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Colonie Function and Fermentation in MenConsuming High Fiber Diets1S. E . FLEM ING , D . M ARTHINSEN A ND H. K UHN LEIN2Dep artm ent of N utritio na l S cien ces, U niversity o fC aliforn ia , B erkeley, C A 94 72 0

ABSTRA CT The relationships between ferm entation in the gut and colonie function w ere studied by using data derived from a hum an m etabolic study. F ive healthym en w ere fed diets that w ere fiber-free or contained cellulose, xylan, pectin or cornb ra n. F erm en ta tio n w as a sse sse d b y m ea su rin g th e e xc re tio n o f fla tu s g as, v ola tile fa tty a cid s (VFA ) in fe ce s a nd fe ca l pH. C olo nie fu nc tio n w as a sse sse d b y m ea su rin g tra nsit tim e, fecal frequency, fecal output and fecal com position. F ibers that w ere onlym arginally ferm en ted in clu ded cellu lo se an d co rn b ran , a nd th ese fibers cau sed larg efecal o utp ut, freq uen t d efecation s and pro lo ng ed the re sid en ce tim e of d ig esta in th egu t; feces co ntain ed h ig h lev els o f n eu tral d eterg ent fib er (NDF ); n eith er diet in fluenced fecal pH nor flatus gas excretion; and only corn bran increased V FA excretionin feces. F ibers that w ere m ostly ferm ented in the gut included xylan and pectin, andthese fibers did not influence fecal frequency or fecal output, but they did decreasetransit tim e; both diets caused high levels of flatus gas to be excreted; pectin causedhigher V FA excretion in feces and low er fecal pH . T he excretion of V FA in feces w ashigh ly correlated w ith to tal fecal ou tp ut, an d h ig h lev els o f V FA w ere asso ciate d w ithlo w flatus g as ex cretio n. M utag enic activ ity in feces w as n eg lig ib le fo r all su bjects onall diets as measured by the fluctuation test. J. Nutr. 113: 2535-2544, 1983.INDEXING KEY WORDS flatus short-chain fatty acids . volatile fattyacids pectin xylan corn bran cellulose fecal pH mu-tagens neutral detergent fiber hum an fecal output

The incorporation of fibers into diets is a glucose challenge test (10) so may be ef-currently being encouraged because of re- fective in treating som e diabetic patients.ported desirable effects on health. D ietary One of the major lim itations to includingfibers are widely distributed in foods and fibers in diets is the intestinal discom fortare highly variable in both chemical and which often results. Anecdotal evidence in-physical characteristics (1, 2). Som e dietary dicates that distension and flatulence arefibers such as cellulose and cereal brans con- undesirable side effects of consum ing hightain insoluble, complex carbohydrates, levels of dietary fiber. This has been con-They have been shown to increase fecal out- firmed by a few studies. In particular,put and, in some cases, to normalize intes- wheat bran was shown to increase the ex-tinal transit tim e (3-5). These effects are cretion of ferm entation-produced gases suchthought to alleviate constipation and diar- as hydrogen in breath (11). Oat gum wasrhea, and to reduce intracolonic pressure sothat the risk of diverticular disease is les-sened (6, 7). Other dietary fibers such as Ap,gAm eri canns ttu tefNutri"on'Re ceiw dorpu b"c atio n2Pectin and plant gUmS are Water Soluble and 'Supported i n part by National Institutes o f Health grant H OI AML 1 -X1.1 n ' ' r IV. -i- 10202, U.S. Department of Agriculture grant 12-14-5001-2,a donation byhave little mtlUenCe On teca! Characteristics the Q uaker Oats Co., C hicago, IL, a nd b y Natural Science and E ngineer-(8, 9). However, they appear to reduce the "gesearchouncilgramA-JUS., , i t '_ * rr _ Present address: Division of Human Nutntion, University of Britishblood glucose and serum insulin resp onses to C olum bia,ancouver,.C.,anada.

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2536 FL EM I NG, MARTHI NSEN AND KUHNLEI Nalso shown to increase f latus excretion (12)and, recently, we reported that pectin andxylan also caused high levels of f latus gasesto be excreted (13). I n addition to thesegases, the microorganisms also producevolatile fatty acids (VFA) including acetate,propionate, butyrate and valerate. Somedietary fibers have been reported to increasethe quantity of V FA that are excreted infeces (14, 15) . These compounds provideuti li zable energy for the host and also maycontribute to fecal output and to diarrhealdiseases since they are an important factorgoverning the rates of sodium and waterabsorption within the colon (16).In this study, we investigated the mechanism by which dietary f ibers inf luence co-Ionic function. We hypothesized that sincedietary f ibers are fermented to various extents by intestinal microbes, it is the degreeof fermentation and the products of thisfermentation that largely determine theinf luence a f iber wil l have on colonie function. To investigate this hypothesis, threepuri fied f ibers and one cereal f iber were fedto healthy men. Gastrointestinal parameterssuch as transit time, fecal f requency, fecaloutput and fecal composition were measured. Additional ly, the excretion of fermentation products such as hydrogen, carbon dioxide and methane were measured inbreath and f latus, and VFA were measuredin feces. The excretion of fermentationproducts was correlated to the measures ofgastrointestinal function in order to investigate their interrelationships.

MATERIALS AND METHODSFive normal-weight males (coded 01, 02,03, 05, 06) aged 21-32 years were selectedf rom the community.3 The subjects wereassessed to be free of gastrointestinal disorders and intestinal parasi tes, and to havenormal small bowel absorption as previously

described (13). The experimental design anddiet formulations were described in detail inthis earlier publication, so these will be onlybriefly outlined.The 63-day metabol ic study was dividedinto seven metabolic periods each of 9 day'sduration. A ll subjects received a basal,fiber-f ree diet during the first metabolicperiod. Subsequently, each subject received

a sequence of six test diets. Two diets werebasal , f iber- free formulations providingeither 100% (basal) or 85% of the energy(low E) requirement for each subject. Thebasal formulation provided 0.8 g protein perki logram body weight dai ly f rom egg albumen (Seymour Foods, Inc. , San Francisco,CA). Fat (butterfat and cottonseed oil, localsuppliers) provided 30% of caloric requirement, and the remainder was provided bycornstarch (CPC International, EnglewoodCliffs, NJ), dextramaltse [American M aizeProducts Co. (mfg) , Monarch Foods, Brisbane, CA (suppl ier) ] and sucrose in a ratioof 5:5:1. The f iber components were cel lulose (Alphacel , ICN Pharmaceuticals, Inc.,C leveland, OH), pectin (Sigma ChemicalCo., St. L ouis, MO ), xylan (I CN Pharmaceuticals, Inc.) and raw corn bran (QuakerOats, Chicago, I L). Cellulose, xylan andpectin were each fed at 0.5 g per kilogrambody weight, and corn bran was fed at 0.6g per ki logram, daily. The fibers were substituted for the other dietary carbohydrateconstituents. These levelsrepresent a reasonable daily intake of dietary fiber, yet anindividual would not consume this quantityof fiber from a single source as is fed hereIn addition, daily supplements of vitamins,minerals and choline were taken.Total fecal collections were made throughout the study. Their handling has been previously described in some detai l ( 15) . Dai lyfecal excretion was determined, and 3-daycollections were pooled and homogenizedwith a known quanti ty of water. At this time,the pH of the homogenate was determined(Beckman Expandometer M odel 76A, combination electrode; Beckman Instruments, PaloA lto, CA ).Aliquots of the homogenate prepared fromfecal specimens produced during the last 3days of each metabolic period were analyzedfor solids. The weight of excreted solids wascalculated by determining the moisture content (25 mm Hg, 60,18 hours). N itrogencontent was determined by the micro-Kjeldahl procedure (17). Fecal volati le fattyacids were determined by steam distillationand gas-liquid chromatography as previouslydescribed (15). Neutral detergent fiber (NDF)

3Thisresearch was evaluated by the Committee for the Protection ofHumans in Research, University of California, Berkeley, CA.

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COLON IC FUNCT ION AND FERMEN TA TI ON W ITH FI BERS 2537analysis was conducted by using the standardAACC (18) procedure.Breath and flatus gases were analyzed ondays 2, 5 and 9 of each metabolic period. Adetai led description of the procedures hasbeen reported (13). Data col lected on days 5and 9 are reported here since the data f romday 2 of ten ref lected the gas excretion fromthe previous metabolic period.Intestinal transit time was determined byadministering a nonabsorbable dye (50 mgFDC Blue No. 2) to the subjects and recording the time of appearance and disappearance of the dye in the feces. The fluctuationtest for fecal mutagens was carried out aspreviously described (19-21) . Salmonel latyphimur ium TA 98 wa s used to a na lyze formutagenic activity. In preparation for analysis, the fecal homogenates were centri -and were sterilized by filtration through 0.4-and 0.2-f im filters (Acrodisc, American Scienti fic Products, M cGaw Park, IL) . Severalblanks, a standard sample and duplicate extracts at either 15 mg dry weight or 30 mg

dry weight were tested in each run.Throughout the study, comparisons between treatments were generally conductedby using a factorial design and analysis ofvariance. D i fferences among means weredetermined by significance of Tukey's Stu-dentized range test and Duncan's multiple-range tests. Correlation coef ficients weredetermined and regression analyses wereperformed when appropriate. The muta-genesis data were compared by using thechi-square test for unrelated samples (22).

RESULTSAND DISCUSSIONTra nsit time a nd feca l outputThe time required for appearance and

then disappearance of the fecal dye markerwas strikingly variable among subjects (f ig.1) but the f iber-containing diets tended tohasten appearance of the dye and this wasparticularly noticeable for the pectin-,xylan- and corn bran-containing diets. Thetime required for the dye to disappear was

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HOUR S FR OM INGES T ION OF DY EFig. 1 Transit t ime of a fecal dye marker in men fed fiber-free diets or diets containing various fibers. Appearance time ()and disappearance time (O) are shown for each subject (codes 01, 02, etc.) and means (bars) areprovided for each diet. The standard deviations for appearance and disappearance, respectively, of the dye areas fol lows: basal , 28, 36 ; low E, 55 , 69; cel lulose, 19, 30; xy lan, 12, 55; pectin, 12, 31; corn bran, 14, 33 .

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2538 FLEM ING, MARTHINSEN AND KUHNLEINmore diff icult to assess, but, with the exception of corn bran, the fiber-containing dietstended to extend the time necessary for totaldisappearance. Other researchers have reported that cellulose and wheat bran, orproducts containing wheat bran, tend toreduce or to normal ize transit time (4, 5, 14,23, 24) . However, cel lulose did not reducetransi t time in this study, and these di fferences may be due to differences in the techniques of measurement. A combination oftransit-time measuring techniques using, forexample, a dye that marks the l iquid phaseand radioopaque pellets that mark the solidphase may have provided a better overallview of the inf luence that these f ibers haveon gut transit.Fecal output and fecal frequency appeared to be closely associated. For instance, both parameters were highest forcorn bran, and showed decreasing values forcellulose and pectin (fig. 2). Both fecalfrequency and fecal output for the cornbran diet were significantly greater than forthe fiber-free or xylan diet. However, dietinf luenced fecal output to a greater extentthan fecal f requency. The average weightsper defecation were calculated to be 87.0and 74.7 g for the f iber- free diets, whereasthe values for the f iber-containing diets increased in the order of xylan (108.3 g),

pectin (118.6 g), cellulose (138.3 g) and cornbran (140.0 g) .Fecal output and fecal frequency werealso related when considered among the fivesubjects ( fig. 3) . For example, subjects 05and 06 had significantly fewer defecationsthan subjects 01, 02, and 03, and subject 03had, statistically, the greatest fecal output.The average weight per defecation was calculated to be 181.1 g for subject 05, whereasthe values for the other four subjects rangedfrom 73 to 128 g.Feca l composi tionFecal dry matter excretion was closely related to total fecal weight ( fig. 2) . The fecaloutput was increased for corn bran and cellulose over the fiber-free diets, and these results confirm those of other workers ( 3, 4,22, 24, 25) . Pectin caused a smal l increase intotal fecal output and in fecal sol ids excre-

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