**1. Introduction**

Pomace is the main residue (a humid, solid material) generated from the pressing of fruits and olives to obtain juices and olive oil, respectively. This residue is heterogeneous and may contain seeds, pulp, stems, and peels, depending on the source [1,2]. In terms of the global production of juices and olive oil, the amount of pomace produced every year achieves several millions of tons [3,4]. Its high organic matter, nutrients, and moisture content favor the growth of microorganisms to decompose this residue (the generation of greenhouse gases, unpleasant odors, and contamination of groundwater) and can attract pests, which ultimately leads to an important environmental impact [5]. Additionally, the consumption of juices [6,7] and olive oil [8–10] is expected to increase in the upcoming years. In this sense, the residues from these two sectors of the food industry are expected to increase.

Another important aspect related to pomaces is the presence of bioactive compounds that are lost when these residues are discarded. One of the most studied classes of phytochemicals are polyphenols. This class of compounds is characterized by the antioxi-

**Citation:** Munekata, P.E.S.; Domínguez, R.; Pateiro, M.; Nawaz, A.; Hano, C.; Walayat, N.; Lorenzo, J.M. Strategies to Increase the Value of Pomaces with Fermentation.

*Fermentation* **2021**, *7*, 299. https:// doi.org/10.3390/fermentation7040299

Academic Editors: Giuseppa Di Bella and Alessia Tropea

Received: 28 October 2021 Accepted: 6 December 2021 Published: 8 December 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

dant [11–13], antimicrobial [3,12], anti-inflammatory [13], and anti-diabetic [14] activities tested in vitro and in vivo. This scenario can be seen as a relevant opportunity to explore strategies to improve the management of pomace and reduce its environmental impact. in vitro and in vivo. This scenario can be seen as a relevant opportunity to explore strategies to improve the management of pomace and reduce its environmental impact. In this sense, the concept of a circular economy is favored to improve the sustainability in this sector of the food industry, i.e., transforming residues into raw materials with

Another important aspect related to pomaces is the presence of bioactive compounds that are lost when these residues are discarded. One of the most studied classes of phytochemicals are polyphenols. This class of compounds is characterized by the antioxidant [11–13], antimicrobial [3,12], anti-inflammatory [13], and anti-diabetic [14] activities tested

*Fermentation* **2021**, *7*, x FOR PEER REVIEW 2 of 22

In this sense, the concept of a circular economy is favored to improve the sustainability in this sector of the food industry, i.e., transforming residues into raw materials with highadded value and connecting them with other chains of food processing [15]. Moreover, a circular economy is one of the principles of the European Green Deal that aims to improve the efficiency of resource use and to cut pollution, for instance [16,17]. Recent publications support the potential utilization of this strategy [18–24]. It is also important to mention that the reutilization of residues of the food industry and the consequent development of food products are concepts supported and well-accepted by consumers [25,26]. high-added value and connecting them with other chains of food processing [15]. Moreover, a circular economy is one of the principles of the European Green Deal that aims to improve the efficiency of resource use and to cut pollution, for instance [16,17]. Recent publications support the potential utilization of this strategy [18–24]. It is also important to mention that the reutilization of residues of the food industry and the consequent development of food products are concepts supported and well-accepted by consumers [25,26]. Among the possible solutions to manage pomaces, fermentation has been suggested

Among the possible solutions to manage pomaces, fermentation has been suggested to obtain high-added value products and compounds. Moreover, fermentation can be seen as an important and more sustainable strategy to treat food industry residues [2,27,28]. Thus, this review aims to provide an overview of the utilization of fermentation (mainly involving lactic acid bacteria and yeasts) and biotransformation (biotransformation) of pomace in the production of silage and supplement feed for animal, enzymes, polyphenols, bioactive compounds (release of bound polyphenols and the synthesis of fatty acids and carotenoids), odor-active volatile compounds, and organic acid production. to obtain high-added value products and compounds. Moreover, fermentation can be seen as an important and more sustainable strategy to treat food industry residues [2,27,28]. Thus, this review aims to provide an overview of the utilization of fermentation (mainly involving lactic acid bacteria and yeasts) and biotransformation (biotransformation) of pomace in the production of silage and supplement feed for animal, enzymes, polyphenols, bioactive compounds (release of bound polyphenols and the synthesis of fatty acids and carotenoids), odor-active volatile compounds, and organic acid production.

#### **2. Utilization in Silage or as a Feed Supplement for Animal Production 2. Utilization in Silage or as a Feed Supplement for Animal Production**

The feeding of animals reared for food production is one of the possible applications of fermented pomaces (Figure 1), for which there are two main strategies: adding the pomace in silage production or fermenting/biotransforming the pomace and using it as feed supplement (Table 1). Regarding the first strategy, the production of silage consists of preserving pasture grass for further use (especially during dry periods). The process occurs mainly by fermenting pasture with bacteria that are naturally or strategically added to acidify the material and delay microbial and biochemical spoilage [29]. Considering the importance of silage and the fermentation process, many studies have explored the effect of pomace in the characteristics of silage and its effect in animal health and performance. The feeding of animals reared for food production is one of the possible applications of fermented pomaces (Figure 1), for which there are two main strategies: adding the pomace in silage production or fermenting/biotransforming the pomace and using it as feed supplement (Table 1). Regarding the first strategy, the production of silage consists of preserving pasture grass for further use (especially during dry periods). The process occurs mainly by fermenting pasture with bacteria that are naturally or strategically added to acidify the material and delay microbial and biochemical spoilage [29]. Considering the importance of silage and the fermentation process, many studies have explored the effect of pomace in the characteristics of silage and its effect in animal health and performance.

**Figure 1. Figure 1.** Schematic representation of strategies to valorize pomaces with fermentation. Schematic representation of strategies to valorize pomaces with fermentation.


**Table 1.** Effect of fermentation in the characteristics of silage produced from apple, white mulberry, and grape pomace.

Using pomace as a raw material for silage production may shift the characteristics of silage and change its content and composition of organic acids, digestible matter, and pH. These results were reported in studies with apple pomace that also indicated a reduction in the production of lactic acid [30,31]. Along with the increase in ethanol content in silage, the pH was increased, and the accumulation of lactic acid was reduced in relation to silage without pomace. However, these studies also indicated an unclear effect in the accumulation of ammonia nitrogen.

In the case of grape pomace, the depletion in lactic acid content and the increase in the production of other organic acids, polyphenol content, effluent and gas loss were also reported in two recent studies [32,33]. Both studies did not indicate significant differences in the pH of silage. It is relevant to mention that the study carried out by Li et al. [33] also evaluated the combination of grape pomace with the starter culture composed of *Lactobacillus plantarum* and *Lactobacillus buchneri*. These microorganisms led to a better control of fermentation and quality of silage by favoring the accumulation of lactic and acetic acid, water soluble carbohydrates, and crude protein. Moreover, ammonia nitrogen levels were reduced and no effect in the neutral detergent fiber content and the pH of silage were reported. A related experiment evaluated the production of silage with white mulberry pomace with meadow grass [34]. In this case, significant effects in organic matter digestibility and metabolizable energy, as well as in gas production, were reported.

Since silage is an important component for animal production in periods and regions of reduced feed availability, some studies reported the effect of silage with pomace and fermented pomace in animal nutrition, health and the composition and characteristics of foods obtained from animals in these experimental diets (Table 2). For instance, recent experiments reported the effect of silage added with apple pomace in the diet of Suffolk wethers [30,31]. In both cases, significant reductions in digestibility and nitrogen retention, in relation to the control diet, were reported. No effect in feed intake between control and experimental diets were indicated in these studies.




106

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IgG: immunoglobulin G, IgM: immunoglobulin M, LAB: lactic acid bacteria, LDL: low-density lipoprotein cholesterol, NDF: neutral detergent fiber, SOD: superoxide dismutase, and SSF: solid-state fermentation.

**Table 2.** *Cont.*

107

A related experiment with pigs fed with silage containing apple pomace indicated minimal or non-significant effects in the growth performance, except for a reduction in daily feed intake and an increase in feed efficiency in animals fed with apple pomace silage [35]. Additionally, this study also indicated a significant increase in the content of some individual polyunsaturated fatty acids in back fat, whereas the content of few saturated and monounsaturated fatty acids in back fat were reduced. This effect was attributed to the dietary fiber found in apple pomace that favored the growth of probiotic microorganisms in pig intestine and led to the potential changes in back fat fatty acid composition.

Another interesting strategy to use silage with apple pomace was reported for the production of fish. Davies et al. [36] studied the effect of a silage produced with apple pomace, minced sardine, and *Lactobacillus plantarum* as a starter culture in the production of juvenile European sea bass. In these animals, the silage with apple pomace improved the health status of fish, whereas growth performance indicators were reduced in relation to the control diet (without apple pomace).

The effect of feeding animals with silage containing grape pomace was also reported in recent studies but contrasting results have been reported. In the experiment carried out by Massaro Junior et al. [37], increasing levels of silage with grape pomace (up to 30% in feed) did not cause significant changes in indicators of growth performance (initial and final body weight, average daily gain and feed conversion ratio), carcass characteristics (hot and cold carcass yield, for instance), and meat quality (such as pH, shear force, lipid oxidation, and color) in lambs. Conversely, the use of silage produced with grape pomace in piglets induced the antioxidant defense system, reduced the indicators of oxidative stress, and the counts of pathogenic microorganisms (*Campylobacter jejuni*, for instance) in fecal samples [38]. Additionally, the meat produced from animals fed with the experimental diet had more omega-3 fatty acids in comparison to the meat from animals fed with the control diet.

Fermentation in a solid state has also been explored to obtain potential feed additives for animal production. In the case of broiler chicks, the incorporation of fermented grape pomace in animal diets produced heavier animals with increased serum levels of catalase (a component of the antioxidant defense system) [39]. Additionally, no significant reductions in other components of the antioxidant defense system, intestinal morphology, and the pH or color of liver in the animals fed with silage containing grape pomace were reported in this study.

Olive pomace has been indicated as an interesting component to improve the diet of chicks [40]. Adding fermented olive pomace in animal feed enhanced the antioxidant status and the antioxidant defense system as well as reduced serum triglycerides and total cholesterol. Conversely, body weight gain was affected and no major effects in liver enzymes were indicated by the authors. The effects on animal health were also observed in meat in terms of reduced fat, cholesterol contents and lipid oxidation levels in breast meat. Another study indicated a favorable effect of solid-state fermented pomace in animal health [41]. In this case, the consumption of fermented tomato pomace improved health indicators (serum lipids and immune and antioxidant defense systems) in Holstein cows. However, the authors indicated no effects in terms of feed intake and milk production and composition (except for vitamins A, C, and E).

The effect of silage produced with pomegranate pomace in broiler chicks was evaluated by Gungor et al. [42]. The oxidative status was improved and some effects in the internal morphology were reported in animals consuming the experimental silage. No significant effects were reported for carcass characteristics, the antioxidant defense system, and meat and liver characteristics (pH and color).

From these experiments, it seems reasonable to consider that mixing pomace with other components for silage production modifies the microbial activity as well as the characteristics of silage. These effects can be attributed to the composition and content of nutrients (such as water-soluble carbohydrates). It is important to mention that the effect is dependent on the extract composition (apple vs. grape pomace, for instance). Additionally, the shift in the fermentation process by using pomace as a raw material in silage production (especially for the production of lactic acid to ethanol) may be reduced from the addition of starter cultures. In terms of animal production, the main benefit seems to be related to animal health and the quality of foods obtained from these animals (chicks, cows, fish, lambs, and pigs), regardless of pomace source. In terms of animal production, the use of either pomace as silage raw material or fermented feed supplement seems to have a negative impact, such as in growth performance. It is worth mentioning that the modification of foods obtained from animals fed with fermented pomace fits in the strategy to naturally enrich foods with nutrients and functional compounds [43]. This strategy is supported by studies with apple [35], grape [38,39], olive and tomato pomaces [40,41]. However, additional studies are still necessary to identify relevant sources due to the controversial results such as those reported for pomegranate pomace in chicken meat [42].
