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Dose-Dependent Effects of Dietary Xylooligosaccharides

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Dose-Dependent Effects of Dietary Xylooligosaccharides molecules Article Dose-Dependent Effects of Dietary Xylooligosaccharides Supplementation on Microbiota, Fermentation and Metabolism in Healthy Adult Cats 1, 1, 2 2 1 Yang Lyu y , Sandra Debevere y , Hermann Bourgeois , Mavis Ran , Bart J.G. Broeckx , Lynn Vanhaecke 3, Tom Van de Wiele 4 and Myriam Hesta 2,* 1 Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium; [email protected] (Y.L.); [email protected] (S.D.); [email protected] (B.J.G.B.) 2 Longlive Biotechnology Co. Ltd., Haier Road 63, Qingdao 266103, China; [email protected] (H.B.); [email protected] (M.R.) 3 Lab of Chemical Analysis, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium; [email protected] 4 Center for Microbial Ecology and Technology (CMET), Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium; [email protected] * Correspondence: [email protected]; Tel.: +32(0)92647827 These authors contributed equally to this work. y Academic Editor: Solomon Habtemariam Received: 6 October 2020; Accepted: 27 October 2020; Published: 29 October 2020 Abstract: In order to investigate the effect and appropriate dose of prebiotics, this study evaluated the effect of two levels of xylooligosaccharides (XOS) in cats. Twenty-four healthy adult cats were divided into three groups: no-XOS control diet with 1% cellulose; low XOS supplementation (LXOS) with 0.04% XOS and 0.96% cellulose; and high XOS supplementation (HXOS) with 0.40% XOS and 0.60% cellulose. Both XOS groups increased blood 3-hydroxybutyryl carnitine levels and decreased hexadecanedioyl carnitine levels. Both XOS treatments displayed an increased bacterial abundance of Blautia, Clostridium XI, and Collinsella and a decreased abundance of Megasphaera and Bifidobacterium. LXOS groups increased fecal pH and bacterial abundance of Streptococcus and Lactobacillus, decreased blood glutaryl carnitine concentration, and Catenibacterium abundance. HXOS group showed a more distinct microbiome profile and higher species richness, and an increased bacterial abundance of Subdoligranulum, Ruminococcaceae genus (unassigned genus), Erysipelotrichaceae genus, and Lachnospiraceae. Correlations between bacterial abundances and blood and fecal parameters were also observed. In conclusion, XOS could benefit feline gut health by altering microbiota; its effects dependant on the dose. The higher-dose XOS increased bacterial populations that possibly promoted intestinal fermentation, while the lower dose altered populations of carbohydrate-metabolic microbiota and possibly modulated host metabolism. Low-dose prebiotics may become a trend in future studies. Keywords: xylooligosaccharides (XOS); microbiome; gut health; prebiotics; cats 1. Introduction Fermentation of prebiotics results in the production of short-chain fatty acids (SCFAs; acetate, propionate, and butyrate), which are generally believed to be beneficial for the host [1]. Human studies have demonstrated that prebiotics can potentially prevent a wide variety of conditions such as obesity, allergy, and inflammatory diseases, amongst others [2–4]. Many studies have already investigated different types of prebiotics and have demonstrated a variety of beneficial effects of those, including the improvement of insulin sensitivity in dogs and horses (short-chain fructooligosaccharides) [5,6]; Molecules 2020, 25, 5030; doi:10.3390/molecules25215030 www.mdpi.com/journal/molecules Molecules 2020, 25, x FOR PEER REVIEW 2 of 13 studies have demonstrated that prebiotics can potentially prevent a wide variety of conditions such as obesity, allergy, and inflammatory diseases, amongst others [2–4]. Many studies have already investigated different types of prebiotics and have demonstrated a variety of beneficial effects of Moleculesthose, including2020, 25, 5030 the improvement of insulin sensitivity in dogs and horses (short-chain2 of 14 fructooligosaccharides) [5,6]; the amelioration of the immune response in piglets (mannan theoligosaccharide) amelioration [7]; of theand immunethe better response performance in piglets in poultry (mannan (lactulose) oligosaccharide) [8]. [7]; and the better performanceXylooligosaccharides in poultry (lactulose) (XOS) are [8 ].polymers of the sugar xylose; they are produced from the xylan fractionXylooligosaccharides in plant fiber [9]. (XOS)As a class are polymers of prebiotics, of the XOS sugar has xylose; beenthey demonstrated are produced to exhibit from the a xylangreat fractionnumber inof health plant fiberbenefits [9]. for As humans a class ofand prebiotics, rodents [10], XOS such has as been the demonstratedimprovement of to bowel exhibit function a great numberand mineral of health absorption, benefits the for regulation humans and of intestinal rodents [microbiota,10], such as the reduction improvement in colon of bowel cancer function risk as andwell mineralas the enhancement absorption, the of regulation antioxidant of intestinalcapacity, microbiota,anti-inflammatory the reduction and antimicrobial in colon cancer functions risk as well[11,12]. as theFurthermore, enhancement XOS of antioxidanthas also been capacity, reported anti-inflammatory to be effective in and regulating antimicrobial lipid functionsmetabolism, [11, 12for]. Furthermore,e.g., reducing XOS the hascholesterol also been and reported triglycerides to be eff ectivein diabetic in regulating rats [13,14], lipid wher metabolism,eas Sheu for et e.g., al. noted reducing an theimprovement cholesterol in and blood triglycerides glucose and in diabeticserum lipids rats [ 13in ,pati14],ents whereas with Sheutype 2 et diabetes al. noted mellitus an improvement [15]. Studies in bloodin adult glucose humans and serumshow lipidsthat the in patientseffective with daily type dose 2 diabetes of XOS mellitus is only [15 1.4]. Studiesg/day as in adultcompared humans to showfructooligosaccharides that the effective dailyand galactooligosaccharides, dose of XOS is only 1.4 g /whichday as have compared a minimum to fructooligosaccharides effective dose of 10.0 and galactooligosaccharides,g/day [16–18]. This makes which it possible have a minimumto use lower effective doses dose of prebiotics of 10.0 g/day so that [16– 18side]. This effects makes (e.g., it possibleexcessive to flatus use lower and borborygmi) doses of prebiotics and production so that side costs effects could (e.g., be excessive reduced. flatus Moreover, and borborygmi) its prominent and productionstability to costsacid and could heat be reduced.compared Moreover, to other itsindigestible prominent polysaccharides stability to acid makes and heat it compareda promising to othersupplement indigestible for pet polysaccharides food [19]. makes it a promising supplement for pet food [19]. Despite a short colon and the lack of a functional caecum as evolutionary adaptations to a strictly carnivorous diet, considerable microbial fermentation occurs occurs in in the the hindgut hindgut of of domestic cats cats [20]. [20]. Microbiota of domestic cats have been demonstrateddemonstrated to be capable of fermenting a broad range of dietary fibers, fibers, including including prebiotics prebiotics [21]. [21]. The The majority majority of of the the information information on on the the benefit benefit of offibers fibers or orprebiotics prebiotics is, is,however, however, extrapolated extrapolated from from human human nutrition. nutrition. Dietary Dietary and and metabolic interspeciesinterspecies didifferencesfferences shouldshould bebe considered, asas domestic cats,cats, which are obligate carnivores, rely on high protein (HP)-containing(HP)-containing animal tissues to meet their uniqueunique nutritionalnutritional requirements and are metabolicallymetabolically adapted to lower lower glucose glucose utilization utilization and and higher higher protein protein metabolism metabolism [22,23]. [22,23 In]. order In order to explore to explore the theeffect eff andect andappropriate appropriate dosage dosage of XOS, of XOS, this thisstudy study was wasestablished established to evaluate to evaluate the effects the eff ofects two of XOS two XOSsupplementation supplementation levels levels in cats. in cats.The antioxidant The antioxidant status, status, fermentation fermentation pattern, pattern, metabolic metabolic profile, profile, and andmicrobial microbial composition composition were were sequentially sequentially determined determined in 24 in healthy 24 healthy spayed spayed adult adult cats. cats. 2. Results During thethe trial,trial, body body weight weight and and body body condition condition did did not not diff erdiffer among among the threethe three groups. groups. All diets All werediets wellwere tolerated well tolerated and did and not did markedly not markedly affect affect food intake. food intake. 2.1. Fecal Parameters The eeffectffect of dietary XOS supplementation on fecalfecal parameters (fecal score, pH and fermentation pattern) is summarised in Figure1 1.. ComparedCompared withwith thethe controlcontrol group,group, thethe lowlow XOSXOS supplementationsupplementation (LXOS)(LXOS) groupgroup had had significantly significantly increased increased fecal fecal pH. TherepH. wasThere no was significant no significant effect on fecaleffect parameters on fecal betweenparameters two between periods, two and periods, no diet and x period no diet interaction x period wasinteraction observed. was Dataobserved. without Data significant without disignificantfferences
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