In western diets, meat and meat products are one of the main sources of high-biological value protein, in addition to containing micronutrients such as minerals (iron, magnesium, potassium, selenium and sodium) and vitamins (A, B12
, folic acid, among others) that are highly bio-available [1
]. Despite these excellent nutritional properties, the intake of meat and meat products is related with a higher incidence of cardiovascular diseases and obesity, increasing the negative perception attached to the consumers of these food products in recent years [2
]. On the other hand, due to its rich nutritional profile, the meat presents a high susceptibility to deterioration due to the microbial growth and oxidation processes that take place when the muscle is transformed in the meat during the meat processing and storage [3
]. To overcome these drawbacks, and in line with the rising awareness by consumers of the relationship between diet and health [7
], in the last few years, the meat industry has had to face the double challenge of offering more healthy meat processed products, and guaranteeing their stability [8
Until now, synthetic antioxidants, such as butylated hydroxytoluene (BHT) and butylated hydroxyanisole (BHA), have been widely used in the food industry as preservative agents to extend the self-life of food products, but their incorporation should be reduced due to their harmful effects on health, as described in in vitro and in vivo studies [4
]. The need to find alternatives to substitute the synthetic additives has led to scientific researchers and meat industries devoting great efforts to using renewable biomass as a natural source of new biomolecules with functional properties [7
]. In this context, the agri-food industry produces large amounts of waste and by-products that usually are underutilized or discarded, but that contain remarkable amounts of bioactive compounds with properties that make them suitable to be used as natural ingredients [16
]. Therefore, this strategy outlines a promising approach that will allow the removal of a residue without economical value through the recovery of extracts rich in biomolecules, that could then be incorporated in the food chain, contributing to a circular economy model [20
Due to the therapeutic properties associated with pomegranate, its consumption in the form of fresh fruit, juices, jams or dietary supplements has increased significantly in the last decade [5
]. The industrial processing of this fruit generates huge amounts of by-products, mainly peels and seeds, which usually are discarded as waste without any valorization [24
]. Among these residues, pomegranate peel (PP, around 40–50% of the total fruit weight) is an excellent source of phenolic compounds (flavonoids, phenolic acids and tannins), protein and bioactive peptides, and polysaccharides, among others [7
]. Several in vitro bioactivities, such as antioxidant, anti-inflammatory, antitumor and antiproliferative activities, have been described for PP extracts in the literature [25
]. The wide variety of biomolecules with different functionalities suggests that PP extracts could be used in the meat industry as a functional ingredient [5
]. In this sense, the reformulation of meat products with extracts from PP could be an alternative for solving the mentioned inconveniences, and it opens the possibility of formulating customizable meat products tailored to the requirements of certain population groups. Due to this, a growing interest in PP is reflected in the research studies concerning this residue.
A key point in the obtaining of biomolecules from agri-food residues is the selection of the adequate extraction technology, since it should be efficient and should maintain the bioactivities in order to guarantee their functionality when they are incorporated in a food matrix [2
]. Traditionally, conventional methods based on organic solvents and their aqueous mixtures have been widely used in the recovery of phytochemicals from agri-food sources. However, due to the fact that they present disadvantages that negatively affect the bioactive properties of the extracted biomolecules, in the last few years, eco-friendly and sustainable avant-garde technologies have been developed and applied in combination with smart solvents, namely deep eutectic solvents and natural deep eutectic solvents, in the field of the recovery of natural functional ingredients. Among these techniques, microwave-assisted extraction (MAE), ultrasound-assisted extraction (UAE), pressurized liquid extraction (PLE) and supercritical fluid extraction (SFE) are being used in the recovery of biomolecules from PP [23
This review collects the research advanced in the last 10 years on the potential use of PP as a suitable source of high-added value biocompounds for formulating tailored functionalized meat products. Aspects such as the main phytochemicals present in PP and their bioactivities are revised. The role of the extracts, in both the technological and health properties of reformulated meat products, are also featured.
4. Role of Pomegranate By-Products in the Formulation of Meat Products
Meat is a complex system that contains water, proteins, lipids, minerals, and a small proportion of carbohydrates. Due to this rich nutritional profile, meat and meat products are easily susceptible to microbial growth and oxidation reactions (degradation of lipids, proteins and pigments), causing the loss of their quality attributes during processing and storage [4
]. Moreover, microbial spoilage in meat contributes to the development of unattractive odors and flavors, discoloration, gas formation, and the visual perception of slime [4
]. To overcome these problems, both the meat industry and academic researchers have proposed different alternatives for improving the quality and shelf life of meat and processed meat products [2
Synthetic antioxidants have been commonly applied in the food industry to both reduce oxidative deterioration and inhibit the growth of spoilage bacteria in meat products [2
]. However, the use of these synthetic preservatives should be limited due to their toxicity and carcinogenicity, as reported in several studies [78
]. The substitution of synthetic additives with natural antioxidants is a suitable strategy for maintaining the sensory and microbiological quality, and extending the shelf life, of meat products [2
]. In this context, the incorporation of pomegranate by-products, which contain high amounts of phenolics, flavonoids and tannins with excellent antioxidant properties, could replace artificial additives for preserving perishable foods. Besides, pomegranate by-products are a good source of dietary fiber, which, besides improving the physicochemical properties of meat products, also enrich their nutritional value, conferring functional properties that are health-promoting.
One meat product, that has been reformulated with pomegranate by-products and studied by several researchers, is meatballs. For instance, Turgut et al. [80
] evaluated the addition of pomegranate peel extract (PPE) to delay lipid and protein oxidation in this meat product. In their study, the pomegranate extracts were incorporated at 0.5% and 1%, and the results were comparable with those obtained using a synthetic antioxidant (BHT at 0.01%) and a control experiment (without any antioxidant) during 8 days of refrigerated storage. The authors found that beef meatballs elaborated with PPE exhibited greater lipid and protein stability, as well as enhanced sensory scores. In particular, the TBARS values recorded at the end of the storage were 1.19, 0.71, 0.60 and 0.56 mg MDA/kg for control, 0.5% PPE, BHT, and 1% PPE, respectively. Regarding the protein, oxidation was evaluated by the protein carbonyl and sulfhydryl levels. The reduction percent of protein carbonyl content was 25% for 1% PPE and BHT, and 12% for 0.5% PPE, as compared to control. In the case of sulfhydryl levels, the highest value (40.17 nmol/mg protein) was obtained for 1% PPE, and the minimum value was for the control sample (24.53 nmol/mg protein). Besides, the sensory evaluation indicated that the inclusion of PPE maintained the dark red or cherry red coloration, and prevented the formation of rancid odors in meatballs, throughout the 8 days of refrigerated storage. These authors also reported the same protective effect of PPE in beef meatballs during frozen storage for 6 months [81
]. In general, the findings reported demonstrate that the high content of phenolic compounds in PPE, as well as their high antioxidant capacity, exert a protective effect against lipid and protein oxidation in meat products, even superior to that of BHT.
In an effort to extend the shelf life and enhance the safety of beef meatballs, Morsy et al. [82
] applied lyophilized pomegranate peel nanoparticles (LPP-NPs) as a natural antioxidant and antimicrobial in their formulation. After 15 days of storage at 4 °C, the indicators of protein degradation (total volatile base nitrogen) and lipid peroxidation (peroxide value and TBARS) of the meatballs containing 1.5% LPP-NPs were lower than those recorded for samples with BHT (0.01%), and for the control without antioxidants. As well, LPP-NPs-treated meatballs presented less microbial growth during storage, attributed to the presence of phenolics and tannins in the LPP-NPs, which exert antimicrobial activity. The results also revealed that the incorporation of LPP-NPs improved the water holding capacity of beef meatballs. This positive effect could be associated with the presence of fiber in the pomegranate peels that acts as a water-binding agent. As in the works previously described, the LPP-NPs-based meatballs showed good acceptance, with high scores in terms of color and odor up to 15 days in refrigerated storage.
Recently, Fourati et al. [83
] investigated the impact of pomegranate peel ethanol extract (PPEE) at three different dosages (0.1%, 0.5% and 1%) on the microbiological, oxidative stability and sensory attributes of minced beef meat. After 21 days of refrigerated storage, the thiobarbituric acid reactive substances (TBARS) values were significantly lower (p
< 0.05) in meat samples with 1% PPEE than those found for the control without antioxidant. The results also indicated that this same extract dose led to a reduction in MetMb (56.68%), the formation of carbonyl groups (65.71%) and the loss of sulfhydryl groups (59.69%), in comparison with the control. Besides, PPEE inhibited the growth of spoilage microorganisms, exhibiting a dose-dependent protective effect. Finally, sensory evaluation, concerning the attributes of color, appearance and odor, as well as the global acceptability, revealed that the meat treated with 1% PPEE had the highest scores. In previous research, Qin et al. [84
] also reported that pomegranate rind powder extract (PRPE), at a dose of 0.02 g extract/100 g meat, displayed a protective effect against lipid oxidation in the raw ground pork meat. Despite the fact that the treated samples presented changes in color and odor, the overall acceptability was higher than in the control group.
Other reformulated meat products based on pomegranate were frankfurters and cooked sausages. For example, Firuzi et al. [85
] incorporated PRPE at 10 mg gallic acid equivalent/100 g in frankfurters, and they observed that the treated samples presented higher stability to lipid oxidation. By the end of the storage period (60 days at 4 °C), PRPE significantly (p
< 0.05) reduced the peroxide value by 65.05% and 59.22%, respectively, in comparison with the control group (without additives). Use of PRPE, as well as BHT and nitrite, resulted in a raising of the lightness, and in a decreasing trend in the redness and yellowness values, in all frankfurter samples. Furthermore, samples containing antioxidants (natural or synthetic) resulted in less color variation (ΔE), indicating their effectiveness in delaying the discoloration of frankfurters during their refrigerated storage.
In another study, cooked sausages made with two concentrations (5‰ and 10‰) of a commercial mix of pomegranate and citrus extracts (Naturmix WM®
, MEC Import, Rome, Italy) resulted in a significant decrease (p
< 0.01) of TBARS values during refrigerated vacuum storage. Regarding sensory analysis, the findings denoted that the addition of natural extracts prolonged the shelf life of cooked sausages by up to 60 and 50 days, for doses of 10‰ and 5‰, respectively, compared to the control batch (42 days) [86
The use of pomegranate by-products in beef burgers [87
], and both lamb and beef patties [88
], has also been evaluated by other authors. Shahamirian et al. [87
] reported that the reformulation of beef burgers with pomegranate rind powder extract (PRPE) at a level of 0.01% resulted in remarkably lower TBARS values, retarded the aerobic bacterial count, and had a positive effect on color stabilization, as compared to the control sample during frozen storage for 90 days. Equally, burgers containing PRPE had the highest scores in terms of color, flavor, odor, texture and total acceptance. In another study, Bouarab-Chibane et al. [89
] also observed that the inclusion of pomegranate peel at 10 g/kg in beef patties inhibited lipid and myoglobin oxidation, and delayed color variation, at the end of storage in a high oxygen atmosphere for 12 days at 4 °C. However, the authors observed that the burgers containing PP had a drier texture, which was attributed to the high amount of added extract. Contrary to the results of these studies, Andrés et al. [88
] found that the addition of aqueous pomegranate by-product extracts (1000 mg/kg) in lamb patties led to TBARS and free thiol values similar to the control treatment. Based on the microbial analysis, the pomegranate extracts showed a strong inhibitory effect on the mesophilic and psychotropic counts, concluding that these extracts could be applied as natural antimicrobial additives in order to prolong the shelf life of lamb.
In an attempt to improve both the nutritional profile and the sensory and technological attributes of meat products, several studies have focused on the development of functional muscle foods based on antioxidant dietary fiber [1
]. Moreover, the dietary fiber (including also pectin) has been reported for its ability to retain water, which might provide the lubricity and melting sensation to low-fat meat products [90
]. For instance, Sharma et al. [91
] elaborated chicken meat patties by adding pomegranate peel (2%) or pomegranate peel powder aqueous extract (6%). Both types of reformulated patties had a higher content of phenolics, fiber and ashes, providing additional nutritional benefits. Moreover, the water holding capacity, emulsion stability and cooking yield were slightly improved in the treated samples. As discussed in some of the previously cited works, the chicken patties with pomegranate peel exhibited a better protection against lipid oxidation and microbial deterioration during refrigerated storage, compared to samples treated with BHT. Similarly, Santhi et al. [92
] proposed the fortifying effect of pomegranate pomace powder (PPP) in the elaboration of low-fat chicken meatballs. According to the authors, the inclusion of dietary fiber in chicken meat would be a suitable and low-cost choice for developing functional meat products with improved nutritional value.
Another study conducted by Devatkal et al. [93
] evaluated the effect of vacuum packaging and PPE on the quality aspects of ground goat meat and cooked goat meat nuggets, over 25 days of refrigerated storage. Three treatments were studied: aerobic packaging (AP), vacuum packaging (VP) and vacuum packaging with PPE at 1% (VP + PPE). Samples treated with PPE showed greater stability to lipid oxidation, with significantly lower TBARS values than AP or VP. The addition of PPE reduced the TBARS level by 41% in ground meat and 40% in nuggets. The results found in this work indicated that the combination of PPE and VP is an adequate strategy for prolonging the shelf life of goat meat and nuggets.
collects the research works developed in the last 10 years on the incorporation of pomegranate products in meat processed foods, and their main effects.