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Departament de Ciència Animal i dels Aliments and * Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain
2To whom correspondence should be addressed. E-mail: josefrancisco.perez{at}uab.es
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • resistant starch • growing pigs • fermentation • short-chain fatty acids
Microbial fermentation of carbohydrates in the large bowel (LB)3 of simple-stomached animals is a focus of considerable interest. In particular, the stable fermentation of carbohydrates has been shown to prevent pathogens or diarrhea (1
), and be of benefit in a variety of digestive and metabolic diseases, such as carcinogenesis in the colon (2
), insulin resistance and diabetes (3
), and chronic renal or hepatic disease (4
). Carbohydrates available for fermentation in the large bowel consist of nonstarch polysaccharides, although starch and products of small intestine starch digestion ([i.e., resistant starch (RS)] are thought to contribute extensively to LB fermentation. For example, there is recent evidence that giving such RS orally to human patients with cholera increases fecal short-chain fatty acid (SCFA) concentration and shortens the duration of diarrhea (5
).
Methods to evaluate fermentation, especially those involving humans, are based on the measurement of breath gas (H2 or CH4) or SCFA in peripheral venous plasma or feces. Fermentation increases the fecal excretion of SCFA (2
) and shifts nitrogen excretion from urine to feces (6
,7
). However, there have been contradictory results in fermentation studies that measure the excretion of SCFA and N in feces. For instance, more highly efficient microbial protein formation has been observed with poorer fermentable substrates, such as cellulose, compared with other more degradable carbohydrates (8
), such as resistant starch. Similarly, Heijnen and Beynen (7
) provided evidence that retrograded RS, but not uncooked RS, shifts N excretion from urine to feces in pigs.
Numerous factors may influence fermentation of starch and production of SCFA in the large bowel. A number of studies have shown that the extent of RS fermentation can increase over time (9
,10
). Adaptive responses may reflect long-term adaptations of the intestinal flora (10
) or the intestinal tract, through hypertrophy of the large bowel and increased retention times for digesta (11
). The present experiment was designed to study the adaptive responses of growing pigs over time to the intake of high amounts of resistant starch, using raw potato starch as reference material. Factors that are likely to affect the excretion of SCFA and microbial N in feces were also evaluated.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Purified starches [native corn starch (CS), 26% amylose, 74% amylopectin; raw potato starch (RPS), 20% amylose, 80% amylopectin] were purchased from Cerestar Iberica (Barcelona, Spain). As determined by enzymic analysis (13
), CS contained 187 g/kg of resistant starch and RPS, 637 g/kg. Animals and diets.
Twelve Landrace x Large White male growing pigs, 18.4 ± 1.0 kg (mean ± SD) live weight (LW), were purchased from La Balcona (Vic, Spain). On arrival, they were housed individually on slat bedding (six pigs) and in metabolic cages (six pigs), and administered a preexperimental ground and solid diet mainly composed of corn, soybean meal, dried whole whey, dried skim milk and fish meal. With an initial body weight of 27.4 ± 1.3 kg (mean ± SD), pigs in each location were randomly divided into two groups and offered two experimental ground diets, containing either 250 g/kg of CS or 250 g/kg of RPS. Diets were formulated (Table 1
) according to nutrient requirements of NRC (14
), that is, 13,690 kJ metabolizable energy (ME)/kg, 189.4 g CP/kg, 11 g lysine/kg, assuming a starch energy content of 16,720 kJ ME/kg. Diets were presented over a 38-d period at a rate of 0.90 of the estimated voluntary intake (14
) in two equal meals at 0800 and 2000 h. Cr2O3 was included (15 g/kg) as an indigestible marker, and a fungicide (Luctamold®) was used to inhibit mold growth during storage.
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One fecal sample per pig was collected for analysis of SCFA concentration on d 0, 4, 7, 21 and 38, and purine base (PB) concentration on d 0, 2, 4, 7, 14, 21, 28 and 38 after dietary presentation. Briefly, the pens were thoroughly cleaned early in the morning and, over the next 3 h, at least two samples of feces were taken and pooled. An amount of 
1 g was acidified with 1 mL of solution containing 50 g/L H3PO4, 10 g/L of mercuric chloride and 50 mmol/L of 3-methyl valerate as internal standard, and stored at -20°C until analysis for SCFA concentration. The rest of the sample was freeze-dried and milled for analysis of PB. On d 8–10, d 15–17 and d 22–24, individual feces were sampled from the 12 pigs for digestibility estimations based on the marker ratio, and total urine was collected from the six pigs in the metabolic cages. Feces were dried at 60°C, ground (1-mm screen) and stored at room temperature for chemical analysis. Urine was collected in buckets containing 200 mL of 1 mol/L H2SO4 to keep pH < 2. Urine weight and specific gravity were recorded daily and two subsamples (2%) were stored immediately at -20°C. On d 38, from 2 to 3 h after feeding, pigs were killed by an intravenous Na-thiobarbital injection (200 mg/kg LW). The abdomen was opened and the whole gut excised and weighed. Ileal digesta was sampled from a 300-mm length segment 100 mm anterior to the ileal-cecal junction. The cecum; proximal, middle and distal colon; and rectum were ligated, excised and weighed. Digesta from the cecum, colon and rectum were sampled for analysis of SCFA as described for feces. Samples of ileum and large bowel digesta were freeze-dried and milled for analysis of PB and chromium. Portions of 20 mm in length of cecum (10 cm caudal from the ileocecal valve) and middle colon (1.5 m from the cecum) tissue were placed in a saline fixative (100 mL formaldehyde/L saline) for measurement of the mucosa thickness. Finally, the voided cecum and colon were weighed, and the small intestine and colon length were measured.
Analytical procedures.
Chemical analyses of the diets and digesta were performed following the methods of the AOAC (15
) for dry matter, ash, crude protein and fat. The total starch of feed and digesta samples was measured by the method of Theander (16
). Briefly, starch was determined as glucose liberated after an enzymatic incubation with thermostable 
-amylase (A-4551; Sigma, St. Louis, MO) for 1 h at 100°C, and amyloglucosidase (A-3514; Sigma) for 4 h at 60°C. Resistant starch was measured by the method of Berry (17
) modified by Champ (13
) as the part of starch not hydrolyzed by incubation with -amylase for 16 h at 37°C. Hydrolysis products were extracted in 800 g/L ethanol and discarded. Resistant starch was then solubilized with 4 mol/L KOH and hydrolyzed with amyloglucosidase for 90 min at 65°C. The SCFA concentration in deproteinized feces and digesta was determined by GLC, following the method proposed by Jouany (18
). Chromium III oxide concentration in feed and digesta was determined by atomic absorption spectrophotometry following the method of Williams et al. (19
). Purine bases in digesta samples (40 mg) were determined by HPLC (20
) after their acid hydrolysis with 2 mL of 2 mol/L perchloric acid at 100°C for 1 h. Mucosa thickness was measured by optical microscopy. Fixed samples were dehydrated, embedded in paraffin wax, sectioned at 4 µm, stained with hematoxylin and eosin and mounted on microscope slides.
Calculations and statistical analysis.
Whole-tract and fractional digestibilities along the large bowel were calculated by the marker (Cr2O3) ratio method. Colonic transit time (TT, h) was estimated as the mass of Cr present in the organ divided by the mean daily chromium intake (±SD) and multiplied by 24 (21
). Data were subjected to ANOVA according to the general linear model procedure of SAS (22
). Repeated measurements over time (digestibility, SCFA and PB in feces) and data obtained from different gut locations (fractional digestibilities, SCFA and PB in digesta) were analyzed by the repeated-measures model (MIXED-type TOEP) of SAS (22
), and the LSMEANS follow-up test was used for comparison of means. A two-tailed P-value of <0.05 was considered significant.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Pigs in both groups consumed the entire portion of food presented. The average daily gain of weight was 700 vs. 740 g/d (SEM, 28.0) and the feed:gain ratio was 2.30 vs. 2.17 (SEM, 0.091) for pigs fed RPS and CS, respectively. However, the weight of carcasses after removing the digestive tract was significantly lower in pigs fed RPS than those fed CS [44.7 kg vs. 48.4 kg (SEM), 6.08, P < 0.03].
Digestibility and urinary N excretion.
Whole-tract digestibilities of organic matter, crude protein and starch were significantly higher in pigs fed CS than in pigs fed RPS (Table 2
). However, organic matter and crude protein digestibilities progressively increased in RPS-fed pigs from d 9 to d 38, and in CS-fed pigs from d 9 to d 16 after feeding, after which there were no further increases. Thus, at the 38-d time point, whole-tract digestibility of organic matter and starch were similar in CS- and RPS-fed pigs, but whole-tract digestibility of protein remained higher in CS-fed pigs. Daily excretion of N in the urine of pigs fed Diet CS (Fig. 1
) increased at 23 d after feeding (P < 0.02). The pigs fed Diet CS tended (P < 0.10) to excrete more urinary N than in those fed RPS on d 23.
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Purine base concentration in feces (Fig. 2A
) ranged from 12.8 to 33.9 µmol/gDM and was higher in pigs fed Diet RPS than CS (P < 0.03). Pigs fed CS and RPS similarly showed the highest PB concentration in feces on d 4, after which it decreased until d 14. As shown in Figure 2
B, SCFA concentrations in feces were highest on d 7 and d 21, with little difference between dietary treatments.
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The digestive tract removed on d 38 from pigs fed Diet RPS was significantly heavier than that from the CS group (P < 0.05, Table 3
). Differences occurred primarily in the colon compartment that, in pigs fed Diet RPS was longer (P < 0.05) and heavier, whether full (P < 0.001) or empty (P < 0.05), than in the CS group. However, the estimated retention times of digesta in the colon were similar (23.0 vs. 16.0 h; P = 0.14) in pigs fed RPS and CS, respectively. The pigs fed RPS had a wider cecal mucosa (P < 0.05) and lower middle colonic mucosa (P < 0.001) than those in pigs fed CS.
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) was lower in pigs fed RPS than in those fed CS (P < 0.0001). However, the fractional digestibility of starch in the pigs fed RPS increased from ileum to rectum, in which most starch is extensively fermented in the cecum and proximal colon compartment. Starch digestibility in the colon and rectum did not differ between groups.
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) and SCFA (Fig. 4
B) concentrations in digesta. Purine base concentrations increased from ileum to cecum and proximal colon (P < 0.001) and decreased from proximal colon to rectum (P < 0.001). PB concentration in cecal and proximal colonic digesta did not differ between groups. However, the PB concentrations in the middle colon were higher in pigs fed RPS than CS, and tended to be higher (P = 0.1) in the distal colon and rectum. In contrast, the SCFA concentration was elevated only in the proximal colon of pigs fed Diet RPS (P < 0.01). The proportion of acetate in the large bowel digesta (mol/mol, Table 4
) was higher in the middle colon (P = 0.06) and rectum (P < 0.05) in the CS group than in the RPS group; conversely, the proportion of propionate was lower in the middle colon (P < 0.05) and rectum (P = 0.066) in the CS group than in the RPS group. Branched-chain SCFA percentages increased through the large bowel in both diet groups (P < 0.012) and in the middle colon were higher in the CS group than in the RPS group (0.039 vs. 0.017, P < 0.05).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Among the different types of RS, raw potato starch is gelatinized poorly and hydrolyzed slowly by -amylase. On this basis, we chose RPS and CS to generate a supply of RS to the large bowel of growing pigs.
The addition of RPS increased the amount of starch entering the large bowel and becoming an available source for the colonic microflora. Differences in the ileum digestibility of starch were similar to the values calculated from in vitro analysis (Table 1)
. However, in vivo digestibility values were higher than estimated in vitro for CS (96.9 vs. 85.0%) and RPS (75.6 vs. 59.3%). In vitro data from recent studies correlate reasonably well with the ileum digestibility of starch when in vitro analysis accounts for physiological variables, including chewing and individual variations in transit (13
,24
). Some procedures of amylolysis (25
) are preceded by a proteolysis step with pepsin and trypsin to liberate encapsulated starch from the protein matrix. Unfortunately, we did not account for this step in our analytical procedure for resistant starch measurement (13
), which could explain the differences between in vivo and in vitro measurements.
A certain amount of starch was resistant over the short-term to whole-tract digestion, which demonstrates a progressive adaptation of growing pigs to the fermentation of starch in the LB. Other investigators have shown that the extent of fermentation of resistant carbohydrates can increase over time in growing pigs (26
) or rats (27
), and justification for a generalized assumption, that fermentation of starch is complete, is not warranted. In fact, on the basis of the total amount of SCFA formed in vitro (28
,29
), RS fermented more slowly than did whole starch, pectin or ß-glucans. It appears that the structure of the resistant starch may limit the penetration of bacteria into the starch granule, which is essential for starch utilization in some bacterial strains (30
). In particular, potato starch takes the form of relatively large spherical or ellipsoidal granules composed of more or less spherical blockets (400–500 nm in diameter), which, by forming a tough layer at the granule surface, are resistant to enzymic hydrolysis (31
).
Theoretically, the increases in LB digestion of carbohydrates may depend on the metabolic activity of LB microflora as they adapt to the substrate (10
) or on marked changes in digesta, including transit time. A certain adaptation of the intestinal flora has been suggested for microorganisms that are efficient in fermenting new cell wall polysaccharides (32
) or resistant starch (10
,33
) entering the LB. The hypothesis is that adaptation to RS results from a progressive selection of particular bacteria populations, most likely starch-fermenting bacteria, such as Clostridium sp., Eubacterium sp., Fusobacterium sp. or Butyrivibrio sp. (10
,34
). Little is known about the contribution of other microorganisms, such as protozoa or fungi. From studies with ruminants, it is known that yeast stimulates growth of cellulolitic microorganisms. Therefore, including fungicide in the diet of the present study appears to limit our study with regard to evaluating colonic RS fermentation.
For quantitative purposes, purine bases are probably the most widely used, naturally occurring microbial markers for rumen studies (35
). In the present experiment, we used PB and SCFA concentration analyses in feces and digesta as indexes of the microbial proliferation or autolysis. Both diets showed a pronounced increase in the PB concentration in feces during the initial period of adaptation and a progressive decrease beginning at d 4. Early changes on PB concentration are likely associated with the dietary change and the pronounced differences between the preexperimental and the experimental diets. Later decreases in PB concentration occurred simultaneously with increases in dietary digestibility and could reflect a decreased expansion of the biomass as the amount of substrate reaching distal compartments during passage of the fecal stream was reduced. The RPS diet promoted a higher excretion of PB in feces (Figs. 2
and 4)
, concomitantly with a higher excretion of N in feces and a lower excretion of urinary N. It may be that RS reduces urea synthesis and excretion (6
,36
), which is its potential role for clinical purposes, such as the management of liver or renal failure. Bacteria inhabiting the colon of single-stomached animals obtain their energy mainly from dietary carbohydrates escaping foregut digestion (37
). As fermentable carbohydrates decrease along the length of the colon, bacteria switch to the degradation of proteinaceous material and autolysis (38
,39
).
Purine base concentrations in digesta decreased in CS- and RPS-fed pigs from the proximal segments of the colon to rectum, although more distal decreases occurred in pigs fed RPS. Moreover, branched-chain SCFA, which are derived from the deamination of amino acids, progressively increased along the large bowel. The response was evident in the proximal segments of the colon of CS-fed pigs and in distal segments of RPS-fed pigs. Given the involvement of proteolytic bacteria in numerous colonic and rectal pathologies (34
) in humans, the potential role of RPS in the dissemination of bacteria in the colon and the associated risk of disease should be evaluated.
In contrast, SCFA concentration responses were less pronounced than PB concentration responses in fecal excretion and LB digesta after RPS intake. SCFA are readily absorbed in the large bowel in a concentration-dependent manner, which could explain the similarities in digesta of CS-fed and RPS-fed pigs, and the observation that neither total SCFA nor the individual acids in the distal colon or feces are predictive of the whole fermentation or the SCFA contents in proximal segments (40
–42
).
Adaptation to increased consumption of RPS resulted in a marked hypertrophy of the colon (Table 3)
, as measured by the weight and length, and a similar prolongation of the transit time of digesta in the colon. Other authors have reported that the transit time of digesta in the large bowel was prolonged after increased RPS intake in rats (11
,43
) and swine (44
). This appears to be an adaptive response aimed at salvaging energy from fermentation.
We were not able to determine the precise contribution of the adaptation of microflora or digestive tract to the time-dependent changes in digestibility after supplying supplementary amounts of RS to growing pigs. The differences in weight of digesta in the colon suggest a physical adaptation of the digestive tract to the extent of RS digestion. However, the variations in the microflora mass and SCFA through the large bowel may suggest a pronounced effect of RS on the proliferation of nonproteolytic bacteria, which deserves a more detailed study. RPS provides a large amount of RS available for LB fermentation. However, the full adaptation of growing pigs to supplementary amounts of RPS requires a period of several weeks to reach complete degradation.
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FOOTNOTES |
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3 Abbreviations used: CS, corn starch; LB, large bowel; LW, live weight; ME, metabolizable energy; PB, purine bases; RPS, raw potato starch; RS, resistant starch; SCFA, short-chain fatty acid; TT, transit time.
Manuscript received 5 June 2002. Initial review completed 11 July 2002. Revision accepted 10 October 2002.
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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