Trends in Food Science & Technology 15 (2004) 176185

Review

Application of functional citrus by-products to meat products

J. Fernandez-Lopez, J.M. Fernandez-Gines, L. Aleson-Carbonell, E. Sendra, E. Sayas-Barbera and J.A. Perez-Alvarez*
Departamento de Tecnologa Agroalimentaria, Escuela Politecnica Superior de Orihuela, Universidad Miguel Hernandez, Ctra. a Beniel Km 3,2 (03312) Orihuela, Alicante, Spain (tel: +34-966-749739; fax: +34-966-749677; e-mail: ja.perez@umh.es)

Introduction
The citrus industry (oranges, lemons and grapefruits) is important in tropical and subtropical zones and particularly in Spain which is one of the major producers and exporters of various kinds of citrus fruits. Per capita consumption of citrus juice in Spain accounts to more than 3.8 L (MAPA, 2001). In contrast with other types of fruits, citrus fruits have a small edible portion and large amounts of waste material such as peels and seeds. Therefore, citrus processing produces a considerable amount of by-products, which are a problem since the plant material is usually prone to microbial spoilage and are commonly used in animal feed or fertilizer (Famyima & Ough, 1982; Nikolic, Cuperlovic, Milijic, Djordjevic, & Krsmanovic, 1986) however some of these by-products could also be useful to the food industry. Residues of citrus juice production are a source of dried pulp and molasses, ber-pectin, cold pressed oils, essences, d-limonene, juice pulps and pulp wash, ethanol, seed oil, pectin, ascorbic acid, limonoids and anonoids (Askar & Treptow, 1998; Braddock, 1995; Ozaki et al., 2000; Siliha, El-Sahy, Sulieman, Carle, & El-Badawy, 2000). Most of these materials from citrus by-products could be used as functional ingredients when designing healthy foods (functional foods), specially non-digestible carbohydrates (dietary ber) and bioactive compounds (ascorbic acid and avonoids) (Marn, Martnez, Uribesalgo, Castillo, & Frutos, 2002; Puupponen-Pimia et al., 2002b).

Consumers are increasingly aware of diet related health problems and therefore demanding natural ingredients which are expected to be safe and health-promoting. Byproducts of citrus fruits processing industries represent a serious problem, but they are also promising sources of materials which may be used in the food industry because of their valuable technological and nutritional properties. Two types of citrus by-products (lemon albedo and orange dietary ber powder), at dierent concentrations, were added to cooked and dry-cured sausages. The purpose of this paper is to describe the latest advances on the potential of citrus by-products as a source of functional compounds and their application in meat products. # 2003 Elsevier Ltd. All rights reserved.

Composition of citrus by-products

Residues of citrus juice production are composed principally by water, soluble sugars, ber, organic acids, amino acids and proteins, minerals, oils and lipids, and also contains avonoids and vitamins. All of these components are found in dierent amounts depending on the fraction of the fruit (juice, albedo, avedo, rag and pulp, and seeds) (Braddock, 1995), and therefore their proportion in citrus juice residues depends on the juice extraction system used (Marn, Martnez et al., 2002).

* Corresponding author.
0924-2244/$ - see front matter # 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tifs.2003.08.007

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Dietary ber fractions

The main advantage of dietary ber from citrus fruits when compared to alternative sources of bre such as cereals, is its higher proportion of soluble dietary ber with about 33% in citrus fruits while only 7% is present in wheat bran (Gorinstein et al., 2001; GriguelmoMiguel & Martn-Belloso, 1999; Prosky, Asp, Schweizer, De Vries, & Furda, 1988). This is an important point taking into account that the requirement for dietary ber intake must be balanced, i.e. the water soluble fraction should represent between 30 and 50% of the total dietary ber (Eastwood, 1987; Spiller, 1986). The content of all dietary ber fractions (total, soluble and insoluble) is higher in peels (65% aprox.) than in peeled citrus fruits, as can be seen in Table 1 (Gorinstein et al., 2001; Marlett, 1992; Marlett & Vollendorf, 1994). The main DF fractions in citrus by-products are, in descending order, cellulose, lignines, pectines and hemicellulose (Table 2).

Ascorbic acid content in citrus fruits could be of considerable importance. Gorinstein et al. (2001) reported that the content of ascorbic acid is higher in peels than in peeled fruits and it is also higher in peeled lemons and oranges and their peels than in peeled grapefruits and their peels (Table 1).

Healthy benets of compounds from citrus by-products

Epidemiological studies have pointed out that the consumption of fruits has health benets, e.g. reduced risk of coronary heart disease and stroke, as well as certain types of cancer. Apart from dietary ber, these health benets are mainly attributed to organic micronutrients such as carotenoids, polyphenolics, tocopherols, vitamin C, and others (Schieber et al., 2001).

Dietary ber
The generally accepted denition of dietary ber includes polysaccharides and lignin that are neither digested nor absorbed in the human small intestine (Asp, 1987). Total dietary ber could be divided into two fractions, one of which is soluble in water at 100 C and pH 67, and another which is insoluble. Both of them have dierent benecial eects on human health. The insoluble DF fraction is mainly associated to intestinal motility. Consumption of this ber delays gastric emptying (Low, 1990; Roberfroid, 1993) and expands the eective unstirred layer, thus slowing the process of absorption once in the small intestine (Blackburn, Holgate, & Read, 1984). This in turn can cause an extended feeling of fullness (Bergmann et al., 1992). A slower emptying rate means delayed digestion and absorption of nutrients (Ritz, Krempf, Cloarec, Champ, & Charbonnel, 1991; Roberfroid, 1993) resulting in decreased

Bioactive compounds
Belitz and Grosch (1999) and Gorinstein et al. (2001) reported that the content of total polyphenols was higher in the peels of citrus fruits than in peeled fruits and that the content of total polyphenols in peeled lemons and their peels was higher than in peeled oranges and grapefruits and their peels, respectively (Table 1). Flavonoids are mostly found in the pulp, peel and rag tissues. The main avonoids found in citrus species are hesperidine, narirutin, naringin and eriocitrin (Mouly, Arzouyan, Gaydou, & Estienne, 1994; Schieber, Stintzing, & Carle, 2001). Peel and other solid residues of lemon wastes contain mainly hesperidin and eriocitrin, while naringin and eriocitrin are predominant in liquid residues (Coll, Coll, Laencina, & Tomas-Barberan, 1998).

Table 1. Dietary ber (DF, g/100 g fresh fruit), polyphenols and ascorbic acid content (mg/100 g fresh fruit) in fresh peeled citrus fruits and their peels Total DF Peeled lemons Peels of lemon Peeled oranges Peels of oranges Peeled grapefruits Peels grapefruits 1.31 0.08 2.49 0.22 1.30 0.08 2.49 0.00 1.32 0.10 2.47 0.22 Insoluble DF (% total DF) 67 6.3 67 6.0 67 5.9 67 3.6 69 4.8 67 4.0 Soluble DF (% total DF) 33 3.3 33 3.1 33 3.0 33 3.3 31 3.7 33 3.3 Total polyphenols 164 10.3 190 10.6 154 10.2 179 10.5 135 10.1 155 10.3 Ascorbic acid 47.9 4.7 59.8 5.4 47.7 4.9 59.6 5.2 35.1 3.5 43.8 4.1

Adapted from Gorinstein et al. (2001). Values are means S.D. of ve measurements.

Table 2. Fiber composition (% dry weight) from dierent citrus by-products Lemon Pectins Hemicellulose Cellulose Lignins 7.50 0.06 11.0 0.09 36.25 2.90 22.50 1.90 Orange 6.50 0.05 6.50 0.05 20.75 1.90 14.75 1.01 Grapefruits 8.50 0.85 5.50 0.06 26.50 2.52 11.50 1.22

Adapted from Marn et al. (2003). Values are means S.D. of seven measurements.

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absorption of energy (Heaton, 1973). The extended presence of nutrients in the upper small intestine may promote satiety (Sepple & Read, 1989). Cummings (2000) reported that the mechanism by which ber may be protective against gastrointestinal diseases is related to the decreased transit time, increased stool weight and decreased intracolonic pressure. The soluble dietary ber fraction is considered to be chiey involved in lowering eects on blood cholesterol and glucose intestinal absorption. It has been documented that the hypocholesterolemic eects of dietary ber are due to increased excretion of bile acids and cholesterol (Bosaeus, Carlsson, Sandberg, & Andersson, 1986). In addition to delaying or interfering with the absorption of cholesterol and bile acids, dietary ber may delay the absorption of macronutients, including fat and carbohydrates. Delayed carbohydrate absorption, in turn, could lead to increased insulin sensitivity (Hallfrisch, Scholeld, & Behall, 1995) and decreased triacylglycerol concentrations (Rivellese et al., 1980) both considered risk factors for coronary heart diseases. Finally, positive benets of ber with respect to colon cancer have been reported (Fuchs et al., 1999; Platz et al., 1997).

Bioactive compounds
Nowadays, it is widely accepted that the benecial health eects of fruits, in the prevention of heart disease and certain types of cancer, are due to their bioactive components (Benavente-Garca, Castillo, Marn, Ortuno, & Del Ro, 1997; Block, 1992; Block, Patter son, & Subar, 1992). Some reports suggest that ascorbic acid (vitamin C) and avonoids may inhibit these diseases due to their antioxidant potential (Hertog, Feskeens, Hollman, Katan, & Kromhout, 1993; Marn, Frutos, Perez-Alvarez, Martnez-Sanchez, & Del Ro, 2002; Salah et al., 1995). The inuence of ascorbic acid in processes such as the absorption of iron, aminoacid metabolism, hormones and cell oxidation and reduction processes, is wellestablished (Buettner, 1993). This had led to the suggestion that vitamin C, as a natural antioxidant, may inhibit the development of major clinical conditions and certain cancers (Diplock, 1991). Flavonoids are also attracting more and more attention due to their properties as antioxidants, anticarcinogenic agents, antiinammatories and because of their lipid antiperoxidation eects (Elangovan, Sekar, & Govindasamy, 1994; Godeberge, 1994; Jean & Bodinier, 1994; Marn, Frutos et al., 2002; Meyer, 1994; Rice Evans, Miller, & Paganda, 1997).

Preparation of high dietary ber powders from citrus by-products

Currently, there is a great variety of raw materials from which dietary bers obtained, such as: wheat, rice,

oat, pineapple cores, guava, etc. (Jimenez-Escrig, Rincon, Pulido, & Saura-Calixto, 2001; Prakongpan, Nitthamyong, & Luangpituksa, 2002; Rinaldi, Nig, & Bennik, 2000). The source of ber is important because diering arrays of plant cells can aect ber properties. Dietary bers from cereals are more frequently intaked than those from fruits, however fruit bers are considered to be of better quality due to their higher total ber by, soluble ber contents, water and oil holding capacities and colonic fermentability, lower levels of phytic acid and lower caloric values (Larrauri, 1999; Saura-Calixto & Larrauri, 1996). Moreover, bers from citrus fruits have an additional advantage over dietary bers from other sources due to the presence of associated bioactive compounds (i.e. avonoids and vitamin C) with antioxidant properties. Albedo is a white, spongy and cellulosic tissue which is the principal citrus peel component. Due to its high ber content albedo could be considered as a potential ber source (Fernandez-Gines et al., 2001; Perez Alvarez, Fernandez-Lopez, Sayas-Barbera, Navarro, & Sendra, 2001). Citrus by-products presented a high water content (80%) which make dicult their application in the food industry, so it is necessary their processing to obtain a powder with a high ber content and an average of 7% water. When the process for the preparation of citrus ber powder was developed, caution was taken to minimize the losses of associated bioactive compounds that include avonoids, polyphenols and vitamin C. Fernandez-Gines, Fernandez-Lopez, Sayas, Sendra, and Perez-Alvarez (2003) developed a process for the preparation of citrus ber using the by-products generated by an orange juice industry as raw material (Fig. 1). Orange ber was prepared by vacuum-packing fresh raw material in 2 kg pouches and promptly frozen to 30 C until further use. After thawing (24 h/25 C) the material was scalded in a water bath. The objective of this step was the selective removal of undesirable compounds associated to dietary ber, and the removal of potentially pathogenic microorganisms (vegetative cells). At the end of the washing and heating step, the ber was pressed using an helical press to remove excess liquid prior to drying. Drying in an oven at 50 5 C during 24 h to improve the ber shelf life without addition of any chemical preservative. A grinder mill and sieves were used to obtain a powder particle size of less than 0.417 mm. The nal powder (7% moisture and 80% ber content) presented a high water holding capacity, which favours its use as a functional ingredient for applications in low-calorie foods, reduce syneresis and modify viscosity and texture of foods.

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Fig. 1. Flow chart of the method to obtain a high dietary ber powder from by-products from orange juice processing.

Applications to meat products

Citrus by-products (lemon albedo and orange ber powder) have been added, at dierent concentrations, to cooked and dry-cured sausages with excellent results. Lemon albedo was obtained directly from commercial lemons (Citrus limon var. verna) in a pilot plant. Two types of albedo were used: raw albedo (obtained directly from lemons; 65% moisture and 30% ber content) and cooked albedo (raw albedo cooked in a water bath at 100 C during 5 min and then refrigerated until room temperature; 72% moisture and 22% ber content). Lemon albedo (raw and cooked) was added at dierent concentrations (0, 2.5, 5, 7.5 and 10%) to cooked sausages (bolognas) and dry-cured sausages, both of them manufactured according to traditional formulas. Three independent replicates of each sausage were made. Analyses included compositional (moisture, ash, protein, fat and crude bre content), physicochemical (pH and colour determinations) and sensory evaluation

(Aleson-Carbonell, Fernandez-Gines, Fernandez Lopez, et al., 2002; Aleson-Carbonell, Fernandez Lopez, Sayas-Barbera, Sendra, & Perez-Alvarez, 2003; Fernandez-Gines et al., 2001; Perez-Alvarez et al., 2001). The most important nding from chemical composition analysis was the behavior of residual nitrite levels (Fig. 2). The incorporation of raw and cooked albedo to both sausages produced a signicantly lowered (P < 0.05) residual nitrite levels (higher in raw than in cooked albedo), probably due to the reactions of nitrite with the active biocompounds present in the albedo (Nagy & Attaway 1992). This reduction in residual nitrite level has healthy eects because reduces the possibility of nitrosamines formation. Nitrosamines formation it is a risk associated to the consumption of meat products with nitrite in their formulation. Yellowness was the only color parameter not aected by albedo type and concentration, in both types of sausages. In bolognas, lightness increased when albedo was added, and this increase was higher in bolognas added with raw than cooked albedo (Fig. 3). These results mean that the addition of albedo resulted in a lightercolored product. In contrast, when albedo was added to dry-cured sausages, lightness values decreased (P < 0.05) especially in the case of cooked albedo, this behavior is related to pH changes. Albedo aected redness evolution in a dierent way depending on the type of sausage: it increased in dry-cured sausages and decreased in cooked sausages (Fig. 4). In sensory evaluation, both types of sausages were similarly rated with hedonic scores. Type and concentration of albedo had a signicant eect on sensory scores. When raw albedo was used, the highest scores were assigned to sausages with up to 5% albedo added, while in the case of cooked albedo the samples with 2.5, 5 and 7.5% albedo added had the highest scores, comparable to control samples. The eect of lemon albedo on the drying step of drycured sausages has been also studied (Aleson-Carbonell, Fernandez-Gines, Sayas-Barbera et al., 2002b). The sausages were dried during 5 days at 15 1 C and 70 10% relative humidity and pH and color parameters were determined daily (three independent replicates of each sausage were made). The presence of albedo decreased the pH. Samples with 5% albedo (raw or cooked) showed at day 1, similar pH values than control samples at the end of drying step (Fig. 5). This decrease in pH could favor water release, reducing the drying time. Color evolution during drying was not aected by the presence of albedo. In all sausages lightness and yellowness decreased and redness increased during drying. Orange ber powder was added at dierent concentrations (0, 0.5, 1, 1.5 and 2%) to cooked sausages (bolognas). The eects of ber addition and storage conditions were evaluated. Bologna sausages added

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with citrus ber were vacuum-packed and stored at 4 C during 28 d under darkness and light exposure. Chemical (moisture, ash, fat, protein and ber content, and TBA analysis), physicochemical (pH, color and textural properties), and sensory evaluation was carried out. Three independent replicates of each sausage were made (Fernandez-Gines et al., 2003; Fernandez-Lopez,

Fernandez-Gines, Sayas-Barbera, Sendra, & Perez Alvarez, 2003; Sayas-Barbera, Fernandez-Lopez, Perez Alvarez, Fernandez-Gines, Sendra, & Navarro, 2002). The behavior of residual nitrite was consistent with that observed when albedo was added. All color parameters increased when citrus ber was added. The increased redness (measured as a* values) could be

Fig. 2. Eect of addition of raw and cooked lemon albedo on the residual level of nitrite in cooked and dry-cured sausages. Values plotted are means of nine measurements.

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attributed to the presence of antioxidant compounds (Nagy & Attaway, 1992) which would favor the reduction of myoglobin and nitrosomyoglobin. During the time of storage only a* values reduction was observed, which could be due to nitrosopigments degradation. Samples stored under light exposure showed a more dramatic reduction in a* values (P < 0.05) than samples stored in darkness. Carballo, Cavestany, and Jimenez-

Colmenero (1991) and Perlo et al. (1995) reported that the light has an oxidative eect which causes reductions in a* values due to nitrosopigments oxidation and degradation. TBA values of samples stored under lighting conditions were higher (P < 0.05) than those of samples stored in darkness, for each time and citrus ber concentration added (Fig. 6). Lipid oxidation was strongly improved

Fig. 3. Lightness (L*) in Bologna sausages with dierent levels of raw and cooked albedo. Values plotted are means of nine measurements.

Fig. 4. Redness (a*) in cooked and dry-cured sausages with dierent levels of raw albedo. Values plotted are means of nine measurements.

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in samples displayed under lighting, in accordance with Andersen and Skibsted (1991) who reported that light is an important prooxidant in the process of lipid oxidation. As can be seen in Fig. 5, TBA values increased faster in control samples than in samples with citrus

ber, which could be due to the presence of ber associated compounds, such as avonoids, polyphenols and carotenes, with antioxidant properties (Gabor, 1988; Wang, Cao, & Prior, 1996). These compounds could protect the product from the photo-oxidation process.

Fig. 5. pH evolution in control and samples with 5% of lemon albedo (raw and cooked) of dry-cured sausages during drying. Values plotted are means of nine measurements.

Fig. 6. TBA (mg malonaldehyde/kg sample) evolution, in control bologna sausage samples with 2% orange ber, during storage at 4 C under darkness and lighting conditions. Values plotted are means of nine measurements.

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Bolognas sausages formulated with ber were harder, less elastic, cohesive and chewy. The texture was not inuenced by the time or conditions of storage. All samples obtained similar hedonic scores with the exception of samples with 2% orange ber which obtained the lowest scores, eventhough they were still acceptable. Neither storage time nor conditions signicantly aected the sensory scores (P < 0.05).

Conclusions
The explotation of by-products of citrus fruit processing as a source of functional compounds and their application to foods is promising, considering that within the food market, the innovative sector of functional foods is growing fast and becoming more important. An additional advantage is the contribution to the use of citrus by-products that could become an environmental issue. The presence of functional dietary ber and antioxidants in citrus by-products allow their application in food processing to obtain healthy products. Overall it could be interesting their incorporation in frequently consumed foods which could help to overcome the ber decit in actual human diet and to prevent the development of cancer and other diseases. The benecial results obtained for ber enrichment of cooked and dry-cured sausages suggest other potential applications for these types of byproducts and the need of further research such as the nutritional enrichment of other meat products and applications in dairy and bakery products.

Acknowledgements
The authors are grateful for the nancial support by the Consellera de Agricultura Pesca y Alimentacion (Generalitat Valenciana) through Project GV-CAPA0007.

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