Prebiotic effects of yacon (Smallanthus sonchifolius Poepp. & Endl), a source of fructooligosaccharides and phenolic compounds with antioxidant activity

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Prebiotic effects of yacon (Smallanthus sonchifolius Poepp. & Endl), a source of fructooligosaccharides and phenolic compounds with antioxidant activity
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  Prebiotic effects of yacon ( Smallanthus sonchifolius  Poepp. & Endl), a sourceof fructooligosaccharides and phenolic compounds with antioxidant activity David Campos a, ⇑ , Indira Betalleluz-Pallardel a , Rosana Chirinos a , Ana Aguilar-Galvez a , Giuliana Noratto b ,Romina Pedreschi c a Instituto de Biotecnología (IBT), Universidad Nacional Agraria La Molina – UNALM, Av. La Molina s/n, Lima, Peru b Department of Nutrition and Food Science, Texas A&M University, College Station, Texas 77843, United States Institute for Obesity Research and Program Evaluation, Texas A&M  AgriLife Research, College Station, TX 77843, United States c Food & Biobased Research, Wageningen UR. Bornse Weilanden 9, 6708WG, The Netherlands a r t i c l e i n f o  Article history: Received 22 February 2012Received in revised form 25 April 2012Accepted 23 May 2012Available online 30 May 2012 Keywords: Yacon Smallanthus sonchifolius AccessionsPhenolic compoundsAntioxidant activityFructooligosaccharides a b s t r a c t Thirty-fivedifferentyacon( Smallanthus sonchifolius Poepp.&Endl)accessionswereevaluatedaspotentialalternative sources of fructooligosaccharides (FOS) and phenolic type natural antioxidants. FOS, totalphenolics (TPC) and antioxidant capacity (AC) contents in the ranges of 6.4–65g/100g of dry mater(DM), 7.9–30.8mg chlorogenic acid (CAE)/g of DM and 23–136 l mol trolox equivalente (TE)/g DM werefound. Accession AJC 5189 sparked attention for its high FOS content while DPA 07011 for its high TPCand AC. In addition, the prebiotic effect of yacon FOS was tested  in vivo  with a guinea pig model. A dietrich in yacon FOS promoted the growth of bifidobacteria and lactobacilli, resulting in high levels of shortchain fatty acids (SCFAs) in the cecal material and enhancement of cell density and crypt formation incaecum tissue, being indicative of colon health benefits. This study allowed identification of yacon culti-vars rich in FOS, AC and/or FOS and AC for nutraceutical applications.   2012 Elsevier Ltd. All rights reserved. 1. Introduction Yacon ( Smallanthus sonchifolius  Poepp. & Endl), an Andean cropthat grows at altitudes of 1000–3200mabove sea level, is particu-larly known as an abundant source of   b -(2 ? 1) fructooligosaccha-rides (FOS) (Goto, Fukai, Hikida, Nanjo, & Hara, 1995). FOS areconsidered as prebiotics and yacon FOS prebiotic effects have beendemonstrated  in vitro  showing that they were selectively fer-mented by bifidobacteria and lactobacilli (Pedreschi, Campos, Nor-atto, Chirinos, & Cisneros-Zevallos, 2003). In addition, yacon rootsare rich in phenolic compounds, mainly chlorogenic (caffeoyl-qui-nic) acid and other caffeic acid derivatives (Takenaka et al., 2003;Yan et al., 1999).YaconrootshavealonghistoryofsafeuseinSouthAmericaandelsewhere with potential health-promoting properties, includingprebiotic, antidiabetic, antioxidative and antimicrobial effects(Ojansivu, Ferreira, & Salminen, 2011). Yacon cultivation has beenexpandedtoseveralcountriessuchasNewZealand,Japan,andBrazilin the last decades, and the production in the Andean region andothercountrieshaveincreasedduetothepresumedmedicinalprop-erties of both roots and leaves (Genta, Cabrera, Grau, & Sánchez,2005). Theantidiabeticeffectsof yaconroot hydroalcoholic extractin streptozotocin (STZ)-induced diabetic rats have been attributedto its antioxidant activity and content in phenolic compounds,mainlychlorogenicacid(Park,Yang,Hwang,Yoo,&Han,2009).Dailyintake of yacon syrup decreased body weight, waist circumferenceand body mass index suggesting a role in obesity management. Inaddition,beneficialeffectshavebeenreportedoninsulinresistanceand serum LDL-cholesterol levels suggesting a role on metabolicsyndromeanddiabetes(Gentaetal.,2009).Stimulatoryeffectsofya-con FOS on Ca intestinal absorption, bone mineral retention andstructural properties in the femoral midshaft of Wistar rats fed  adlibitum  with diets supplemented with yacon flour, have also beenreported(Lobo,Colli,Alvares,&Filisetti,2007).Mostofthebeneficialeffectsofyaconconsumptionhavebeenattributedtoitscontentof phenoliccompounds,antioxidantsandprebiotics(FOS).ThelargestdiversityofyacongermoplasmismainlyfoundintheeasternAndeanslopesofPeruandBolivia(Grau&Rea,1997).Uptodate,onlyafewstudieshaverelatedthebiodiversitytothephysicaland chemical characteristics of yacon. Large differences in FOS andsugarcontentshavebeenreportedfortendifferentyaconaccessions(Hermann,Freire,&Pazos,1997).Therearealsodifferencesintubershape, weight, content of oligofructans, as well as in leaf isozymes,phenolics,andrelativeDNAcontentsreportedforfouryaconacces-sionscultivatedunderfieldconditions(Valentováetal.,2006).Inan 0308-8146/$ - see front matter   2012 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.foodchem.2012.05.088 ⇑ Corresponding author. Tel./fax: +511 3495764. E-mail address:  dcampos@lamolina.edu.pe (D. Campos).Food Chemistry 135 (2012) 1592–1599 Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem  effort to investigate the intra-specific genetic variability in  S.sonchifolius  for prediction of its total phenolic content, molecularmarkers have recentlybeen investigated (Milellaet al., 2011).The objectives of this study are: (i) to evaluate total phenoliccompounds (TPC), antioxidant capacity (AC), reducing sugars(RS), sucrose and FOS in 35 yacon accessions to identify accessionswith potential to be used as sources of prebiotics and other bioac-tive compounds and (ii) to investigate  in vivo  the prebiotic effectsof yacon FOS compared to the gold standard ‘inulin’. 2. Materials and methods  2.1. Plant material and chemicals Thirty-five accessions of yacon roots were kindly supplied bythe International Potato Center (CIP) located in Lima (Peru). Theroots were grown in the region of Huancayo (Peru) at approxi-mately 3200m above sea level, at   80% relative humidity and17  C (average temperature). Three independent samples of   0.5kg were collected for each accession. Samples were collectedat optimal harvest date (8months of cultivation) and stored at  20  C for further use. Moisture content was determined in yaconflesh and DM was calculated by difference (AOAC, 1995).The standards used for analysis of phenolic acids (  p -coumaric, o -coumaric, protocatechuic, ferulic, gallic, caffeic, chlorogenic and  p -hydroxybenzoic acids), flavonols (quercetin, rutin, myricetinand kaempherol), flavones (luteolin and apigenin) and flavanones(naringenin) were purchased from Sigma Chemical Co. (St. Louis,MO). Flavan-3-ols (cathechin and epicathechin) were purchasedfrom ChromaDexTM (Santa Clara, CA). Trolox (6-hydroxy-2,5,7,8-tetramethyl chroman- 2-carboxylic acid) and 2N Folin–Ciocalteureagent, 2,2 0 -azinobis(3-ethylbenzothiazoline-6-sulfonic acid)(ABTS) were purchased from Sigma Chemicals Co. (St. Louis, MO).HPLC grade acetonitrile and other solvents and reagents were pur-chased from Merck (Darmstadt, Germany).  2.2. Chemical analysis 2.2.1. Antioxidant capacity (AC) and total phenolic compounds (TPC) Yacon flesh (  5.0g) was homogenized with 100ml of acidified80% methanol (formic acid, pH 2.0). The mixture was vortexed for30s and flushed with nitrogen for 2min. After 60min of intermit-tent shaking (200rpm) at room temperature, the extract was cen-trifuged at 6000  g   for 10min at 4  C, and the supernatant wascollected. The pellet was submitted to a second extraction for30min with 50ml of solvent. The supernatants were combinedand evaporated on a rotary evaporator at 40  C for further AC,TPC, and HPLC-PAD (photodiode array detection) analysis.AC was determined using the ABTS assay (Arnao, Cano, & Aco-sta, 2001) and expressed as  l mol of trolox equivalents (TE)/g of DM from a standard curve developed with trolox. TPC were deter-minedusingastandardcurveof chlorogenicacid(CA) accordingtoSingleton and Rossi (1965) and the results were expressed as mil-ligram of chlorogenic acid equivalents (CAE)/g of DM.  2.2.2. HPLC-PAD analysis of phenolic compounds Phenolic compound profiles were analyzed by HPLC-PAD aspreviously reported (Chirinos et al., 2008). Briefly, phenolics wereseparated using a X-terra RP-C 18  (5 l m, 250  4.6mm) column(Waters, Milford, MA) and a 2.0  4.6mm guard column at 30  Con a Waters 2695 Separation Module (Waters, Milford, MA)equipped with an auto-injector, a 2996 photodiode array detector(PDA) and the Empower software. Spectral data were recordedfrom200 to 700nm. The mobile phase was solvent (A) water: ace-tic acid (94:6, v/v, pH 2.2) and solvent (B) acetonitrile. The solventgradientwas:0–15%Bin40min,15–45%Bin40minand45–100%Bin10min.Aflowrateof0.5ml/minwasusedand20 l lofsamplewere injected. Samples and mobile phases were filtered through a0.22 l m Millipore filter, type GV (Millipore, Bedford, MA) prior toHPLC injection. Each sample was analyzed in duplicate. Phenoliccompounds were identified and quantified by comparing theirretention time and UV–Vis spectral data to standards.  2.2.3. Quantitate of reducing sugars, FOS and sucrose SugarsandFOSwereextractedfromyaconfleshaccordingtothemethod reported by Jaime, Martín-Cabrejas, Mollá, López-Andréu,& Esteban, 2001 with some modifications ( Jaime et al., 2001). Briefly, 5g of yacon was homogenized in an ultra-turrax homoge-nizer (IKA, Germany) with 50ml of 70% ethanol (v/v) and immedi-ately heated at 100  C for 10min. The mixture was centrifuged at6000  g   for 15min and the supernatant was collected. The yaconcakeswerere-extractedtwomoretimesunderthesameconditions.The supernatants were combined and vacuum evaporated in arotary evaporator at 50  C. The residue was re-dissolved in 50mlof deionized water, and this aqueous extract was kept for furtheranalysisof reducingsugars (RS), sucrose(S) andfructooligosaccha-rides (FOS). RS were determined according to the method reportedby Miller (1959) using dinitrosalicilic acid as reagent and fructoseasstandard,absorbancewasmeasuredat550nm.FOScontentwasdetermined by HPLC-IR as reported by Campos, Betalleluz, Tauqu-ino, Chirinos and Pedreschi (2009). Briefly, a NH 2 P-50 4E (5 l m,250  4.6mm) column (Shodex, Japan) and a NH 2 P-50G 4A(4.6  10mm) guard column were used. The mobile phase wascomposed of water: acetonitrile (30:70, v/v) at a flow rate of 1ml/min and 30  C. Twenty ml of sample was injected. Samples,standards (glucose, fructose and sucrose) and mobile phase werefiltered through a 0.22 l m Millipore filter, type GV (Millipore,Bedford, MA) prior to HPLC injection. The results were expressedas g of fructans per 100g of DM.  2.3. Prebiotic effects of yacon FOS using an in vivo guinea pig model Yacon roots were obtained from a local market in Lima, Peru.Rootswereboiled(99.5  Cfor25min)toinactiveenzymes,cutintoslices and dried (  7% moisture) using a hot-air tunnel (relativehumidityof   22%andairflowrateof2.5m/s)at65  C.Driedyaconslices were milled to obtain yacon flour composed of FOS, 42%; RS33% and sucrose 4.9% for further use in the diet formulation pre-sented in Table 1. Pellets were obtained using a Hessen Boxtel–Holland (Robinson Milling Systems, Lima, Peru) machine.Male guinea pigs ( Cavia porcellus ) of 14±2days age and230±30g weight were purchased from a commercial guinea pig  Table 1 Formulation of experimental diets (g/100 g). Ingredients Diet control Diet inulin a Diet yacon flour a Yellow maize 28.06 27.97 25.28Wheat by-product 34.95 34.79 30.84Rice husk 5.00 0.00 0.00Inulin (Orafti  P95) 0.00 5.26 0.00Yacon flour 0.00 0.00 11.9Alfalfa hey 6.1 6.1 6.1Soya cake 20.62 20.61 20.61Vegetal oil 2.35 2.35 2.35Mix (vitamins+minerals) 2.76 2.76 2.76Anti-fungal 0.1 0.1 0.1Vitamin C 0.06 0.06 0.06Diet Composition: protein 18.0 (%), fibre 9.0 (%), fat 5.0 (%), lysine 0.84 (%),methionine+cysteine 0.79 (%), arginine 1.39(%), tryptophan0.28 (%), treonine 0.69(%), calcium 0.80 (%), phosphorus 0.80 (%), sodium 0.20 (%) vitamin C 200 (mg/100g). Gross energy 12.14 (Mj/kg). a The content of inulin or FOS in the diet was 5 %. D. Campos et al./Food Chemistry 135 (2012) 1592–1599  1593  farm (Universidad Nacional Agraria La Molina, Cieneguilla, Perú).The guinea pigs were kept in ventilated cages covered with ricepeel. Food and water were provided  ad libitum . Animals were al-lowed to adjust to their environment for 4days before initiationof the experiments and randomly assigned to three experimentalgroups ( n  =16). Experimental groups received a basal diet (controlgroup), a diet with inulin Orafti  P95 (positive control group) or adiet with yacon flour (Table 1). Food intake and body weight wererecorded weekly during eight weeks. Body weight gain and feedefficiency (ratio of weight gain to food consumption) were calcu-lated. At the end of the study (8weeks), animals were humanelysacrificed using ether anesthesia following institutional regula-tions. Caecum was removed and the cecal content collected andfrozen in liquid nitrogen. Cecal material and caecum tissues werestored at  80  C for further analysis.  2.3.1. Bacteriological analysis of cecal material Onegramofcecalmaterialwastransferredintoasteriletubeandmixedwith9mlofsterilesalinephosphatesolution(PBS,SigmaAl-drich) containing 1% of hydrochloride  L  -cysteine (Scharlau Chemie,  Table 2 Total phenolic compounds, antioxidant capacity, dry matter, reducing sugars, sucrose and fructooligosaccharides in 35 yacon accessions. Cultivar TPC (mg CAE/g DM) AC ( l mol TE/g DM) D M (g/100g) R S (g/100g DM) S (g/100g DM) FOS (g/100g DM)ARV 5073 9.0±0.3 43.3±2.4 15.1±1.3 32.8±0.8 7.1±0.2 29.7±2.3ARB 5564 8.9±1.2 42.5±5.0 11.0±0.2 32.3±0.1 5.1±0.9 41.5±3.6ARB 5185 10.3±1.0 43.5±6.5 14.2±1.4 36.8±3.2 4.8±0.1 32.4±4.7AJC 5189 7.9±0.8 45.4±6.0 19.1±1.2 19.7±0.3 2.6±0.2 65.0±2.0ARB 5184 12.0±0.4 40.4±4.7 9.1±0.4 39.0±2.8 6.4±0.4 30.2±2.8DPA 07008 11.7±0.5 39.5±1.3 11.5±0.8 43.1±6.1 4.4±0.2 47.2±4.3AMM 5163 10.9±0.7 52.6±4.4 18.6±1.2 26.3±2.6 4.0±0.0 49.7±7.5ARB 5027 18.2±1.2 69.8±0.1 10.3±0.9 43.3±1.1 7.2±0.8 37.5±2.5DPA 07010 11.8±1.3 88.4±1.2 7.5±0.2 49.1±3.9 8.9±0.4 38.5±0.2DPA 07004 14.9±0.8 57.3±1.8 10.2±0.1 43.1±2.5 4.8±0.6 28.4±0.3ARB 5382 13.0±0.9 38.7±5.1 11.3±0.7 52.7±2.2 2.2±0.6 21.4±2.8DPA 07007 10.0±0.8 59.6±0.1 12.5±1.4 45.8±1.4 3.7±0.1 38.6±1.1ARB 5125 10.3±0.4 23.3±2.5 13.6±0.2 27.3±3.2 2.0±0.1 47.1±4.5AKW 5075 11.0±0.4 38.1±2.3 17.1±0.7 30.8±0.8 3.3±0.7 51.3±3.6ARB 5124 11.3±1.3 60.4±3.4 17.0±0.6 28.4±3.4 5.9±1.6 47.0±2.0DPA 7001 26.3±0.3 122.0±0.1 10.6±0.0 56.1±3.1 16.8±0.5 12.2±0.5DPA 7005 25.8±0.1 133.8±2.9 12.2±0.2 59.9±1.7 6.1±0.5 20.0±0.2DPA 7006 24.0±0.1 110.7±1.7 13.0±0.5 55.4±1.0 5.9±0.1 22.6±0.0DPA 7002 24.5±0.0 112.3±0.1 12.7±0.3 45.7±0.4 14.1±0.3 17.0±0.6ARB 5563 22.3±0.1 136.0±6.1 14.8±0.0 42.7±0.5 7.2±1.4 34.4±0.0P 1385 14.3±0.4 72.5±5.4 16.2±0.1 45.6±0.7 2.0±0.1 32.9±0.5AMM 5129 12.4±0.2 57.9±6.4 15.7±0.6 33.2±0.4 2.1±0.0 45.1±1.3DPA 7009 26.0±0.0 118.4±0.2 12.0±1.3 59.1±0.4 4.2±0.3 29.3±1.3SAL 136 14.9±0.5 73.3±2.8 15.3±0.2 45.2±1.0 5.8±0.2 38.2±4.3Y. MORA. 11.2±0.3 67.8±0.1 13.1±0.0 48.2±0.0 6.9±0.4 27.9±2.1ARB 5537 22.6±0.2 83.2±2.6 13.6±0.1 54.9±0.7 7.9±1.2 26.4±1.5P 1185 20.6±0.0 83.8±6.1 13.0±0.0 58.7±0.5 5.0±0.3 20.4±0.9GOM 130 19.7±0.2 91.8±4.6 14.6±0.0 48.7±0.7 7.3±0.1 32.8±0.2AMM 5135 19.7±0.2 99.2±7.2 16.3±0.1 45.3±0.0 4.9±0.1 42.0±0.6Y. BLANCO 28.3±0.1 135.7±4.5 11.1±0.1 67.5±0.0 5.2±0.0 19.3±0.6AME 5186 25.6±0.0 95.9±7.2 11.0±0.0 75.9±4.3 6.6±1.5 6.4±2.5AMM 5150 18.9±0.1 92.2±6.1 15.5±0.0 51.6±0.4 6.5±0.5 31.3±0.3AMM 5136 22.4±0.0 111.6±4.3 13.6±0.0 75.1±1.6 8.3±0.2 23.8±0.1DPA 07011 30.8±0.1 135.1±0.1 10.1±0.0 66.0±3.5 8.0±1.2 6.9±0.7DPA 7003 23.3±0.1 124.0±4.4 13.3±0.0 56.1±0.1 4.8±0.0 25.8±0.1Values are mean ( n  =3)±SD. Fig. 1.  HPLC-PAD phenolic compounds profile for yacon root accession DPA 07011 at 320nm.1594  D. Campos et al./Food Chemistry 135 (2012) 1592–1599  Barcelona, Spain)andthenseriallydiluted(from10  1 to10  7 ). Bif-idobacteria were quantified using Beerens medium (brain heartinfusion agar Difco™, glucose, citrate of iron III, L-cysteine, sodiumhydroxide and propionic acid) (Beerens, 1990). Lactobacilli andenterobacteria were quantified in MRS agar (Merck, Frankfurt,Germany) and McConkey agar (Difco™), respectively. Incubationwasperformedat37  Cunderanaerobicconditionsusingtheanaer-obic jar with Anaerogen  for bifidobacteria or CO 2  Gen  sachet forlactobacilli and enterobacteria. Number of cells was recorded ascfu/g of cecal material after 24h incubation for lactobacilli or 72hfor enterobacteria and bifidobacteria.  2.3.2. Histological analysis of caecum tissues Caecum tissues were fixed in 10 % formalin. Tissue fragmentswere imbibed inparaffin and stainedwithhaematoxylin and eosin(H&E) for histological examination.  2.3.3. Short-chain fatty acid (SCFAs) analysis Propionic, butyric and acetic acids (SCFAs) were quantified incecal material as previously reported (Tzortzis, Goulas, Gee, & Gib-son, 2005). Briefly, cecal samples were mixed with MilliQ water ina proportion of 1:1.5 (v:v), centrifuged at 12000  g   for 10min.Supernatants were then filtered through a 0.22 l mMillipore filter,type GV (Millipore, Bedford, MA) and analyzed by HPLC, using aprepackedAminexHPX-87Hstrongcation-exchangeresincolumn(300  7.8mm i.d.), fitted with an ion exclusion microguard refillcartridge (Bio-Rad Laboratories, Richmond, Calif.) in a Waters2695 Separation Module (Waters, Milford, MA) equipped with anautoinjector, a 2996 photodiode array detector (PAD) and the Em-powersoftwarewereusedforHPLCanalysis.Asampleof20 l lwaseluted with 0.005mol/L sulfuric acid at 0.6ml/min and 50  C.SCFAswereidentifiedandquantifiedbycomparingretentiontimesand UV–visible spectral data to known standards.  2.4. Statistical analysis Quantitative data are mean±standard deviation (SD) values.Data were analyzed using SPSS for Windows 14.0 (SPSS, Chicago,IL, USA). One-way analysis of variance (ANOVA) followed by pair-wise comparisons post hoc Duncan test (  p  <0.05) were performed.For multivariate statistical analysis, principal component analysis(PCA) was performed on mean-centered and standardized datausing Unscrambler 9.8 (CAMO A/S, Trondheim, Norway). 3. Results and discussion  3.1. Antioxidant capacity (AC) and total phenolic compounds (TPC) AC values for the 35 yacon accessions ranged from 23 to136 l mol TE/g DM or 3.2–20.1 l mol TE/g fresh weigh (FW) (Ta-ble 2). The highest values were found in ARB 5563, Y. BLANCOand DPA 07011 accessions, while the lowest values were foundin ARB 5125, AKW 5075 and ARB 5382. Previous studies have re-ported AC values of 1.25 l mol TE/g FW for yacon roots quantifiedby the DPPH assay (Mikami, Yamaguchi, Shinmoto, & Tsushida,2009). In general, the AC values found in the 35 yacon accessionswere within the range reported for other Andean tuber crops, suchas potato ( Solanum  sp.), mashua ( Tropaeolum tuberosum ), oca ( Ox-alis tuberosa ) and olluco ( Ullucus tuberosus ) (3.4–15.1, 3.8–39.2,6.5–19.8 and 1.9–6.1  l mol TE/g FW, respectively) (Campos et al.,2006), and similar to chicuru ( Stangea rhizantha ) (3.9 l mol TE/gFW), another FOS rich Andean crop (Campos et al., 2009).TPCvaluesvariedfrom7.9to30.8mgCAE/gDMor0.9–3.3mgof CAE/gFW.ThehighestvalueswerefoundinDPA07011,Y.BLANCO,andDPA7001;whilethelowestvalueswerefoundinAJC5189,ARB5564 and ARV 5073 (Table 2). These findings are consistent withprevious studies showing that TPC for yacon roots are around38mg CAE/g DM (Yan et al., 1999), and 5.7–3.5mg of gallicacid equivalent/g DM (Simonovska, Vovk, Andrenšek, Valentová & FOSRSSTPCACDM -1-0,8-0,6-0,4-0,200,20,40,60,81-1-0,8-0,6-0,4-0,200,20,40,60,81 PC 1    P   C    2  ARV 5073ARB 5564ARB 5185AJC 5189ARB 5184DPA 07008AMM 5163 ARB 5027DPA 07010DPA 07004ARB 5382DPA 07007ARB 5125AKW 5075 ARB 5124DPA 7001DPA 7005DPA 7006DPA 7002ARB 5563P 1385 AMM 5129DPA 7009SAL 136Y.MORAARB 5537P 1185GOM 130Y. BLANCOAME 5186AMM 5150AMM 5136DPA 07011DPA 7003AMM 5135 Fig. 2.  Principal component analysis (PCA) biplot. Score and loading plots are superimposed. Samples (score plot) correspond to the different yacon accessions. Variablesmeasured (correlation loading plot) correspond to fructooligosaccharides (FOS), dry matter (DM), RS (reducing sugars), S (sucrose), TPC (total phenolic content) and AC(antioxidant capacity). The scores representing each accession (different labels used) indicate differences for the 35 yacon accessions. The variables (FOS, DM, RS, S, TPC andAC) that are important in the discrimination are characterized by large loadings. Thus, the further the variable from the srcin, the more influential is that variable in thediscrimination among the different accessions. The closer an accession is to a particular variable is indicative of high positive correlation to that variable. D. Campos et al./Food Chemistry 135 (2012) 1592–1599  1595  Ulrichová, 2003). Likewise, values reported for other Andean cropswere within the range 0.47–3.31mg CAE/g FW (Campos et al.,2006).Anthocyaninswerenotdetectedintheyaconaccessionsthatpresented either purple peel and/or purple spots in the flesh byusing a spectrophotometric method (Giusti & Wrolstad, 2001),most likely due to the low concentrations. Similarly, the yellow ororange flesh accessions contained very low and non detectableamountsofcarotenoids,quantifiedaspreviouslydescribed(Talcott& Howard, 1999). This finding was related to the low lipophilic AC(0.05–0.35 l mol TE/g FM) content quantified by the ABTS assay(Arnao et al., 2001). In general, a high correlation between AC andTPC ( r   =0.89,  p  <0.01) was found, being indicative that phenoliccompounds are mainly responsible for the AC of yacon roots.HPLC-PAD analysis performed for 5 yacon accessions showedsimilar phenolic profiles. Chromatograms at 320nm showed 14peaksofhydroxycinamicacidderivatives,beingoneofthemchlor-ogenic acid (5-O-caffeoylquinic acid) (Fig. 1). The chlorogenic acidcontent for the five accessions varied from 1.8 to 7.5mg/100g FW(15–24% of total phenolics quantified by HPLC-PDA). This wasconsistent with previous investigations that reported chlorogenicacid (4.9±1.3mg/100g FW) (Yan et al., 1999), and caffeic acidderivatives, mainly esters of caffeic acid with the hydroxy groupsof aldaric acid (Takenaka et al., 2003) as main phenolics identifiedin yacon roots. In addition, tryptophan was detected within therange 0.5–2.8mg/100g. These values were consistent with previ-ously reported values for yacon roots (1.46±0.07mg/100g FW)(Yan et al., 1999).  3.2. Dry mater (DM), Reducing sugars (RS), sucrose (S), and fructooligosacharides (FOS) The content of RS, S, and FOS based on DM are presented in Ta-ble 2 Results showed that DM varied from 7.5 to 19.1g/100g;accordingly RS varied from 19.7 to 75.9g/100g DM (3.5 to 8.5g/100g FW), S varied from 2 to 16.8g/100g DM (0.3 to 1.8g/100gFW), and FOS varied from 6.4 to 65.0g/100g DM (0.7 to 12.3g/100g FW). The highest FOS contents were found in AJC 5189 fol-lowed by AKW 5075 and AMM 5163 with values of 65.0, 51.3and 49.7g FOS/100g DM respectively (Table 2). The content of RS in yacon accessions was inversely correlated to the FOS content 0 200400600800100012001400    B  o   d  y  w  e   i  g   h   t   (  g   ) Yacon flour InulinControl iiihhhgggff f eeedddcccbbbaaa 0255075100125150175200    M  e  a  n  a  v  e  r  a  g  e  w  e  e   k   l  y  w  e   i  g   h   t   (  g   ) aaabbbcccdddeeef f f ggghii 0.000.100.200.300.400.500.60 12345678    M  e  a  n   f  e  e   d  e   f   f   i  c   i  e  n  c  y Weeks  jk jkiiihhhgggef ef cdcdbbbaaa abc Fig. 3.  Effects of yacon flour diet on (a) body weight, (b) body weight gain, and (c) feed efficiency (weight gain/food consumption). Data are mean values ( n  =16±SD),different letters at each time point indicate statistically significant differences (  p  <0.05).1596  D. Campos et al./Food Chemistry 135 (2012) 1592–1599
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