Introduction

Currently, there is a growing demand for rabbit meat, due to the high concentration of high biological value proteins, essential amino acids, and low concentration of saturated fat, cholesterol, purines, and uric acid (Fang et al. 2020Fang, S., Chen, X., Ye, X., Zhou, L., Xue, S. & Gan, Q. 2020. Effects of gut microbiome and short-chain fatty acids (SCFAs) on finishing weight of meat rabbits. Frontiers in Microbiology, 11: 1835, ISSN: 1664-302X. https://doi.org/10.3389/fmicb.2020.01835.). However, these productions are characterized by high production intensity, which causes changes in the intestinal microbiota, microbial dysbiosis, digestive diseases, immunosuppression, and decreased productive efficiency in rabbits. Due to these recurring problems, many producers and enterprises use antibiotic growth promoters in the diet or drinking water, either at critical stages or during the productive life of the animals (Dumont et al. 2020Dumont, B., Puillet, L., Martin, G., Savietto, D., Aubin, J., Ingrand, S. & Thomas, M. 2020. Incorporating diversity into animal production systems can increase their performance and strengthen their resilience. Frontiers in Sustainable Food Systems, 4: 109, ISSN: 2571-581X. https://doi.org/10.3389/fsufs.2020.00109.).

It is known that the European Union and other countries have banned antibiotic growth promoters (Vidovic and Vidovic 2020Vidovic, N. & Vidovic, S. 2020. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics, 9(2): 52, ISSN: 2079-6382. https://doi.org/10.3390/antibiotics9020052.). However, in Latin America, these synthetic products are constantly used in animal production, even though their indiscriminate use promotes antimicrobial resistance of pathogenic strains and causes changes in the ecological balance of the intestinal microbiota, which affects the appearance of gastrointestinal disorders (Glajzner et al. 2023Glajzner, P., Szewczyk, E.M., & Szemraj, M. 2023. Pathogenic potential and antimicrobial resistance of Staphylococcus pseudintermedius isolated from human and animals. Folia microbiologica, 68(2): 231-243, ISSN: 1874-9356. https://doi.org/10.1007/s12223-022-01007-x.). Also, they can leave traces of chemical residues in products of animal origin, which directly affects human health (Treiber and Beranek-Knauer 2021Treiber, F.M. &Beranek-Knauer, H. 2021. Antimicrobial residues in food from animal origin—A review of the literature focusing on products collected in stores and markets worldwide. Antibiotics, 10(5): 534, ISSN: 2079-6382. https://doi.org/10.3390/antibiotics10050534.). Although subtherapeutic antibiotics have been investigated and used more in poultry and pigs than in rabbit breeding, some studies have recommended the oral use of bacitracin Zn to control the population of Enterobacteriaceae and alleviate its implications for animal health (Haj-Ayed and Ben Saïd 2008Haj-Ayed, M. & Ben-Saïd, B. 2008. Effect of Tiamulin or Rescue-kit (R) on diet utilisation, growth and carcass yield of growing rabbits. World Rabbit Science, 16(3): 183-188, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2008.627.).

Nutraceutical additives are bioactive components present in natural products, with beneficial effects on the health of humans and animals (Chandra et al. 2022Chandra, S., Saklani, S., Kumar, P., Kim, B. & Coutinho, H.D. 2022. Nutraceuticals: Pharmacologically active potent dietary supplements. BioMed Research International, 2022(1): 2051017, ISSN: 2314-6141. https://doi.org/10.1155/2022/2051017.). In this sense, nutraceuticals can prevent or treat one or more diseases and improve the physiological performance of the host (Mali et al. 2022Mali, S., Rathod, S., Kale, N. & Shinde, N. 2022. Overview of nutraceuticals. Asian Journal of Pharmaceutical Research, 12(1): 61-70, ISSN: 2231-5691. https://doi.org/10.52711/2231-5691.2022.00010.). Multiple studies show that medicinal plants, probiotics, and prebiotics, as the most studied nutraceuticals, are reliable alternatives to replace the indiscriminate use of antibiotic growth promoters in animals (Haj-Ayed and Ben Saïd 2008Haj-Ayed, M. & Ben-Saïd, B. 2008. Effect of Tiamulin or Rescue-kit (R) on diet utilisation, growth and carcass yield of growing rabbits. World Rabbit Science, 16(3): 183-188, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2008.627.). Scientific research on alternatives to preventive antibiotics focuses on evaluating different biological indicators, with emphasis on growth, reproduction, intestinal health and possible antimicrobial, anti-inflammatory and antioxidant effects (Colitti et al. 2019Colitti, M., Stefanon, B., Gabai, G., Gelain, M.E. & Bonsembiante, F. 2019. Oxidative stress and nutraceuticals in the modulation of the immune function: current knowledge in animals of veterinary interest. Antioxidants, 8(1): 28, ISSN: 2076-3921. https://doi.org/10.3390/antiox8010028.). Furthermore, dietary components have a direct influence on cecal pH and intestinal integrity, and microbiology, affecting host genetic expression (Sun et al. 2016Sun, H., Ni, X., Song, X., Wen, B., Zhou, Y., Zou, F. & Wang, P. 2016. Fermented Yupingfeng polysaccharides enhance immunity by improving the foregut microflora and intestinal barrier in weaning rex rabbits. Applied Microbiology and Biotechnology,100: 8105-8120, ISSN: 1432-0614. https://doi.org/10.1007/s00253-016-7619-0.). Nowadays, new natural additives with diverse biological properties are emerging, which demonstrate their beneficial effects in vivo in rabbits. The aim of this review was to generate updated information on the role of zootechnical additives (mainly phytobiotics, probiotics, and prebiotics) in the main productive and health indicators in different rabbit categories.

New phytobiotics in rabbit breeding

Phytobiotics are characterized by secondary metabolites, synthesized by plants that perform non-essential functions. These compounds intervene in the ecological interactions between plants and their environment. They also differ from primary metabolites in that each of them has a restricted distribution in the plant kingdom, sometimes to a single species or a group of them (El-Sabrout et al. 2023El-Sabrout, K., Khalifah, A. & Ciani, F. 2023. Current applications and trends in rabbit nutraceuticals. Agriculture, 13(7): 1424, ISSN: 2077-0472. https://doi.org/10.3390/agriculture13071424.). The most common secondary metabolites are alkaloids, non-protein amino acids, steroids, phenols, flavonoids, glycosides, coumarins, quinones, tannins, and terpenoids, which have defensive functions against insects, bacteria, fungi, and others.

The highest concentrations of these chemical compounds are found in flowers, leaves, and seeds (Akinpelu 2021Akinpelu, D.A. 2021. Antimicrobial activity of Anacardium occidentale bark. Fitoterapia, 72: 286–287, ISSN: 1873-6971. https://doi.org/10.1016/S0367-326X(00)00310-5.). Some phytochemicals used in small concentrations have bacteriostatic or bactericidal action or inhibit the adhesion of pathogenic bacteria to the intestinal and urinary mucosa. They also have an antioxidant effect by reducing free radical reactive oxygen species (ROS) produced in the organism, as part of normal cell metabolism, as well as anti-inflammatory and immune effects in the presence of pathogenic microorganisms or inflammatory processes (Chouegouong et al. 2021Chouegouong, M.T., Majoumouo, M.S., Menkem, E.Z.O., Yimgang, L.V., Toghueo, R.M.K., Etchu, K.A. & Boyom, F.F. 2021. Ethnopharmacological survey and antibacterial activity of medicinal plant extracts used against bacterial enteritis in rabbits. Advances in Traditional Medicine, 1-11, ISSN: 2662-4060. https://doi.org/10.1007/s13596-021-00615-1.).

Many phytobiotics have been used to promote biological indicators in rabbits and reduce the use of subtherapeutic antibiotics. Recent studies found that the dietary inclusion of 0.6, 0.12, and 0.18 % of thyme (Thymus spp.) essential oil improved productivity, semen quality, and serum testosterone concentration and decreased aspartate transaminase, alanine transaminase, urea, and creatinine compared to a diet without additives and another with oxytetracycline. The authors justified these results to the anti-inflammatory, antioxidant, and antimicrobial activity of this natural product (Abdel-Wareth and Metwally 2020Abdel-Wareth, A.A. & Metwally, A.E. 2020. Productive and physiological response of male rabbits to dietary supplementation with thyme essential oil. Animals, 10(10): 1844, ISSN: 2076-2615. https://doi.org/10.3390/ani10101844.).

Ayala et al. (2011)Ayala, L., Silvana, N., Zocarrato, I. & Gómez, S. 2011. Utilización del orégano vulgar (Origanum vulgare) como fitobiótico en conejos de ceba. Revista Cubana de Ciencia Agrícola, 45(2): 159-161, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193022245011.pdf. reported that carvacrol is the major secondary metabolite in oregano (Origanum vulgare) and that the inclusion of 1 % of this medicinal product dried at 60 ºC improved viability, feed intake, body weight gain, and feed conversion ratio. In another study by Ayala et al. (2012)Ayala, L., Nicola, S., Zoccarato, I., Caro, Y. & Gómez, S. 2012. Salvia spp. como aditivo promotor de crecimiento en dietas de conejos destetados. Revista Unellez de Ciencia y Tecnología, 30: 61-63, ISSN: 1012-7054. http://app.vpa.unellez.edu.ve/revistas/index.php/rucyt/article/view/270/294. it is mentioned that the dietary inclusion of 1 % of two species of sage (S. lavandulifolia and S. officinalis), dried at 60 ºC, promoted body weight, weight gain and viability (especially S. lavandulifolia), due to the high concentration of camphor and α-thujene in these medicinal plants.

Johnson et al. (2022)Johnson, N.C., Ogbamgba, V.M. & Mbachiantim, J.T. 2022. Growth Responses of Weaner Rabbits to Dietary Ginger (Zinger officinale) and Garlic (Allium sativum). European Journal of Science, Innovation and Technology, 2(1): 13-16, ISSN: 2786-4936. https://ejsit-journal.com/index.php/ejsit/article/view/59. confirmed that the inclusion of 1 % garlic (Allium sativum) and ginger (Zingiber officinale) in the diet improves the productive efficiency and carcass yield of fattening rabbits. Also, Liu et al. (2019)Liu, L., Zuo, W. & Li, F. 2019. Dietary addition of Artemisia argyi reduces diarrhea and modulates the gut immune function without affecting growth performances of rabbits after weaning. Journal of Animal Science, 97(4): 1693-1700, ISSN: 1525-3163. https://doi.org/10.1093/jas/skz047. reported that 3 % of Chinese mugwort (Artemisia argyi) in the diet decreased diarrheal syndrome in weaned rabbits and the authors attributed this finding to the increased in immunoglobulin A content and the genetic expression of binding proteins, such as zonula occludin-1 and claudin-1. However, Olorunsogbon et al. (2022)Olorunsogbon, B.F., Sangosina, M.I. & Olorunsogbon, A.M. 2022. Effect of orally administered aqueous extract of ginger and almond fruit extract on haematological and biochemical indices of weaned rabbits. Nigerian Journal of Animal Production, 49(2): 123-129, ISSN: 1596-5570. https://doi.org/10.51791/njap.v49i2.3469. stated that the use of the aqueous extract of ginger (Zingiber officinale) and almond fruit (Terminalia catappa) in drinking water did not change the hematological parameters and blood biochemistry of weaned rabbits.

Other authors reported that aqueous extract of black cumin (Nigella sativa) decreased the growth of Staphylococcus aureus in vitro and in vivo tests. The use of 0.125, 0.25 and 0.50 % of this natural product increased digestive enzymes and genetic expression of binding proteins, such as occludin, claudin-1 (CLDN-1), junctional adhesion molecule-2 (JAM-2) and secretory glycoprotein mucin-2 (MUC2), which provoked a natural growth-promoting effect and decreased the adverse effects of infection with Staphylococcus aureus (Elmowalid et al. 2022Elmowalid, G.A.E., Ahmad, A.A.M., El-Hamid, M.I.A., Ibrahim, D., Wahdan, A., El Oksh, A.S. & Elnahriry, S.S. 2022. Nigella sativa extract potentially inhibited methicillin resistant Staphylococcus aureus induced infection in rabbits: potential immunomodulatory and growth promoting properties. Animals, 12(19): 2635, ISSN: 2076-2615. https://doi.org/10.3390/ani12192635.). Moreover, the dietary inclusion of 0.15 and 0.25 % of cinnamon (Cinnamomum verum) and clove (Syzygium aromaticum) increased body weight, average daily gain, meat quality, and serum concentration of total protein, albumin and globulin in blood plasma and decreased concentration of glucose, cholesterol, triglycerides, aspartate aminotransferase and alanine aminotransferase (Abdel-Azeem and El-Kader 2022Abdel-Azeem, A.A.S. & El-Kader, I.A.A. 2022. Growth performance, carcass attributes, blood hematology and biochemical constituents of growing rabbits supplemented with cinnamon and clove powder. Animal Science Papers & Reports, 40(3), ISSN: 2300-8342. https://www.igbzpan.pl/uploaded/FSiBundleContentBlockBundleModelTranslatableFilesElement/filePath/2207/str351-370.pdf.). Furthermore, Ingweye et al. (2020)Ingweye, J.N., Anaele, O. & Ologbose, F.I. 2020. Response of rabbit bucks to diets containing Aidan (Tetrapleura tetraptera) as feed additive. Animal Research International, 17(2): 3691-3705, ISSN: 1597-3115. https://www.ajol.info/index.php/ari/article/view/199329. found that the inclusion of up to 1 % Aidan pod powder (Tetrapleura tetraptera) in diets without antibiotic growth promoters improved the performance of weaned rabbits, however, higher inclusion of this natural product increased abdominal fat yield in these animals.

Dalle-Zotte et al. (2016)Dalle-Zotte, A., Celia, C. & Szendrő, Z. 2016. Herbs and spices inclusion as feedstuff or additive in growing rabbit diets and as additive in rabbit meat: A review. Livestock Science, 189: 82-90, ISSN: 1878-0490. https://doi.org/10.1016/j.livsci.2016.04.024. mentioned that medicinal plants such as fennel (Foeniculum vulgare), lupin (Lupinus albus L.), fenugreek (Trigonella foenum-graecum L.) and khartoum (Cassia senna L.), rich in lipid-soluble secondary metabolites (essential oils) and in the hydroalcoholic extract, have antimicrobial effects in vivo on Clostridium coccoides and Clostridium leptum in rabbits and anti-inflammatory, immunomodulatory and antioxidant effects, which benefits the antioxidant capacity of meat and meat products. Likewise, the dietary use of 0.17 and 0.34 % daidzein (isoflavones extracted from soybeans) in breeders improved fertility and increased the weight of the young rabbits at birth and at weaning. The cited authors found a direct relationship between the bioactive compound (isoflavones) and the anti-inflammatory, antioxidant and immune response in breeding animals and their offspring (Xie et al. 2022Xie, H., Yu, E., Wen, H., Jiang, B., Fu, G., Sun, H. & He, J. 2022. Effects of dietary daidzein supplementation on reproductive performance, immunity, and antioxidative capacity of New Zealand White does.Animal Feed Science and Technology, 292: 115431, ISSN: 1873-2216. https://doi.org/10.1016/j.anifeedsci.2022.115431. and Xie et al. 2023Xie, H., Yu, E., Wen, H., Jiang, B., Fu, G., Sun, H. & He, J. 2023. Maternal Daidzein Supplementation during Lactation Promotes Growth Performance, Immunity, and Intestinal Health in Neonatal Rabbits.Agriculture, 13(9): 1654, ISSN: 2077-0472. https://doi.org/10.3390/agriculture13091654.). The beneficial effects of medicinal plants, considered phytobiotics, will depend on the type, concentration, and inclusion of secondary metabolites in the diets, in addition to the age, raw materials, productive purpose, and health status of the rabbits.

New probiotics in rabbit breeding

Probiotics are zootechnical additives composed of live microorganisms, which can colonize and modify the intestinal microflora or provoke microbial eubiosis and produce enzymes that help the organic functioning of animals (Mancini and Paci 2021Mancini, S. & Paci, G. 2021. Probiotics in rabbit farming: Growth performance, health status, and meat quality. Animals, 11(12): 3388, ISSN: 2076-2615. https://doi.org/10.3390/ani11123388.). They confer benefits for the health and physiology of the host (FAO/WHO 2006FAO/WHO. 2006. Probiotics in food: Health and nutritional properties and guidelines for evaluation. Roma, Italy: Food and Agriculture Organization of the United Nations, World Health Organization, Rome, Italy.), although it will depend on the type of microbial strain, concentration, and level of inclusion of the probiotic, age, and health status of the host. According to Florido et al. (2017)Florido, G.M., Laurencio, M., Rondón, A.J., Pérez, M., Arteaga, F., Bocourt, R. & Beruvides, A. 2017. Methodology for the isolation, identification and selection of Bacillus spp. strains for the preparation of animal additives. Cuban Journal of Agricultural Science, 51(2): 197-207, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193057228005.pdf., these natural products protect against physiological stress, modulate the intestinal microbiota and the epithelial barrier in the intestine and stimulate the antioxidant capacity and the immune system. However, there are various scientific contradictions about the beneficial effect of some bacterial strains, demonstrated by studies with inconclusive hypotheses, different effects between animal species and productive categories, low tolerance to feed pelleting and chlorine in drinking water. The most used probiotics are Pediococcus pentosaceus, Lactobacillus casei, Enterococcus faecalis, Lactobacillus helveticus, Lactobacillus lactis, Lactobacillus salivarius, Lactobacillus plantarum, Enterococcus faecium and Lactobacillus acidophilus (Krysiak et al. 2021Krysiak, K., Konkol, D. & Korczyński, M. 2021. Overview of the use of probiotics in poultry production. Animals, 11(6), ISSN: 2076-2615. https://doi.org/1620.10.3390/ani11061620.).

Other beneficial bacteria of the Bacillus genus, which are Gram-positive spore-forming bacteria of the Firmicutes division that do not colonize the gastrointestinal tract, are frequently used as probiotics in animal production (Lee et al. 2019Lee, N.K., Kim, W.S. & Paik, H.D. 2019. Bacillus strains as human probiotics: characterization, safety, microbiome, and probiotic carrier. Food Science and Biotechnology, 28: 1297-1305, ISSN: 2092-6456. https://doi.org/10.1007/s10068-019-00691-9.). The most used strains are B. cereus, B. subtilis, B. coagulans, B. polyfermenticus, B. licheniformis, B. pumilus, and B. clausii. These probiotics produce enzymes and vitamins and have antioxidant and microbial properties (Florido et al. 2017Florido, G.M., Laurencio, M., Rondón, A.J., Pérez, M., Arteaga, F., Bocourt, R. & Beruvides, A. 2017. Methodology for the isolation, identification and selection of Bacillus spp. strains for the preparation of animal additives. Cuban Journal of Agricultural Science, 51(2): 197-207, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193057228005.pdf.). Some live yeasts, such as Saccharomyces boulardii and Saccharomyces cerevisiae, can cause microbial eubiosis and improve gut health, also to producing vitamins and enzymes (García-Mazcorro et al. 2020Garcia-Mazcorro, J.F., Ishaq, S.L., Rodriguez-Herrera, M.V., Garcia-Hernandez, C.A., Kawas, J.R. & Nagaraja, T.G. 2020. Are there indigenous Saccharomyces in the digestive tract of livestock animal species? Implications for health, nutrition and productivity traits. Animal, 14(1): 22-30, ISSN: 1751-732X. https://doi.org/10.1017/S1751731119001599.).

Suárez-Machín et al. (2022)Suárez-Machín, C., Mora-Castellanos, L.M., Savón-Valdés, L.L., Carrera-Bocourt, E. & Díaz-de Villegas, M.E. 2022. Caracterización físico-química y microbiológica del Lebame para su uso como probiótico en la alimentación de conejos, en crecimiento-ceba. Revista ICIDCA, 56:1, ISSN: 2410-8529. https://www.revista.icidca.azcuba.cu/wp-content/uploads/2024/02/articulo-3-1.pdf. reported that a probiotic mixture (Bacillus subtilis B/23-45-10 Nato, Lactobacillus bulgaricum B/103-4-1 and Saccharomyces cereviciae L-25-7-12) improved the intestinal health of rabbits by increasing the count of beneficial bacteria in the gastrointestinal tract and the production of volatile fatty acids, which provoked a significant decrease in pH in the small intestine and cecum and, therefore, higher feed efficiency in these animals. Also, Abd El-Hamid et al. (2022)Abd El-Hamid, M.I., Ibrahim, D., Hamed, R.I., Nossieur, H.H., Elbanna, M.H., Baz, H. & Awad, N.F. 2022. Modulatory impacts of multi-strain probiotics on rabbits’ growth, nutrient transporters, tight junctions and immune system to fight against Listeria monocytogenes infection. Animals, 12(16): 2082, ISSN: 2076-2615. https://doi.org/10.3390/ani12162082. informed that a mixture of several bacterial strains increased the productivity, digestibility, genetic expression of binding proteins and viability of rabbits infected with Listeria monocytogenes. These authors concluded that these probiotic bacteria have adjuvant and immune effects. Likewise, oral administration of Aspergillus awamori improved the health status of intoxicated weaned rabbits with ochratoxin, causing an increase in the height and width of intestinal villi and higher protection against liver damage, which benefited the productive efficiency of these animals (El-Deep et al. 2020El-Deep, M.H., Amber, K.A., Elgendy, S., Dawood, M.A., Elwakeel, E.M. & Paray, B.A. 2020. Oxidative stress, hemato-immunological, and intestinal morphometry changes induced by ochratoxin A in APRI rabbits and the protective role of probiotics. Environmental Science and Pollution Research, 27: 35439-35448, ISSN: 0944-1344. https://doi.org/10.1007/s11356-020-09837-3.). The use of lactic acid bacteria and live yeasts can also reduce the serum concentration of harmful lipids, as well as positively modify the immune system and improve the antioxidant capacity of rabbit meat (Adli et al. 2023Adli, D.N., Sjofjan, O., Sholikin, M.M., Hidayat, C., Utama, D.T., Jayanegara, A. & Puspita, P.S. 2023. The effects of lactic acid bacteria and yeast as probiotics on the performance, blood parameters, nutrient digestibility, and carcase quality of rabbits: a meta-analysis. Italian Journal of Animal Science, 22(1): 157-168, ISSN: 1828-051X. https://doi.org/10.1080/1828051X.2023.2172467.).

Abdel-Wareth et al. (2021)Abdel-Wareth, A.A., Elkhateeb, F.S., Ismail, Z.S., Ghazalah, A.A. & Lohakare, J. 2021. Combined effects of fenugreek seeds and probiotics on growth performance, nutrient digestibility, carcass criteria, and serum hormones in growing rabbits. Livestock Science, 251: 104616, ISSN: 1878-0490. https://doi.org/10.1016/j.livsci.2021.104616., using a mixture of probiotics and phytobiotics up to 0.3 % in the diet, found improvements in the digestibility of crude protein, ether extract, and crude fiber. This experimental treatment exacerbated the concentration of testosterone and estrogens in male and female rabbits, respectively, which led to better productive efficiency and higher carcass yield in these animals. Diaz-Fuente et al. (2022)Diaz-Fuentes, K., Jerez-Collazo, L.R., López-Valoy, B. & Benítez-González, H.R. 2022. Efectos de un bioproducto con microorganismos eficientes como aditivo alimentario en conejos en ceba. Revista CIGET, 1(2): 28-38, ISSN: 1027-2127. https://www.redalyc.org/journal/1813/181373019011/html/. reported that the use of a probiotic bioproduct based on efficient microorganisms, at doses of 10 and 15 mL per liter of drinking water for 70 d, increased body weight and weight gain by 6.98 and 4.34 % compared to the control treatment, respectively.

Nwachukwu et al. (2021)Nwachukwu, C.U., Aliyu, K.I. & Ewuola, E.O. 2021. Growth indices, intestinal histomorphology, and blood profile of rabbits fed probiotics-and prebiotics-supplemented diets. Translational Animal Science, 5(3): txab096, ISSN: 2573-2102. https://doi.org/10.1093/tas/txab096. found that a probiotic mixture (Lactobacillus acidophilus) and prebiotic) mixture of fructooligosaccharides) promoted growth, nutrient digestibility, villus height, nutrient absorption, and immunoglobulin production in growing rabbits.

Another study recommended oral administration of a mixture of Lactobacillus rhamnosus GG, Bifidobacterium animalis subsp. Lactis BB-12 and Saccharomyces boulardii CNCM I-745 to improve productivity, electrolyte and immunoglobulin concentrations and decrease harmful lipid concentrations (Kadja et al. 2021Kadja, L., Dib, A.L., Lakhdara, N., Bouaziz, A., Espigares, E. & Gagaoua, M. 2021. Influence of three probiotics strains, Lactobacillus rhamnosus GG, Bifidobacterium animalis subsp. lactis BB-12 and Saccharomyces boulardii CNCM I-745 on the biochemical and Haematological profiles and body weight of healthy rabbits. Biology, 10(11): 1194, ISSN: 2079-7737. https://doi.org/10.3390/biology10111194.). Likewise, oral administration of Pediococcus acidilactici CNCM I-4622 improved weight gain and feed efficiency and controlled the physiological triad (respiratory rate, rectal temperature, and heart rate) in heat-stressed rabbits, without affecting the relative weight of viscera, digestive tract, and edible portions (Ayyat et al. 2018Ayyat, M.S., Al-Sagheer, A.A., Abd El-Latif, K.M. & Khalil, B.A. 2018. Organic selenium, probiotics, and prebiotics effects on growth, blood biochemistry, and carcass traits of growing rabbits during summer and winter seasons. Biological Trace Element Research, 186: 162-173, ISSN: 1559-0720. https://doi.org/10.1007/s12011-018-1293-2.). Despite the availability of several studies on rabbits, these are still limited compared to poultry, and pigs. Further research is needed to elucidate the benefits of probiotics in these herbivorous monogastric at different productive stages, ages, and health statuses.

New prebiotics in rabbit breeding

Prebiotics are chemical compounds that selectively stimulate the growth of some beneficial bacteria in the large intestine, mainly Bifidobacteria and Lactobacilli. These bacteria use the prebiotics that mainly reach the colon to produce volatile fatty acids and release minerals, which are absorbed and utilized by the host (Wlazło et al. 2021Wlazło, Ł., Kowalska, D., Bielański, P., Chmielowiec-Korzeniowska, A., Ossowski, M., Łukaszewicz, M. & Nowakowicz-Dębek, B. 2021. Effect of fermented rapeseed meal on the gastrointestinal microbiota and immune status of rabbit (Oryctolagus cuniculus).Animals, 11(3): 716, ISSN: 2076-2615. https://doi.org/10.3390/ani11030716.). The most widely marketed prebiotics are rich in fructo-oligosaccharide, α galacto-oligosaccharide, transgalacto-oligosaccharide, β-glucans, mannan-oligosaccharide and xylo-oligosaccharide. Thus, changes in the intestinal environment, produced by including prebiotics in the diet, can prevent or reduce the incidence of colibacillosis and other diseases (Zhu et al. 2021Zhu, Y.T., Yue, S.M., Li, R.T., Qiu, S.X., Xu, Z.Y., Wu, Y. & Li, Y. 2021. Prebiotics inulin metabolism by lactic acid bacteria from young rabbits.Frontiers in Veterinary Science, 8: 719927, ISSN: 2297-1769. https://doi.org/10.3389/fvets.2021.719927.). Other research has shown that prebiotics have a marked impact on the metabolic activity of the intestinal microbiota (Pogány-Simonová et al. 2020Pogány-Simonová, M., Chrastinová, Ľ. & Lauková, A. 2020. Autochtonous strain Enterococcus faecium EF2019 (CCM7420), its bacteriocin and their beneficial effects in broiler rabbits—A review. Animals, 10(7): 1188, ISSN: 2076-2615. https://doi.org/10.3390/ani10071188.). These natural products stimulate the immune system, regulate glucose levels and lipid metabolism, as well as increase the mineral bioavailability and decrease intestinal inflammatory responses (El-Ashram et al. 2019El-Ashram, S.A., Aboelhadid, S.M., Abdel-Kafy, E.S.M., Hashem, S.A., Mahrous, L.N., Farghly, E.M. & Kamel, A.A. 2019. Prophylactic and therapeutic efficacy of prebiotic supplementation against intestinal coccidiosis in rabbits. Animals, 9(11): 965, ISSN: 2076-2615. https://doi.org/10.3390/ani9110965.). Furthermore, prebiotics modify the antioxidant capacity and intestinal competitive exclusion, which reduces intestinal pH and the population of pathogenic bacteria, directly benefiting animals (Bosscher et al. 2006Bosscher, D., Van Loo, J. & Franck, A. 2006. Inulin and oligofructose as prebiotics in the prevention of intestinal infections and diseases. Nutrition Research Reviews, 19(2): 216-226, ISSN: 1475-2700. https://doi.org/10.1017/S0954422407249686.).

Ayyat et al. (2018)Ayyat, M.S., Al-Sagheer, A.A., Abd El-Latif, K.M. & Khalil, B.A. 2018. Organic selenium, probiotics, and prebiotics effects on growth, blood biochemistry, and carcass traits of growing rabbits during summer and winter seasons. Biological Trace Element Research, 186: 162-173, ISSN: 1559-0720. https://doi.org/10.1007/s12011-018-1293-2. reported that the dietary use of a commercial prebiotic promoted productive efficiency and increased serum concentrations of hemoglobin, total protein, and globulin. This natural product decreased respiratory and heart rates and body temperature in rabbits under heat stress. Likewise, dietary inclusion with 0.1 % mannan-oligosaccharides and arabinoxylan oligosaccharides improved daily weight gain, cecal volatile fatty acid production, and ileal villus height and decreased cecal coliform population in male rabbits (Bosscher et al. 2006Bosscher, D., Van Loo, J. & Franck, A. 2006. Inulin and oligofructose as prebiotics in the prevention of intestinal infections and diseases. Nutrition Research Reviews, 19(2): 216-226, ISSN: 1475-2700. https://doi.org/10.1017/S0954422407249686.). Moreover, the dietary inclusion with 0.5 % Trigonella foenum-graecum seed meal rich in dietary fiber and galactomannan decreased intestinal pH and NH₃-N concentration and increased total cecal volatile fatty acid production (Zemzmi et al. 2020Zemzmi, J., Ródenas, L., Blas, E., Abdouli, H., Najar, T., & Pascual, J.J. 2020. Preliminary evaluation of fenugreek (Trigonella foenum-graecum) seed gum as a potential prebiotic for growing rabbits in Tunisia: effects on in vivo faecal digestibility and in vitro fermentation.World Rabbit Science, 28(3): 113-122, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2020.12994.). Oral administration of fructooligosaccharides improved weight gain and feed conversion ratio, without affecting nutrient digestibility and serum harmful lipids in fattening rabbits (Abo El-Maaty et al. 2019Abo El-Maaty, H., Aziz, H.A., Dorra, T.M., El Moghazy, G.M. & Eid, R.H. 2019. Replacement of dietary yellow corn by wheat bran with or without multi-enzymes or prebiotic supplementation on nutrient digestibility and blood parameters in growing rabbits. Egyptian Journal of Nutrition and Feeds, 22(2): 359-373, ISSN: 1110-6360. https://doi.org/10.21608/ejnf.2019.79430.).

Agaves are plants with a high content of fructans synthesized and stored in the stems and made up of fructose polymers, derived from the sucrose molecule and with glucose as the terminal monomer (Peralta-García et al. 2020Peralta-García, I., González-Muñoz, F., Elena, R.A.M., Sánchez-Flores, A. & López Munguía, A. 2020. Evolution of fructans in aguamiel (Agave sap) during the plant production lifetime. Frontiers in Nutrition, 7: 566950, ISSN: 2296-861X. https://doi.org/10.3389/fnut.2020.566950.). Several investigations (Iser et al. 2016Iser, M., Martínez, Y., Valdivié, M., Chipres, D.S. & Cortés, M.R. 2016. Comportamiento productivo y características de la canal de conejos alimentados con harina de Agave tequilana. REDVET. Revista Electrónica de Veterinaria, 17(10): 1-12, ISSN: 1695-7504. https://www.redalyc.org/pdf/636/63647454008.pdf. and Iser et al. 2019Iser, M., Valdivié, M., Sánchez, D., Rosales, M., Más, D. & Martínez, Y. 2019. Effect of diet supplementation with meal of Agave tequilana stems on hematological indicators and blood biochemistry of fattening rabbits. Cuban Journal of Agricultural Science, 53(4): 403-412, ISSN: 2079-3480. https://cjascience.com/index.php/CJAS/article/view/920.) demonstrated that the dietary inclusion of up to 1.5 % of Agave tequilana stem powder improved productivity and meat quality, with a hypolipidemic effect, although without changes in the blood count of rabbits. Also, the inclusion of this natural product (Agave tequilana) increased the thickness of the muscular and mucosal layers, and the height, width, and number of villi in the duodenum, which provoked a natural non-antibiotic growth-promoting effect (Martínez et al. 2021Martínez, Y., Iser, M., Valdivié, M., Galindo, J. & Sánchez, D. 2021. Supplementation with Agave fourcroydes powder on growth performance, carcass traits, organ weights, gut morphometry, and blood biochemistry in broiler rabbits. Revista Mexicana de Ciencias Pecuarias, 12(3): 756-772, ISSN: 2448-6698. https://doi.org/10.22319/rmcp.v12i3.5892.). Furthermore, the dietary use of 1.5 % Agave fourcroydes stem powder promoted body weight and feed efficiency, although it decreased the serum concentration of glucose, cholesterol, triglycerides, and atherogenic index, without affecting the concentration of urea nitrogen, creatinine, and very low-density lipoproteins and the relative weight of the digestive organs and viscera of fattening rabbits (Martínez et al. 2022Martínez, Y., Iser, M., Valdivié, M., Rosales, M., Albarrán, E., & Sánchez, D. 2022. Dietary supplementation with Agave tequilana (weber var. Blue) stem powder improves the performance and intestinal integrity of broiler rabbits. Animals, 12(9): 1117, ISSN: 2076-2615. https://doi.org/10.3390/ani12091117.).

Dead yeasts and their chemical compounds, mainly β-glucans, mannoproteins, and chitin, have also been used as prebiotics in animal diets (Klassen et al. 2023Klassen, L., Reintjes, G., Li, M., Jin, L., Amundsen, C., Xing, X. & Abbott, D.W. 2023. Fluorescence activated cell sorting and fermentation analysis to study rumen microbiome responses to administered live microbials and yeast cell wall derived prebiotics. Frontiers in Microbiology, 13: 1020250, ISSN: 1664-302X. https://doi.org/10.3389/fmicb.2022.1020250.). The inclusion of 0.12 g of yeast/kg of feed improved weight gain, productive efficiency, viability, loin yield, and intestinal histomorphometry. This natural product reduced harmful lipids (triglycerides and cholesterol) and increased proteins produced by the liver in weaned rabbits (Abd El-Aziz et al. 2021Abd El-Aziz, A.H., Mahrose, K.M., El-Kasrawy, N.I. & Alsenosy, A.E.W.A. 2021. Yeast as growth promoter in two breeds of growing rabbits with special reference to its economic implications. Anais da Academia Brasileira de Ciências, 93: e20190274, ISSN: 1678-2690. https://doi.org/10.1590/0001-3765202120190274.). β-glucans, derived from yeasts with prebiotic function, demonstrated adjuvant effects, due to antioxidant, immunomodulatory, and anti-inflammatory activity in rabbits intoxicated with Pythium insidiosum (Santurio et al. 2020Santurio, J.M., Alves, S.H., Pereira, D.I.B., Vetvicka, V. & Oliveira, C. 2020. Effect of yeast purified β-glucan in experimental treatment of pythiosis in rabbits. International Clinical Pathology Journal, 8: 14-20, ISSN: 2471-0016. https://doi.org/10.15406/icpjl.2020.08.00199.).

A study, where rabbit diets were formulated with yeast cell walls, enzymes, and a mixture of both, showed that all treatments improved growth performance, intestinal health, and nutrient digestibility, without causing changes in meat quality (Khan et al. 2021Khan, K., Aziz, K., Khan, N.A., Khan, S. & Ayasan, T. 2021. Effect of enzyme and yeast-based feed additives on growth, nutrient digestibility, meat quality and intestinal morphology of fattening rabbits. Journal of the Hellenic Veterinary Medical Society, 72(4): 3511-3518, ISSN: 2585-3724. https://doi.org/10.12681/jhvms.29404.). New technologies have recommended the encapsulation of prebiotics to achieve higher resistance to gastric and intestinal digestion. An experiment confirmed that prebiotics and phytobiotics encapsulated in rabbit diets stimulated the population of lactic acid bacteria and yeasts and decreased cecal pathogenic bacteria and proinflammatory and oxidative stress patterns, which promoted phagocytic and lysosomal activity (Hashem et al. 2020Hashem, N.M., El-Desoky, N., Hosny, N.S. & Shehata, M.G. 2020. Gastrointestinal microflora homeostasis, immunity and growth performance of rabbits supplemented with innovative non-encapsulated or encapsulated synbiotic. Proceedings, 73: 5, ISSN: 2504-3900. https://doi.org/10.3390/IECA2020-08894.).

Currently, fungal bioproducts have been recommended to replace preventive antibiotics in animal diets (Morris et al. 2018Morris-Quevedo, H. J., Llauradó-Maury, G., Bermúdez-Savón, R. C., Cos, P., Lebeque-Pérez, Y., Beltrán-Delgado, Y. & Gaime-Perraud, I. 2018. Evaluation of the immunomodulatory activity of bioproducts obtained from the edible-medicinal mushroom Pleurotus ostreatus. Biotecnología Aplicada, 35(3): 3511-3514, ISSN: 1027-2852. https://www.medigraphic.com/pdfs/biotecapl/ba-2018/ba183e.pdf.). Lebeque-Pérez et al. (2022Lebeque-Pérez, Y., Fong-Lores, O., Rodríguez-Leblanch, E., Llauradó-Maury, G. & Serrat-Díaz, M.J. 2022. Evaluación in vivo de la pirogenicidad de bioproductos fúngicos con potencial prebiótico. Revista Información Científica, 101(3), ISSN: 1028-9933. http://scielo.sld.cu/scielo.php?pid=S1028-99332022000300008&script=sci_arttext.) identified high concentrations of β-glucans, mannan-oligosaccharide, crude protein, nucleic acids, and total carbohydrates in two biopreparations, based on Kluyveromyces marxianus and Pleurotus ostreatus. In vivo studies confirmed that the inclusion of 0.5 % of both natural products promoted feed efficiency and viability of rabbits, without causing pyrogenicity, due to the absence of endotoxins in the biopreparation.

Considering that rabbit diets, due to their physiological characteristics, require high fiber content, and that many fibrous feeds have high concentrations of chemical compounds with a prebiotic effect, the use of these additives could apparently be a viable alternative to eliminate antibiotic growth promoters. However, it will depend on the chemical structure and distribution of the prebiotics, as well as on the age, health status, diet, and zootechnical management.

Table 1 summarizes the main effects of phytobiotics, probiotics and prebiotics on rabbit breeding.

Conclusions

New phytobiotics, prebiotics, and probiotics represent effective alternatives to the common use of subtherapeutic antibiotics in rabbit production. These nutraceutical additives can modulate intestinal microflora, permeability, and histomorphometry, as well as antioxidant capacity, immune activity, and the concentration of harmful lipids, which has a positive effect on weight gain, feed conversion ratio, nutrient digestibility, intestinal health, and meat quality. They can also alleviate problems associated with diarrheal syndrome, bacterial infections, and mycotoxin in rabbits.

Introducción

Actualmente, existe una demanda creciente de la carne de conejos, debido a la alta concentración de proteínas de alto valor biológico, aminoácidos esenciales y baja concentración de grasa saturada, colesterol, purinas y ácido úrico (Fang et al. 2020Fang, S., Chen, X., Ye, X., Zhou, L., Xue, S. & Gan, Q. 2020. Effects of gut microbiome and short-chain fatty acids (SCFAs) on finishing weight of meat rabbits. Frontiers in Microbiology, 11: 1835, ISSN: 1664-302X. https://doi.org/10.3389/fmicb.2020.01835.). Sin embargo, estas producciones se caracterizan por la alta intensidad productiva, lo que provoca cambios en la microbiota intestinal, disbiosis microbiana, enfermedades digestivas, inmunosupresión y disminución de la eficiencia productiva en los conejos. Debido a estos problemas recurrentes, muchos productores y empresas utilizan los antibióticos promotores de crecimiento en la dieta o en el agua de bebida, ya sea en la etapas críticas o durante la vida productiva de los animales (Dumont et al. 2020Dumont, B., Puillet, L., Martin, G., Savietto, D., Aubin, J., Ingrand, S. & Thomas, M. 2020. Incorporating diversity into animal production systems can increase their performance and strengthen their resilience. Frontiers in Sustainable Food Systems, 4: 109, ISSN: 2571-581X. https://doi.org/10.3389/fsufs.2020.00109.).

Se sabe que la Unión Europea y otros países prohibieron el uso de los antibióticos promotores de crecimiento (Vidovic y Vidovic 2020Vidovic, N. & Vidovic, S. 2020. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics, 9(2): 52, ISSN: 2079-6382. https://doi.org/10.3390/antibiotics9020052.). No obstante, en Latinoamérica, estos productos sintéticos se utilizan constantemente en la producción animal, a pesar de que su uso indiscriminado promueve la resistencia antimicrobiana de cepas patógenas y provoca cambios en el equilibrio ecológico de la biota intestinal, lo que incide en la aparición de trastornos gastrointestinales (Glajzner et al. 2023Glajzner, P., Szewczyk, E.M., & Szemraj, M. 2023. Pathogenic potential and antimicrobial resistance of Staphylococcus pseudintermedius isolated from human and animals. Folia microbiologica, 68(2): 231-243, ISSN: 1874-9356. https://doi.org/10.1007/s12223-022-01007-x.). Además, pueden dejar trazas de residuos químicos en productos de origen animal, lo que afecta directamente la salud humana (Treiber y Beranek-Knauer 2021Treiber, F.M. &Beranek-Knauer, H. 2021. Antimicrobial residues in food from animal origin—A review of the literature focusing on products collected in stores and markets worldwide. Antibiotics, 10(5): 534, ISSN: 2079-6382. https://doi.org/10.3390/antibiotics10050534.). Aunque los antibióticos subterapéuticos han sido investigados y utilizados más en las aves y en los cerdos que en la producción cunícola, algunos estudios han recomendado el uso oral de la bacitracina Zn para controlar la población de Enterobacteriaceae y paliar sus implicaciones en la salud animal (Haj-Ayed y Ben Saïd 2008Haj-Ayed, M. & Ben-Saïd, B. 2008. Effect of Tiamulin or Rescue-kit (R) on diet utilisation, growth and carcass yield of growing rabbits. World Rabbit Science, 16(3): 183-188, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2008.627.).

Los aditivos nutracéuticos son componentes bioactivos presentes en los productos naturales, con efectos benéficos para la salud de los humanos y los animales (Chandra et al. 2022Chandra, S., Saklani, S., Kumar, P., Kim, B. & Coutinho, H.D. 2022. Nutraceuticals: Pharmacologically active potent dietary supplements. BioMed Research International, 2022(1): 2051017, ISSN: 2314-6141. https://doi.org/10.1155/2022/2051017.). En este sentido, los nutraceúticos pueden prevenir o tratar una o más enfermedades y mejorar el rendimiento fisiológico del hospedero (Mali et al. 2022Mali, S., Rathod, S., Kale, N. & Shinde, N. 2022. Overview of nutraceuticals. Asian Journal of Pharmaceutical Research, 12(1): 61-70, ISSN: 2231-5691. https://doi.org/10.52711/2231-5691.2022.00010.). Múltiples estudios demuestran que las plantas medicinales, probióticos y prebióticos, como los nutracéuticos más estudiados, son alternativas fiables para reemplazar el uso indiscriminado de los antibióticos promotores de crecimiento en los animales (Haj-Ayed y Ben Saïd 2008Haj-Ayed, M. & Ben-Saïd, B. 2008. Effect of Tiamulin or Rescue-kit (R) on diet utilisation, growth and carcass yield of growing rabbits. World Rabbit Science, 16(3): 183-188, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2008.627.). Los trabajos científicos con alternativas a los antibióticos preventivos se centran en evaluar diferentes indicadores biológicos, con énfasis en el crecimiento, reproducción, salud intestinal y posibles efectos antimicrobianos, antiinflamatorios y antioxidantes (Colitti et al. 2019Colitti, M., Stefanon, B., Gabai, G., Gelain, M.E. & Bonsembiante, F. 2019. Oxidative stress and nutraceuticals in the modulation of the immune function: current knowledge in animals of veterinary interest. Antioxidants, 8(1): 28, ISSN: 2076-3921. https://doi.org/10.3390/antiox8010028.). También, los componentes de la dieta tienen influencia directa en el pH cecal y en la integridad y microbiología intestinal, lo que repercute en la expresión genética del hospedero (Sun et al. 2016Sun, H., Ni, X., Song, X., Wen, B., Zhou, Y., Zou, F. & Wang, P. 2016. Fermented Yupingfeng polysaccharides enhance immunity by improving the foregut microflora and intestinal barrier in weaning rex rabbits. Applied Microbiology and Biotechnology,100: 8105-8120, ISSN: 1432-0614. https://doi.org/10.1007/s00253-016-7619-0.). Actualmente, surgen nuevos aditivos naturales con diversas propiedades biológicas, que comprueban in vivo sus efectos benéficos en los conejos. El objetivo de esta revisión fue generar información actualizada de la función de los aditivos zootécnicos (principalmente fitobióticos, probióticos y prebióticos) en los principales indicadores productivos y de salud en diferentes categorías cunícolas.

Nuevos fitobióticos en la producción cunícola

Los fitobióticos están caracterizados por metabolitos secundarios, sintetizados por plantas que cumplen funciones no esenciales. Estos compuestos intervienen en las interacciones ecológicas entre las plantas y su ambiente. También se diferencian de los metabolitos primarios en que cada uno de ellos tiene una distribución restringida en el reino vegetal, a veces a una sola especie o a un grupo de ellas (El-Sabrout et al. 2023El-Sabrout, K., Khalifah, A. & Ciani, F. 2023. Current applications and trends in rabbit nutraceuticals. Agriculture, 13(7): 1424, ISSN: 2077-0472. https://doi.org/10.3390/agriculture13071424.). Los metabolitos secundarios más comunes son alcaloides, aminoácidos no proteicos, esteroides, fenoles, flavonoides, glucósidos, cumarinas, quinonas, taninos y terpenoides, que poseen funciones defensivas contra insectos, bacterias, hongos y otros.

Las concentraciones más altas de estos compuestos químicos se encuentran en flores, hojas y semillas (Akinpelu 2021Akinpelu, D.A. 2021. Antimicrobial activity of Anacardium occidentale bark. Fitoterapia, 72: 286–287, ISSN: 1873-6971. https://doi.org/10.1016/S0367-326X(00)00310-5.). Algunos fitoquímicos utilizados en pequeñas concentraciones tienen acción bacteriostática o bactericida, o inhiben la adhesión de bacterias patógenas a la mucosa intestinal y urinaria. También tienen efecto antioxidante al reducir las especies de oxígeno reactivas a los radicales libres (ROS) que se producen en el organismo, como parte del metabolismo normal de las células, así como efectos antinflamatorios e inmunes ante la presencia de microorganismos patógenos o procesos inflamatorios (Chouegouong et al. 2021Chouegouong, M.T., Majoumouo, M.S., Menkem, E.Z.O., Yimgang, L.V., Toghueo, R.M.K., Etchu, K.A. & Boyom, F.F. 2021. Ethnopharmacological survey and antibacterial activity of medicinal plant extracts used against bacterial enteritis in rabbits. Advances in Traditional Medicine, 1-11, ISSN: 2662-4060. https://doi.org/10.1007/s13596-021-00615-1.).

Muchos fitobióticos se han empleado para promover los indicadores biológicos en los conejos y reducir el uso de los antibióticos subterapéuticos. Estudios recientes encontraron que la inclusión de 0.6, 0.12 y 0.18 % de aceite esencial de tomillo (Thymus spp.) mejoró la productividad, calidad del semen y concentración sérica de testosterona y disminuyó el aspartato transaminasa, alanina transaminasa, urea y creatinina en comparación con una dieta sin aditivos y otra con oxitetraciclina. Los autores justificaron estos resultados a la actividad antinflamatoria, antioxidante y antimicrobiana de este producto natural (Abdel-Wareth y Metwally 2020Abdel-Wareth, A.A. & Metwally, A.E. 2020. Productive and physiological response of male rabbits to dietary supplementation with thyme essential oil. Animals, 10(10): 1844, ISSN: 2076-2615. https://doi.org/10.3390/ani10101844.).

Ayala et al. (2011)Ayala, L., Silvana, N., Zocarrato, I. & Gómez, S. 2011. Utilización del orégano vulgar (Origanum vulgare) como fitobiótico en conejos de ceba. Revista Cubana de Ciencia Agrícola, 45(2): 159-161, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193022245011.pdf. informaron que el carvacrol es el metabolito secundario mayoritario en el orégano (Origanum vulgare) y que la inclusión de 1 % de este producto medicinal seco a 60 ºC mejoró la viabilidad, consumo de alimento, ganancia de peso vivo y la conversión alimentaria. En otro estudio de Ayala et al. (2012)Ayala, L., Nicola, S., Zoccarato, I., Caro, Y. & Gómez, S. 2012. Salvia spp. como aditivo promotor de crecimiento en dietas de conejos destetados. Revista Unellez de Ciencia y Tecnología, 30: 61-63, ISSN: 1012-7054. http://app.vpa.unellez.edu.ve/revistas/index.php/rucyt/article/view/270/294. se hace referencia a que la inclusión dietética de 1 % de dos especies de salvia (S. lavandulifolia y S. officinalis), secadas a 60 ºC promovieron el peso vivo, ganancia de peso y la viabilidad (con mayor énfasis con S. lavandulifolia), debido a la alta concentración de alcanfor y α-tujeno en estas plantas medicinales.

Johnson et al. (2022)Johnson, N.C., Ogbamgba, V.M. & Mbachiantim, J.T. 2022. Growth Responses of Weaner Rabbits to Dietary Ginger (Zinger officinale) and Garlic (Allium sativum). European Journal of Science, Innovation and Technology, 2(1): 13-16, ISSN: 2786-4936. https://ejsit-journal.com/index.php/ejsit/article/view/59. confirmaron que la inclusión de 1 % de ajo (Allium sativum) y jengibre (Zingiber officinale) en la dieta mejora la eficiencia productiva y el rendimiento de la canal de los conejos de ceba. También, Liu et al. (2019)Liu, L., Zuo, W. & Li, F. 2019. Dietary addition of Artemisia argyi reduces diarrhea and modulates the gut immune function without affecting growth performances of rabbits after weaning. Journal of Animal Science, 97(4): 1693-1700, ISSN: 1525-3163. https://doi.org/10.1093/jas/skz047. refirieron que 3 % de artemisa china (Artemisia argyi) en la dieta disminuyó el síndrome diarreico en conejos destetados y atribuyeron este hallazgo al incremento del contenido de inmunoglubulina A y a la expresión genética de las proteínas de unión, como zonula ocludina-1 y claudina-1. Sin embargo, Olorunsogbon et al. (2022)Olorunsogbon, B.F., Sangosina, M.I. & Olorunsogbon, A.M. 2022. Effect of orally administered aqueous extract of ginger and almond fruit extract on haematological and biochemical indices of weaned rabbits. Nigerian Journal of Animal Production, 49(2): 123-129, ISSN: 1596-5570. https://doi.org/10.51791/njap.v49i2.3469. señalaron que la utilización del extracto acuoso de jengibre (Zingiber officinale) y del fruto de almendra (Terminalia catappa) en el agua de bebida no cambió los indicadores hematológicos y la bioquímica sanguínea de los conejos destetados.

Otros autores informaron que el extracto acuoso de comino negro (Nigella sativa) disminuyó el crecimiento de Staphylococcus aureus en las pruebas in vitro e in vivo. La utilización de 0.125, 0.25 y 0.50 % de este producto natural incrementó las enzimas digestivas y la expresión genética de las proteínas de unión, como la ocludina, claudina-1 (CLDN-1), molécula de adhesión de unión-2 (JAM-2) y la glicoproteína secretora mucina-2 (MUC2), lo que provocó acción promotora del crecimiento natural y disminuyó los efectos adversos de la infección con Staphylococcus aureus (Elmowalid et al. 2022Elmowalid, G.A.E., Ahmad, A.A.M., El-Hamid, M.I.A., Ibrahim, D., Wahdan, A., El Oksh, A.S. & Elnahriry, S.S. 2022. Nigella sativa extract potentially inhibited methicillin resistant Staphylococcus aureus induced infection in rabbits: potential immunomodulatory and growth promoting properties. Animals, 12(19): 2635, ISSN: 2076-2615. https://doi.org/10.3390/ani12192635.). También, la inclusión de 0.15 y 0.25 % de canela (Cinnamomum verum) y clavo (Syzygium aromaticum) incrementó el peso vivo, la ganancia media diaria y la calidad de la carne y la concentración sérica de proteína total, albúmina y globulina en el plasma sanguíneo y redujo concentración de glucosa, colesterol, triglicéridos, aspartato aminotransferasa y alanina aminotransferasa (Abdel -Azeem y El-Kader 2022Abdel-Azeem, A.A.S. & El-Kader, I.A.A. 2022. Growth performance, carcass attributes, blood hematology and biochemical constituents of growing rabbits supplemented with cinnamon and clove powder. Animal Science Papers & Reports, 40(3), ISSN: 2300-8342. https://www.igbzpan.pl/uploaded/FSiBundleContentBlockBundleModelTranslatableFilesElement/filePath/2207/str351-370.pdf.). Ingweye et al. (2020)Ingweye, J.N., Anaele, O. & Ologbose, F.I. 2020. Response of rabbit bucks to diets containing Aidan (Tetrapleura tetraptera) as feed additive. Animal Research International, 17(2): 3691-3705, ISSN: 1597-3115. https://www.ajol.info/index.php/ari/article/view/199329., al utilizar hasta 1 % de polvo de vaina de aidan (Tetrapleura tetraptera) en dietas sin antibióticos promotores de crecimiento informaron mejoras en el crecimiento de los conejos destetados. Sin embargo, una mayor inclusión de este producto natural incrementó el rendimiento de grasa abdominal en estos animales.

Dalle-Zotte et al. (2016)Dalle-Zotte, A., Celia, C. & Szendrő, Z. 2016. Herbs and spices inclusion as feedstuff or additive in growing rabbit diets and as additive in rabbit meat: A review. Livestock Science, 189: 82-90, ISSN: 1878-0490. https://doi.org/10.1016/j.livsci.2016.04.024. mencionaron que plantas medicinales como hinojo (Foeniculum vulgare), lupino (Lupinus albus L.), fenogreco (Trigonella foenum-graecum L.) y Jartum (Cassia senna L.), ricas en metabolitos secundarios solubles en lípidos (aceites esenciales) y en el extracto hidroalcohólico, tienen efectos antimicrobianos in vivo sobre Clostridium coccoides y Clostridium leptum en conejos y efectos antinflamatorios, inmunomoduladores y antioxidantes, lo que beneficia la capacidad antioxidante de la carne y los productos cárnicos. Asimismo, el uso de daidzeina (isoflavonas), extraído del frijol de soya en las dietas (0.17 y 0.34 %) de las reproductoras, mejoró la fertilidad e incrementó el peso de los gazapos al nacimiento y al destete. Los autores citados encontraron una relación directa entre el compuesto bioactivo (isoflavonas) y la respuesta antinflamatoria, antioxidante e inmunidad en reproductoras y sus descendientes (Xie et al. 2022Xie, H., Yu, E., Wen, H., Jiang, B., Fu, G., Sun, H. & He, J. 2022. Effects of dietary daidzein supplementation on reproductive performance, immunity, and antioxidative capacity of New Zealand White does.Animal Feed Science and Technology, 292: 115431, ISSN: 1873-2216. https://doi.org/10.1016/j.anifeedsci.2022.115431. y Xie et al. 2023Xie, H., Yu, E., Wen, H., Jiang, B., Fu, G., Sun, H. & He, J. 2023. Maternal Daidzein Supplementation during Lactation Promotes Growth Performance, Immunity, and Intestinal Health in Neonatal Rabbits.Agriculture, 13(9): 1654, ISSN: 2077-0472. https://doi.org/10.3390/agriculture13091654.). Los efectos benéficos de las plantas medicinales, consideradas fitobióticas, dependerán del tipo, concentración e inclusión de los metabolitos secundarios en las dietas, además de la edad, materias primas, fin productivo y estado de salud de los conejos.

Nuevos probióticos en la producción cunícola

Los probióticos son aditivos zootécnicos compuestos por microorganismos vivos, que pueden colonizar y modificar la microflora intestinal o provocar eubiosis microbiana y producir enzimas que ayudan al funcionamiento orgánico de los animales (Mancini y Paci 2021Mancini, S. & Paci, G. 2021. Probiotics in rabbit farming: Growth performance, health status, and meat quality. Animals, 11(12): 3388, ISSN: 2076-2615. https://doi.org/10.3390/ani11123388.). Confieren beneficios para la salud y fisiología del huésped (FAO/WHO 2006FAO/WHO. 2006. Probiotics in food: Health and nutritional properties and guidelines for evaluation. Roma, Italy: Food and Agriculture Organization of the United Nations, World Health Organization, Rome, Italy.), aunque dependerá del tipo de cepa microbiana, concentración y nivel de inclusión del probiótico, la edad y el estado de salud del hospedero. Según Florido et al. (2017)Florido, G.M., Laurencio, M., Rondón, A.J., Pérez, M., Arteaga, F., Bocourt, R. & Beruvides, A. 2017. Methodology for the isolation, identification and selection of Bacillus spp. strains for the preparation of animal additives. Cuban Journal of Agricultural Science, 51(2): 197-207, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193057228005.pdf., estos productos naturales protegen del estrés fisiológico, modulan la microbiota intestinal y la barrera epitelial en el intestino y estimulan la capacidad antioxidante y el sistema inmunológico. Sin embargo, existen diversas contradicciones científicas acerca del efecto benéfico de algunas cepas bacterianas, demostradas por estudios con hipótesis inconclusas, efectos diferentes entre especies animales y categorías productivas, baja tolerancia a la peletización del alimento y al cloro en el agua de bebida. Los probióticos más utilizados son Pediococcus pentosaceus, Lactobacillus casei, Enterococcus faecalis, Lactobacillus helveticus, Lactobacillus lactis, Lactobacillus salivarius, Lactobacillus plantarum, Enterococcus faecium y Lactobacillus acidophilus (Krysiak et al. 2021Krysiak, K., Konkol, D. & Korczyński, M. 2021. Overview of the use of probiotics in poultry production. Animals, 11(6), ISSN: 2076-2615. https://doi.org/1620.10.3390/ani11061620.).

Otras bacterias benéficas del género Bacillus, que son Gram positivas esporuladas de la división Firmicutes, que no colonizan el tracto gastrointestinal, se usan con frecuencia como probiótico en la producción animal (Lee et al. 2019Lee, N.K., Kim, W.S. & Paik, H.D. 2019. Bacillus strains as human probiotics: characterization, safety, microbiome, and probiotic carrier. Food Science and Biotechnology, 28: 1297-1305, ISSN: 2092-6456. https://doi.org/10.1007/s10068-019-00691-9.). Las cepas más utilizadas son, B. cereus, B. subtilis, B. coagulans, B. polyfermenticus, B. licheniformis, B. pumilus y B. clausii. Estos probióticos producen enzimas y vitaminas y tienen propiedades antioxidantes y microbianas (Florido et al. 2017Florido, G.M., Laurencio, M., Rondón, A.J., Pérez, M., Arteaga, F., Bocourt, R. & Beruvides, A. 2017. Methodology for the isolation, identification and selection of Bacillus spp. strains for the preparation of animal additives. Cuban Journal of Agricultural Science, 51(2): 197-207, ISSN: 2079-3480. https://www.redalyc.org/pdf/1930/193057228005.pdf.). Algunas levaduras vivas, como Saccharomyces boulardii y Saccharomyces cerevisiae, pueden provocar eubiosis microbiana y mejorar la salud intestinal, además de producir vitaminas y enzimas (Garcia-Mazcorro et al. 2020Garcia-Mazcorro, J.F., Ishaq, S.L., Rodriguez-Herrera, M.V., Garcia-Hernandez, C.A., Kawas, J.R. & Nagaraja, T.G. 2020. Are there indigenous Saccharomyces in the digestive tract of livestock animal species? Implications for health, nutrition and productivity traits. Animal, 14(1): 22-30, ISSN: 1751-732X. https://doi.org/10.1017/S1751731119001599.).

Suárez-Machín et al. (2022)Suárez-Machín, C., Mora-Castellanos, L.M., Savón-Valdés, L.L., Carrera-Bocourt, E. & Díaz-de Villegas, M.E. 2022. Caracterización físico-química y microbiológica del Lebame para su uso como probiótico en la alimentación de conejos, en crecimiento-ceba. Revista ICIDCA, 56:1, ISSN: 2410-8529. https://www.revista.icidca.azcuba.cu/wp-content/uploads/2024/02/articulo-3-1.pdf. refirieron que una mezcla probiótica (Bacillus subtilis B/23-45-10 Nato, Lactobacillus bulgaricum B/103-4-1 y Saccharomyces cereviciae L-25-7-12) mejoró la salud intestinal de los conejos, al incrementar el conteo de bacterias benéficas en el tracto gastrointestinal y la producción de ácidos grasos volátiles, lo que provocó disminución significativa del pH en el intestino delgado y ciego y, por ende, mayor eficiencia alimentaria en estos animales. También, Abd El-Hamid et al. (2022)Abd El-Hamid, M.I., Ibrahim, D., Hamed, R.I., Nossieur, H.H., Elbanna, M.H., Baz, H. & Awad, N.F. 2022. Modulatory impacts of multi-strain probiotics on rabbits’ growth, nutrient transporters, tight junctions and immune system to fight against Listeria monocytogenes infection. Animals, 12(16): 2082, ISSN: 2076-2615. https://doi.org/10.3390/ani12162082. señalan que una mezcla de varias cepas bacterianas mejoró la productividad, digestibilidad, expresión genética de las proteínas de unión y la viabilidad de los conejos infectados con Listeria monocytogenes. Concluyeron que estas bacterias probióticas tienen efectos coadyuvantes e inmunitarios. El uso oral de Aspergillus awamori aminoró el estado de salud de conejos destetados, intoxicados con ocratoxina, además, aumentó la altura y ancho de las vellosidades intestinales y disminuyó el daño hepático, lo que benefició la eficiencia productiva de estos animales (El-Deep et al. 2020El-Deep, M.H., Amber, K.A., Elgendy, S., Dawood, M.A., Elwakeel, E.M. & Paray, B.A. 2020. Oxidative stress, hemato-immunological, and intestinal morphometry changes induced by ochratoxin A in APRI rabbits and the protective role of probiotics. Environmental Science and Pollution Research, 27: 35439-35448, ISSN: 0944-1344. https://doi.org/10.1007/s11356-020-09837-3.). La utilización de las bacterias ácido-lácticas y las levaduras vivas también puede disminuir la concentración sérica de lípidos perjudiciales, así como modificar positivamente el sistema inmune y mejorar la capacidad antioxidante de la carne de conejos (Adli et al. 2023Adli, D.N., Sjofjan, O., Sholikin, M.M., Hidayat, C., Utama, D.T., Jayanegara, A. & Puspita, P.S. 2023. The effects of lactic acid bacteria and yeast as probiotics on the performance, blood parameters, nutrient digestibility, and carcase quality of rabbits: a meta-analysis. Italian Journal of Animal Science, 22(1): 157-168, ISSN: 1828-051X. https://doi.org/10.1080/1828051X.2023.2172467.).

Abdel-Wareth et al. (2021)Abdel-Wareth, A.A., Elkhateeb, F.S., Ismail, Z.S., Ghazalah, A.A. & Lohakare, J. 2021. Combined effects of fenugreek seeds and probiotics on growth performance, nutrient digestibility, carcass criteria, and serum hormones in growing rabbits. Livestock Science, 251: 104616, ISSN: 1878-0490. https://doi.org/10.1016/j.livsci.2021.104616., al utilizar una mezcla de probióticos y fitobióticos hasta 0.3 % en la dieta, encontraron mejoras en la digestibilidad de la proteína bruta, extracto etéreo y fibra bruta. Este tratamiento experimental exacerbó la concentración de testosterona y estrógenos en conejos machos y hembras, respectivamente, lo que provocó mejor eficiencia productiva y mayor rendimiento de la canal en estos animales. Diaz-Fuente et al. (2022)Diaz-Fuentes, K., Jerez-Collazo, L.R., López-Valoy, B. & Benítez-González, H.R. 2022. Efectos de un bioproducto con microorganismos eficientes como aditivo alimentario en conejos en ceba. Revista CIGET, 1(2): 28-38, ISSN: 1027-2127. https://www.redalyc.org/journal/1813/181373019011/html/. informaron que el uso de un bioproducto probiótico basado en microorganismos eficientes, en dosis de 10 y 15 mL por litro de agua de bebida durante 70 d, incrementó el peso vivo y la ganancia de peso en 6.98 y 4.34 % con relación al tratamiento control, respectivamente.

Nwachukwu et al. (2021)Nwachukwu, C.U., Aliyu, K.I. & Ewuola, E.O. 2021. Growth indices, intestinal histomorphology, and blood profile of rabbits fed probiotics-and prebiotics-supplemented diets. Translational Animal Science, 5(3): txab096, ISSN: 2573-2102. https://doi.org/10.1093/tas/txab096. encontraron mejor productividad de los conejos de ceba cuando usaron una mezcla con probióticos (Lactobacillus acidophilus) y prebióticos (mezcla de fructooligosacáridos). Justificaron sus hallazgos en que estos productos naturales incrementaron la digestibilidad de los nutrientes, debido a la mayor altura de las vellosidades, lo que promovió la absorción de nutrientes y la producción de inmunoglobulinas.

En otro estudio se recomendó el uso oral de una mezcla de Lactobacillus rhamnosus GG, Bifidobacterium animalis subsp. Lactis BB-12 y Saccharomyces boulardii CNCM I-745 para mejorar la productividad y disminuir la concentración de los lípidos perjudiciales. Se refirió, también a mayor concentración de electrólitos e inmunoglobulinas (Kadja et al. 2021Kadja, L., Dib, A.L., Lakhdara, N., Bouaziz, A., Espigares, E. & Gagaoua, M. 2021. Influence of three probiotics strains, Lactobacillus rhamnosus GG, Bifidobacterium animalis subsp. lactis BB-12 and Saccharomyces boulardii CNCM I-745 on the biochemical and Haematological profiles and body weight of healthy rabbits. Biology, 10(11): 1194, ISSN: 2079-7737. https://doi.org/10.3390/biology10111194.). Asimismo, la administración oral de Pediococcus acidilactici CNCM I-4622 mejoró la ganancia de peso y la eficiencia alimentaria y controló la triada fisiológica (frecuencia respiratoria, temperatura rectal y frecuencia cardíaca) en conejos con estrés térmico, sin afectar el peso relativo de las vísceras digestivas y porciones comestibles (Ayyat et al. 2018Ayyat, M.S., Al-Sagheer, A.A., Abd El-Latif, K.M. & Khalil, B.A. 2018. Organic selenium, probiotics, and prebiotics effects on growth, blood biochemistry, and carcass traits of growing rabbits during summer and winter seasons. Biological Trace Element Research, 186: 162-173, ISSN: 1559-0720. https://doi.org/10.1007/s12011-018-1293-2.). A pesar de la disponibilidad de varios estudios en conejos, siguen siendo limitados con respecto a aves y cerdos. Son necesarias más investigaciones para dilucidar los beneficios de los probióticos en estos monogástricos herbívoros en diferentes etapas productivas, edad y estado de salud.

Nuevos prebióticos en la producción cunícola

Los prebióticos son compuestos químicos que estimulan selectivamente el crecimiento de algunas bacterias benéficas en el intestino grueso, principalmente Bifidobacterias y Lactobacilos. Estas bacterias utilizan los prebióticos que llegan principalmente al colon para producir ácidos grasos volátiles y liberar minerales, absorbidos y aprovechados por el hospedero (Wlazło et al. 2021Wlazło, Ł., Kowalska, D., Bielański, P., Chmielowiec-Korzeniowska, A., Ossowski, M., Łukaszewicz, M. & Nowakowicz-Dębek, B. 2021. Effect of fermented rapeseed meal on the gastrointestinal microbiota and immune status of rabbit (Oryctolagus cuniculus).Animals, 11(3): 716, ISSN: 2076-2615. https://doi.org/10.3390/ani11030716.). Los prebióticos más comercializados son ricos en fructo-oligosacárido, α galacto-oligosacárido, transgalacto-oligosacárido, β-glucanos, manano-oligosacárido y xilo-oligosacárido. Así, los cambios en el ambiente intestinal, producidos por la inclusión de prebióticos en la dieta, pueden prevenir o reducir la incidencia de colibacilosis y otras enfermedades (Zhu et al. 2021Zhu, Y.T., Yue, S.M., Li, R.T., Qiu, S.X., Xu, Z.Y., Wu, Y. & Li, Y. 2021. Prebiotics inulin metabolism by lactic acid bacteria from young rabbits.Frontiers in Veterinary Science, 8: 719927, ISSN: 2297-1769. https://doi.org/10.3389/fvets.2021.719927.). Otras investigaciones han demostrado que los prebióticos tienen marcada incidencia en la actividad metabólica de la microbiota intestinal (Pogány-Simonová et al. 2020Pogány-Simonová, M., Chrastinová, Ľ. & Lauková, A. 2020. Autochtonous strain Enterococcus faecium EF2019 (CCM7420), its bacteriocin and their beneficial effects in broiler rabbits—A review. Animals, 10(7): 1188, ISSN: 2076-2615. https://doi.org/10.3390/ani10071188.). Estos productos naturales estimulan el sistema inmune, regulan los niveles de glucosa y el metabolismo lipídico e incrementan la biodisponibilidad de minerales y disminuyen las respuestas inflamatorias intestinales (El-Ashram et al. 2019El-Ashram, S.A., Aboelhadid, S.M., Abdel-Kafy, E.S.M., Hashem, S.A., Mahrous, L.N., Farghly, E.M. & Kamel, A.A. 2019. Prophylactic and therapeutic efficacy of prebiotic supplementation against intestinal coccidiosis in rabbits. Animals, 9(11): 965, ISSN: 2076-2615. https://doi.org/10.3390/ani9110965.). Asimismo, los prebióticos modifican la capacidad antioxidante y la exclusión competitiva intestinal, lo que reduce el pH intestinal y la población de las bacterias patógenas y benefician directamente a los animales (Bosscher et al. 2006Bosscher, D., Van Loo, J. & Franck, A. 2006. Inulin and oligofructose as prebiotics in the prevention of intestinal infections and diseases. Nutrition Research Reviews, 19(2): 216-226, ISSN: 1475-2700. https://doi.org/10.1017/S0954422407249686.).

Ayyat et al. (2018)Ayyat, M.S., Al-Sagheer, A.A., Abd El-Latif, K.M. & Khalil, B.A. 2018. Organic selenium, probiotics, and prebiotics effects on growth, blood biochemistry, and carcass traits of growing rabbits during summer and winter seasons. Biological Trace Element Research, 186: 162-173, ISSN: 1559-0720. https://doi.org/10.1007/s12011-018-1293-2. informaron que el empleo de un prebiótico comercial en la dieta promovió la eficiencia productiva e incrementó la concentración sérica de hemoglobina, proteína total y globulina. Este producto natural redujo la frecuencia respiratoria y cardiaca y la temperatura corporal de conejos bajo estrés térmico. Asimismo, la inclusión dietética de 0.1 % de manano-oligosacáridos y oligosacáridos de arabinoxilanos mejoró la ganancia diaria de peso, la concentración de ácidos grasos volátiles cecales y la altura de las vellosidades ileales y disminuyó la población de los coliformes cecales en conejos machos (Bosscher et al. 2006Bosscher, D., Van Loo, J. & Franck, A. 2006. Inulin and oligofructose as prebiotics in the prevention of intestinal infections and diseases. Nutrition Research Reviews, 19(2): 216-226, ISSN: 1475-2700. https://doi.org/10.1017/S0954422407249686.). También, la inclusión dietética de 0.5 % de la harina semilla de Trigonella foenum-graecum rica en fibra dietética y galactomanano disminuyó el pH intestinal y la concentración de N-NH₃ e incrementó la producción total de ácidos grasos volátiles cecales (Zemzmi et al. 2020Zemzmi, J., Ródenas, L., Blas, E., Abdouli, H., Najar, T., & Pascual, J.J. 2020. Preliminary evaluation of fenugreek (Trigonella foenum-graecum) seed gum as a potential prebiotic for growing rabbits in Tunisia: effects on in vivo faecal digestibility and in vitro fermentation.World Rabbit Science, 28(3): 113-122, ISSN: 1989-8886. https://doi.org/10.4995/wrs.2020.12994.). El uso oral de fructooligosacáridos mejoró la ganancia de peso y el índice de conversión alimentaria, sin afectar la digestibilidad de nutrientes y los lípidos perjudiciales séricos en conejos de engorde (Abo El-Maaty et al. 2019Abo El-Maaty, H., Aziz, H.A., Dorra, T.M., El Moghazy, G.M. & Eid, R.H. 2019. Replacement of dietary yellow corn by wheat bran with or without multi-enzymes or prebiotic supplementation on nutrient digestibility and blood parameters in growing rabbits. Egyptian Journal of Nutrition and Feeds, 22(2): 359-373, ISSN: 1110-6360. https://doi.org/10.21608/ejnf.2019.79430.).

Los agaves son plantas con alto contenido de fructanos sintetizados y almacenados en los tallos y constituidos por polímeros de fructosa, derivados de la molécula de sacarosa y con glucosa como monómero terminal (Peralta-García et al. 2020Peralta-García, I., González-Muñoz, F., Elena, R.A.M., Sánchez-Flores, A. & López Munguía, A. 2020. Evolution of fructans in aguamiel (Agave sap) during the plant production lifetime. Frontiers in Nutrition, 7: 566950, ISSN: 2296-861X. https://doi.org/10.3389/fnut.2020.566950.). Varias investigaciones (Iser et al. 2016Iser, M., Martínez, Y., Valdivié, M., Chipres, D.S. & Cortés, M.R. 2016. Comportamiento productivo y características de la canal de conejos alimentados con harina de Agave tequilana. REDVET. Revista Electrónica de Veterinaria, 17(10): 1-12, ISSN: 1695-7504. https://www.redalyc.org/pdf/636/63647454008.pdf. y Iser et al. 2019Iser, M., Valdivié, M., Sánchez, D., Rosales, M., Más, D. & Martínez, Y. 2019. Effect of diet supplementation with meal of Agave tequilana stems on hematological indicators and blood biochemistry of fattening rabbits. Cuban Journal of Agricultural Science, 53(4): 403-412, ISSN: 2079-3480. https://cjascience.com/index.php/CJAS/article/view/920.) demostraron que la inclusión dietética hasta 1.5 % del polvo de tallo de Agave tequilana mejoró la productividad, las características de la calidad de la carne, con efecto hipolipidémico, aunque sin cambios en el hemograma de los conejos. También la inclusión de este producto natural (Agave tequilana) incrementó el grosor de las capas muscular y mucosa, y la altura, ancho y número de vellosidades en el duodeno, lo que provocó un efecto promotor del crecimiento natural no antibiótico (Martínez et al. 2021Martínez, Y., Iser, M., Valdivié, M., Galindo, J. & Sánchez, D. 2021. Supplementation with Agave fourcroydes powder on growth performance, carcass traits, organ weights, gut morphometry, and blood biochemistry in broiler rabbits. Revista Mexicana de Ciencias Pecuarias, 12(3): 756-772, ISSN: 2448-6698. https://doi.org/10.22319/rmcp.v12i3.5892.). El empleo de 1.5 % del polvo de tallo de Agave fourcroydes promovió el peso vivo, disminuyó la conversión alimentaria y redujo la concentración sérica de glucosa, colesterol, triglicéridos e índice aterogénico, aunque sin cambios para el nitrógeno ureico, creatinina y lipoproteína de muy baja densidad y para el peso relativo de los órganos digestivos y vísceras de conejos de ceba (Martínez et al. 2022Martínez, Y., Iser, M., Valdivié, M., Rosales, M., Albarrán, E., & Sánchez, D. 2022. Dietary supplementation with Agave tequilana (weber var. Blue) stem powder improves the performance and intestinal integrity of broiler rabbits. Animals, 12(9): 1117, ISSN: 2076-2615. https://doi.org/10.3390/ani12091117.).

Las levaduras muertas y sus compuestos químicos, principalmente β-glucanos, manoproteínas y quitina, también se han utilizado como prebióticos en las dietas de los animales (Klassen et al. 2023Klassen, L., Reintjes, G., Li, M., Jin, L., Amundsen, C., Xing, X. & Abbott, D.W. 2023. Fluorescence activated cell sorting and fermentation analysis to study rumen microbiome responses to administered live microbials and yeast cell wall derived prebiotics. Frontiers in Microbiology, 13: 1020250, ISSN: 1664-302X. https://doi.org/10.3389/fmicb.2022.1020250.). La inclusión 0.12 g levadura/kg de ración mejoró la ganancia de peso, eficiencia productiva, viabilidad, rendimiento del lomo y la histomorfometría intestinal. Este producto natural redujo los lípidos perjudiciales (triglicéridos y colesterol) e incrementó las proteínas producidas por el hígado en conejos destetados (Abd El-Aziz et al. 2021Abd El-Aziz, A.H., Mahrose, K.M., El-Kasrawy, N.I. & Alsenosy, A.E.W.A. 2021. Yeast as growth promoter in two breeds of growing rabbits with special reference to its economic implications. Anais da Academia Brasileira de Ciências, 93: e20190274, ISSN: 1678-2690. https://doi.org/10.1590/0001-3765202120190274.). Los β-glucanos, derivados de levaduras con función prebiótica, demostraron efectos coadyuvantes, debido a la actividad antioxidante, inmunomoduladora y antiinflamatoria en conejos intoxicados con Pythium insidiosum (Santurio et al. 2020Santurio, J.M., Alves, S.H., Pereira, D.I.B., Vetvicka, V. & Oliveira, C. 2020. Effect of yeast purified β-glucan in experimental treatment of pythiosis in rabbits. International Clinical Pathology Journal, 8: 14-20, ISSN: 2471-0016. https://doi.org/10.15406/icpjl.2020.08.00199.).

Un estudio, donde se formularon dietas para conejos con pared celular de levaduras, enzimas y mezcla de ambos, dejó ver que todos los tratamientos mejoraron el comportamiento productivo, la salud intestinal y la digestibilidad de los nutrientes, sin provocar cambios en la calidad de la carne (Khan et al. 2021Khan, K., Aziz, K., Khan, N.A., Khan, S. & Ayasan, T. 2021. Effect of enzyme and yeast-based feed additives on growth, nutrient digestibility, meat quality and intestinal morphology of fattening rabbits. Journal of the Hellenic Veterinary Medical Society, 72(4): 3511-3518, ISSN: 2585-3724. https://doi.org/10.12681/jhvms.29404.). Las nuevas tecnologías han recomendado la encapsulación de prebióticos para lograr mayor resistencia ante la digestión gástrica e intestinal. Un experimento confirmó que prebióticos y fitobióticos, encapsulados en las dietas de los conejos, estimularon la población de bacterias ácidos-lácticas y levaduras y disminuyeron las bacterias patógenas cecales y los patrones proinflamatorios y de estrés oxidativo y provocaron mayor actividad fagocítica y lisosomal (Hashem et al. 2020Hashem, N.M., El-Desoky, N., Hosny, N.S. & Shehata, M.G. 2020. Gastrointestinal microflora homeostasis, immunity and growth performance of rabbits supplemented with innovative non-encapsulated or encapsulated synbiotic. Proceedings, 73: 5, ISSN: 2504-3900. https://doi.org/10.3390/IECA2020-08894.).

Actualmente, los bioproductos fúngicos se han recomendado para sustituir a los antibióticos preventivos en la dieta de los animales (Morris et al. 2018Morris-Quevedo, H. J., Llauradó-Maury, G., Bermúdez-Savón, R. C., Cos, P., Lebeque-Pérez, Y., Beltrán-Delgado, Y. & Gaime-Perraud, I. 2018. Evaluation of the immunomodulatory activity of bioproducts obtained from the edible-medicinal mushroom Pleurotus ostreatus. Biotecnología Aplicada, 35(3): 3511-3514, ISSN: 1027-2852. https://www.medigraphic.com/pdfs/biotecapl/ba-2018/ba183e.pdf.). Lebeque-Pérez et al. (2022)Lebeque-Pérez, Y., Fong-Lores, O., Rodríguez-Leblanch, E., Llauradó-Maury, G. & Serrat-Díaz, M.J. 2022. Evaluación in vivo de la pirogenicidad de bioproductos fúngicos con potencial prebiótico. Revista Información Científica, 101(3), ISSN: 1028-9933. http://scielo.sld.cu/scielo.php?pid=S1028-99332022000300008&script=sci_arttext. identificaron alta concentración de β-glucanos, manano-oligosacárido, proteína bruta, ácidos nucleicos y carbohidratos totales en dos biopreparados, basados en Kluyveromyces marxianus y Pleurotus ostreatus. Estudios in vivo confirmaron que la inclusión de 0.5 % de ambos productos naturales promovieron la eficiencia alimentaria y la viabilidad de los conejos, sin provocar pirogenicidad, debido a la ausencia de endotoxinas en el biopreparado.

Al considerar que las dietas de los conejos, por sus particularidades fisiológicas, requieren altos contenidos de fibra, y que muchos alimentos fibrosos poseen altas concentraciones de compuestos químicos con efecto prebiótico, la utilización de estos aditivos, al parecer, podría ser una alternativa viable para eliminar los antibióticos promotores de crecimiento. Sin embargo, dependerá de la estructura química y la distribución de los prebióticos, así como de la edad, estado de salud, dieta y manejo zootécnico.

La tabla 1 resume los principales efectos de los fitobióticos, probióticos y prebióticos en la producción cunícula.

Conclusiones

Los nuevos fitobióticos, prebióticos y probióticos representan alternativas eficaces al uso común de los antibióticos subterapéuticos en la producción cunícola. Estos aditivos nutracéuticos pueden modular la microflora, permeabilidad y la histomorfometría intestinal, así como la capacidad antioxidante, actividad inmune y la concentración de lípidos perjudiciales, lo que tiene un efecto positivo en la ganancia de peso, conversión alimentaria, digestibilidad de los nutrientes, salud intestinal y calidad de la carne. También pueden paliar problemas asociados al síndrome diarreico, infecciones bacterianas e intoxicaciones con micotoxinas en los conejos.