Meta-analysis of dietary supplementation with flavonoids in small ruminants: Growth performance, antioxidant status, nutrient digestibility, ruminal fermentation, and meat quality

Author links open overlay panelFernando Lucio-Ruíz a, Juan Eduardo Godina-Rodríguez b, Lorenzo Danilo Granados-Rivera c, José Felipe Orzuna-Orzuna d, Santiago Joaquín-Cancino e, Pedro Abel Hernández-García f

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Highlights

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  Dietary supplementation with flavonoids improves growth performance in sheep and goats.

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  Dietary supplementation with flavonoids improves antioxidant status in blood serum of sheep and goats.

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  Dietary supplementation with flavonoids improves the digestibility of nutrients in sheep and goats.

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  Dietary supplementation with flavonoids improves ruminal fermentation in sheep and goats.

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  Dietary supplementation with flavonoids improves tenderness and oxidative stability in meat of sheep and goats.

Abstract

This study aimed to evaluate the effects of dietary supplementation with flavonoids on growth performance, antioxidant status, nutrient digestibility, ruminal fermentation, and meat quality of small ruminants through a meta-analytic approach. The data used in the meta-analysis were extracted from 29 scientific articles identified through systematic searches following the PRISMA methodology. Der-Simonian and Laird, random effects models, were used to assess effect sizes using weighted mean differences. Dietary supplementation with flavonoids increased (P < 0.05) dry matter intake, average daily gain, hot carcass weight, hot carcass yield, Longissimus dorsi muscle area, and backfat thickness. In contrast, the feed conversion ratio decreased (P < 0.05) in response to dietary flavonoid supplementation. Dietary supplementation with flavonoids increased (P < 0.001) the serum concentration of superoxide dismutase, catalase, glutathione peroxidase, and total antioxidant capacity but decreased (P < 0.001) the serum concentration of malondialdehyde (MDA). The digestibility of dry matter, organic matter, crude protein, neutral detergent fiber, and acid detergent fiber increased (P < 0.05) in response to dietary flavonoid supplementation. Dietary supplementation with flavonoids decreased (P < 0.001) the ruminal concentration of ammonia nitrogen and increased (P < 0.001) the ruminal concentration of total volatile fatty acids and acetate. Dietary supplementation with flavonoids decreased (P < 0.001) cooking loss, shear force, and MDA in meat. In conclusion, dietary supplementation with flavonoids can be used as a nutritional strategy to improve growth performance, antioxidant status in blood serum, nutrient digestibility, ruminal fermentation, and meat quality in small ruminants.

Introduction

According to recent studies (Stanišić et al., 2024, Mazhangara et al., 2019), the global demand for small ruminant meat (mainly lamb) is estimated to increase annually to 3.5 % until 2030. To meet this demand, Hernández-García et al. (2024) mention that it is necessary to increase growth performance and decrease the age at slaughter in small ruminants. Some authors (Zhan et al., 2023, Paixão et al., 2022) indicate that dietary supplementation with feed additives can stimulate growth rate, improve feed efficiency, decrease slaughter age, and increase carcass yield in small ruminants. Particularly, in finishing lambs fed high-concentrate diets (≥ 60 %), Qin et al. (2020) reported that dietary supplementation with flavonoids increases skeletal muscle synthesis through increased expression of the mammalian target of rapamycin (mTOR) protein, which improves animal growth performance and carcass traits. However, in small ruminants fed maintenance diets with a high proportion of forage (≥ 50 %), growth performance is not modified (Paixão et al., 2022).

Flavonoids are the largest group of polyphenols, and generally, each contains 15 carbon atoms with two benzene rings linked by a three-carbon bridge (Olagaray and Bradford, 2019). Flavonoids are abundant in various plants, fruits, and seeds (Días et al., 2021) and have immunostimulant, antimicrobial, anti-inflammatory, and antioxidant effects under in vivo conditions in beef cattle, dairy cows, broiler chickens and laying hens (Orzuna-Orzuna et al., 2023, Prihambodo et al., 2022, Prihambodo et al., 2021, North et al., 2019). Furthermore, Días et al. (2021) indicate that flavonoids can be substitutes for synthetic products, such as selenium and vitamin E, to improve food quality. Specifically in small ruminants, several studies have been published in the recent decade evaluating the effects of flavonoids on growth performance (Ding et al., 2021, Qi et al., 2017), antioxidant status in blood serum (Feng et al., 2023), nutrient digestibility (Hao et al., 2023, Paixão et al., 2022), ruminal fermentation (Taethaisong et al., 2022, Zhao et al., 2022a, Zhao et al., 2022b), and meat quality (Zhan et al., 2023, Tian et al., 2022). However, in several of these studies, the results obtained have been contradictory, which makes it difficult to obtain a scientifically reliable conclusion on the effect of the treatment. For example, some authors (Qi et al., 2017, Suong et al., 2022) reported a positive impact of dietary supplementation with low doses (between 11 and 85 mg/kg DM) of flavonoids (anthocyanins and mixtures) on growth performance and antioxidant status in blood serum of small ruminants. Likewise, other studies (Hao et al., 2023, Taethaisong et al., 2022) reported an increase in nutrient digestibility and ruminal concentration of volatile fatty acids in small ruminants supplemented with moderate to high doses (300–7974 mg/kg DM) of mixtures of flavonoids or anthocyanins. In contrast, recent studies (Zhan et al., 2023, Tian et al., 2022, Ding et al., 2021) did not detect positive effects of dietary supplementation with low to moderate doses (1.4–662.5 mg/kg DM) of rutin, anthocyanin or flavonoid mixtures on growth performance, blood serum antioxidant status, and meat quality of lambs and goats. Likewise, Paixão et al. (2022) and Sun et al. (2022) reported that dietary supplementation with flavonoids kaempferol and naringin (59.5–500 mg/kg DM) did not affect nutrient digestibility or ruminal fermentation in finishing lambs and goats. According to several authors (Orzuna-Orzuna et al., 2023, Olagaray and Bradford, 2019, Kalantar, 2018), the species and physiological stage of the animal, the period and dose of flavonoid supplementation, the type of flavonoid and the amount of concentrate included in the diet are factors related to the variability of the effects of flavonoids in ruminants.

While traditional literature reviews lack methodological rigor (Tawfik et al., 2019), meta-analyses are highly reliable because they use rigorous statistical procedures to systematically combine and synthesize data from several scientific articles (Paul and Barari, 2022). Meta-analyses have been used to evaluate the effects of dietary supplementation with flavonoids in broiler chickens (Prihambodo et al., 2021), laying hens (Prihambodo et al., 2022), and beef and dairy cattle (Orzuna-Orzuna et al., 2023). However, based on the reviewed background, meta-analytic statistical procedures have not been used to evaluate the effects of flavonoid inclusion in small ruminant diets. The present study's hypothesis states that dietary supplementation with flavonoids will positively impact growth performance, antioxidant status, nutrient digestibility, ruminal parameters, and meat quality of small ruminants. Therefore, this study aimed to evaluate the effects of dietary supplementation with flavonoids on growth performance, antioxidant status in blood serum, nutrient digestibility, ruminal fermentation, and meat quality of small ruminants through meta-analytical statistical procedures.

Section snippets

Literature search

The PICO (Population, Intervention, Comparison, and Outcome) format described by several authors (Nishikawa-Pacher, 2022, Santos et al., 2007) was used to formulate the research question in the current meta-analysis. The population (P) was small ruminants (growing sheep and goats), the intervention (I) was dietary supplementation with flavonoids, the comparison (C) was between diets supplemented with flavonoids and diets without flavonoids, and the outcome (O) was each of the treatment means

Growth performance and carcass traits

Dietary supplementation with flavonoids increased (P < 0.05) DMI, ADG, HCW, HCY, LDMA, and BFT (Table 2). In contrast, FCR decreased (P < 0.05) in response to dietary flavonoid supplementation. Furthermore, CCW was not affected (P > 0.05) by the dietary inclusion of flavonoids.

Antioxidant status in blood serum

Dietary supplementation with flavonoids increased (P < 0.001) the serum concentration of SOD, CAT, GSH-Px, and T-AOC (Table 3). In contrast, a lower (P < 0.001) serum MDA concentration was observed in response to dietary

Growth performance

According to several authors (Olagaray and Bradford, 2019, Li et al., 2020), flavonoids have a high potential as feed additives to improve growth performance in ruminants due to their biological properties. In the current study, dietary supplementation with flavonoids increased DMI and ADG and, at the same time, decreased FCR. These results suggest that the inclusion of flavonoids in small ruminant diets could successfully stimulate DMI and improve the growth rate and feed efficiency of the

Conclusion

Dietary supplementation with flavonoids can be used as a nutritional strategy to stimulate feed intake and improve growth rate, feed efficiency, and carcass yield and quality in small ruminants. Likewise, dietary supplementation with flavonoids improves serum antioxidant status, nutrient digestibility, and ruminal fermentation in small ruminants by reducing ruminal ammonia nitrogen concentration and increasing ruminal total volatile fatty acid and acetate concentration. Furthermore, dietary

Ethics approval

Not applicable.

Funding

This research received no external funding.

CRediT authorship contribution statement

Fernando Lucio-Ruíz: Writing – original draft, Visualization, Methodology, Formal analysis, Data curation. José Felipe Orzuna-Orzuna: Writing – review & editing, Supervision, Resources, Methodology, Formal analysis, Data curation, Conceptualization. Lorenzo Danilo Granados-Rivera: Writing – review & editing, Supervision, Resources, Methodology. Juan Eduardo Godina-Rodríguez: Writing – review & editing, Supervision, Resources, Methodology, Formal analysis, Data curation. Pedro Abel

Declaration of Competing Interest

We the authors declare that we have no conflicts of interest.

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