Next Article in Journal
Risk Factors for Antimicrobial Use on Irish Pig Farms
Next Article in Special Issue
The Effect of Different Concentrations of Total Polyphenols from Paulownia Hybrid Leaves on Ruminal Fermentation, Methane Production and Microorganisms
Previous Article in Journal
Analysis of Expression Profiles of CircRNA and MiRNA in Oviduct during the Follicular and Luteal Phases of Sheep with Two Fecundity (FecB Gene) Genotypes
Previous Article in Special Issue
Effect of Slow-Release Urea Administration on Production Performance, Health Status, Diet Digestibility, and Environmental Sustainability in Lactating Dairy Cows
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 11
Issue 10
10.3390/ani11102827
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Potential Effects of Delphinidin-3-O-Sambubioside and Cyanidin-3-O-Sambubioside of Hibiscus sabdariffa L. on Ruminant Meat and Milk Quality

by
Rosalba Lazalde-Cruz
1,
Luis Alberto Miranda-Romero
1,
Deli Nazmín Tirado-González
2,*,
María Isabel Carrillo-Díaz
3,
Sergio Ernesto Medina-Cuéllar
4,
Germán David Mendoza-Martínez
5,
Alejandro Lara-Bueno
1,
Gustavo Tirado-Estrada
6,* and
Abdelfattah Z. M. Salem
7,*
1
Posgrado en Producción Animal, Departamento de Zootecnia, Universidad Autónoma Chapingo, Carretera México-Texcoco km 38.5, Texcoco 56230, Estado de México, Mexico
2
Centro Nacional de Investigación Disciplinaria Agricultura Familiar (CENID AF), Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Carretera Lagos de Moreno-Jalisco km 8.5, Ojuelos de Jalisco 47540, Jalisco, Mexico
3
Facultad de Medicina Veterinaria y Zootecnia, Universidad de Colima, Autopista Colima-Manzanillo km 40, Tecomán 28100, Colima, Mexico
4
Departamento de Arte y Empresa, División de Ingenierías Campus Irapuato-Salamanca, Universidad de Guanajuato, Carretera Salamanca-Valle de Santiago km 3.5 + 1.8, Salamanca 36885, Guanajuato, Mexico
5
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de México-Xochimilco, Calzada del Hueso 1100, Coapa, Villa Quietud, Coyoacán 04960, Ciudad de Mexico, Mexico
6
Instituto Tecnológico El Llano Aguascalientes (ITEL), Tecnológico Nacional de México (TecNM), Carretera Aguascalientes-S.L.P. km 18.5, El Llano 20330, Aguascalientes, Mexico
7
Facultad de Veterinaria y Zootecnia, Universidad Autónoma del Estado de México, Toluca 50295, Estado de Mexico, Mexico
*
Authors to whom correspondence should be addressed.
Animals 2021, 11(10), 2827; https://doi.org/10.3390/ani11102827
Submission received: 14 September 2021 / Accepted: 23 September 2021 / Published: 28 September 2021
(This article belongs to the Special Issue Environment, Food Production, Health and Welfare Challenges in the Nutrition of Ruminants)
Browse Figure
Versions Notes

Abstract

:

Simple Summary

Hibiscus sabdariffa (HS) calyxes are widely used as nutraceutical supplements in humans; however, stalks, leaves, and seeds are considered as agriculture by-products. Including HS by-products in animal feeding could reduce economic costs and environmental problems, and due to their bioactive compounds, could even improve the quality of meat and milk. However, although HS antioxidants have not been tested enough in ruminants, comparison with other by-products rich in polyphenols allows for hypothesizing on the potential effects of including HS by-products and calyxes in nutrition, animal performance, and meat and milk quality. Antioxidants of HS might affect ruminal fiber degradability, fermentation patterns, fatty acids biohydrogenation (BH), and reduce the methane emissions. After antioxidants cross into the bloodstream and deposit into ruminants’ milk and meat, they increase the quality of fatty acids, the antioxidant activity, and the shelf-life stability of dairy products and meat, which leads to positive effects in consumers’ health. In other animals, the specific anthocyanins of HS have improved blood pressure, which leads to positive clinical and chemicals effects, and those could affect some productive variables in ruminants. The HS by-products rich in polyphenols and anthocyanins can improve fatty acid quality and reduce the oxidative effects on the color, odor, and flavor of milk products and meat.

Abstract

The objective was to review the potential effects of adding anthocyanin delphinidin-3-O-sambubioside (DOS) and cyanidin-3-O-sambubioside (COS) of HS in animal diets. One hundred and four scientific articles published before 2021 in clinics, pharmacology, nutrition, and animal production were included. The grains/concentrate, metabolic exigency, and caloric stress contribute to increasing the reactive oxygen species (ROS). COS and DOS have antioxidant, antibacterial, antiviral, and anthelmintic activities. In the rumen, anthocyanin might obtain interactions and/or synergisms with substrates, microorganisms, and enzymes which could affect the fiber degradability and decrease potential methane (CH4) emissions; since anthocyanin interferes with ruminal fatty acids biohydrogenation (BH), they can increase the n-3 and n-6 polyunsaturated fatty acids (PUFA), linoleic acid (LA), and conjugated linoleic acid (CLA) in milk and meat, as well as improving their quality. Anthocyanins reduce plasma oxidation and can be deposited in milk and meat, increasing antioxidant activities. Therefore, the reduction of the oxidation of fats and proteins improves shelf-life. Although studies in ruminants are required, COS and DOS act as inhibitors of the angiotensin-converting enzyme (ACEi) and rennin expression, regulating the homeostatic control and possibly the milk yield and body weight. By-products of HS contain polyphenols as calyces with positive effects on the average daily gain and fat meat quality.

1. Introduction

Hibiscus sabdariffa L. (HS) is a type of shrub of Malvaceae family from India [1,2], adapted to spring–summer and subtropical or tropical environments (Aw/As—Köppen climate classification) [2,3,4]. In Mexico, HS production has increased 10.54% from 2003 to 2018 [5,6] of shrubs of the Malvaceae family from India [1,2], adapted to spring–summer and subtropical or tropical environments (Aw/As—Köppen climate classification) [2,3,4].
According to FAO [7], the HS calyxes are one of the most demanded products by industry for human feeding [8,9]. Due to fatty acids, HS contents and proportions [10,11], antioxidants [12,13,14], antimicrobial (Gramm negative bacteria) [15], antiviral [16], and anthelmintic properties [17], might lead to improvements in human health [12,18,19].
Calyxes of HS contain 15.76–0.04% of a linoleic fatty acid (n-3) [10,11] and flavonoids classified as anthocyanins [20]. Factors such as the HS type variety, crop management, processing, storage, extraction of extracts, and cell contents affect the antioxidant contents [21,22,23]. However, the highest proportions of HS flavonoids are the anthocyanins cyanidid-3-O-sambubioside (COS) (25.9 to 46.2%) and delphinidin-3-O-sambubioside (DOS) (48.4 to 59.2%) [13,15,23,24], whose clinical effects on humans are different from other kinds of flavonoids supplements such as green teas (Camelia sinensis), which mainly contain epigalocathechin-3-gallate (EGCG), epigallocatechin (EGC), epicahechin-3-gallate (ECG), and epicatechin (EC) [25].
The leaves, stalks, and seeds of HS, as well as other agro-industrial residues, can be used to feed livestock and reduce environmental impact and production costs. Moreover, their phytochemicals such as polyphenols and vitamins could improve the meat and milk quality as well as their shelf-life stability [17,26,27].
Overall, polyphenols and other kinds of antioxidants such as selenium and a-tocopherol reduce the free radicals and chelate pro-oxidant metals [9,14,28,29,30] and can affect the ruminal digestibility and fermentation kinetics [31,32,33], as well as in animal productive behavior [33], reducing the effects of the oxidative stress in ruminants [34,35,36] caused by the high grain and concentrate proportions on diets [25,37,38], the metabolic exigency, and the heat stress [38], and therefore also improve the oxide-reductive potential of products derived for human feed [39].
The objective of the present study was to conduct a critical review about the potential effects of HS anthocyanins, COS and DOS, on ruminant diets, meat and milk quality, and their shelf-life stability.

2. Hibiscus sabdariffa L. By-Products

Figure 1 summarizes how the agricultural wastes and by-products of HS such as seeds, stalks, and leaves can reduce the economic and environmental livestock costs [40,41]. Additionally, optimal inclusion of by-products and wastes of HS in balanced ruminant diets should not have negative effects on animal productive behavior [42,43,44,45] but rather improve the meat and milk quality.
The phenolic and antioxidant activities of HS seeds have been previously assayed, and results were similar or better than those in calyxes [46]. However, the comparison of the potential effects of seeds with calyxes should be assayed in ruminal liquid, including a test to interpret the ruminal microorganisms, fibrolytic enzymes, with the feedstuff’s cell walls.
Table 1 shows the chemical composition of HS seeds reported by different authors, and on average, HS seeds contain: crude protein (CP), 27.9 ± 10 g/100 g of dry matter (DM); fat, 18.8 ± 8.6 g/100 g DM; crude fiber (CF), 16.8 ± 11.1 g/100 DM; and ashes, 5.86 ± 3.2 g/100 DM [43,47].
The CP content of HS seeds is comparable to soybean and canola seeds [59], as their fatty acids are primarily oleic and linoleic acids (LA) (n-9 and n-6 polyunsaturated fatty acids (PUFA)) (37.68 ± 1.10% and 34.14 ± 1.25%); however, calyxes contains similar contents of LA and more α-linoleic acids than seeds (LA: 34.14% vs. 32.65%, and α-linoleic: 1.77% vs. 15.76%, seeds vs. calyxes) (Table 2) [10,58,60], and its DM and CP in situ degradability had been similar to sunflower and peanut seeds [61].

3. Oxidative Stress in Ruminants

Inflammatory and environmental processes increase the endogenous reactive oxygen species (ROS). Unbalance between pro-oxidants and antioxidants might promote oxidative stress and molecular damage [38].
In dairy cows and beef cattle, the environmental pollution and the high metabolic exigency during pregnancy, milk production, heat stress, respiratory diseases, inflammatory process, and parasites promote ROS releasing (O2, OH, RO2, RO, HO2, H2O2, HOCl, O3, etc.); meanwhile, the adipose mobilization increases the pro-inflammatory cytokines [38]. The potential negative effects on animal wealth would also worsen in the future because of the population increment and therefore the milk and meat demand [28].
The ROS contribute to inflammatory processes through necroptosis activation (NF-κβ) via phosphorylation interleukin (I-κβ) and because of the production of pro-inflammatory cytokines such as tumoral factors (TNF-α). In addition, protein carbonylation is mediated by the ROS and metals (Fe2+, Cu+, etc.), producing oxidative by-products and advanced oxidative protein products (AOPP): (1) carbohydrates and lipids have reactive compounds to carbonyl from glycoxidation and lipoperoxidation that might bond to protein residues; (2) oxidized proteins are degraded by proteases, but chemically modified proteins (by di-tyrosine and disulfide cross linkages) might not be substrates to proteolysis, contributing to deposits in tissues and organ damages [62,63,64,65,66,67].
High grain and concentrate proportions in ruminant diets increases lipoperoxidation, decreasing the α-tocopherol and the ferric reductive availability in blood plasma [22] and increasing the amount of AOPP, which is negatively related with milk yield because of the oxide-reductive unbalance. Including high-grain diets and therefore the reduction of forage proportion rises the abnormal amount and types of metabolites in rumen [38].
In viral, bacterial, and fungal infections, phagocytes and neutrophils are sources of ROS that interfere in a chain of chemical reactions which increase the hypochlorous oxidant potential and which might be useful to combat the photogenes, but while also damaging tissues. Besides this, parasites induce inflammation followed by an increase in eosinophils, which also contribute to tissue damage. Lactation and heat stress are potential sources of AOPP and thereby of TNF-α expression and potential mammal glandule diseases, increasing the milk and meat contents of ROS [68,69].
Oxidized milk and meat contribute to a higher ROS content in blood plasma which would be a threat to human health [39].

4. Potential Clinic Effects of Antioxidants

Polyphenols are a wide variety of secondary plant metabolites with at least one -OH that can be structurally simple (egallic and gallic acids) or complex (dimers, oligomeric, and polymeric with high molecular weight). Antioxidants can be classified as flavonoids or non-flavonoids. Thus, flavonoids can be flavones, flavanones, isoflavones, flavonols, flavan-3-ols; on the other hand, anthocyanins (from flavan-3-ols derived the condensed tannins (non-hydrolysable)), phenolic acids, hydrolysable tannins, and stilbenes are clustered as non-flavonoids [17].
Because of the structural differences among complexes, total phenolic compounds cannot directly be related with total antioxidant availability [21,22]. EGCG, primarily found in green tea, was found to have a galloyl group in the third position and an o-trihydroxy in the β-ring which protects cells from ROS damage [64,70]; by the regulation the overexpression of genes, EGCG has anti-inflammatory and antioxidant effects in reduction of apoptosis, cell fibrosis, and tumoral growing via regulation and reduction of kinases, signal transduction, and transcription activation [66,71]. EGCG can [72]:
(1)
Promote the cytotoxicity to increase the antitumoral activities by producing H2O2 with its pyrogallol moiety or the reduction of Fe(III) to Fe(II), generating -OH ROS (although cysteine N-acetyl protect cells from cytotoxicity of H2O2, it does not avoid cell death process).
(2)
Promote apoptosis through mitochondrial damage, membrane depolarization, and cytochrome c release, and protects against mitochondrial damage-related cell death without changes in superoxide dismutase (SOD), glutathione peroxidase, Nrf2, Bcl2, and oxidative stress. Modulates gene expression by inhibiting various transcription factors (including Sp1, NF-κB, AP-1, STAT1, STAT3, and FOXO1) and the expression of NF-κB and AP-1. EGCG inhibits STAT1 to mediate protective effects on myocardial injury.
(3)
Increase second messengers, such as Ca2+, cAMP, and cGMP. EGCG elevates cytosolic Ca2+ without electrical stimulation by inhibition of sarcoplasmic/endoplasmic reticulum Ca2+-ATPase activity (SERCA), which affects the activities of Ca2+-requiring enzymes, such as calmodulin (CAM)-dependent protein kinase II and CAMKKβ (CAMKKβ is an upstream regulator of AMP-dependent kinase (AMPK), which plays crucial roles in energy metabolism and cardiovascular functions). If it stimulates vasorelaxation by increasing cAMP and cGMP in the aorta, then it may stimulate the production of cyclic nucleotides with beneficial biological effects in cardiovascular physiology.
(4)
Inhibit the transcription of FOXO1 to lead to the suppression of basal levels of endothelin-1 and differentiation of adipocytes. In mitochondria, EGCG enhances fat utilization, reducing the expression of leptin and stearyl-CoA desaturase while increasing fat oxidation. Moreover, EGCG regulates activities of cell surface growth factor receptors, especially receptor tyrosine kinases (RTK), including epidermal growth factor receptor (EGFR), vascular endothelial growth factor receptor (VEGFR), insulin-like growth factor receptor (IGFR), and the insulin receptor (InsR).
(5)
Inhibit DNA methyltransferase, which reverses methylation-induced gene silencing.
(6)
Inhibit autophagy, leading to apoptosis in macrophage cell lines.
Although the extracts of HS also change the oxidative potential of blood plasma, increasing the glutathione intracellular, its primarily action is on the Renin–Angiotensin–Aldosterone System (RAS) interfering with electrolytic regulation, blood pressure, and cardiac function [73], as well as the increasing of adrenalin, catecholamines, and noradrenalin (by specifically angiotensin (AngII)) [74].
Guerrero et al. [75] tested the activity of the Angiotensin Converting Enzyme inhibitor (ACEi) of 17 different types of flavonoids, and the ACEi increased when: (1) the catechol group was in the β-ring (3’, 4’-dihidroxy); (2) there is a double bond between C2 and C3 of carbon rings; and (3) there is a ketone in the C4 of the carbon ring. The absence of C4 in the carbonyl group of EGCG reduces the ACEi ability; the DOS and COS chemical structures have primarily ACEi potential.
Studies including in vivo cells [73] have shown that DOS and COS inhibit 43 to 50% of the ACE (COS and COS vs. control, and 30% less than captopril); furthermore, anthocyanins interfered in the RAS reductive process (RT-qPCR mARN of ACE and renin were analyzed), reducing 37 to 52% of the rARN expression for renin. To test the clinical effect of anthocyanins of HS, Nurfaradilla et al. [76] blocked the left renal artery of mice (2KlC hypertension) and treated them with HS extracts (30 mg/200 g BW), captopril, and captopril+HS mixtures; HS extracts reduced the systolic blood pressure 17% (average 150 vs. 88, and 80, control vs. HS, and captopril). Although captopril and HS reduced the renin and AngII in plasma, HS reduced the ACE activity (1.5 µmol/mL/min control vs. 0.40 µmol/mL/min HS, vs. 0.30 µmol/mL/min captopril).
Other potential pharmacological properties of HS antioxidants are anti-hypercholesterolemia, antipyretic, antibacterial, antiviral, and anthelminthic [13,77].

5. Effect of Anthocyanins on Diet Nutritive Value and Productive Behavior in Ruminants

5.1. Effects on Ruminal Digestibility, Volatile Fatty Acids, and Methane Emission

Antioxidants might maintain their activities in a ruminal environment and reach to the bowel without major modifications. Anthocyanins can improve the ruminal antioxidant potential [31,32].
Although some in vitro studies show no differences among ruminal gas production [31,32,78], some flavonoids (e.g., tannins) have effects on ruminal microbiota [17,68], modifying the gas production kinetics and the volatile fatty acids (VFA) proportions, sometimes improving the acetate: propionate ratio [17,41].
The chemical structure, distribution, and elimination of flavonoids affect the interaction and/or synergism between them and the ruminal microbiota.
Although there are many unknown ruminal interactions among some components of feedstuffs, microorganisms, and endogenous enzymes, anthocyanins could reduce the protozoa and microorganisms that may influence the rumen fermentation. However, feeding animals on residues with a high anthocyanin content as such berries seemed to have a low effect on fermentation patterns [44]. Some doses of proanthocyanidin may have a toxic effect (by altering the membranes’ permeability) on Ruminococcus albus and Peptostreptococcus anaerobius; meanwhile condensed tannins have a direct inhibitory effect on hemicellulases, endoglucanases, and proteolytic enzymes produced by Fibrobacter succinogenes, Butyrivibrio fibrisolvens, Ruminobacter amylophilus, and Streptococcus bovis [17]. Therefore, polyphenols have been associated with the reduction of fibrolytic enzymes and bacteria [17]. Moreover, some non-desirable antioxidant effects are the reduction of the endogenous fibrolytic enzymes activities and thereby the potential fiber digestibility and protein absorption [26].
Ruminal bacteria such as Anaerovibrio lipolytica, Butyrivibrio, Clostridium, Popionivacterium, Staphlylococcus, Selenomonas, and Pseudomonas aeruginosa have lipolytic activity, while Butyrivibrio fibrisolvens, Butyrivibrio hungatei, Clostridium strains, Propionibacterium, and Eubacterium participate in fatty acids biohydrogenation (BH) [17]. However, polyphenols could alter the ruminal microorganisms [79], altering some steps of BH. The lipolysis of dietary triglycerides, phospholipids, and glycolipids are sources of unsaturated fatty acids (UFA) to obtain stearic acid (C18:0) after sequential isomerization and saturation steps that involve the production of positional and geometrical isomers (C18:3, C18:2, C18:1 fatty acids). For example, regardless the type of polyphenol, in vitro studies have shown their negative effects on the growth of B. fibrisolvens that seem to lead to the accumulation of vaccenic acid and reduction of stearic acid [79]. There is not enough evidence clarify how specific changes in microbiota affect the BH.
The antioxidant activities of anthocyanin also affect increased desaturase enzymes activity for converting monounsaturated fatty acid (MUFA) to PUFA or inserting additional unsaturated bonds into already existing PUFA [17,27]. Studies have suggested that PUFAs have antimicrobial activities and are toxic to cellulolytic microorganisms by altering the bacterial cell membranes and the various essential processes that occur within and at the membrane; therefore, PUFAs can also reduce the microbial colonization with the fed particles and reduce the rumen digestibility of fiber [80].
In addition, as with other polyphenols sources, some HS components with high-lignin contents have low DM digestibility, and therefore, depending on the ruminant species and doses, the inclusion of by-products rich in polyphenols should not affect the DM intake or decrease the voluntary feed intake [26]. However, some authors suggest that adding certain antioxidants might not alter digestibility of DM, organic matter (OM), and neutral detergent fiber (NDF) [41], or even can reduce oxidative stress and increase the NDF, acid detergent fiber (ADF), and DM digestibility [40,41,80].
Novel molecular techniques (amplifying 16S rRNA) have shown that some flavonoids can increase the amount of Bacteroidetes, Firmicutes, and Tenericutes, and reduce the phyla Proteobacteria, Verrucomicrobia, and Actonobacteria [17].
The antioxidant and antimicrobial activities of HS are also related to the reduction of methane and N-ammonia (CH4 and NH3) caused by the changes of the by-products that affect the growth of methanogenic microorganisms [68]. Although it is not confirmed, different by-products rich in polyphenols (such as grapes, purple corn stover, Paulownia leaves, and other antioxidants) can affect the microorganisms participating in the production of hydrogen such as utilizing hydrogen to produce CH4 and therefore reduce it [17,40,41,44,45]. Thus, polyphenols can be associated with reductions of CH4 due to: (1) flavonoids indirectly reducing ruminal methanogenesis, acting as H2 sinks, (2) reduction of fiber digestion contributing to lower methane production, and (3) acting through the inhibition of the growth and activity of methanogens and hydrogen-producing microbes [17].

5.2. Post-Ruminal Effects of Anthocyanins

Some polyphenols are hydrolyzed and transformed through endogenous enzymatic activities and ruminal bacteria [81]; therefore, the secondary metabolites cross through the ruminal epithelium and the non-absorbed are bio-converted in the small bowel (as it occurs in monogastric) [81] and pass to the bloodstream [26,35,82,83] to deposit in tissues [68,82].
Anthocyanins can improve the blood plasma resistance to oxidation [33,84,85]. The COS and DOS can be deposited in lung, cardiac, renal, and hepatic tissues [69], suggesting that anthocyanins can improve the potential meat and milk antioxidants. However, improve of ruminal fatty acids biohydrogenation is associated with increased anthocyanins in animal products to human feed.
Although milk yield and fat have improvements related to anthocyanin addition in ruminant diets [85], the potential clinical effects of DOS and COS of HS on RAS could interfere in the homeostatic balance of ruminants and affect milk yield [84]. In mice, lactation led to upregulation and downregulation of selected RAS [86].
Reports about the potential effects of HS anthocyanins on fertility parameters are not consistent; however, other sources of polyphenols such as coffee can improve the semen quality [87] and reduce the fertilization rates even when progesterone, estradiol, and follicle-stimulating hormone remain constant [60]. In contrast, other types of antioxidants such as selenium and a-tocopherol might increase some reproductive parameters in dairy cattle [28]. Therefore, further studies could be focused on the effect of HS anthocyanins on estrous as well as milk and meat production.
Substituting 75% of total CP with HS seeds might not negatively affect animal performance in beef cattle [47]. Previously, the inclusion of ≤25% of the total DM of sheep diets with HS seeds increased the final body weight and carcass proportion [88]; however, in other studies, adding 10–20% of HS seeds improved the organoleptic and quality fatty acid properties of sheep meat [52].

6. Antioxidants Effect on Milk and Meat Quality as well as Shelf-Life

6.1. Anthocyanins and Polyphenols in Milk and Meat Fatty Acids Composition

Besides the positive effects of increasing the meat and milk antioxidants on human welfare, anthocyanins could increase the shelf-life of animal products [42,89,90]. Overall, polyphenols avoid lipid and protein oxidation (hyper-peroxides, aldehydes, and ketones), autolysis, and microbial pollution [29,91,92,93]. Increasing the long-chain fatty acids (n-3, n-6, and n-9) in ruminant diets improved the fatty acids composition of milk and meat [94,95,96].
Although there are not enough studies that analyze the effect of HS on milk fatty acids, among the literature, consistently including other products rich in polyphenols and anthocyanins increased the total PUFA, MUFA, and overall improved the milk fat C18:1, C18:2, cis-9, trans-11, n-3, n6, and concentrations of LA and conjugated linoleic acid (CLA) [26,41,44,45,79].
The antioxidant activity of milk and dairy products can be enhanced by phytochemicals rich in antioxidants [97]. Including by-products rich in polyphenols in dairy cows’ diets can increase the PUFA, lactose, and lactoglobulin in milk and its derived products, which have been associated with anticarcinogenic effects, and CLA and LA, which are associated with the reduction of atherogenic and thrombogenic indices [33].
In beef, by-products rich in polyphenols can alter the composition of fatty acids in meat through the effects of antioxidants on ruminal bacteria and the mechanism of absorption and transportation of these fatty acids from small intestine to muscle. However, some levels of antioxidants, primarily polyphenols and anthocyanins in ruminant diets, are associated with increases in the proportions of n-3 and n-6 PUFA [27]. Indeed, improving the contents of n-3 and n-6 PUFA in ruminant products have positive effects on human health, i.e., rumenic acid and LA isomers (cis-9, trans-11), which have demonstrated effects such as antiatherosclerosis, anticarcinogenic, antidiabetic, and anti-inflammatory activities in laboratory animals, and anticholesterolemic and anti-atherosclerosis effects in humans.

6.2. Anthocyanins and Polyphenols in Milk and Meat Shelf-Life

Antioxidants change the oxidative balance in dairy products and derivatives. Lipid oxidation is the main reason for the chemical spoilage of food and dairy products, decreasing their nutritional value, flavor, and texture.
Although milk proteins such as β and κ caseins have shown antioxidant activity, supplementation with different antioxidants such as vitamin C, tocopherol, vitamin E, zinc, and selenium can enhance the antioxidant activity of milk [97]. Recent reviews have been discussing the potential of using by-products of HS comparing their potential effects with other by-products rich in polyphenols and sources of anthocyanins (such as berries, grapes, grape pomace, etc.), to improve milk quality and fatty acids composition [26,33,41,44,45,79]. However, antioxidant compounds can also contribute to extending the shelf-life of dairy products and derivatives, reducing oxidative reactions that contribute to the deterioration of foods characterized by highly unsaturated lipids, which are extremely susceptible to oxidation [26], and reducing oxidized flavors in milk [98].
The fatty acid profiles of cheese have been shown to have the same variations as evidenced in milk. The quality of animal-derived foods is strongly associated with the characteristics of their lipid fractions [26]. Ianni et al. [33] monitored the extent of the oxidative damage in fresh and ripened cheeses through the evaluation thiobarbituric acid-reactive substances (TBARS), using malondialdehyde (MDA) as oxidative marker, and found that cheese from the milk of cows fed grape pomace did not increase MDA values 30 d after the ripening began, despite their greater contents of PUFAS vs. control (cows that did not feed on grape pomace) which went through oxidation. Grape pomace also reduced the concentrations of butanoic and hexanoic acids, associated with flavor changes and rancidity in both fresh and ripened cheeses. In addition, grape pomace increased aminobutyric acid (GABA) in cheese at the end of the ripening period that potentially can reduce the blood pressure, protect against chronic diseases, and improve immunity in consumers, but is also associated with specific fermentative bacteria (Lactobacillus acidophilus and Lactobacillus hilgardii) responsible for catalyzing the decarboxylation of l-glutamate to GABA.
Meat color, flavor, and odor are affected by oxidation which is shown as the conversion of red color muscle pigment myoglobin to brown metmyoglobin and the development of rancid odors and flavors [27].
In addition to the negative impact on meat pigments, odors, and flavors, lipid peroxidation causes toxic compounds implicated in several human pathologies, including aging processes, atherosclerosis, inflammation, and cancer [27]. Lipid oxidation in meat increases after 4 to 7 days of storage, and shelf-life and quality can be improved by natural antioxidants in meat by adding antioxidants in animal diets [98].
Protein-carbonyl determines protein oxidation in meat, and it increases during chilled storage. However, antioxidant and anthocyanin supplementation can slow increases in protein carbonyl during storage [27]. The HS by-products could have effects on meat lipid and protein oxidation comparable to other sources of by-products rich in anthocyanins, as previously studied [27,98,99,100].
In dairy cows, animals fed antioxidants improve the CLA and cis-9, trans-11 CLA, associated with the level of fatness. Feeding antioxidants in some stages of meat production can reduce the microbial growth and lipid oxidation during storage, increasing the shelf-life and meat quality [99]. Cattle fed other sources of antioxidants such as anthocyanins had a higher proportion of n-3 PUFA and show greater color stability and lower oxidation of lipid, protein, and myoglobin than meat from cattle fed with high oxidant diets (such as a high proportion of grains) [27].
Specifically, cattle fed antioxidants (primarily cyaniding-3-glucoside) had shown a more stable color depending on the dose of inclusion in diets. Maggiolino et al. [100] fed Merino lambs with lemon and red oranges rich in anthocyanins, finding that rheological, colorimetric, and oxidative parameters of Longissimus lumborum muscle sampled for 7 days were negatively affected by the time, but positively by the dose of anthocyanins supplemented. In this study, TBARS and hydroperoxides were also reduced, enhancing meat oxidative stability and improving the color in meet from lambs fed anthocyanins along the sampled period.

7. Limitations and Perspectives

The potential relationship among the antioxidant activities of calyxes, seeds, and stalks anthocyanins of HS with the ruminal microbiota and fibrolytic enzymes remain unknown. In comparison to the studies included in the present review that evaluated other polyphenols in the ruminal environment, hypothetically the positive effects of HS anthocyanins would be the potential reduction of CH4 and the fatty acids biohydrogenation process, but also it could reduce the potential fiber degradability [26,68,101,102,103].
Since antioxidants have a potential reduction of AOPP which is related with milk yield improvement, the available information about biochemical and RAS changes promoted by DOS and COS of HS [75,86] could be considered in further in vivo studies to find inclusion doses that would improve the composition of the antioxidant and fatty acids as well as improve milk yield. However, optimal inclusion should avoid potential negative effects on animal performance and reproductive parameters.

8. Conclusions

Including HS by-products might reduce the environmental and economic cost of livestock and potentially improve the quality of ruminant’s products. The excess of ROS unbalances the oxide-reductive potential primarily in ruminants fed. The HS contain flavonoids primarily classified as anthocyanins (mainly COS and DOS) that show specific actions on RAS regulation, increasing the ACEi action and reducing the expression of renin genes that could affect the animal productive behavior. As with other antioxidants, anthocyanins can reduce ruminal methanogens microorganisms and interact with substrates, fibrolytic microbiota, and enzymes affecting the fiber degradability and the biohydrogenation of lipids, improving the quality of milk and meat fatty acids composition; reducing the oxidation; improving the color, flavor, and odor stability; and extending the shelf-life of products. Changes in fatty acids composition can be beneficial for human consumers’ health.

Author Contributions

The present study was conceptualized, designed, and directed by D.N.T.-G. Although all authors were actively involved in data collection, analysis, and discussion process, L.A.M.-R., G.T.-E., and A.Z.M.S. analyzed and defined the criteria of articles inclusion and technical revision. R.L.-C. and M.I.C.-D. revised and analyzed the included articles. S.E.M.-C. contributed to the analysis of the economic and environmental impact. G.D.M.-M. and A.L.-B. analyzed the validity of derived conclusions. D.N.T.-G. was responsible for the visualization and formal analysis of results and wrote the draft paper. G.T.-E. and A.Z.M.S. were responsible of the technical analysis of the final version of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external founding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

Thanks to Universidad Autónoma Chapingo, Tecnológico Nacional de México (TecNM), and Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP) for the technical support.

Conflicts of Interest

The authors declare no conflict of interest. Financial funding sources had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

ACE, angiotensin converting enzyme; ACEi, inhibitor Angiotensin Converting Enzyme; ADF, acid detergent fiber; AMPK, AMP-dependent kinase; AngII, angiotensin II; AOPP, advanced oxidative protein products; BH, fatty acids biohydrogenation; CAM, calmodulin; CH4, methane; CLA, conjugated linoleic acid; CP, crude protein; CF, crude fiber; COS, cianidin-3-O-sambubioside; DM, dry matter; DOS, delphinidin-3-O-sambubioside; EGCG, epigalocathechin-3-gallate; EGC, epigallocatechin; ECG, epichatechin-3-gallate; EC, epicatechin; EGFR, epidermal growth factor receptor; GABA, aminobutyric acid. HS, Hibiscus sabadariffa L.; IGFR, insulin-like growth factor receptor; InsR, insulin receptor; I-κβ, interleukin; LA, linoleic acid; MDA, malondialdehyde; MUFA, monounsaturated fatty acids; NDF, neutral detergent fiber; NH3, N-ammonia; NF-κβ, necroptosis factor; OM, organic matter; PUFA, polyunsaturated fatty acids; SERCA, sarcoplasmic/endoplasmic reticulum Ca2+-ATPase activity; RAS, renin–angiotensin–aldosterone system; ROS, reactive oxygen species; RTK, receptor tyrosine kinase; SOD, superoxide dismutase; TBARS, thiobarbituric acid; TNF-α, tumoral factor; UFA, unsaturated fatty acids; VFA, volatile fatty acids.

References

  1. Sáyago, A.S.G.; Arranz, S.; Serrano, J.; Goñi, I. Dietary fiber content and associated antioxidant compounds in Roselle flower (Hibiscus sabdariffa L.) beverage. J. Agric. Food Chem. 2007, 55, 7886–7890. [Google Scholar] [CrossRef] [PubMed]
  2. Fagbenhro, O.A. Soybean meal substitution with Roselle (Hibiscus sabdariffa L.) seed meal in dry practical diets for fingerlings of the African Catfish, Clarias gariepinus (Burchell 1822). J. Anim. Vet. Adv. 2005, 4, 473–477. [Google Scholar]
  3. SAGARPA—Secretaria de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. Plan Rector Nacional Sistema Producto Jamaica. Comité Nacional Sistema Producto Jamaica. 2012. Available online: https://docplayer.es/8913342-Plan.-rector-del-sistema-producto-jamaica.html. (accessed on 30 January 2021).
  4. Ariza, F.R.; Serrano, A.V.; Navarro, G.S.; Ovando, C.M.; Vázquez, G.E.; Barrios, A.A.; Michel-Aceves, A.C.; Guzman-Maldonado, S.H.; Otero-Sanchez, M.A. Variedades mexicanas de jamaica (Hibiscus sabdariffa L.) ‘alma blanca’ y ‘rosalíz’ de color claro, y ‘cotzaltzin’ y ‘tecoanapa’ de color rojo. Rev. Fitotec. Mex. 2014, 37, 181–185. [Google Scholar]
  5. Aragón, G.A.; Torija, T.; Avelleira, C.R.; Tapia, R.; Contreras, M.I.R.; López, O.J.F. Control de plagas de la jamaica (Hibiscus sabdariffa L.) con Gliricidia sepium (Jacq.) en Chiautla de Tapia, Puebla. Rev. AIA 2008, 12, 33–42. [Google Scholar]
  6. SIAP—Servicio de Información Agroalimentaria y Pesquera. Producción Agrícola. 2018. Available online: http://nube.siap.gob.mx/cierre_agricola/ (accessed on 30 January 2021).
  7. FAO. Food and Agriculture Organization of the United Nations. Hibiscus: Post-harvest Operations. INPhO-Post-harvet Compendium. Roma, Italia. 2004. Available online: http://www.fao.org/fileadmin/user_upload/inpho/docs/Post_Harvest_Compendium_-_Hibiscus.pdf (accessed on 30 January 2021).
  8. Cid, O.S.; Guerrero, B.J.A. Propiedades funcionales de la Jamaica (Hibiscus sabdariffa L.). Rev. TSIA 2012, 6, 47–63. [Google Scholar]
  9. Da-Costa, R.I.; Bonnlaender, B.; Sievers, H.; Pischel, I.; Heinrich, M. Hibiscus sabdariffa L. A phytochemical and pharmacological review. Food Chem. 2014, 165, 424–443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Rustan, A.C.; Devron, C. Fatty acids: Structures and properties. In Encyclopedia of Life Sciences; John Wiley and Sons: New York, NY, USA, 2005; pp. 1–7. [Google Scholar]
  11. Jabeur, I.; Pereira, E.; Barros, L.; Calhelha, R.C.; Sokovic, M.; Oliveira, M.B.; Ferreira, I.C.F.R. Hibiscus sabdariffa L. as a source of nutrients, bioactive compounds and colouring agents. Food Res. Int. 2017, 100, 717–723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Formagio, A.S.N.; Ramos, D.D.; Vieira, M.C.; Ramalho, S.R.; Silva, M.M.; Zárate, N.A.H.; Foglio, M.A.; Calvalho, J.E. Phenolic compounds of Hibiscus sabdariffa and influence of organic residues on its antioxidant and antitumoral properties. Braz. J. Biol. 2015, 75, 69–76. [Google Scholar] [CrossRef] [Green Version]
  13. Ali, B.H.; Wabel, N.A.; Bluden, G. Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: A review. Phytother Res. 2005, 19, 369–375. [Google Scholar] [CrossRef]
  14. Bergmeier, D.; Berres, P.H.D.; Filippi, D.; Bilibio, D.; Bettiol, V.R.; Priamo, W.L. Extraction of total polyphenols from hibiscus (Hibiscus sabdariffa L.) and waxweed/“sete-sangrias” (Cuphea carthagenensis) and evaluation of their antioxidant potential. Acta Sci. Technol. 2014, 36, 545–551. [Google Scholar] [CrossRef] [Green Version]
  15. Borrás-Linares, I.; Fernández-Arroyo, S.; Arráez-Roman, D.; Palmeros-Suárez, P.A.; del Val-Díaz, R.; Andrade-Gonzáles, I.; Fernández-Gutiérrez, A.; Gómez-Leyva, J.F.; Segura-Carretero, A. Characterization of phenolic compounds, anthocyanidin, antioxidant and antimicrobial activity of 25 varieties of Mexican Rosselle (Hibiscus sabdariffa). Ind. Crop. Prod. 2015, 69, 385–394. [Google Scholar] [CrossRef]
  16. Pour, P.M.; Fakhri, S.; Asgary, S.; Farzaei, M.H.; Echeverría, J. The signaling pathways, and therapeutical targets of antiviral agents: Focusing on the antiviral approaches and clinical perspectives of anthocyanin in the management of viral diseases. Front. Pharmacol. 2019, 10, 1207. [Google Scholar] [CrossRef] [Green Version]
  17. Vasta, V.; Daghio, M.; Cappucci, A.; Buccioni, A.; Serra, A.; Viti, C.; Mele, M. Invited review: Plant polyphenols and rumen microbiota responsable for fatty acid biohydrogenation, fiber digestion, and methane emission: Experimental evidence and methodological approaches. J. Dairy Sci. 2019, 102, 3781–3804. [Google Scholar] [CrossRef]
  18. Guardiola, S.; Mach, N. Potencial terapéutico del Hibiscus sabdariffa: Una revisión de las evidencias científicas. Endocrinol. Nutr. 2014, 61, 274–295. [Google Scholar] [CrossRef]
  19. Hygreeva, D.; Pandey, M.C.; Radhakrishna, K. Potential applications of plant-based derivatives as fat replacers, antioxidants and antimicrobials in fresh and processed meat products. Meat Sci. 2014, 98, 47–57. [Google Scholar] [CrossRef] [PubMed]
  20. Agüero, M.; Segura, C.; Parra, J. Análisis comparativo de compuestos fenólicos totales y actividad antioxidante de cuatro marcas de tisanas de Hibiscus sabdariffa (Malvaceae) comercializadas en Costa Rica. Uniciencia 2014, 28, 34–42. [Google Scholar]
  21. Satúe-Gracia, M.T.; Heinonen, M.; Frankel, E.N. Anthocyanins as Antioxidants on Human Low-Density Lipoprotein and Lecithin−Liposome Systems. J. Agric. Food Chem. 1997, 45, 3362–3367. [Google Scholar] [CrossRef]
  22. Kähkönen, M.P.; Hopia, A.I.; Vuorela, H.J.; Rauha, J.P.; Pihlaja, K.; Kujala, T.S.; Heinonen, M. Antioxidant Activity of Plant Extracts Containing Phenolic Compounds. J. Agric. Food Chem. 1999, 47, 3954–3962. [Google Scholar] [CrossRef] [PubMed]
  23. Galicia-Flores, L.A.; Salinas-Moreno, Y.; Espinoza-García, B.M.; Sánchez-Feria, C. Caracterización fisicoquímica y actividad antioxidante de extractos de jamaica (Hibiscus Sabdariffa L.) Nacional e importada. Rev. Chapingo Ser. Hortic. 2008, 14, 121–129. [Google Scholar]
  24. Sindi, H.A.; Marshall, L.J.; Morgan, M.R.A. Comparative chemical andbiochemical analysis of extracts of Hibiscus sabdariffa. Food Chem. 2014, 164, 23–29. [Google Scholar] [CrossRef] [Green Version]
  25. Chu, C.; Deng, J.; Man, Y.; Qu, Y. Green Tea Extracts Epigallocatechin-3-gallate for Different Treatments. Biomed. Res. Int. 2017, 5615647. [Google Scholar] [CrossRef] [Green Version]
  26. Corredeu, F.; Lunesu, M.L.; Buffa, G.; Atzori, A.S.; Nudda, A.; Battacone, G.; Pulina, G. Can agro-industrial by-products rich in polyphenols be advantageously used in feeding and nutrition of dairy small ruminants? Animals 2020, 10, 131. [Google Scholar] [CrossRef] [Green Version]
  27. Prommachart, R.; Cherdthong, A.; Navanokraw, C.; Pongdontri, P.; Taron, W.; Uriyapongson, J.; Uriyapongson, S. Effect of dietary anthocyanin-extracted residue on meat oxidation and fatty acid profile of male dairy cattle. Animals 2021, 11, 322. [Google Scholar] [CrossRef] [PubMed]
  28. Chauhan, S.S.; Celi, P.; Ponnampalam, E.N.; Leury, B.J.; Lui, F.; Dunshea, F.R. Antioxidant dynamics in the live animal and implications for ruminant health and product (milk/meat) quality: Role of vitamin E and selenium. Anim. Prod. Sci. 2014, 54, 1525–1536. [Google Scholar] [CrossRef]
  29. Cuhna, L.C.M.; Monteiro, M.L.; Lorenzo, J.M.; Munekata, P.E.; Muchenje, V.; Carvalho, F.A.; Conte-Junior, C.A. Natural antioxidants in processing and storage stability of sheep and goat meat products. Food Res. Int. 2018, 111, 379–390. [Google Scholar]
  30. Lorenzo, J.M.; Pateiro, M.; Domínguez, R.; Barba, F.J.; Putnik, P.; Bursac, K.D.; Shpigelman, A.; Granato, D.; Franco, D. Berries extracts as natural antioxidants in meat products: A review. Food Res. Int. 2018, 106, 1095–1104. [Google Scholar] [CrossRef]
  31. Hosoda, K.; Sasahara, H.; Matsushita, K.; Tamura, Y.; Miyaji, M.; Matsuyama, H. Anthocyanin and proanthocyanidin contents, antioxidant activity, and in situ degradability of black and red rice grains. Asian-Aust. J. Anim. Sci. 2018, 31, 1213–1220. [Google Scholar] [CrossRef]
  32. Tian, X.; Paengkoum, P.; Paengkoum, S.; Thongpea, S.; Ban, C. Comparison of forage yield, silage fermentative quality, anthocyanin stability, antioxidant activity, and in vitro rumen fermentation of anthocyanin-rich purple corn (Zea mays L.) stover and sticky corn stover. J. Integr. Agric. 2018, 17, 2082–2095. [Google Scholar] [CrossRef] [Green Version]
  33. Ianni, A.; Martino, G. Dietary grape pomace supplementation in dairy cows: Effect on nutritional quality of milk and its derived dairy products. Foods 2020, 9, 168. [Google Scholar] [CrossRef] [Green Version]
  34. Theodorou, M.K.; Kingston-Smith, A.H.; Winters, A.L.; Lee, M.R.F.; Minchin, F.R.; Morris, P.; MacRae, J. Polyphenols and their influence on gut function and health in ruminants: A review. Environ. Chem. Lett. 2006, 4, 121–126. [Google Scholar] [CrossRef]
  35. Gladine, C.; Rock, E.; Morand, C.; Bauchart, D.; Durand, D. Bioavailability and antioxidant capacity of plant extracts rich in polyphenols, given as a single acute dose, in sheep made highly susceptible to lipoperoxidation. Br. J. Nutr. 2007, 98, 691–701. [Google Scholar] [CrossRef] [Green Version]
  36. Olagaray, K.E.; Bradford, B.J. Plant flavonoids to improve productivity of ruminants—A review. Anim. Feed Sci. Technol. 2019, 251, 21–36. [Google Scholar] [CrossRef]
  37. Ametaj, B.N.; Zebeli, Q.; Saleem, F.; Psychogios, N.; Lewis, M.J.; Dunn, S.M.; Xia, J.; Wishart, D.S. Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 2010, 6, 583–594. [Google Scholar] [CrossRef]
  38. Celi, P.; Gabal, G. Oxidant/antioxidant balance in animal nutrition and health: The role of protein oxidation. Front. Vet. Sci. 2015, 2, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Estévez, M.; Li, Z.; Soladoye, O.P.; van-Hecke, T. Health risks of food oxidation. Adv. Food Nutr Res. 2017, 82, 45–81. [Google Scholar]
  40. Huang, H.; Szumacher-Strabel, M.; Kumar, P.A.; Slusarcyk, S.; Lechniak, D.; Vazirigohar, M.; Varadyova, Z.; Kozlowska, M.; Cieslak, A. Chemical and phytcochemical composition, in vitro ruminal fermentation, methane production, and nutrient degradability of fresh and ensiled Paulownia hybrid leaves. Anim. Feed Sci. Technol. 2021, 279, 115038. [Google Scholar] [CrossRef]
  41. Khonkhaeng, B.; Cherdthong, A.; Chantaprasarn, N.; Harvatine, K.J.; Foiklang, S.; Chanjula, P.; Wanapat, M.; So, S.; Polyorach, S. Comparative effect of Volvariella volvacea-trated rice straw and purple corn stover fed at different levels on predicted methane production and milk fatty acid profiles in tropical dairy cows. Livestock Sci. 2021, 251, 104626. [Google Scholar] [CrossRef]
  42. Nikmaram, N.; Budaraju, S.; Barba, F.J.; Lorenzo, J.M.; Cox, R.B.; Mallikarjunan, K.; Roohinejad, S. Application of plant extracts to improve the shelf-life, nutritional and health-related properties of ready-to-eat meat products. Meat Sci. 2018, 145, 245–255. [Google Scholar] [CrossRef]
  43. Maffo, T.; Agbor, E.E.; Mekoudjou, N.H.; Kengne, S.C.N.; Gouado, I. Proximate and mineral composition, protein quality of Hibiscus sabdariffa L. (Roselle) seeds cultivated in two agroecological areas in Cameroon. Int. J. Nutr. Food Sci. 2014, 3, 251–258. [Google Scholar]
  44. Bryszak, M.; Szumacher-Strabel, M.; El-Sherbiny, M.; Stochmal, A.; Oleszek, W.; Roj, E.; Kumar, O.A.; Cieslak, A. Effects of berry seed residues on ruminal fermentation, methane concentration, milk production, and fatty acid proportions in the rumen and milk of dairy cows. J. Dairy Sci. 2019, 102, 1257–1273. [Google Scholar] [CrossRef] [Green Version]
  45. Moate, P.J.; Jacobs, J.L.; Hixson, L.J.; Deighton, M.H.; Hanna, M.C.; Morris, G.L.; Ribaux, B.E.; Wales, W.J.; Williams, S.R.O. Effects of feeding either red or white grape marc on milk production and methane emissions from early-lactation dairy cows. Animals 2020, 10, 976. [Google Scholar] [CrossRef]
  46. Mohd-Esa, N.; Shin, H.F.; Ismail, A.; Lye, Y.C. Antioxidant activity in different parts of roselle (Hibiscus sabdariffa L.) extracts a potential exploration of the seeds. Food Chem. 2010, 122, 1055–1060. [Google Scholar] [CrossRef]
  47. Sulliman, G.M.; Babiker, S.A.; Eichinger, H.M. Effect of Hibiscus seed-based diet on chemical composition, carcass characteristics and meat quality traits of cattle. Indian J. Anim. Res. 2017, 51, 694–699. [Google Scholar] [CrossRef] [Green Version]
  48. Wang, M.L.; Morris, B.; Tonnis, B.; Davis, J.; Pederson, G.A. Assessment of oil Content and fatty acid composition variability in two economically important Hibiscus species. J. Agric. Food Chem. 2012, 60, 6620–6626. [Google Scholar] [CrossRef]
  49. Ismail, A.; Khairul, I.E.; Mohd, N.H. Roselle (Hibiscus sabdariffa L.) seeds-nutritional composition, protein quality and health benefits. Glob. Sci. Book Food 2008, 2, 1–16. [Google Scholar]
  50. Shaheen, M.A.; El-Nakhlawy, F.S.; Al-Shareef, A.R. Roselle (Hibiscus sabdariffa L.) seeds as unconventional nutritional source. Afr. J. Biotech. 2012, 11, 9821–9824. [Google Scholar]
  51. Udayasekhara, R.P. Nutrient composition and biological evaluation of mesta (Hibbiscus sabdariffa) seeds. Plant Foods Hum. Nutr. 1996, 49, 27–34. [Google Scholar] [CrossRef] [PubMed]
  52. Beshir, A.A.; Babiker, S.A. The effect of feeding diet with graded levels of roselle (Hibiscus sabdariffa) seed on carcass characteristics and meat quality of Sudan desert lamb. Res. J. Animal Vet. Sci. 2009, 4, 35–44. [Google Scholar]
  53. Jínez, M.T.; Cortés, C.A.; Ávila, G.E.; Casaubon, M.A.; Salcedo, E.R. Efecto de niveles elevados de semilla de Jamaica (Hibiscus sabdariffa) en dietas para pollos sobre el comportamiento productivo y funcionamiento hepático. Vet. Mex. 1998, 29, 35–40. [Google Scholar]
  54. Kwari, I.D.; Igwebuike, J.U.; Mohammed, I.D.; Diarra, S.S. Growth, haematology and serum chemistry of broiler chickens fed raw or differently processed sorrel (Hibiscus sabdariffa) seed meal in a semi-arid environment. IJSN 2011, 2, 22–27. [Google Scholar]
  55. Mukhtar, A.M. The Effect of Feeding Rosella (Hibiscus sabdariffa) Seed on Broiler Chick’s Performance. Res. J. Anim. Vet. Sci. 2007, 2, 21–23. [Google Scholar]
  56. Soriano, T.J.; Tejada, H.I. Estudio preliminar del valor nutritivo de la semilla de Jamaica (Hibiscus sabdariffa) para el pollo de engorda. Téc. Pecu. Mex. 1995, 33, 48–52. [Google Scholar]
  57. Anhwange, B.A.; Ajibola, V.O.; Okibe, F.G. Nutritive value and anti-nutritional factors in Hibiscus sabdariffa. J. Fish. Int. 2006, 1, 73–76. [Google Scholar]
  58. Tounkara, F.; Amadou, I.; Le, G.; Shi, Y. Effect of boiling on the physicochemical properties of Roselle seeds (Hibiscus sabdariffa L.) cultivated in Mali. Afr. J. Biotech. 2011, 10, 18160–18166. [Google Scholar]
  59. Bellaloui, N.; Bruns, H.A.; Abbas, H.K.; Mengisty, A.; Fisher, D.K.; Reddy, K.N. Agricutural practices altered soybean protein, oil, fatty acids, sugars, and minerals in the Midsouth USA. Front. Plant. Sci. 2015, 6, 1–14. [Google Scholar] [CrossRef]
  60. Mahmoud, A.A.; Selim, K.A.; Abdel-Baki, M.R. Physico-chemical and oxidative stability characteristics of roselle (Hibiscus sabdariffa L.) seed oil as by-product. Egypt J. Appl. Sci. 2008, 23, 247–257. [Google Scholar]
  61. Rahman, A.A.; Salih, A.M.; Turki, I.Y.; Abdulatee, S.O.; Elbasheir, O.M.; Magboul, M.M. Determination of dry matter and crude protein degradability of Roselle seed (Hibiscus sabdariffa) using bags nylon technique. Sudan J. Sci. Tech. 2016, 17, 58–65. [Google Scholar]
  62. Daley, C.A.; Abbot, A.; Doyle, P.; Nader, G.A.; Larson, S. A review of fatty acid profiles and antioxidant content in grass-fed and grain-fed beef. Nutr. J. 2010, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
  63. He, Y.; Tan, D.; Mi, Y.; Zhou, Q.; Ji, S. Epigallocatechin-3-gallet attenuates cerebral cortex damage and promotes brain regeneration in acrylamide-treated rats. Food Funct. 2017, 8, 2275–2282. [Google Scholar] [CrossRef]
  64. Wang, Y.; Wang, B.; Du, F.; Su, X.; Sun, G.; Zhou, G.; Bian, X.; Liu, N. Epigallocatechin-3-gallate attenuates ureteral obstruction-induced renal interstitial fibrosis in mice. J. Histochem. Cytochem. 2015, 63, 270–279. [Google Scholar] [CrossRef] [Green Version]
  65. Palabiyik, S.S.; Dincer, B.; Cadirici, E.; Cinar, E.; Gundogdu, C.; Polat, B.; Yayla, M.; Halici, Z. A new update for radiocontrast-induced nephropathy aggravated with glycerol in rats: The protective potential of epigallocatechin-3-gallate. Ren. Fail. 2017, 39, 314–322. [Google Scholar] [CrossRef] [Green Version]
  66. Chen, L.L.; Xu, Y. Epigallocateichin gallate attenuates uric acid-induced injury rat renal interstitial fibroblasts NRK-49F by up-regulation of miR-9. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 7458–7469. [Google Scholar]
  67. Ortíz-Romero, P.; Borralleras, C.; Campuzano, V. Epigallocatechin-3-gallate improves cardiac hypertrophy and short-term memory deficits in a Williams-Beuren syndrome mouse model. PLoS ONE 2018, 13, e0194476. [Google Scholar] [CrossRef] [Green Version]
  68. Klantar, M. The importance of flavonoids in ruminant nutrition. Arch. Anim. Husb. Dairy Sci. 2018, 1, 1–4. [Google Scholar]
  69. Sandoval-Ramírez, B.A.; Catalán, U.; Fernández-Castillejo, S.; Rubio, L.; Macia, A.; Sola, R. Anthocyanin tissue bioavailability in animals: Possible implications for human health. A systematic review. J. Agric. Food Chem. 2018, 66, 11531–11543. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Xiao, X.; Du, C.; Yan, Z.; Shi, Y.; Duan, H.; Ren, Y. Inhibition of necroptosis attenuates kidney inflammation and interstitial fibrosis induced by unilateral ureteral obstruction. Am. J. Nephrol. 2017, 46, 131–138. [Google Scholar] [CrossRef]
  71. Kakuta, Y.; Okumi, M.; Isaka, Y.; Tsutahara, K.; Abe, T.; Yazawa, K.; Ichumaru, N.; Matsumura, K.; Hyon, S.; Takahara, S.; et al. Epigallocatechin-3-gallate protects kidneys from ischemia rerperfusion injury by HO-1 upregulation and inhibition of macrophage infiltration. Transpl. Int. 2011, 24, 514–522. [Google Scholar] [CrossRef] [PubMed]
  72. Kim, H.-S.; Quon, M.J.; Kim, J.A. New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol. 2014, 2, 187–195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Parichatikanond, W.; Pinthong, D.; Mangmool, S. Blockade of the renin-angiotensin system with delphinidin, cyanin, and quiercetin. Planta Med. 2012, 78, 1626–1632. [Google Scholar]
  74. Nakamura, K.; Shimizu, T.; Yanagita, T.; Nemoto, T.; Taniuchi, K.; Shimizu, S.; Dimitriadis, F.; Yawata, T.; Higashi, Y.; Ueba, T.; et al. Angiotensin II acting on brain AT1 receptors induces adrenaline secretion and pressor responses in the rat. Sci. Rep. 2014, 4, 7248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Guerrero, L.; Castillo, J.; Quiñones, M.; Garcia-Vallvé, S.; Arola, L.; Pujadas, G.; Muguerza, B. Inhibition of angiotensin-converting enzyme activity by flavonoids: Structure-activity relationship studies. PLoS ONE 2012, 7, e49493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Nurfaradilla, S.A.; Saputri, F.C.; Harahap, Y. Effects of Hibiscus sabdariffa calyces aqueous extract on the antihypertensive potency of captopril in the two-kidney-one-clip rat hypertension model. Evid. Based Complement. Altern. Med. 2019, 2019, 9694212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Nileeka, B.W.; Rupasinghe, H.P. Plant flavonoids as angiotensin converting enzyme inhibitors in regulation of hypertension. J. Funct. Food Health Dis. 2011, 1, 172–188. [Google Scholar] [CrossRef]
  78. Elahi, M.Y.; Rouzbehan, Y.; Rezaee, A. Effects of phenolic compounds in three oak species on in vitro gas production using inoculums of two breeds of indigenous Iranian goats. Anim. Feed Sci. Technol. 2012, 176, 26–31. [Google Scholar] [CrossRef]
  79. Wang, Y.M.; Wang, J.H.; Wang, C.; Chen, B.; Liu, J.X.; Cao, H.; Guo, F.C.; Vázquez-Arañón, M. Effect of different rumen-inert fatty acids supplemented with a dietary antioxidant on performance and antioxidative status of early-lactation cows. J. Dairy Sci. 2010, 93, 3738–3745. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Zeoula, L.M.; Machado, E.; Carraro, J.; Aguiar, S.C.; Yoshimura, E.H.; Calvo, A.B.; Seiji, S.F.; Woruby, S.N. Antioxidant action in diets with ground soybeans on ruminal microbial production, digestion, and fermentation in buffaloes. Braz. J. Vet. Res. Anim. Sci. 2019, 48, e20180167. [Google Scholar] [CrossRef] [Green Version]
  81. Gessner, D.K.; Ringseis, R.; Eder, K. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J. Anim. Physiol. Anim. Nutr. 2016, 101, 605–628. [Google Scholar] [CrossRef]
  82. Castillo, C.; Hernández, J.; López-Alonso, M.; Miranda, M.; Benedito, J.L. Values of plasma lipid hydroperoxides and total antioxidant status in healthy dairy cows: Preliminary observations. Arch. Tierz. 2003, 46, 227–233. [Google Scholar] [CrossRef]
  83. Salinas-Rios, T.; Sánchez-Torres-Esqueda, M.T.; Díaz-Cruz, A.; Cordero-Mora, J.L.; Cárdenas-León, M.; Hernández-Bautista, J.; Nava-Cuellar, C.; Nieto-Aquino, R. Oxidative status and fertility of ewes supplemented coffee pulp during estrous synchronization and early pregnancy. Rev. Colomb. Cienc. Pecu. 2016, 29, 255–263. [Google Scholar] [CrossRef] [Green Version]
  84. Hosoda, K.; Eruden, B.; Matsuyama, H.; Shioya, S. Effect of anthocyanin-rich corn silage on digestibility, milk production and plasma enzyme activities in lactating dairy cows. Anim. Sci. J. 2012, 83, 453–459. [Google Scholar] [CrossRef]
  85. Hosoda, K.; Miyaji, M.; Matsuyama, H.; Haga, S.; Ishizaki, H.; Nonaka, K. Effect of supplementation of purple pigment from anthocyanin-rich corn (Zea mays L.) on blood antioxidant activity and oxidation resistance in sheep. Livest. Sci. 2012, 145, 266–270. [Google Scholar] [CrossRef]
  86. La Rosa, M.; Kechichian, T.; Olson, G.; Saade, G.; Prewit, E.B. Lactation leads to modifications in maternal Renin-Angiotensin System in later life. Obstet. Gynecol. 2020, 27, 260–266. [Google Scholar] [CrossRef] [PubMed]
  87. Janegrad, P.A.; Kia, H.A.; Moghaddam, G.; Ebrahimi, M. Evaluating caffeine antioxidant properties on Ghezel ram sperm quality after freeze-thawing. Rev. Méd. Vét. 2018, 169, 233–240. [Google Scholar]
  88. Elamin, K.M.; Hassan, H.E.; Abdalla, H.O.; Arabi, O.H.; Tameem, E.A.A. Effect of feeding crushed roselle seed (Hibiscus sabdariffa L.) on carcass characteristics of sudan desert sheep. Asian J. Anim. Sci. 2012, 6, 240–248. [Google Scholar] [CrossRef] [Green Version]
  89. Zhang, M.; Hettiarachchy, N.S.; Horax, R.; Kannan, A.; Praisoody, A.M.D.; Muhundan, A.; Mallangi, C.R. Phytochemicals, antioxidant and antimicrobial activity of Hibiscus sabdariffa, Centella asiatica, Moringa oleifera and Murraya koenigii leaves. J. Med. Plant. Res. 2011, 5, 6672–6680. [Google Scholar]
  90. Valenzuela, V.C.; Pérez, P.M. Actualización en el uso de antioxidantes naturales derivados de frutas y verduras para prolongar la vida útil de la carne y productos cárneos. Rev. Chil. Nutr. 2016, 43, 188–195. [Google Scholar] [CrossRef] [Green Version]
  91. Karre, L.; Lopez, K.; Getty, K.J. Natural antioxidants in meat and poultry products. Meat Sci. 2013, 94, 220–227. [Google Scholar] [CrossRef] [PubMed]
  92. Falowo, A.B.; Fayemi, P.O.; Muchenje, V. Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: A review. Food Res. Int. 2014, 64, 171–181. [Google Scholar] [CrossRef]
  93. Jiang, J.; Xiong, Y.L. Natural antioxidants as food and feed additives to promote health benefits and quality of meat products: A review. Meat Sci. 2016, 120, 107–117. [Google Scholar] [CrossRef] [Green Version]
  94. Christensen, R.A.; Drackley, J.K.; LaCount, D.W.; Clark, J.H. Infusion of four long-chain fatty acids mixtures into de abomasum of lactating dairy cows. J. Dairy Sci. 1994, 77, 1052–1069. [Google Scholar] [CrossRef]
  95. Martínez-Borraz, A.; Moya-Camarena, S.Y.; González-Ríos, H.; Hernández, J.; Pinelli-Saavedra, A. Conjugated linoleic acid (CLA) content in milk from confined Holstein cows during summer months in Northwestern Mexico. Rev. Mex. Cienc. Pecu. 2010, 1, 221–235. [Google Scholar]
  96. Hernández, A.; Kholif, A.E.; Lugo-Coyote, R.; Elghandour, M.M.Y.; Cipriano, M.; Rodríguez, G.B.; Odongo, N.E.; Salem, A.Z.M. The effect of garlic oil, xylanase enzyme and yeast on biomethane and carbon dioxide production from 60-d old Holstein dairy calves fed a high concentrate diet. J. Clean. Prod. 2017, 148, 616–623. [Google Scholar] [CrossRef] [Green Version]
  97. Taj, K.I.; Nadeem, M.; Imran, M.; Ullah, R.; Ajmal, M.; Hayat, J.M. Antioxidants properties of milk and dairy products: A comprehensive review of the current knowledge. Lipids Health Dis. 2019, 18, 41. [Google Scholar]
  98. Castillo, C.; Pereira, V.; Abuelo, A.; Hernández, J. Effect of supplementation with antioxidants on the quality of bovine milk and meat production. Sci. World J. 2013, 616098. [Google Scholar] [CrossRef]
  99. Velasco, V.; Williams, P. Improvement meat quality through natural antioxidants. Chil. JAR 2011, 7, 313–322. [Google Scholar]
  100. Maggiolino, A.; Bragaglio, A.; Rufrano, D.; Claps, S.; Sepe, L.; Damiano, S.; Ciarcia, R.; Dinardo, F.R.; Hopkins, D.L.; Neglia, G.; et al. Dietary supplementation of suckling lambs with anthocyanins: Effects on growth, carcass, oxidative and meat quality traits. Anim. Feed Sci. Tecnol. 2021, 276, 114925. [Google Scholar] [CrossRef]
  101. Morales, R.; Ungerfeld, E.M. Use of tannins to improve fatty acids profile of meat and milk quality in ruminants: A review. Chil. J. Agric. Res. 2015, 75, 239–248. [Google Scholar] [CrossRef] [Green Version]
  102. Carmo, T.J.; Peripolli, V.; Goncalves, J.B.C.; Bergmann, T.C.; Soares, F.M.C.; Restle, J.; Kindlein, L.; McManus, C. Carcass characteristics and meat evaluation of Nelore cattle subjected to different antioxidant treatments. Rev. Bras. Zootec. 2017, 46, 138–142. [Google Scholar] [CrossRef] [Green Version]
  103. Dewanckele, L.; Toral, P.G.; Vlaeminck, B.; Fievez, V. Invited review: Role of rumen biohydrogenation intermediates and rumen microbes in diet-induced milk fat depression: An update. J. Dairy Sci. 2019, 103, 7655–7681. [Google Scholar] [CrossRef] [PubMed]
Animals 11 02827 g001 550
Figure 1. Overall economic, environmental, and productive effects of including Hibsicus sabdariffa L. calyxes and by-products in ruminant diets.
Figure 1. Overall economic, environmental, and productive effects of including Hibsicus sabdariffa L. calyxes and by-products in ruminant diets.
Animals 11 02827 g001
Table
Table 1. Hibiscus sabdariffa L. chemical composition.
Table 1. Hibiscus sabdariffa L. chemical composition.
AuthorsDMCPEECFAshes
g/100 gg/100 DM
Fagbrnhro [2]92.639.46.117.711.4
Maffo et al. [43]90.022.022.020.06.1
Wang et al. [48]NRNR18.0NRNR
Ismail et al. [49]90.033.522.118.3NR
Shaheen and El-Nakhlawy [50] *NR31.423.24.295.5
Udayasekhara [51] **92.420.621.041.15.4
Beshir and Babikier [52]96.630.311.15.15.6
Jínez et al. [53]92.520.618.023.76.7
Kwari et al. [54]NR38.6NR13.5NR
Mukhtar [55]91.821.417.412.05.3
Soriano y Tejeda [56]92.724.817.822.91.6
Anhwange et al. [57]94.019.828.06.35.6
Tounkara et al. [58]91.827.320.8NR4.5
DM, dry matter; CP, crude protein; EE, ether; CF, crude fiber; NR, not reported; * Average from three varieties; ** Average from two varieties.
Table
Table 2. Proportion of fatty acids in Hibiscus sabdariffa L. seeds and calyxes.
Table 2. Proportion of fatty acids in Hibiscus sabdariffa L. seeds and calyxes.
SeedsCalyxes
Tounkara et al. [58]Mahmoud et al. [60]Jabeur et al. [11]
Saturated fatty acids (%)
Myristic (C14:0)0.210.261.24 ± 0.01
Palmitic (C16:0)19.2120.5227.73 ± 0.02
Stearic (C18:0)5.135.794.46 ± 0.01
Arachidonic (C20:0)0.67 1.02 ± 0.05
Polyunsaturated fatty acids (%)
Palmitoleic (C16:1)0.36 1.32 ± 0.04
Oleic (C18:1)36.938.469.1 ± 0.1
Linoleic (C18:2)35.0233.2532.65 ± 0.07
α-linoleic (C18:3)1.851.6915.76 ± 0.04
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Lazalde-Cruz, R.; Miranda-Romero, L.A.; Tirado-González, D.N.; Carrillo-Díaz, M.I.; Medina-Cuéllar, S.E.; Mendoza-Martínez, G.D.; Lara-Bueno, A.; Tirado-Estrada, G.; Salem, A.Z.M. Potential Effects of Delphinidin-3-O-Sambubioside and Cyanidin-3-O-Sambubioside of Hibiscus sabdariffa L. on Ruminant Meat and Milk Quality. Animals 2021, 11, 2827. https://doi.org/10.3390/ani11102827

AMA Style

Lazalde-Cruz R, Miranda-Romero LA, Tirado-González DN, Carrillo-Díaz MI, Medina-Cuéllar SE, Mendoza-Martínez GD, Lara-Bueno A, Tirado-Estrada G, Salem AZM. Potential Effects of Delphinidin-3-O-Sambubioside and Cyanidin-3-O-Sambubioside of Hibiscus sabdariffa L. on Ruminant Meat and Milk Quality. Animals. 2021; 11(10):2827. https://doi.org/10.3390/ani11102827

Chicago/Turabian Style

Lazalde-Cruz, Rosalba, Luis Alberto Miranda-Romero, Deli Nazmín Tirado-González, María Isabel Carrillo-Díaz, Sergio Ernesto Medina-Cuéllar, Germán David Mendoza-Martínez, Alejandro Lara-Bueno, Gustavo Tirado-Estrada, and Abdelfattah Z. M. Salem. 2021. "Potential Effects of Delphinidin-3-O-Sambubioside and Cyanidin-3-O-Sambubioside of Hibiscus sabdariffa L. on Ruminant Meat and Milk Quality" Animals 11, no. 10: 2827. https://doi.org/10.3390/ani11102827

APA Style

Lazalde-Cruz, R., Miranda-Romero, L. A., Tirado-González, D. N., Carrillo-Díaz, M. I., Medina-Cuéllar, S. E., Mendoza-Martínez, G. D., Lara-Bueno, A., Tirado-Estrada, G., & Salem, A. Z. M. (2021). Potential Effects of Delphinidin-3-O-Sambubioside and Cyanidin-3-O-Sambubioside of Hibiscus sabdariffa L. on Ruminant Meat and Milk Quality. Animals, 11(10), 2827. https://doi.org/10.3390/ani11102827

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop