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Effects of different additives on cattle feed intake and performance - a systematic review and meta-analysis

Abstract

In the last few years, there has been a growing interest in the use of natural feed additives in animal feed. These can be used as replacements for antibiotics, to alter rumen fermentation and increase feed efficiency in ruminants. Therefore, the objective of this study is to evaluate the effects of adding different feed additives in the diet of beef and dairy cattle on their performance, dry matter intake (DMI) and feed efficiency, through a systematic review followed by meta-analysis. The systematic review suggested 43 peer-reviewed publications, according to the pre-established criteria. In beef cattle, the ionophore antibiotics reduced the DMI, improved the feed efficiency without interfering in the average daily gain (ADG). Non-ionophore antibiotics and propolis extract increased the ADG. In dairy cattle, the ionophores, yeast-based additives, and enzyme additives increased the feed efficiency, DMI, and daily milk production (MY), respectively. Essential oil supplementation in beef and dairy cattle had no effect on the feed intake and animal performance. The systematic review and meta-analysis allowed us to conclude that different feed additives have different effects on cattle performance, however, our results suggest that there are a few gaps regarding their effects on animal performance.

Key words
Antimicrobials; essential oil; feed efficiency; ionophores; nutrition; ruminants

INTRODUCTION

Ruminant animals play an important role in supplying the current and growing demand for meat and milk consumed by humans (Malmuthuge & Guan 2017MALMUTHUGE N & GUAN LL. 2017. Understanding host-microbial interactions in rumen: searching the best opportunity for microbiota manipulation. J Animal Sci Biotechnol 8: 8.). With approximately 200 species described, ruminants constitute the most important group of large herbivorous terrestrial mammals (Fernández & Vrba 2005FERNÁNDEZ MH & VRBA ES. 2005. A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev 80: 269-302.). The complex microbiota that inhabits the rumen of ruminant animals is responsible for the ability of these animals to convert indigestible vegetable mass into energy and protein for the animal (Jami & Mizrahi 2012JAMI E & MIZRAHI I. 2012. Composition and similarity of bovine rumen microbiota across individual animals. PLoS ONE 7: e33306., Soltis et al. 2023SOLTIS MP, MOOREY SE, EGERT-MCLEAN AM, VOY BH, SHEPHERD EA & MYER PR. 2023. Rumen Biogeographical Regions and Microbiome Variation. Microorganisms 11: 747-758.).

This microbial community can convert the otherwise unusable organic matter into usable protein and energy and provide up to 70% of the animal’s protein and energy needs in the form of microbial protein and volatile organic acids (Abbas et al. 2020ABBAS W, HOWARD JT, PAZ HA, HALES KE, WELLS JE, KUEHN LA, ERICKSON GE, SPANGLER ML & FERNANDO SC. 2020. Influence of host genetics in shaping the rumen bacterial community in beef cattle. Sci Rep 10: 15101., Li et al. 2022LI Z ET AL. 2022. Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates. ISME J 16: 2775-2787.). Therefore, the ruminal microbiota is a potential target for manipulation, to improve the productivity and health of ruminants (Li et al. 2019LI F, LI C, CHEN Y, LIU J, ZHANG C, IRVING B, FITZSIMMONS C, PLASTOW G & GUAN LL. 2019. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome 7: 92.).

Ruminal fermentation manipulation is considered an important tool to improve production efficiency, which is the main objective of the studies on ruminant nutrition. Moreover, the use of feed additives is considered a direct strategy for ruminal fermentation manipulation (Stivari et al. 2014STIVARI TSS, RAINERI C, SARTORELLO GL, GAMEIRO AH & SILVA JBA. 2014. Aditivos enzimáticos na alimentação de ruminantes: estratégia para a produção animal. PUBVET 8: 1283-1415., Clemmons et al. 2019CLEMMONS BA, VOY BH & MYER PR. 2019. Altering the gut microbiome of cattle: Considerations of host-microbiome interactions for persistent microbiome manipulation. Microb Ecol 77: 523-536.). Antibiotics, probiotics, and feed additives disrupt the microbial ecosystem of the rumen, which can provide targeted, immediate, and acute alterations to the rumen microbial profile (Clemmons et al. 2019CLEMMONS BA, VOY BH & MYER PR. 2019. Altering the gut microbiome of cattle: Considerations of host-microbiome interactions for persistent microbiome manipulation. Microb Ecol 77: 523-536.). However, among the potential feed additives used in ruminant nutrition, the most widespread are ionophore antibiotics (El-Waziry et al. 2022EL-WAZIRY AM, BASMAEIL SM, ALHIDARY IA, SULIMAN GM, ABDELRAHMAN MM & AL-GARADI MA. 2022. Ionophores: their effects on ruminal fermentation, animal performance and carcass characteristics and meat quality. Adv Anim Vet Sci 10: 2641-2649.).

In the last few years, there is a growing interest in the use of natural feed additives in animal feed, including probiotics, organic acids, exogenous enzymes, propolis extracts, and secondary plant metabolites, which can be used as replacements for antibiotics, to alter the rumen fermentation and increase feed efficiency in ruminants (Clemmons et al. 2019CLEMMONS BA, VOY BH & MYER PR. 2019. Altering the gut microbiome of cattle: Considerations of host-microbiome interactions for persistent microbiome manipulation. Microb Ecol 77: 523-536., Al-Suwaiegh et al. 2020AL-SUWAIEGH SB, MORSHEDY SA, MANSOUR AT, AHMED MH, ZAHRAN SM, ALNEMR TM & SALLAM SMA. 2020. Effect of an essential oil blend on dairy cow performance during treatment and post-treatment periods. Sustainability 12: 9123.).

Natural feed additives have the ability to modify microbial populations in the rumen or hindgut, change their fermentation pattern, increase the flow of nutrients to the small intestine, and enhance the digestibility of the feed (Clemmons et al. 2019CLEMMONS BA, VOY BH & MYER PR. 2019. Altering the gut microbiome of cattle: Considerations of host-microbiome interactions for persistent microbiome manipulation. Microb Ecol 77: 523-536., Gheller et al. 2020GHELLER LS ET AL. 2020. Effects of organic acid-based products added to total mixed ration on performance and ruminal fermentation of dairy cows. Anim Feed Sci Technol 261: 114406., Oliveira et al. 2023OLIVEIRA LN, PEREIRA MAN, OLIVEIRA CDS, OLIVEIRA CC, SILVA RB, PEREIRA RAN, DEVRIES TJ & PEREIRA MN. 2023. Effect of low dietary concentrations of Acacia mearnsii tannin extract on chewing, ruminal fermentation, digestibility, nitrogen partition, and performance of dairy cows. J Dairy Sci 106: 3203-3216., Meenongyai et al. 2023MEENONGYAI W, RASRI K, RODJAPOT S, DUANGPHAYAP T, KHEJORNSART P, WONGPANIT K, PHONGKAEW P, BASHAR A & ISLAM Z. 2023. Effect of coated cysteamine hydrochloride and probiotics supplemented alone or in combination on feed intake, nutrients digestibility, ruminal fermentation, and blood metabolites of Kamphaeng Saen beef heifers. Trop Anim Health Prod 55: 69-78., Varela et al. 2023VARELA AMG, LIMA JR DM, ARAÚJO TLAC, SOUZA JR JBF, COSTA LLM, PEREIRA MWF, BATISTA NV, MELO VLL & LIMA PO. 2023. The effect of propolis extract on milk production and composition, serum biochemistry, and physiological parameters of heat-stressed dairy cows. Trop Anim Health Prod 55: 244-251.). The supplementation of probiotics can enhance livestock performance through the maintenance of healthy rumen and enhancing breakdown of the fibrous feed in the rumen by improving the uptake of nutrients, thereby resulting in an increased yield of livestock products (Arowolo & He 2018AROWOLO MA & HE J. 2018. Use of probiotics and botanical extracts to improve ruminant production in the tropics: a review. Anim Nutr 4(3): 241-249.). Yeast is a commonly used probiotic in ruminant nutrition and has been proven to be effective in restoring gut microbial balance, especially during digestive disorders (McAllister et al. 2011MCALLISTER TA, BEAUCHEMIN KA, ALAZZEH AY, BAAH J, TEATHER RM & STANFORD K. 2011. Review: the use of direct fed microbials to mitigate pathogens and methane production in cattle. Can J Anim Sci 91: 193e211.).

Therefore, as there is a growing interest in the use of alternative additives in cattle feed, there are a growing number of studies that analyze the effects of these feed additives in the diet of ruminants (Arriola et al. 2011ARRIOLA KG, KIM SC, STAPLES CR & ADESOGAN AT. 2011. Effect of fibrolytic enzyme application to low-and high-concentrate diets on the performance of lactating dairy cattle. J Dairy Sci 94: 832-841., Gómez-Vázquez et al. 2011GÓMEZ-VÁZQUEZ A, MENDOZA GD, ARANDA E, PÉREZ J, HERNÁNDEZ A & PINOS-RODRÍGUEZ JM. 2011. Influence of fibrolytic enzymes on growth performance and digestion in steers grazing stargrass and supplemented with fermented sugarcane. J Appl Anim Res 39: 77-79., Aguiar et al. 2012AGUIAR SC, ZEOULA LM, MOURA LPP, PRADO IND, PAULA EMD & SAMENSARI RB. 2012. Performance, digestibility, microbial production and carcass characteristics of feedlot young bulls fed diets containing propolis. Acta Sci Anim Sci 34: 393-400., Afzalani et al. 2015AFZALANI, ZEIN M, JAMARUN N & MUSNANDAR E. 2015. Effect of increasing doses of essential oil extracted from Berastagi orange (Citrus sinensis L.) peels on performance, rumen fermentation and blood metabolites in fattening Bali cattle. Pak J Nutr 14: 480-486., Jesus et al. 2016JESUS EF, DEL VALLE TA, CALOMENI GD, SILVA TH, TAKIYA CS, VENDRAMINI THA, PAIVA PG, SILVA GG, NETTO AS & RENNÓ FP. 2016. Influence of a blend of functional oils or monensin on nutrient intake and digestibility, ruminal fermentation and milk production of dairy cows. Anim Feed Sci Technol 219: 59-67., Aboagye et al. 2018ABOAGYE IA, OBA M, CASTILLO AR, KOENIG KM, IWAASA AD & BEAUCHEMIN KA. 2018. Effects of hydrolyzable tannin with or without condensed tannin on methane emissions, nitrogen use, and performance of beef cattle fed a high-forage diet. J Anim Sci 96: 5276-5286., Al-Suwaiegh et al. 2020AL-SUWAIEGH SB, MORSHEDY SA, MANSOUR AT, AHMED MH, ZAHRAN SM, ALNEMR TM & SALLAM SMA. 2020. Effect of an essential oil blend on dairy cow performance during treatment and post-treatment periods. Sustainability 12: 9123.). Hence, it is important to evaluate, summarize, and draw conclusions from the information available through systematic reviews and meta-analytic methods.

It is hypothesized that antibiotics as feed additives can positively affect animal performance and that alternative additives to antibiotics are able to efficiently replace them. The objective of the present study is to evaluate the effects of adding different feed additives in the diet of beef and dairy cattle on their performance, dry matter intake (DMI) and feed efficiency, through a systematic review followed by meta-analysis.

Our results revealed that supplementation with ionophore antibiotics reduced DMI in beef cattle, and increased feed efficiency in beef and dairy cattle. Supplementation of beef cattle with non-ionophore antibiotics and propolis extract increased the average daily gain. Supplementation with yeast-based additives increased DMI and supplementation with enzyme additives decreased milk production in dairy cattle.

MATERIALS AND METHODS

Literary identification - systematic review

A systematic review of scientific studies was carried out to identify feed additives, antibiotics, and antibiotic substitutes used in cattle farming, as manipulators of ruminal fermentation and their impact on cattle performance. An electronic search in the Scopus database (https://www.scopus.com) was carried out from August to November 2020. The review was conducted based on the reported items used for systematic reviews and meta-analyses (Prisma) (Moher et al. 2009MOHER D, LIBERATI A, TETZLAFF J & ALTMAN DG. 2009. Prisma Group. Preferred reporting items for systematic reviews and me-ta-analyses: the PRISMA statement. PLoS Medicine 6: e1000097.).

The search query consisted of combining the search terms and keywords, with the boolean operators (AND and OR). The terms that were sought for pursued the following criteria: (a) Terms related to the species or animal group (cattle, bovine, cow, steers, bulls, ruminants); (b) terms related to the evaluated characteristic (performance, “feed efficiency”, “milk production”, “weight gain”) and (c) terms related to the feed component evaluated (additive, “feed additive”). Thus, the combination between keywords and boolean operators used for the search was: cattle OR bovine OR cow OR steers OR bulls OR ruminant AND performance OR “feed efficiency” OR “milk production” OR “weight gain” AND additive OR “feed additive”.

Screening and evaluation of the studies

The selection of scientific studies started with the verification of the presence of at least one keyword of each search criterion in the title, abstract, or keywords of the studies. Studies that met this criterion were selected.

The second step was a screening of the selected studies, according to the following criteria: (1) The studies had to deal with the use of feed additives for ruminal manipulation; (2) the studies had to be published in English; (3) the full text of the studies had to be available; (4) the study should not be a literature review or meta-analysis; (5) the bovines used had to be of productive age, had to have females in lactation or males in growth or finishing, which were not being submitted to any sanitary challenge; (6) the animals should not have received any hormonal implants; (7) the studies had to present data on animal performance and dry matter intake; (8) the study had to have a control treatment group; and (9) the methodology used had to be provided.

Thus, the studies that met all the criteria described above were submitted to the full text review phase.

Data extraction

After reviewing the full text, the following data were extracted from the studies that met all these criteria: The group of feed additives used (ionophore antibiotics, non-ionophore antibiotics, essential oils or their active components, yeasts, tannins, enzymatic additives); the number of animals used (n); the experimental period (days); the age (months); and dry matter intake (DMI, kg/day) and feed efficiency. For studies referring to beef cattle, data on average daily gain (ADG, g/day) were extracted and for studies referring to dairy cows, data on daily milk production (MY, kg/day) were extracted.

Statistical analysis

In the meta-analysis, the Inverse Variance Method and the DerSimonian-Laird methods were used to estimate the variance between the studies (τ2). The mean difference is given by the mean value of the variable for animals supplemented with different types of feed additives minus the mean value of the variable for non-supplemented animals (control). This was used as the measure of effect.

A fixed-effects or random-effects model was used for the meta-analysis, depending on the existence or non-existence of heterogeneity, was checked for significance at 5% of the test applied for the value of the Q statistic. The magnitude of heterogeneity (I2 ) was interpreted as: Close to 0% indicated the absence of heterogeneity between studies, close to 25% indicated low heterogeneity, close to 50% indicated moderate heterogeneity, and close to 75% indicated high heterogeneity between the studies (Higgins et al. 2003HIGGINS JPT, THOMPSON SG, DEEKS JJ & ALTMAN DG. 2003. Measuring inconsistency in meta-analyses. BMJ 327: 557-560., Santos & Cunha 2013SANTOS E & CUNHA M. 2013. Interpretação crítica dos resultados estatísticos de uma meta-análise: estratégias metodológicas. Millenium 44: 85-98.).

The meta-analysis was performed using the meta package (Schwarze 2007, Balduzzi et al. 2019BALDUZZI S, RÜCKER G & SCHWARZER G. 2019. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health 22: 153-160.) of the statistical software R (R Development Core Team 2020R DEVELOPMENT CORE TEAM. 2020. R: a language and environment for statistical computing; R Foundation for Statistical Compu-ting: Vienna, Austria.). Differences were considered significant at P < 0.05 and as trends when 0.05 ≥ P < 0.10.

RESULTS

The systematic search registered 1,770 scientific studies. After screening each title, abstract, and keyword, 325 studies were excluded for not presenting at least one keyword for each search criteria (Figure 1). Of the remaining 1,445 studies, 1,045 were excluded because they did not address the topic of interest (n = 974) or because they were review studies, meta-analysis, or they were not published in English (n = 71) (Figure 1). Of the remaining 400 studies, 357 studies were excluded because the full text was not available (n = 16) or because they did not meet the eligibility criteria (n = 341) (Figure 1). Finally, 43 publications were included in the meta-analysis (Figure 1 and Table I).

Figure 1
PRISMA flow diagram of all the records searched and included in the meta-analysis.
Table I
Summary of the studies included in the meta-analysis.

For studies referring to beef cattle (Table I), meta-analyses were performed on each group of feed additives, for each measure of interest: Average daily gain (ADG), dry matter intake (DMI), and feed efficiency. Likewise, for studies referring to dairy cattle (Table I), the measures of interest were: Daily milk yield (MY), dry matter intake (DMI), and feed efficiency.

In the evaluated studies, the inclusion of ionophore antibiotics in the diet reduced the DMI (MD = - 0.48 kg/day, P = 0.0004), and improved the feed efficiency (MD = 0.01, P = 0.0067) in beef cattle (Table II). When analyzing the studies with the inclusion of non-ionophore antibiotics (MD = 0.07 kg/day, P = 0.0128) and propolis extract (MD = 0.16 kg/day, P = 0.0350) in the diet, it was observed that both groups of feed additives increased the ADG of beef cattle (Table II).

Table II
Performance of beef cattle supplemented with different types of feed additives.

Including ionophore antibiotics in the diet increased (MD = 0.06, P = 0.0079) the feed efficiency in dairy cattle (Table III). Yeast-based additives to the diet of dairy cows increased the DMI (MD = 0.59 kg/day, P = 0.0001) and the inclusion of enzyme additives increased the MY (MD = 0.69 kg/day, P = 0.0408) (Table III).

Table III
Performance of dairy cows supplemented with different types of feed additives.

DISCUSSION

Ionophore or non-ionophore antibiotics, methane (CH4) inhibitors, defaunating agents, and other chemical additives in ruminant diets have been explored to modulate rumen fermentation, enhance salivary secretions, regulate ruminal pH, prevent metabolic disorders, increase growth and milk production, as well as increase intake and feed efficiency (Kholif & Olafadehan 2021KHOLIF AE & OLAFADEHAN OA. 2021. Essential oils and phytogenic feed additives in ruminant diet: chemistry, ruminal microbiota and fermentation, feed utilization and productive performance. Phytochem Rev 20: 1087-1108., Rivera-Chacon et al. 2022RIVERA-CHACON R, CASTILLO-LOPEZ E, RICCI S, PETRI RM, REISINGER N & ZEBELI Q. 2022. Supplementing a phytogenic feed additive modulates the risk of subacute rumen acidosis, rumen fermentation and systemic inflammation in cattle fed acidogenic diets. Animals 12: 1201.). The significant effects of ionophore antibiotics are increased feed efficiency, increased rate of weight gain, and decreased dry matter intake. However, some studies found no increase in weight gain or feed efficiency (Ensley 2020ENSLEY S. 2020. Ionophore use and toxicosis in cattle. Vet Clin Food Anim Pract 36: 641-652.).

Among the studies with the inclusion of ionophore antibiotics in the diet of beef cattle, 75% used sodium monensin (Table I). This ionophore is the most used among those available for use in beef production, in Brazil (Neumann et al. 2016NEUMANN M, UENO RK, HORST EH, KOWALSKI LH, ETO AK, BARCELLOS JOJ & MIZUBUTI IY. 2016. Growth performance and safety of meat from cattle feedlot finished with salinomycin in the diet. Semina: Cienc Agrar 37: 4221-4234.). When the studies with the inclusion of ionophore antibiotics in the diet of dairy cattle were analyzed, it was observed that 78.6% of them used sodium monensin (Table I).

According to Silva et al. (2018)SILVA GG, TAKIYA CS, DEL VALLE TA, JESUS EF, GRIGOLETTO NTS, NAKADONARI B, CORTINHAS CS, ACEDO TS & RENNÓ FP. 2018. Nutrient digestibility, ruminal fermentation, and milk yield in dairy cows fed a blend of essential oils and amylase. J Dairy Sci 101: 9815-9826., monensin is the main ionophore antibiotic used in dairy cow diets, with the objective of improving feed efficiency or decreasing the risk of metabolic disorders, such as, acidosis and ketosis. An increase in feed efficiency was observed with the inclusion of ionophore antibiotics in the diet of dairy cows (Table III).

According to Ensley (2020)ENSLEY S. 2020. Ionophore use and toxicosis in cattle. Vet Clin Food Anim Pract 36: 641-652., the increase in the rate of gain and feed efficiency when ionophores are used is due to changes in the production of volatile organic acids in the rumen. Laidlomycin, monensin, narasin, salinomycin, and lasalocide alter the molar ratio of volatile organic acids produced by the rumen bacteria, increasing the production of propionic acid, and reducing the production of butyric and acetic acids, without changing the total production of volatile organic acids in cattle or altering fermentation (Ensley 2020ENSLEY S. 2020. Ionophore use and toxicosis in cattle. Vet Clin Food Anim Pract 36: 641-652.). In addition, there are reports in the literature that ionophores reduce ruminal methane production, reduce protein digestion. and ammonia utilization by ruminal bacteria, increasing nitrogen retention and absorption (Ensley 2020ENSLEY S. 2020. Ionophore use and toxicosis in cattle. Vet Clin Food Anim Pract 36: 641-652.). Ionophores are also related to the delay of digestive disturbances resulting from abnormal ruminal fermentation, such as ruminal acidosis and ruminal bloat (Azzaz et al. 2015AZZAZ HH, MURAD HA & MORSY TA. 2015. Utility of ionophores for ruminant animals: a review. Asian J Anim Sci 9: 254-265.).

Among the studies used in this meta-analysis that dealt with the inclusion of non-ionophore antibiotics in the diet of beef cattle, 100% used virginiamycin (VM) (Table I). Although it should be carefully interpreted, due to the small number of studies, as the results showed that VM influenced the ADG of animals, however, it did not influence the DMI and feed efficiency (Table II). Most VM treatments used grazing cattle or cattle fed on a large proportion of forage in the diet. In the literature, most studies evaluating VM supplementation were carried out in animals that were confined, receiving diets rich in grains, or supplemented with non-structural carbohydrate sources (Costa et al. 2018COSTA JPR, JESUS RB, OLIVEIRA IM, RESENDE FD, SIQUEIRA GR & MALHEIROS EB. 2018. Does virginiamycin supplementation affect the metabolism and performance of Nellore bulls grazing under low and high gain rates? Anim Sci J 89: 1432-1441.). However, little is known about the effects of VM where pasture is the source of nitrogen and energy (Costa et al. 2018COSTA JPR, JESUS RB, OLIVEIRA IM, RESENDE FD, SIQUEIRA GR & MALHEIROS EB. 2018. Does virginiamycin supplementation affect the metabolism and performance of Nellore bulls grazing under low and high gain rates? Anim Sci J 89: 1432-1441.). According to Neto et al. (2018)NETO JAA, OLIVEIRA IM, MORETTI MH, GONÇALVES PH, ALVES MAP, FERNANDES JJR, RESENDE FD & SIQUEIRA GR. 2018. Determining the optimal dose of virginiamycin for ruminal parameters and performance of Nellore cattle on pasture. Semina: Cienc Agrar 39: 1749-1758., there are no studies evaluating the optimal dose-response to VM in cattle on tropical pastures.

Despite the lack of effect on feed efficiency and DMI, there was an effect on ADG, which could be explained by the production of ammonia and butyrate, as VM did not affect the acetate: propionate ratio produced in the rumen (Neto et al. 2018NETO JAA, OLIVEIRA IM, MORETTI MH, GONÇALVES PH, ALVES MAP, FERNANDES JJR, RESENDE FD & SIQUEIRA GR. 2018. Determining the optimal dose of virginiamycin for ruminal parameters and performance of Nellore cattle on pasture. Semina: Cienc Agrar 39: 1749-1758.). For grazing animals, the increased availability of ammonia nitrogen in the rumen improves the production of microbial enzymes, because ammonia nitrogen is preferentially used by fibrolytic microorganisms as a precursor for amino acid synthesis (Detmann et al. 2014DETMANN E, PAULINO MF, VALADARES FILHO SC & HUHTANEN P. 2014. Nutritional aspects applied to grazing cattle in the tropics: a review based on Brazilian results. Semina: Cienc Agrar 35: 2829-2854.). Butyrate contributes to approximately 70% of the daily metabolizable energy requirements of ruminants and is the main source of energy for the rumen epithelial cells (Li et al. 2012LI RW, WU S, BALDWIN VI RL, LI W & LI C. 2012. Perturbation dynamics of the rumen microbiota in response to exogenous butyrate. PLoS ONE 7: e29392.).

Oliveira et al. (2017)OLIVEIRA VS, NETO JAS, VALENÇA RL & SANTOS ACP. 2017. Estratégias para mitigar a produção de metano entérico. Vet Not 23(1): 39-70. and Lemos et al. (2016)LEMOS BJM, CASTRO FGF, SANTOS LS, MENDONÇA BPC, COUTO VRM & FERNANDES JJR. 2016. Monensin, virginiamycin, and flavomycin in a no-roughage finishing diet fed to zebu cattle. J Anim Sci 94: 4307-4314., also demonstrated that VM has the potential to stabilize ruminal fermentation, because it controls the production of lactate and methane, as VM acts directly on the ruminal microbial species that produce lactate and methane.

There is growing interest in the use of natural feed additives in animal feed, including probiotics (Astuti et al. 2022ASTUTI WD, RIDWAN R, FIDRIYANTO R, ROHMATUSSOLIHAT R, SARI NF, SARWONO KA, FITRI A & WIDYASTUTI Y. 2022. Changes in rumen fermentation and bacterial profiles after administering Lactiplantibacillus plantarum as a probiotic. Vet World 15: 1969-1974., Meenongyai et al. 2023MEENONGYAI W, RASRI K, RODJAPOT S, DUANGPHAYAP T, KHEJORNSART P, WONGPANIT K, PHONGKAEW P, BASHAR A & ISLAM Z. 2023. Effect of coated cysteamine hydrochloride and probiotics supplemented alone or in combination on feed intake, nutrients digestibility, ruminal fermentation, and blood metabolites of Kamphaeng Saen beef heifers. Trop Anim Health Prod 55: 69-78.), organic acids (Gheller et al. 2020GHELLER LS ET AL. 2020. Effects of organic acid-based products added to total mixed ration on performance and ruminal fermentation of dairy cows. Anim Feed Sci Technol 261: 114406.), exogenous enzymes (Bugoni et al. 2023BUGONI M, TAKIYA CS, GRIGOLETTO NTS, VITTORAZZI JÚNIOR PC, NUNES AT, CHESINI RG, SILVA GG, DURMAN T, PETTIGREW JE & RENNÓ FP. 2023. Feeding amylolytic and proteolytic exogenous enzymes: Effects on nutrient digestibility, ruminal fermentation, and performance in dairy cows. J Dairy Sci 106: 3192-3202.), propolis (Varela et al. 2023VARELA AMG, LIMA JR DM, ARAÚJO TLAC, SOUZA JR JBF, COSTA LLM, PEREIRA MWF, BATISTA NV, MELO VLL & LIMA PO. 2023. The effect of propolis extract on milk production and composition, serum biochemistry, and physiological parameters of heat-stressed dairy cows. Trop Anim Health Prod 55: 244-251.), and secondary plant compounds (Al-Suwaiegh et al. 2020AL-SUWAIEGH SB, MORSHEDY SA, MANSOUR AT, AHMED MH, ZAHRAN SM, ALNEMR TM & SALLAM SMA. 2020. Effect of an essential oil blend on dairy cow performance during treatment and post-treatment periods. Sustainability 12: 9123., Oliveira et al. 2023OLIVEIRA LN, PEREIRA MAN, OLIVEIRA CDS, OLIVEIRA CC, SILVA RB, PEREIRA RAN, DEVRIES TJ & PEREIRA MN. 2023. Effect of low dietary concentrations of Acacia mearnsii tannin extract on chewing, ruminal fermentation, digestibility, nitrogen partition, and performance of dairy cows. J Dairy Sci 106: 3203-3216.). These compounds can be used as antibiotic replacements to alter ruminal fermentation and increase feed efficiency in ruminants (Al-Suwaiegh et al. 2020AL-SUWAIEGH SB, MORSHEDY SA, MANSOUR AT, AHMED MH, ZAHRAN SM, ALNEMR TM & SALLAM SMA. 2020. Effect of an essential oil blend on dairy cow performance during treatment and post-treatment periods. Sustainability 12: 9123.). The antibiotic substitutes likely to be found in this systematic review were: propolis, essential oils and their active components, tannins, yeast-based additives, and enzyme additives.

The inclusion of propolis in the diet of beef cattle had a positive effect on the ADG of the animals, however, it did not influence the DMI and feed efficiency (Table II). According to Aguiar et al. (2012)AGUIAR SC, ZEOULA LM, MOURA LPP, PRADO IND, PAULA EMD & SAMENSARI RB. 2012. Performance, digestibility, microbial production and carcass characteristics of feedlot young bulls fed diets containing propolis. Acta Sci Anim Sci 34: 393-400., the inclusion of propolis in the diet of crossbred bulls did not influence P > 0.05) DMI, ADG, and feed conversion (FC). However, Zawadzki et al. (2011)ZAWADZKI F, PRADO IN, MARQUES JA, ZEOULA LM, ROTTA PP, SESTARI BB, VALERO MV & RIVAROLI DC. 2011. Sodium monensin or propolis extract in the diets of feedlot-finished bulls: effects on animal performance and carcass characteristics. J Anim Feed Sci 20: 16-25., when using the same propolis-based product used by Aguiar et al. (2012)AGUIAR SC, ZEOULA LM, MOURA LPP, PRADO IND, PAULA EMD & SAMENSARI RB. 2012. Performance, digestibility, microbial production and carcass characteristics of feedlot young bulls fed diets containing propolis. Acta Sci Anim Sci 34: 393-400., in a higher dosage (0.0054 mg/g), in bulls finished in the feedlot, found higher ADG and better FC (P < 0.05) in animals that received propolis in the diet.

Varela et al. (2023)VARELA AMG, LIMA JR DM, ARAÚJO TLAC, SOUZA JR JBF, COSTA LLM, PEREIRA MWF, BATISTA NV, MELO VLL & LIMA PO. 2023. The effect of propolis extract on milk production and composition, serum biochemistry, and physiological parameters of heat-stressed dairy cows. Trop Anim Health Prod 55: 244-251., found that supplementation with 64 mL/day of propolis extract in dairy cows increased feeding time, milk production, and feed efficiency. and did not influence dry matter intake, crude protein intake, neutral detergent-insoluble fiber intake, milk composition, or blood parameters. Thus, it is possible to assume that the dosage of propolis administered to animals has an influence on the results and needs to contain a sufficient quantity of phenolic compounds, so that there is an effect on the ruminal microbiota, and consequently, on animal performance.

With the wide variation in the bioactive composition of propolis, it is still a challenge to optimize the dosage and obtain consistent results (Soltan & Patra 2020SOLTAN YA & PATRA AK. 2020. Bee propolis as a natural feed additive: bioactive compounds and effects on ruminal fermentation pattern as well as productivity of ruminants. Indian J Anim Health 59: 50-61.). The concentration of propolis and the alcohol content used in the extraction of active substances can also influence the chemical composition of the propolis extract (Cottica et al. 2011COTTICA SM, SAWAYA AC, EBERLIN MN, FRANCO SL, ZEOULA LM & VISENTAINER JV. 2011. Antioxidant activity and composition of propolis obtained by different methods of extraction. J Braz Chem Soc 22: 929-935., Morsy et al. 2021MORSY AS, SOLTAN YA, EL-ZAIATBE HM, ALENCAR SM & ABDALLA AL. 2021. Bee propolis extract as a phytogenic feed additive to enhance diet digestibility, rumen microbial biosynthesis, mitigating methane formation and health status of late pregnant ewes. Anim Feed Sci Technol 273: 114834.).

Both essential oils and tannins, the so-called phytochemicals or secondary plant metabolites, have antimicrobial properties that make them attractive feed additives to alter rumen fermentation and improve dietary utilization and animal performance (Morsy et al. 2018MORSY TA, KHOLIF AE, MATLOUP OH, ELELLA AA, ANELE UY & CATON JS. 2018. Mustard and cumin seeds improve feed utilization, milk production and milk fatty acids of Damascus goats. J Dairy Res 85: 142-151.). It was possible to observe the absence of effects on any of the variables in question, both in beef cattle and dairy cows, with the inclusion of essential oils or their active components in the animals’ diet (Tables II, III). Likewise, no difference was observed in MY and DMI of tannin-fed dairy cattle (Table III).

Oliveira et al. (2023)OLIVEIRA LN, PEREIRA MAN, OLIVEIRA CDS, OLIVEIRA CC, SILVA RB, PEREIRA RAN, DEVRIES TJ & PEREIRA MN. 2023. Effect of low dietary concentrations of Acacia mearnsii tannin extract on chewing, ruminal fermentation, digestibility, nitrogen partition, and performance of dairy cows. J Dairy Sci 106: 3203-3216., demonstrated that supplementation with different doses (0, 0.14, 0.29, or 0.43% of the diet based on DM) of tannin extract in dairy cattle had no effect on DMI, milk production, or composition. However, a linear increase in the molar proportion of butyrate and reduction in the molar proportion of propionate was observed.

Kholif & Olafadehan (2021)KHOLIF AE & OLAFADEHAN OA. 2021. Essential oils and phytogenic feed additives in ruminant diet: chemistry, ruminal microbiota and fermentation, feed utilization and productive performance. Phytochem Rev 20: 1087-1108., point out that many factors determine the effectiveness of phytochemicals (including essential oils and tannins) in altering dietary digestion and ruminal fermentation. Consequently, it can include animal performance, which depends on diet digestion and ruminal fermentation. Among the factors, are the type and concentration of compounds in the plant, the solvent used to extract them, and the dilution and extraction conditions, the dose used, the type of diet, the age of the animals, the physiological state, and the infestation load by worms, among others (Kholif & Olafadehan 2021KHOLIF AE & OLAFADEHAN OA. 2021. Essential oils and phytogenic feed additives in ruminant diet: chemistry, ruminal microbiota and fermentation, feed utilization and productive performance. Phytochem Rev 20: 1087-1108.). The results of in vivo experiments are variable and need further experimentation before practical application in livestock production (Alemneh & Getabalew 2019ALEMNEH T & GETABALEW M. 2019. Strategies to reduce methane emission in ruminants. Int J Ecol Ecosolution 6: 16-22.).

Yeasts are an important source for obtaining products with probiotic activity, whether they are live strains or derived from their cell walls (Elghandour et al. 2020ELGHANDOUR MMY, TAN ZL, ABU HAFSA SH, ADEGBEYE MJ, GREINER R, UGBOGU EA, CEDILLO MONROY J & SALEM AZM. 2020. Saccharomyces cerevisiae as a probiotic feed additive to non and pseudo-ruminant feeding: a review. J Appl Microbiol 128: 658-674., Gunun et al. 2022GUNUN N ET AL. 2022. Effect of dietary supplementation of hydrolyzed yeast on growth performance, digestibility, rumen fermentation, and hematology in growing beef cattle. Animals 12: 2473.). For many years, yeast and live yeast cultures have been used to stabilize rumen fermentation and prevent metabolic disturbances, increase feed intake, nutrient digestibility, lactational performance, and to improve carcass characteristics (Sallam et al. 2019SALLAM SMA, ABDELMALEK MLR, KHOLIF AE, ZAHRAN SM, AHMED MH, ZEWEIL HS, ATTIA MFA, MATLOUP OH & OLAFADEHAN OA. 2019. The effect of Saccharomyces cerevisiae live cells and Aspergillus oryzae fermentation extract on the lactational performance of dairy cows. Anim Biotechnol 31: 491-497., Amin & Mao 2021AMIN AB & MAO S. 2021. Influence of yeast on rumen fermentation, growth performance and quality of products in ruminants: A review. Anim Nutr 7: 31-41.).

It is believed that yeasts stimulate the growth of microorganisms that digest fiber and cellulose, and that use lactate, resulting in increased feed intake and improved animal performance (Amin & Mao 2021AMIN AB & MAO S. 2021. Influence of yeast on rumen fermentation, growth performance and quality of products in ruminants: A review. Anim Nutr 7: 31-41.). It was confirmed that the addition of yeast-based additives to the diet of dairy cows increased DMI, however, no effects were observed on the MY and feed efficiency (Table III). In the literature, there are still many inconsistent results with the use of yeast in ruminant nutrition, and its mechanism of action is not fully understood, which makes it difficult to draw conclusions about its effects (Amin & Mao 2021AMIN AB & MAO S. 2021. Influence of yeast on rumen fermentation, growth performance and quality of products in ruminants: A review. Anim Nutr 7: 31-41.).

According to Meale et al. (2014)MEALE SJ, BEAUCHEMIN KA, HRISTOV AN, CHAVES AV & MCALLISTER TA. 2014. Board-invited review: opportunities and challenges in using exogenous enzymes to improve ruminant production. J Anim Sci 92: 427-442. and Bugoni et al. (2023)BUGONI M, TAKIYA CS, GRIGOLETTO NTS, VITTORAZZI JÚNIOR PC, NUNES AT, CHESINI RG, SILVA GG, DURMAN T, PETTIGREW JE & RENNÓ FP. 2023. Feeding amylolytic and proteolytic exogenous enzymes: Effects on nutrient digestibility, ruminal fermentation, and performance in dairy cows. J Dairy Sci 106: 3192-3202., exogenous enzymes are increasingly considered as a means of improving feed efficiency and milk yield, as they improve fiber and starch digestibility, and apparently have minor effects on ruminal fermentation. However, the production responses obtained are still highly variable. In the present meta-analysis, the inclusion of enzyme additives, enzymes, and yeast fermentation extracts in the diet of dairy cows increased the MY, without modifying the DMI and feed efficiency (Table III).

Although commercial enzyme preparations are commonly referred to as cellulases and xylanases, the activities of secondary enzymes such as amylases, proteases, esterases, and pectinases are invariably present, as these preparations rarely consist of a single pure enzyme (McAllister et al. 2001MCALLISTER TA, HRISTOV AN, BEAUCHEMIN KA, RODE LM & CHENG KJ. 2001. Enzymes in ruminants diets. In: BED-FORD MR & PARTRIDGE GG (Eds), Enzymes in farm animal nutrition. Wiltshire: CAB International.). According to Meale et al. (2014)MEALE SJ, BEAUCHEMIN KA, HRISTOV AN, CHAVES AV & MCALLISTER TA. 2014. Board-invited review: opportunities and challenges in using exogenous enzymes to improve ruminant production. J Anim Sci 92: 427-442., it is virtually impossible to compare exogenous enzyme preparations on an equal activity basis, as there is a clear lack of standardization in the methodology used to assess enzyme activities across laboratories. Even though the same methods are used, it is difficult to standardize enzyme products, as they contain several activities and can only be standardized for one or two activities at a time (Meale et al. 2014MEALE SJ, BEAUCHEMIN KA, HRISTOV AN, CHAVES AV & MCALLISTER TA. 2014. Board-invited review: opportunities and challenges in using exogenous enzymes to improve ruminant production. J Anim Sci 92: 427-442.).

Another common limitation of the enzyme literature is the lack of repeatability of the effects and repeated investigations of a common exogenous enzyme preparation, as most of them are only examined in a single experiment (Meale et al. 2014MEALE SJ, BEAUCHEMIN KA, HRISTOV AN, CHAVES AV & MCALLISTER TA. 2014. Board-invited review: opportunities and challenges in using exogenous enzymes to improve ruminant production. J Anim Sci 92: 427-442., Bugoni et al. 2023BUGONI M, TAKIYA CS, GRIGOLETTO NTS, VITTORAZZI JÚNIOR PC, NUNES AT, CHESINI RG, SILVA GG, DURMAN T, PETTIGREW JE & RENNÓ FP. 2023. Feeding amylolytic and proteolytic exogenous enzymes: Effects on nutrient digestibility, ruminal fermentation, and performance in dairy cows. J Dairy Sci 106: 3192-3202.).

The present systematic review and meta-analysis concluded that supplementation with ionophore antibiotics reduced dry matter intake in beef cattle, and increased feed efficiency in beef and dairy cattle. Supplementation of beef cattle with non-ionophore antibiotics and propolis extract increased the average daily gain. Supplementation with yeast-based additives increased dry matter intake and supplementation with enzyme additives decreased daily milk production in dairy cattle. Benefits of including additives in the diet of cattle reported in the literature range from the prevention of metabolic disorders, improvement in performance, and reduction of enteric methane emissions. However, the results found in the present study suggest that there are still gaps regarding the effects of the supplementation of these additives on animal performance.

ACKNOWLEDGMENTS

This research was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Brasília, Brazil), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brasília, Brazil) and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG; Belo Horizonte, Brazil).

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Publication Dates

  • Publication in this collection
    14 June 2024
  • Date of issue
    2024

History

  • Received
    16 Feb 2023
  • Accepted
    02 Oct 2023
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