palmine Olive O C S OC OS Olive 11 Plantd Palm Cottonseed Olive Soybean Olive Rened, bleached and deodorized palm Palm stearin

Liquid Liquid Liquid Liquid Pre-emulsied/ SCa Pre-emulsied/SC Pre-emulsied/SC

5.9e7.3 e e 3.1e4.5 e e 0.33 1.74 1.95 1.79 e e e e e e 0.61 0.49 0.44 e e 0.06e0.11 0.23e0.59 0.08 e e e e

1 2 3 4 5 6

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Beef frankfurters and cooked salamis

Frankfurter Frankfurter

Liquid Liquid Liquid Liquid Solid Pre-emulsied/SC Pre-emulsied/SC

8 9

Frankfurter Emulsied meatballs (Kung-wans) Frankfurter

Pre-emulsied/SC Liquid and solid Interesteried Interesteried Interesteried Liquid Liquid Melted (55  C) Melted (55  C)

10 11 12

Spreadable liver sausage Frankfurter Chicken frankfurters

13 14

1. Park et al., 1989; 2. Marquez et al., 1989; 3. Park et al., 1990; 4. Bishop et al., 1993; 5. Bloukas & Paneras, 1993; 6. Paneras & Bloukas, 1994; 7. Ambrosiadis et al., 1996; 8. Bloukas et al., 1997; 9. Paneras et al., 1998; 10. Pappa et al., 2000; 11. Hsu & Yu, 2002; 12. Vural et al., 2004; 13. Hong et al., 2004; 13. Luruena-Martinez et al., 2004; 14. Tan et al., 2006. a SC, Sodium caseinate. b Versus the control sample. c Estimated using 0.950 as conversion factor to give total fatty acids in fat. d Coconut, sunower, palm, corn, peanut, soybean, tea seed and olive oils, and hydrogenated oils from coconut, palm and soybean.

Table 3. Fermented meat products formulated with different non-meat fats nez-Colmenero / Trends in Food Science & Technology 18 (2007) 567e578 F. Jime Products Oil Incorporation Fat contentb (g/100 g) 25 23 31 26e27 26e27 e 20 31e34 29e33 27 30e32 39 40 35 39 39 Oil content (g/100 g) 3.3e6.6 3.3e6.6 1.31e3.95 3e16 3e16 e 3e9 1.97e3.28 0.5e1.1 3.3 3.3 4.5 3.0e6.0 6.0 3.0e6.0 4.5 % of Cholesterol reductionc e e 4e22 e e e 12e35 0 0 31 e e e e e e n-3 PUFA g/100 g e e e e e e e 0.51e0.62d 0.56e1.01d 1.41 2.44d 3.82d 2.38e4.72d 4.33d 0.75e0.89d 0.38d MUFA g/100 g e e 14.2e16.3 e e e e 14.3e13.1d 12.6e13.8d 11.98 11.8d 13.34d 16.4e15.4d 13.61d 17.9e18.0d 17.0d n-6/n-3 PUFA e e e e e e e 11 7.7e5.3 3.0 1.7e2.1 1.06 1.93e1.05 0.87 6.94e5.12 9.59 PUFA/SFA Source

Fermented sausages Spanish fermented sausage chorizo Turkish semi-dry fermented sausages Salami Dry fermented sausage Turkish soudjouk Spanish fermented sausage chorizo Dry fermented sausage Dry fermented sausage Dry fermented sausage Dutch style fermented sausage

Olive Olive Olive Palm Cottonseed Extra virgin olive Olive Soy Fish oil extract Deodorized sh oil Linseed Flaxseed Flaxseed Flaxseed Canola Fish

Liquid Pre-emulsion/ISPa Pre-emulsion/ISP Interesteried Interesteried Liquid: pre-mixed with SCa Pre-emulsion/ISP Pre-emulsion/ISP Pre-emulsion/ISP Pre-emulsion/ISP Pre-emulsion/ISP Encapsulated Pre-emulsion/ISP Pre-emulsion/SCa Pre-emulsion/ISP Encapsulated

e e 0.42e0.61 0.07e0.11 0.15e0.80 e 0.01e0.02 0.51e0.73 0.50e0.58 0.56 0.6e.07 0.59 0.49e0.71 0.69 0.42e0.48 0.31

1 2 3 4 5 6 7 8 9 10

1. Bloukas et al., 1997; 2. Muguerza et al., 2001; 3. Vural, 2003; 4. Severini et al., 2003; 5. Kayaardi & Gok, 2003; 6. Muguerza, Ansorena, & Astiasaran, 2003; 7. Muguerza, Ansorena, et al., 2004; 8. Valencia et al., 2006; 9. Ansorena & Astiasaran, 2004; 10. Pelser et al., 2007. a ISP, isolated soy protein; SC, sodium caseinate. b Initial fat content. c Versus the control sample. d Estimated using 0.950 as conversion factor to give total fatty acids in fat.

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incorporated by addition of high-oleic acid sunower oil (Park, Rhee, Keeton, & Rhee, 1989; Park, Rhee, & Ziprin, 1990). Animal fat has been partially replaced with various vegetable oils (cottonseed, corn, soybean, peanut, etc.) to increase PUFA levels, improve fatty acid proles (PUFA/ SFA ratio) and reduce cholesterol contents of different meat products (Tables 1e3). Cottonseed and corn oils are very rich in PUFAs and contain very high concentrations of linoleic acid (LA, 18n2:6) (>56% of total fatty acid); their addition to meat products does reduce PUFA/SFA ratios, but it also has the unwanted effect of raising the n-6/ n-3 PUFA ratio (Paneras & Bloukas, 1994; Paneras, Bloukas, & Filis, 1998). Soybean oil contains high levels of both LA (56.1% of total fatty acid) and ALNA (7.3%) (Paneras et al., 1998). Canola oils (with 20% LA and 8% ALNA) have been used to increase the PUFA/SFA ratio in fermented sausages (Pelser, Linssen, Legger, & Houben, 2007). Animal fat has been substituted by groundnut and maize oils, which are cholesterol-free and have a higher ratio of unsaturated to saturated fatty acids, to improve the nutritional value of ground beef (Dzudie, Kouebou, EssiaNgang, & Mbofung, 2004). When added to restructured beef roast, rice bran oil not only favours the presence of LA but also has useful antioxidant activity and vitamin E stabilizing effects (Kim, Godber, & Prinaywiwatkul, 2000). Palm oil and its products are used in the reformulation of meat products (Tables 1e3) because of a number of desirable characteristics (easy to use at normal ambient temperature, cholesterol-free and naturally contain antioxidants) (Babji et al., 1998; Babji, Alina, Yusoff, & Wan Sulaiman, 2001). However, palm fat has a high content of the saturated palmitic acid, which is considered a risk factor for CVD. Vegetable and marine oils have been used to supply substantial amounts of n-3 PUFAs in order to produce n-3 PUFA-enriched meat products (Tables 1e3). Linseed oil containing 57% ALNA (Pelser et al., 2007) has been used to alter the PUFA/SFA and n-6/n-3 PUFA ratios (Ansorena & Astiasaran, 2004; Pelser et al., 2007; Valencia, Ansorena, & Astiasaran, 2006). Fish oils containing approximately 22% EPA, 3% DPA and 22% DHA (Pelser et al., 2007) are one of the food sources of long chain n-3 PUFAs. The two main problems associated with them are susceptibility to lipid oxidation and a residual shy aroma and taste. These problems can often be minimized by rening and deodorizing the oil, and by applying various antioxidant strategies (Garg et al., 2006). Fish oil has been used in various forms and levels to enrich different food products with long chain n-3 PUFAs (Kolanowski & Laufenberg, 2006), including some meat derivatives (Tables 2 and 3). Some marine algae produce DHA-rich oil, which is processed in the same way as most vegetable oils. After extraction, the oil is desolventized, winterized, rened, bleached, deodorized and nally diluted with vegetable oil (high-oleic sunower oil) to

bring the DHA level to 40% (Becker & Kyle, 1998). Algal oil has been used to produce meat products (Lee, Faustman, et al., 2006; Lee, Hernandez, et al., 2006). Numerous plant materials have been used as ingredients in meat products essentially for purposes of economy, technology and composition (nutrition and health). In some of these non-meat ingredients the lipid component plays a critical role both quantitatively and qualitatively, and one example of this is the development of meat-based functional foods with walnut. Walnuts have a high fat content (62e68%) and are rich in MUFAs (oleic acid, 18% of total fatty acids) and PUFAs (LA and ALNA, which respectively account for 58% and 12% of total fatty acids). Olmedilla-Alonso, Granado-Lorencio, Herrero-Barbudo, and Blanco-Navarro (2006) reported health benets of walnut consumption with respect to the risk of coronary heart disease and proposed a nutritional basis for and a technological approach to the development of functional meat-based products with potential for the reduction of CVD risk. The FDA recently authorized a qualied health claim indicating that eating 42.5 g per day of walnuts, as part of a lowsaturated-fat and low-cholesterol diet not resulting in increased caloric intake, may reduce the risk of CVD (FDA, 2004). The effect of walnut addition on the nutritional prole of restructured beefsteak (Serrano et al., 2005) and frankfurter sausage (Ayo et al., in press) has been reported. Conjugated linoleic acid (CLA), a component of ruminant meat, has been shown to have benecial effects such as anticarcinogenic and antiatherogenic activity, and to alter the partition of energy toward protein deposition instead of fat (Enser, 2000). Fatty acid proles of meat products have been improved by direct addition of CLA to pork patties (Joo, Lee, Hah, Ha, & Park, 2000) or beef patties (Chae, Keeton, & Smith, 2004; Hur et al., 2004) and by injection into beef strip loin (Baublits et al., 2007). Other lipid materials (e.g., ginger and basil essential oils) have been added to meat products less to induce quantitative or qualitative changes in fatty acid proles than to harness specic desirable activities e e.g., antioxidant e or some other components (e.g., aromatic substances). Technology options for replacement of meat fats Both liquid oils and plastic fats (solid at room temperature) have been used to produce healthier content and lipid prole formulations in meat-based functional foods (Tables 1e3). Compared to habitually used meat fats, these new lipid materials (of plant or marine origin) have different physicochemical characteristics which may mean that meat processing conditions have to be adjusted to induce the desired quality attributes in the reformulated product. The procedures used to incorporate natural or processed plant and marine lipids in meat products range from direct addition as liquid oils or as solids (including interesteried oils) to incorporation in encapsulated or pre-emulsied form or as part of plant ingredients. The potential of these

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approaches varies, among other factors, according to the type of product. The following is an account of the different technology options for meat fat replacement that have been assayed for the development of healthier lipid meat products. Incorporation as liquid oil Oils are among the most commonly used lipid materials for animal fat replacement. Since they are liquid at room temperature or even under refrigeration, incorporation in some types of processed meat can pose technological difculties. The oil needs to be incorporated in the form of stable oil droplets which do not coalesce during product processing or cooking, as otherwise this would result in liquid loss and poor quality. Another vital aspect is that they are more susceptible to lipid oxidation because of their highly unsaturated fatty acids. Liquid oil has been incorporated in a variety of meat products (Tables 1e3). Incorporation conditions vary according to factors connected with the type of product (intact muscle tissue, fresh, gel/emulsion-based or fermented products) and with the characteristics and amount of the incorporated oil. In meat products made with intact muscle tissue, liquid oil has been added by micro-injection. This procedure generally needs to be accompanied by other ingredients and mechanical processes in order to favour product characteristics (Domazakies, 2005). Liquid oils have been added directly to products like beef patties (Dzudie et al., 2004; Shiota et al., 1995), fermented sausages (Bloukas et al., 1997) and salami (Severini, De Pilli, & Baiano, 2003). However, Bloukas et al. (1997) reported that direct incorporation of olive oil in fermented sausage produced an unacceptable appearance and very soft texture. End chopping temperature is crucial in determining the emulsion stability of meat batters, although the ideal chopping temperature is highly dependent on the degree of comminution and percentage of fats present in the formulation (Whiting, 1987). Liquid oil is added to gel/emulsion products at the end of the emulsication process both with (Ambrosiadis, Vareltzis, & Georgakis, 1996) and without (Hong, Lee, & Min, 2004) temperature control. In order to increase the viscosity of liquid oils, Luruena-Martinez et al. (2004) used olive oil at 6  C to replace 5% of pork fat in lowfat frankfurters. Incorporation as pre-emulsied oils Pre-emulsion is generally used when incorporating fats that are difcult to stabilize. A pre-emulsion is an oilin-water emulsion with an emulsier, typically a protein of non-meat origin. It is made prior to meat product manufacture and is added as a fat ingredient to meat products. Oil pre-emulsion technology with a non-meat protein improves the systems fat binding ability, since the oils can be stabilized or immobilized in a protein matrix. This reduces the chances of bulk oil physically separating from the structure of the meat product so that it remains stable

throughout the range of environmental conditions that are likely to be encountered during processing, storage and consumption (Djordjevic, McClements, & Decker, 2004). Besides being physically stable throughout a products lifetime, oil-in-water emulsions constitute an excellent means of enhancing the oxidative stability of lipids in bulk oils, as additional protective measures such as antioxidants can be used to inhibit lipid oxidation. Also, oil-inwater emulsions are easier to disperse into water-based systems such as muscle foods (Djordjevic et al., 2004). Because of their physicochemical characteristics, preemulsions are suitable for use in the formulation of a wide variety of meat products (Tables 1e3). A number of procedures have been reported for producing an oil (plant or marine) pre-emulsion for incorporation in meat derivatives. The most commonly applied is one proposed by Hoogenkamp, which has been used in numerous applications (Ansorena & Astiasaran, 2004; Bloukas & Paneras, 1993; Bloukas et al., 1997; Paneras & Bloukas, 1994; Pappa, Bloukas, & Arvanitoyannis, 2000; Pelser et al., 2007; Valencia et al., 2006). The pre-emulsion was prepared by mixing eight parts of hot water (50e60  C) with one part of sodium caseinate or isolated soy protein for 2 min. The mixture is emulsied with 10 parts of oil for another 3 min. Pre-emulsions of olive, linseed, deodorized sh or canola oils have been prepared using this method (Tables 2 and 3). Generally speaking, sodium caseinate (SC) has been used as an emulsier in sausagetype products, whereas soy protein isolate (SPI) has been used in fermented products (Tables 2 and 3). Pelser et al. (2007) report that SC appeared not to be suitable for preemulsication of axseed oil for use in the preparation of Dutch style fermented sausages; they explain that emulsication was inadequate and a lm formed between casing and meat so that the product was not completely dried. Other pre-emulsion procedures basically entail altering the proportion of watereemulsiereoil and the emulsifying conditions. For example, a pre-emulsion of corn oil was prepared by adding the oil, water and sodium caseinate (ratio 8:8:1) simultaneously to the bowl chopper and chopping for 5 min (Bishop, Olson, & Knipe, 1993). The olive oil pre-emulsion used in the preparation of a traditional Turkish fermented dry sausage was prepared with water, isolated soy protein and olive oil in the proportion 5:1:5 (Kayaardi & Gok, 2003). Djordjevic et al. (2004) described the preparation of an oil-in-water emulsion with 25 wt % algal oil or menhaden oil stabilized by whey protein isolate (WPI) or sodium caseinate and antioxidants (tocopherol and EDTA), at pH 3. They found that WPI-stabilized algal oil-in-water emulsions were stable to oxidation and physically stable at pH 3. On the basis of that procedure, Lee, Faustman, et al. (2006) and Lee, Hernandez, et al. (2006) prepared an algal oil pre-emulsion (pasteurized for 30 min at 75  C), which was used to make fresh ground turkey, fresh pork sausage and restructured ham.

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Pre-emulsied corn oil with SPI has been incorporated in the place of animal fat in model comminuted meat gels (Mourtzinos & Kiosseoglou, 2005). Oil-in-water emulsions (30% oil) were prepared by rst dissolving soy protein isolated at pH 6.5, followed by dropwise addition of corn oil to the continuous phase (1% protein) while mixing with the aid of a mechanical stirrer. The resulting crude emulsions were used to prepare the comminuted meat gels. Pre-emulsions were prepared the day before production of meat products (Bishop et al., 1993; Pappa et al., 2000) or on the day of use (Bloukas & Paneras, 1993; Paneras et al., 1998). Incorporation as encapsulated oil The food industry uses microencapsulation for a number of purposes, such as stabilization of active substances, controlled release of active substances, or masking an unpleasant taste or smell (Kolanowski & Laufenberg, 2006). Microencapsulation of oils facilitates their handling and incorporation in food products, where they delay/inhibit oxidation, help to mask undesirable odours or avours in nal products and improve bioavailability of n-3 PUFAs (Garg et al., 2006). Most microencapsulated oil products are based on the formation of sh oil emulsions using proteins, polysaccharides, lecithin and other low molecular weight emulsiers. The emulsions are then spray-dried (the low-cost microencapsulation technology commonly used in the food industry) to form microcapsules. The amount of oil that can be delivered in this format varies from 1% to 30%; the levels of incorporation that can be achieved with existing technologies are very low and the amount of (long chain) n-3 PUFAs required to meet recommended allowances is impractical in most cases (Garg et al., 2006). These technologies have been used to fortify frequently consumed food (breads, soups, etc.) with reasonable consumer acceptability (Garg et al., 2006), although their use in meat products has been very limited (Table 3). Encapsulated axseed oil and sh oil have been used to replace 15% of animal fat (pork backfat) in fermented sausages (Pelser et al., 2007). Incorporation as solid fat Natural or processed solid vegetable fats have been used to prepare a number of meat products (Tables 1e3). Some vegetable fats like palm oil present high consistency at ambient temperature because of their high solid glyceride content. A wide range of functionalities and plasticity can be achieved in palm oil products by varying the blend of stearin and olein. Palm oils, oleins and stearins blended together with food additives have been incorporated in several meat products (Babji et al., 2001). Their specic physicochemical characteristics can require some variations in meat processing conditions. For instance, when plastic fats are incorporated into meat batters during chopping, higher energy input is needed to sufciently disperse the

fats, and the heat generated can lead to the formation of a less stable meat emulsion (Tan, Aminah, Zhang, & Abdul, 2006). Whiting (1987) attributed the poor emulsion stability of meat batters containing fats with high melting points to the limited ability of chopping equipment to disperse fats sufciently into small particles. It has been suggested that melting of these fats before incorporation into meat batters could overcome the emulsion breakdown problem, as they would become viscous enough to be readily mixed into the meat batters (Tan et al., 2006). It is also the case that the melting point affects sensory attributes of meat products. For example, fat which is solid at 35e40  C confers a waxy texture. If the melting point is below these temperatures, there is no undesirable waxy aftertaste, which is caused by incomplete melting of fat in the mouth and can affect consumer acceptance (Babji et al., 1998, 2001). Processes like partial hydrogenation and interesterication are used to simulate the consistency of highmelting-point fats. To produce a solid form, vegetable oils are hydrogenated to eliminate double bonds by direct addition of hydrogen to unsaturated fatty acids. It is well known that the hydrogenation process, in which SFAs e and particularly the trans fatty acid (TFA) e are formed, presents various adverse effects on health (Simopoulos, 2002). Partially hydrogenated plant oils (corn, cottonseed palm, peanut and soybean) have been substituted for beef fat in lean (10% fat) ground beef patties (Liu, Huffman, & Egbert, 1991). Also, partially hydrogenated palm oil has been used in the formulation of beef burgers (Babji et al., 1998). Interesterication has been used to modify physicochemical properties of vegetable oils. In this process, which can be achieved by either chemical or enzymatic means, the positions of an acyl group are changed within a triglyceride or among triglyceride molecules. The result is a higher melting point, but without any formation of SFAs or TFAs. Interesterication lacks the adverse effects of hydrogenation, so that interesteried oils offer an attractive alternative as fat replacers in meat products. Interesteried vegetable oils prepared from different plant sources (palm, cottonseed and olive) have been used as fat replacers to modify the fatty acid composition of frankfurters and semi-dry fermented sausage (Javidipour & Vural, 2002; Javidipour, Vural, Ozen, Ozbas, & Tekin, 2005; Vural, 2003; Vural, Javidipour, & Ozbas, 2004). Healthier lipid product composition and contribution to fatty acid intake goals One of the most important aspects of the design of potential functional foods is the scale of the alterations needed to achieve potential health-promoting functions. One of the possible limitations affecting fortied products is that large quantities may need to be consumed to assure recommended intake levels (Garg et al., 2006). This being so, an analysis of the different meat products that have been formulated (Tables 1e3) would help to assess the importance

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of the composition changes that have been made and how they affect intake levels when consumed on a regular basis. Fresh meat products Non-meat fat (plant oils and algal oil) in various forms and concentrations has been used to improve the lipid composition of various fresh meat products (Table 1). The effort required to replace animal fat varies widely depending on the fat content of the meat product. In products containing low fat (<10%), regardless of the percentage of fat replaced, the presence of non-meat fat in the product is limited ( 5 g/100 g). In medium- to high-fat products, more animal fat is replaced and hence there is a larger intake of healthier non-meat lipids when the new product is consumed in its normal form. A variety of fresh products have been reformulated in order to improve their healthy lipid prole, but little has been done to conrm the consequences of this as regards composition (cholesterol reduction, n-6/n-3 PUFA, n-3 PUFA intake, etc.) (Table 1). To achieve 500 mg n-3 PUFA/ 110 g of product, Lee, Faustman, et al. (2006) and Lee, Hernandez, et al. (2006) prepared fortied fresh ground turkey and fresh pork sausage using algal oil. The actual level of n-3 PUFA incorporation in both meat products (430e450 mg/110 g) was greater than 87% (Lee, Faustman, et al., 2006), although cooking resulted in some loss of the n-3 PUFAs used to fortify meat products (Lee, Her nandez, et al., 2006). In restructured beefsteak (13% fat) formulated with 20% added walnut, around 90% of the fat content came from walnut (Serrano et al., 2005). MUFAs and PUFAs together accounted for almost 90% of total fatty acids, with n-6/n-3 PUFA <4 and PUFA/SFA >6.5. One hundred grams of this kind of restructured steak would supply 20 g of walnut to the diet; that is almost half (47%) of the daily amount recommended by the FDA (2004) to allow a qualied health claim for product labels for walnut and to reduce the risk of coronary heart disease. Cooked meat products Most research on healthier cooked product formulation deals with meat-based gel/emulsion products, especially frankfurters, largely low-fat and in some cases with limited amounts of non-meat fats (Table 2). A large variety of plant and marine oils (olive, cottonseed, sunower, soyseed, high-oleic acid sunower, palm, sh, etc.) have been used to produce healthier cooked products; they have been added in different forms: directly to the emulsion (in liquid or solid form at the end of the process), pre-emulsied (generally with sodium caseinate) or interesteried (Table 2). Large proportions of vegetable fat have also been added as part of a non-meat ingredient such as walnut (Ayo et al., in press). As in fresh meat products, much of the effort that has gone into the design of products has not been accompanied by an assessment of the consequences for their lipid

proles. In products of this kind the benets of composition changes have been estimated mainly in terms of modications to MUFA/SFA and PUFA/SFA ratios and to a lesser extent in terms of reduced cholesterol and n-6/n-3 PUFA ratios (Table 2). While varying according to the type of oil used, the results suggest that MUFA/SFA and PUFA/SFA ratios are increased by replacing meat fat with non-meat fats. Frankfurters made with MUFA-rich oils such as olive or high-oleic acid sunower (Paneras & Bloukas, 1994; Paneras et al., 1998; Park et al., 1989) contain between 3 and 12 g of MUFAs per 100 g of product, which would account for 1e5% of energy intake in a 2000 kcal/day diet. In products of this kind the presence of these oils produces no great changes in n-6/n-3 PUFA ratios. This contrasts with the addition of linoleic acid-rich oils like cottonseed (Paneras et al., 1998) or corn (Paneras & Bloukas, 1994), which produces frankfurters with high n-6/n-3 PUFA ratios (Table 2). Products formulated with soybean oils are different in that although containing high levels of LA, they also present high concentrations of ALNA, so that a high n-6/n-3 PUFA ratio is not attained (Paneras & Bloukas, 1994). Nonetheless, it has been recommended to keep n-6 PUFA in the diet as low as possible to optimize the benets from n-3 PUFA (Garg et al., 2006). The data from studies on cooked meat products show that by and large the presence of n-3 PUFAs is very slight, generally less than 0.15 g/100 g (Table 2), and hence they contribute little in terms of dietary recommendations. This does not apply to frankfurters reformulated with 25% added walnut (Ayo et al., in press), which present a healthy polyunsaturated fatty acid prole, with an n-6/ n-3 PUFA ratio of 4.89 and a PUFA/SFA ratio of 5.9 (versus 13e15 and 0.35e0.40, respectively, in full-fat meat products). Almost 70% of total fatty acids were PUFAs and 88% MUFAs PUFAs. Fermented sausages There have been numerous studies reporting new formulations for healthy fermented sausages using vegetable and marine oils as partial substitutes of animal fat (Table 3). A variety of products have been prepared with different types of oils (olive, soy, linseed, canola, sh, etc.) added in liquid, encapsulated or interesteried forms, but the most widely assayed method is pre-emulsication, mainly with soy protein isolate. Modication of the lipid fraction in fermented sausages poses considerable difculties in terms of manufacturing technology and physicochemical characteristics (Muguerza, Gimeno, et al., 2004). This is assuredly one of the reasons why, although the products analysed contain high fat concentrations (20e40%), less than 6 g/ 100 g of non-meat fat has generally been incorporated, that is below the levels assayed in other kinds of products (Tables 1 and 2). The improvement in nutritional quality that is achieved by modication of the lipid fraction through changes in the formulation of fermented products depends on the

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type and amount of oil that is incorporated. In general, the addition of oils raises PUFA/SFA ratios and reduces n-6/n-3 PUFA ratios, bringing values closer to the recommended goals (Table 3). The range of cholesterol reduction is 4e 35% (Table 3), but sh oil raises the content by 31% as compared to products with only pork fat (Valencia et al., 2006). One hundred grams of healthier fermented sausages can supply n-3 PUFA in quantities ranging from 380 to 4720 mg (Table 3), which is a considerable amount in terms of dietary recommendations (Kolanowski et al., 1999). The amount of MUFAs is generally between 12 and 18 g per 100 g of edible portion. In the context of a 2000 kcal diet this means that 5.4e8.1% of energy intake is from MUFAs and 0.17e2.1% n-3 from PUFAs. Inuence of reformulation on processing and quality characteristics Various different strategies have been tried to minimize the consequences of composition change for processing and product characteristics. One of the main potential problems posed by these modications is how they may inuence the rate and extent of lipid oxidation, which in turn affects quality characteristics and has health implications. There are a number of factors determining the scale of this phenomenon. Susceptibility to lipid oxidation can be augmented by an increment in unsaturated fatty acids, particularly polyunsaturated, processing conditions like grinding, cooking, drying, etc. which entail exposure to high temperatures, decompartmentalization of prooxidants and antioxidants or enhanced access of oxygen to the substrate (Lee, Hernandez, et al., 2006). The addition of maize oil and essential oils (natural antioxidants) has been found to minimize lipid oxidation in beef patties (Dzudie et al., 2004). An antioxidant combination containing a radical quencher (rosemary extract), a sequestrant (sodium citrate) and a reductant (sodium erythorbate) incorporated into n-3 PUFA-fortied meat products (fresh ground turkey, fresh pork sausage and restructured ham) effectively minimizes lipid oxidation during fresh and post-cooking storage (Lee, Faustman, et al., 2006; Lee, Hernandez, et al., 2006). No specic problems have generally been reported in connection with oxidative stability in gel/emulsion meatbased products formulated with healthier lipid proles (Table 2). This fact has been put down to a variety of factors: the presence of a curing mixture ingredient containing substances such as nitrite, phosphate or ascorbate which act as antioxidants (Marquez, Ahmed, West, & Johnson, 1989); the natural presence of various antioxidant substances (tocopherols, phenolic compounds) in several of the plant oils used e for example, olive oil (Bloukas et al., 1997) or corn oil (Bishop et al., 1993) e or nally the absence of phospholipids in rened oils (Bishop et al., 1993). No oxidation problems have been detected in partial substitution of pork backfat by olive oil (Bloukas et al., 1997; Muguerza, Gimeno, Ansorena, Bloukas, & Astiasaran,

2001; Severini et al., 2003) or linseed oil (Ansorena & Astiasaran, 2004; Valencia et al., 2006) in fermented meat products. Replacing beef fat with olive oil has been reported to favour lipid oxidation in traditional Turkish dry fermented sausage (Kayaardi & Gok, 2003). Oxidation has been reported in dry fermented sausage containing sh oil extract during curing (Muguerza, Ansorena, & Astiasaran, 2004), but Valencia et al. (2006) found no signs of oxidation in products enriched with n-3 PUFAs from sh oil in the presence of antioxidants (BHA BHT). Pelser et al. (2007) have reported that addition of canola oil and encapsulated axseed oil in Dutch style fermented sausages did not reduce the shelf life in terms of lipid oxidation, but that addition of axseed oil and encapsulated sh oil increased lipid oxidation during storage. Challenges for formulation of healthier lipid meat products It has been suggested that foods that are strategically or naturally enriched in healthier fatty acids can be used to achieve desired biochemical effects without the ingestion of supplements or changes in dietary habit. As one of the commonest foods in our diet, meats are an especially suitable vehicle for adding healthier lipids. This has not escaped the notice of the industry, which has marketed a wide variety of healthier lipid (MUFA and PUFA) enriched foods worldwide, including various meat products (Jimenez-Colmenero et al., 2006; Kolanoswski & Laufenberg, 2006). However, there are a number of aspects relating to product design, technologies for incorporation of exogenous lipids, assessment of the consequences of composition changes from production to consumer, and health benets, which need to be taken into account when planning new developments. One fundamental requirement of the design and reformulation of these products with a view to potential health benets is to assure that the lipid content and prole are optimum. The nal product should contain enough concentrations of these benecial compounds so that the quantity of the product that a person can reasonably be expected to consume supplies enough of the nutrient to produce the nutritional or physiological effect claimed on the basis of generally accepted scientic data. This aspect is essential for nutrition and health claims on foods (Regulation (EC) No 1924/2006). These and other considerations may mean that meat products with very low or high fat content do not present sufcient merits in terms of the recommendations for optimal intake. In any event, in order to expand and improve the possibilities of developing meat derivatives of this kind, better procedures are needed for incorporation of the various types of healthier non-meat fat in the right amounts and conditions. Particular attention needs to be paid to the effect of processing, storage, preparation and composition of reformulated products, since signicant amounts of specic components can be lost, and this can limit their potential

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health benets. At the same time, combined research efforts are required to demonstrate satisfactorily that regular consumption of a product has a benecial effect on one or more specic functions in the organism and that it is therefore a functional food. Acknowledgments This research was supported under project AGL2005 07204-C02-02 of the Plan Nacional de Investigacion Cientca, Desarrollo e Innovacion Tecnologica (IDI), Ministerio de Ciencia y Tecnologa. References
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