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Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Effects of the citrus flavonoid extract Bioflavex or its pure components on rumen fermentation of intensively reared beef steers

A. R. Seradj A , A. Gimeno B , M. Fondevila B , J. Crespo C , R. Armengol A and J. Balcells A D
+ Author Affiliations
- Author Affiliations

A Departament de Ciencia Animal, ETSEA, Alcalde Rovira Roure 191, 25198 Lleida, Spain.

B Departamento de Producción Animal y Ciencia de los Alimentos, Instituto Agroalimentario de Aragón (IA2), Universidad de Zaragoza-CITA, Miguel Servet 177, 50013 Zaragoza, Spain.

C Interquim S. A. (FerrerHealthTech), Sant Cugat, 08173 Barcelona, Spain.

D Corresponding author. Email: balcells@prodan.udl.cat

Animal Production Science 58(3) 553-560 https://doi.org/10.1071/AN15146
Submitted: 17 March 2015  Accepted: 8 September 2016   Published: 29 November 2016

Abstract

Two experiments were performed to study the effects of the citrus flavonoid extract Bioflavex (BF; Interquim SA, FerrerHealthTech, Sant Cugat, Barcelona, Spain) or its components on the rumen fermentation of a high-concentrate diet. In an in vivo experiment, eight Friesian steers (398 ± 12.2 kg bodyweight) fitted with a rumen cannula were given a basal concentrate (CTR) or a CTR supplemented with BF (450 mg/kg dry matter, DM) in a 2 × 4 crossover design. No differences were observed in performance parameters of BF and CTR steers. Diet BF increased pH values and the molar proportion of propionate and reduced lactate concentration as a result of an increase in the relative abundance of lactate-consuming microorganism Selenomomas ruminantium (P < 0.01) and Megaesphaera elsdenii (P = 0.06). In an in vitro experiment, the effect of BF and its pure flavonoid components added to the incubation medium was studied separately. Bioflavex and its main components naringine, neohesperidine (NH) and poncirine (PC) were added to the incubation medium at 500 µg/g DM, with the unsupplemented substrate also included as a control (CTR). After 12 h of incubation, flavonoid mixture and NH and PC reduced (P < 0.01) the volume of gas produced and the molar proportion of acetate (P < 0.01), and increased that of propionate (P < 0.01). PC reduced the relative quantification of Streptococcus bovis, whereas NH and BF increased the relative quantification of M. elsdenii in relation to CTR (P < 0.01). Bioflavex supplementation in steers in feedlot was effective in preventing a collapse in pH and it enhanced rumen fermentation efficiency through modifying the activity of lactate-consuming bacteria and a greater molar proportion of propionate and a reduction of that of acetate, suggesting its positive role in modulating the activity of rumen microbiota.

Additional keywords: Holstein steers, intensive beef production, in vivo, in vitro, plant secondary metabolites.


References

AOAC (1990) ‘Official methods of analysis.’ 15th edn. (Association of Official Analytical Chemists.: Arlington, VA)

Balcells J, Aris A, Serrano A, Seradj AR, Crespo J, Devant M (2012) Effects of an extract of plant flavonoids (Bioflavex) on rumen fermentation and performance in heifers fed high-concentrate diets. Journal of Animal Science 90, 4975–4984.
Effects of an extract of plant flavonoids (Bioflavex) on rumen fermentation and performance in heifers fed high-concentrate diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisFSjs7o%3D&md5=d8f8468a302153a8b3ff6fc44ab4a240CAS |

Beauchemin KA, Buchanan-Smith JG (1990) Effects of fiber source and method of feeding on chewing activities, digestive function, and productivity of dairy cows. Journal of Dairy Science 73, 749–762.
Effects of fiber source and method of feeding on chewing activities, digestive function, and productivity of dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3lslWqtg%3D%3D&md5=5342d836bf4cfba5f31b3e47643542abCAS |

Beauchemin KA, Yang WZ, Rode LM (2001) Effects of barley grain processing on the site and extent of digestion of beef feedlot finishing diets. Journal of Animal Science 79, 1925–1936.
Effects of barley grain processing on the site and extent of digestion of beef feedlot finishing diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVCjtLg%3D&md5=7953352674248fadff3c321e30615325CAS |

Bevans DW, Beauchemin KA, Schwartzkopf-Genswein KS, McKinnon JJ, McAllister TA (2005) Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle. Journal of Animal Science 83, 1116–1132.
Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslShtLw%3D&md5=1930af429867c4364a3455a8d8583a62CAS |

Broudiscou LP, Lassalas B (2000) Effects of Lavandula officinalis and Equisetum arvense dry extracts and isoquercitrin on the fermentation of diets varying in forage contents by rumen microorganisms in batch culture. Reproduction, Nutrition, Development 40, 431–440.
Effects of Lavandula officinalis and Equisetum arvense dry extracts and isoquercitrin on the fermentation of diets varying in forage contents by rumen microorganisms in batch culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFSiug%3D%3D&md5=fc0c539a6e61798ccf2966bd8cbc6c3fCAS |

Broudiscou LP, Papon Y, Broudiscou AF (2002) Effects of dry plant extracts on feed degradation and the production of rumen microbial biomass in a dual outflow fermenter. Animal Feed Science and Technology 101, 183–189.
Effects of dry plant extracts on feed degradation and the production of rumen microbial biomass in a dual outflow fermenter.Crossref | GoogleScholarGoogle Scholar |

Burrin DG, Britton RA (1986) Response to monensin in cattle during subacute acidosis. Journal of Animal Science 63, 888–893.
Response to monensin in cattle during subacute acidosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlsFajs74%3D&md5=2a9138c0ae2515dc2a688dcb1db34665CAS |

Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132.

Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Doré J, Blaut M (2005) Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Applied and Environmental Microbiology 71, 6077–6085.
Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFajtbnM&md5=9b90c694a0999773637e844cca7ebbfbCAS |

European Communities (2003) Regulation EC No 1831/2003 of the European Parliament and Council of 22 September 2003 on additives for use in animal nutrition. Official Journal of the European Union, L 268, 29–43.

Gibson GR, Beatty ER, Wang X, Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.
Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1emt7g%3D&md5=c5498d705c430436f9119ceb452d2db9CAS |

Gladine C, Rock E, Morand C, Bauchart D, Durand D (2007) Bioavailability and antioxidant capacity of plant extracts rich in polyphenols, given as a single acute dose, in sheep made highly susceptible to lipoperoxidation. British Journal of Nutrition 98, 691–701.
Bioavailability and antioxidant capacity of plant extracts rich in polyphenols, given as a single acute dose, in sheep made highly susceptible to lipoperoxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWhsrvK&md5=12f734dabde1b915d6b33eaf3154f468CAS |

Goad DW, Goad CL, Nagaraja TG (1998) Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers. Journal of Animal Science 76, 234–241.
Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVKgtg%3D%3D&md5=393d85a7a923b4f3de07cddb32554a10CAS |

Jouany JP (1982) Volatile fatty acid and alcohol determination in digestive contents, silage juices, bacterial cultures and anaerobic fermentor contents. Sciences des Aliments 2, 131–144.

Koenig KM, Beauchemin KA, Rode LM (2003) Effect of grain processing and silage on microbial protein synthesis and nutrient digestibility in beef cattle fed barley-based diets. Journal of Animal Science 81, 1057–1067.
Effect of grain processing and silage on microbial protein synthesis and nutrient digestibility in beef cattle fed barley-based diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFCmt74%3D&md5=b2ec43703e0bb521f57288a56f34fac9CAS |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=a2bb0322e83c81548725a72106b83b36CAS |

Maeda H, Fujimoto C, Haruki Y, Maeda T, Kokeguchi S, Petelin M, Arai H, Tanimoto I, Nishimura F, Takashiba S (2003) Quantitative real-time PCR using TaqMan and SYBR green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunology and Medical Microbiology 39, 81–86.
Quantitative real-time PCR using TaqMan and SYBR green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvFWitrg%3D&md5=7fefb6b705233bf08bfb1725db533ec3CAS |

Mould FL, Morgan R, Kliem KE, Krystallidou E (2005) A review and simplification of the in vitro incubation medium. Animal Feed Science and Technology 123–124, 155–172.
A review and simplification of the in vitro incubation medium.Crossref | GoogleScholarGoogle Scholar |

Nagaraja TG, Avery TB, Galitzer SJ, Harmon DL (1985) Effect of ionophore antibiotics on experimentally induced lactic acidosis in cattle. American Journal of Veterinary Research 46, 2444–2452.

Ouwerkerk D, Klieve AV, Forster RJ (2002) Enumeration of Megasphaera elsdenii in rumen contents by real-time Taq nuclease assay. Journal of Applied Microbiology 92, 753–758.
Enumeration of Megasphaera elsdenii in rumen contents by real-time Taq nuclease assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVKhs70%3D&md5=792b1b21908e49efec3203eb936cde4eCAS |

Owens FN, Secrist DS, Hill WJ, Gill DR (1998) Acidosis in cattle: a review. Journal of Animal Science 76, 275–286.
Acidosis in cattle: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVKnsw%3D%3D&md5=06662ab75f1994647cc016c44fcdffbfCAS |

Patra AK, Saxena J (2009) Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 96, 363–375.
Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12msLrK&md5=ba3fa3644e8426c98bf05588045c90dbCAS |

Rhodes MJC (1996) Physiologically-active compounds in plant foods: an overview. The Proceedings of the Nutrition Society 55, 371–384.
Physiologically-active compounds in plant foods: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvVajtbc%3D&md5=f263a18fbdccbf490939a24bf767e778CAS |

Sauvant D, Meschy F, Mertens D (1999) Les composantes de l’acidose ruminale et les effets acidogènes des rations. Productions Animales 12, 49–60.

Schelling GT (1984) Monensin mode of action in the rumen. Journal of Animal Science 58, 1518–1527.
Monensin mode of action in the rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlsV2rs70%3D&md5=68eaec22e89c93e1bbc5233473a36de0CAS |

Schoefer L, Mohan R, Braune A, Birringer M, Blaut M (2002) Anaerobic C-ring cleavage of genistein and daidzein by Eubacterium ramulus. FEMS Microbiology Letters 208, 197–202.
Anaerobic C-ring cleavage of genistein and daidzein by Eubacterium ramulus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVagsbs%3D&md5=5f3bbc428add7ff548687c76935502f0CAS |

Seradj AR, Abecia L, Crespo J, Villalba D, Fondevila M, Balcells J (2014) The effect of Bioflavex® and its pure flavonoid components on in vitro fermentation parameters and methane production in rumen fluid from steers given high concentrate diets. Animal Feed Science and Technology 197, 85–91.
The effect of Bioflavex® and its pure flavonoid components on in vitro fermentation parameters and methane production in rumen fluid from steers given high concentrate diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFGltb7F&md5=0d4361f322f69134efb3df1d195b4b5cCAS |

Stack RJ, Hungate RE, Opsahl WP (1983) Phenylacetic acid stimulation of cellulose digestion by Ruminococcus albus 8. Applied and Environmental Microbiology 46, 539–544.

Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, Benno Y (2001) Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Applied and Environmental Microbiology 67, 2766–2774.
Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1CitLs%3D&md5=a7b215ba4fae8365db32bfec740b6f01CAS |

Taylor KACC (1996) A simple colorimetric assay for muramic acid and lactic acid. Applied Biochemistry and Biotechnology: Part A: Enzyme Engineering and Biotechnology 56, 49–58.
A simple colorimetric assay for muramic acid and lactic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVGqsr0%3D&md5=beaf7b1c9129b6a6a6b4f05d26dfd2b3CAS |

Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology 48, 185–197.
A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds.Crossref | GoogleScholarGoogle Scholar |

Tzounis X, Vulevic J, Kuhnle GGC, George T, Leonczak J, Gibson GR, Kwik-Uribe C, Spencer JPE (2008) Flavanol monomer-induced changes to the human faecal microflora. British Journal of Nutrition 99, 782–792.
Flavanol monomer-induced changes to the human faecal microflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFegsLg%3D&md5=c46741170c196914641c3aa3d97761e0CAS |

Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnvVCltA%3D%3D&md5=5ac74045d70ec4fdb1b477d24fb39c1dCAS |

Winter J, Moore LH, Dowell VR, Bokkenheuser VD (1989) C-ring cleavage of flavonoids by human intestinal bacteria. Applied and Environmental Microbiology 55, 1203–1208.

Wu VCH, Qiu X, de los Reyes BG, Lin CS, Pan Y (2009) Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157:H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa. Food Microbiology 26, 32–38.
Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157:H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa.Crossref | GoogleScholarGoogle Scholar |