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Unité Mixte de Recherche sur le Veau et le Porc, INRA-Agrocampus Rennes, Domaine de la Prise, 35590 Saint-Gilles, France
2To whom correspondence should be addressed. E-mail: Jean-Paul.Lalles{at}rennes.inra.fr.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • viscosity • intestine • piglet • goblet cells • mucin
The gastrointestinal tract is covered by a mucous layer secreted by goblet cells. Mucus constitutes a protective barrier against microorganisms, physical and chemical attacks, and has the role of lubrication of the digestive tract (1). Mucin is the major glycoprotein of mucin gel and is responsible for its functional properties. Mucin subunits are comprised of a protein backbone and a large number of carbohydrate side chains that contain neutral sugars including hexosamines. Carbohydrate chains are often ended by sulfate alone or linked to sialic acid (2). This carbohydrate composition allows the distinguishing of epithelial goblet cell subtypes with neutral, acidic, and acidic-sulfated mucins according to specific histochemical staining (3). An intact mucous layer is required at the gut epithelial surface for optimal protection, depending on both quantitative (thickness) and qualitative (sugar composition of carbohydrate chains) aspects (4,5). Mucus gel is in a dynamic balance between mucin synthesis and secretion from goblet cells of the underlying epithelium and erosion on the lumenal side releasing mucin in the gut lumen.
Diet features may positively influence characteristics of the intestinal mucus in vivo. There is now evidence in monogastric animals that mucin is influenced by the diet, in particular by the nature and origin of fiber. In rats, adding 5% citrus fiber to a fiber-free diet increased the concentrations of lumenal mucin in the stomach and small intestine by 3.5- and 2-fold, respectively (6). In rats fed a diet containing cereal fiber, compared with cellulose, the number of acidic mucin-containing cells was greater in jejunal tissue (7). In pigs, increasing fiber intake enhanced the ileal excretion of hexosamines (8,9).
In monogastrics, dietary fiber is considered to have antinutritional properties, particularly in young animals. Fiber decreases the apparent digestibility of the diet and increases endogenous nitrogen secretion (10,11). This is attributed mainly to fermentable properties and an effect on the viscosity of the intestinal contents (12). The importance of viscous properties of fiber was confirmed by the use of experimental diets supplemented with carboxymethylcellulose (CMC)3 (13,14). This high-viscosity synthetic polysaccharide is water soluble and is resistant to microbial fermentation. Therefore, it allows the study of the effects of viscosity independently of fermentation. We used this model in weaned piglets to study the effect of viscosity on crude mucous ileal output, diet apparent ileal digestibility, and intestinal goblet cell histochemistry. We hypothesized that CMC increases both the ileal mucin output and goblet cell density.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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At the end of the experimental period, 2 h after the last meal, the piglets were anesthetized by electronarcosis and killed by exsanguination. The gastrointestinal tract was removed, and then the small intestine was dissected. The last third of the length of the small intestine (ileum) was weighed full and empty. All ileal digesta were collected and the pH was measured. Ileal digesta (
10 g) were collected for viscosity measurements (see below); the remaining digesta were mixed with sodium benzoate and phenylmethylsulfonyl fluoride (10 and 37 g/kg of digesta, respectively) to minimize protein breakdown, immediately stored at –20°C, and freeze-dried until analysis.
Tissue samples from the ileum were collected in the middle of the last third of the small intestine (ileal segment) for assessment of mucin histochemistry. Briefly, specimens (4–5 cm) were excised, rinsed in physiologic saline, and fixed in phosphate-buffered formalin (10%, pH 7.6) for 48 h. Then they were rinsed with ethanol:water (3:1, vol:vol) and dehydrated using an automatic machine (Citadel 1000, Shandon SA) before being embedded in paraffin (Thermomodule TM-1, Paraffin Dispenser WD-4 and Cooling Plate CP-4, Kunz Instruments).
pH and viscosity measurements. The pH of fresh ileal digesta was determined using a pHmeter (704 model, Metrohm) immediately upon collection. For viscosity measurement, diets and ileal digesta were diluted (1:1) with distilled water and homogenized for 20 min at room temperature before centrifugation at 12,000 x g for 8 min (model J2–21, Beckman Instruments). The viscosity of the supernatant (8 mL) from diets and digesta was measured at 25°C using a viscometer with coaxial cylinders and a mobile rotor of diameter 40.2 mm and height 60 mm (Rheomat Haake RV2). Viscosity was measured at a shear rate of 60 s–1 as recommended (13).
Chemical analysis. Diets and ileal digesta were analyzed as follows. Dry matter was determined by drying at +105°C to constant weight, and ash by incineration at +550°C for 16 h. Nitrogen content was measured with an elementary analyzer according to the Dumas method (Leco FP 428 analyzer, Leco) and data were expressed on a crude protein basis using 6.25 as a conversion factor. Chromium was estimated according to the method of Siddons et al. (16) slightly modified by Lallès and Poncet (17). Crude mucin content was determined by an ethanol precipitation method (18,19). The concentrations of mucin and chromium in the digesta were used to calculate mucin output at the ileum.
Intestinal goblet cell histochemistry. Serial sections of tissue (5 µm thick) were cut perpendicular to the axis of the intestine samples embedded in paraffin using a microtome (RM2145, Leica Microsystems SA). Sections were stained with periodic acid-Schiff reaction for neutral mucin, Alcian blue 8 GX at pH 2.5 for acid mucin, high-iron-diamine reaction without prior oxidation for sulfomucin (with a slight modification: 40 instead of 10% FeCl3), and with a combined staining of Alcian blue 8 GX at pH 2.5 and periodic acid-Schiff reaction for total mucin. All sections were stained in 1 batch to minimize differences in technical manipulations. For each staining, the histological slides were coded and examined without knowledge of origin for quantification.
Mucin-containing cells in ileal tissues were counted in 20 full-length villi and crypts, using an optical microscope (Eclipse E400), a camera (Digital camera DXM1200, Nikon), and an image analyzer (Lucia software) (20). The values obtained were averaged per villi and crypts for each tissue sample. The villous height and crypt depth were measured in the same way.
Digesta flow and digestibility calculations. The ileal flow of DM in g/d was calculated individually by measuring the dilution factor of the indigestible marker as explained previously (21). The ileal flow of other constituents including organic matter, crude protein, minerals, and mucin and ileal apparent digestibility of dietary constituents were calculated as presented previously (21).
Statistical analysis. The variance homogeneity of the data was assessed by the F test using Statview (22). Data were analyzed using the General Linear Models procedure of SAS (23). The effect of replication was tested using the residual variation between pairs as error. Diet and diet x replication effects were tested using residual variation within pairs as the error term. The effects of covariates on mucin ileal concentration and output also were tested according to the General Linear Models procedure. When the slopes of regression did not differ between diets, differences in mucin output were estimated as the differences in elevation of 2 parallel regression lines (adjusted means). When neither the slope of regression nor the elevation differed, data from the 2 diets were pooled and a single regression line was determined. Student’s t test was used for comparisons of adjusted least square means (LSMeans). Values are presented as LSMeans ± SEM. Differences were declared significant at P < 0.05.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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56% higher (P < 0.05) in piglets fed the CMC diet than in those fed the control diet regardless of the total DM output value (Fig. 1).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Influence of high-viscosity CMC diet on ileal goblet cell numbers. The major result of the present study was the ileal goblet cell expansion observed with the addition of high-viscosity CMC. Evidence for variations in goblet cell numbers in the small intestine have already been shown with fiber feeding. When rats were fed a wheat bran–based diet, for example, the villi contained more goblet cells (26). In broiler chickens, the addition of methylated citrus pectin increased the number of goblet cells/villus (27). The increase in number of goblet cells in the small intestinal villi may potentially increase the mucin secretion capacity of the mucosa. This hypothesis is supported by the concomitant increase in the ileal flow of mucin, as shown here.
The observed goblet cell expansion raises the interesting question of the underlying cellular mechanisms. Earlier studies with rabbits demonstrated a proliferative zone at or near the crypt basis in the cecum and proximal colon (28), as in the small intestine, whereas these populations of proliferating cells exist at multiple levels in the crypt column of the distal colon (29). It was also shown that in the cecum and proximal colon, epithelial cells migrate toward the luminal surface epithelium in 3 d, whereas goblet cell turnover rate would take 5–6 wk (28). In a neonatal piglet model of total parenteral nutrition, an increase in goblet cell densities in the small intestine was also documented recently (30). It was hypothesized that this represented a primary defense triggered by (reduced) epithelial cell renewal to prevent intestinal barrier failure. The actual mechanisms of clonal expansion of goblet cell progenitors or reduced turnover/migration rate are still unknown. In the present study, goblet cell expansion in ileal tissues of piglets fed the CMC diet was not associated with alterations in small intestinal morphology. This would suggest that changes in epithelial cell renewal were not the cause for increased goblet cell densities. Thus, it is possible that CMC directly modulated goblet cell migration rates. Although an indirect effect through changes in the intestinal microflora cannot be excluded, our limited microbiology data do not support this possibility.
Role of the intestinal microflora in intestinal goblet cell expansion. Studies carried out with highly viscous compounds in broiler chicks demonstrated the influence of viscosity on the gut microflora and the implication of the flora in small intestinal alterations after an increase in intestinal content viscosity. Chicken fed a diet containing a high-viscosity CMC displayed a lower level of ileal digesta pH together with increased numbers of total anaerobes, Escherichia coli, Lactobacilli, and Bacteroides in the contents of duodenum plus jejunum (without significant changes in the ileum) (14). In a second study with citrus pectins differing in their degree of methylation, the decreased digestibility of dietary components was shown to be associated with increased counts of Enterococci, Bacteroidaceae, Clostridia, and E. coli with the high-methylated citrus pectin (27). Interestingly, there was also an increased density of goblet cells in the ileal tissues of the birds fed either of the methylated citrus pectins, whereas alteration in ileal morphology was present only with the high-methylated compound (27). Finally, no change in the percentages of sialo- vs. sulfo-mucin positive goblet cells was noted (27). A more recent study demonstrated unequivocally the role played by the gut flora on both digesta viscosity and intestinal morphology alterations (31). The increase in digesta viscosity and the reduction in ileal digesta pH following high-methylated citrus pectin consumption were more pronounced in conventional than in germ-free birds. In addition, the intestinal architecture was affected only in conventional birds. Here, we did not study the intestinal microflora extensively, but fecal counts of aerobes and E. coli did not differ between the control and CMC piglets (data not shown), nor did ileal digesta pH or morphology. Dietary component digestibility was also not affected. Conversely, goblet cell density in ileal villi was higher in total, and for acidic and acidic-sulfated mucin-containing cells in piglets fed the CMC diet. Taken together, our results suggest a direct influence of CMC on ileal goblet cell dynamics. The reason why this effect was not observed in the proximal colon (data not shown) remains unclear.
Intestinal mucin sulfation. Sulfation of mucin is considered to be an indicator of mucin maturity and is associated with increased protection of the intestinal epithelium. Sulfomucin can increase intestinal resistance to attacks by bacteria and proteases (32,33). Conversely, reduced mucin sulfation is closely correlated with colitis in humans (34) and interleukin-10–deficient mice models (35). The composition of mucin is, therefore, a key factor in the resistance of mucosa to bacterial infection and has an influence on the gut bacterial colonization (36). In a study of chicks fed viscous high-methylated citrus pectin, the authors did not demonstrate a shift toward increased intestinal mucin sulfation (27). By contrast, our piglets fed high-viscosity CMC displayed more sulfated mucin-containing cells in the intestine. This was also observed in the jejunum of rats fed a diet containing cereal fiber compared with cellulose (7). Our results suggest that CMC might increase intestinal epithelial protection in young piglets after weaning. This hypothesis is at variance with Australian studies in which CMC was detrimental to small intestinal architecture and function (13,37). This discrepancy could be explained by differences in environmental conditions, diet composition, and possibly porcine breeds.
Links between intestinal goblet cells and luminal mucin. In the present study, we found increases in both the number of goblet cells per villi in ileal tissues (+25%) and the ileal flow of mucin (+59%) in piglets fed the CMC diet compared with the control. However, no significant relation existed between these 2 variables. This is not totally surprising because the ileal flow of mucin provides information on the net output of the nondigested fraction of mucin produced in the stomach and along the small intestine (38), whereas goblet cell histology here provides an image of a limited area of the distal small intestine. In addition to cell numbers, some authors have considered goblet cell size to be an indicator of the goblet cell secretory capacity. It was shown that conventional, compared with germ-free, BALB/c mice displayed small intestinal goblet cells with a doubled size, in addition to a higher goblet cell tissue density (39). Also, various types of fiber sources, including oat bran, rye bran, and soybean hull increased both goblet cell numbers and volumes in the small intestine of golden hamsters (40). Unfortunately, no study reported any data related to the intestinal flow of mucin along the small intestine. We did not actually measure intestinal goblet cell size in the present work.
Dietary influence on intestinal flow of crude mucin.
A significant increase in ileal crude mucin concentration and output was shown in this work. Several studies in monogastric animals revealed that some dietary fibers increase the output of mucin at the terminal ileum. In rats, the concentration of lumenal immunoreactive mucin detected by ELISA was 350 and 200% higher in the stomach and small intestine, respectively, with the addition of 5% citrus fiber in the diet compared with a fiber-free diet (6). When increasing amounts of pea fiber were added to pig diets, there was a trend toward a linear increase in ileal crude mucin output with increasing pea fiber consumption (19). Also, ileal glucosamine and galactosamine excretion increased continuously with fiber intake in growing pigs fed a protein-free diet (8,9).
A significant regression within diets of DM on mucin ileal outputs also was shown. This suggests that when the DM output increased, the mucin output also increased. But our results showed that the mucin output was higher in CMC-fed piglets than in those fed the control diet regardless of ileal DM output. We found a higher viscosity of ileal digesta in CMC-fed piglets than in those fed the control diet. However, there was a linear relation between the duodenal, but not the ileal flow of endogenous nitrogen and the viscosity of duodenal digesta in growing pigs (11). Similarly, despite the large variation in viscosity in pigs fed the CMC diet, there was no correlation with mucin output within this group. Nevertheless, a significant although low correlation (R2 = 0.91, P = 0.0026, n = 22) could be calculated between viscosity and mucin output when data from the 2 diets were pooled.
The mechanism by which CMC or the viscosity could modify mucin characteristics is not well understood. It is possible that CMC acts by direct physicochemical interactions with mucin because a rheological synergism between the 2 polymers was documented (41). Alternatively, the "mechanical action" hypothesis that an increase in the bulk of digesta may affect the mucous layer by stretching the intestinal mucosa is not supported here because the difference in the weight of fresh digesta in the ileum was not significant. However, we speculate that even without a difference in total ileal contents, differential stretching forces may affect the mucosa due to discontinuous passage of digesta.
Effect of high viscosity CMC diet on ileal digestibility in weaned piglets. The present results revealed no effect on the ileal apparent digestibility of DM, organic matter, nitrogen, and minerals. This is in agreement with a recent study (11) using diets based on cornstarch and soybean protein isolate; the CMC diet contained 2% high viscosity CMC. Digestibility values at the ileum in that study were very close to our data. The lack of effects of CMC on diet digestibility may also be explained by the high digestibility of the semisynthetic diets used. Interestingly, the authors reported a 47% increase in the duodenal flow of nitrogen, suggesting effects of CMC on stomach emptying. Differences in the ileal flow of nitrogen were not significant between the piglets fed the control and CMC diets, but the amount of endogenous nitrogen was increased by 12% in piglets fed CMC. This would fit with an increase in the ileal flow of mucin in our study. A number of studies in broilers and rats demonstrated a reduction of the nutrient digestibility (27,42,43) and absorption of minerals (44) from the gastrointestinal tract in the case of digesta with high viscosity. In pigs, Schulze et al. (45) observed a linear decrease in DM, nitrogen, and ash apparent ileal digestibility when increasing amounts of neutral detergent fiber from wheat were added to diet. However, the effect of the viscous nature of dietary fiber is conflicting. When different levels of CMC were tested in rats, there was no evidence of any effect on apparent ileal nitrogen or amino acid digestibility (46).
In conclusion, dietary CMC drastically increased the viscosity of ileal digesta without modification of nutrient digestibility in weaned piglets. However, crude mucin concentration and output were higher at the ileum in CMC-fed piglets than in those fed the control diet. Increases in ileal goblet cell numbers in villi and increases in goblet cells with acidic and acidic sulfated mucins were also observed. Further work is required to highlight the cellular mechanisms involved in this goblet cell expansion and the respective roles of CMC itself and of the intestinal microflora.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: CMC, carboxymethylcellulose; DM, dry matter; DMI, dry matter intake.
Manuscript received 6 July 2004. Initial review completed 26 August 2004. Revision accepted 6 October 2004.
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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M. Lessard, G. Boudry, B. Seve, I. P. Oswald, and J.-P. Lalles Intestinal Physiology and Peptidase Activity in Male Pigs Are Modulated by Consumption of Corn Culture Extracts Containing Fumonisins J. Nutr., July 1, 2009; 139(7): 1303 - 1307. [Abstract] [Full Text] [PDF]
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T. Morita, H. Tanabe, H. Ito, S. Yuto, T. Matsubara, T. Matsuda, K. Sugiyama, and S. Kiriyama Increased Luminal Mucin Does Not Disturb Glucose or Ovalbumin Absorption in Rats Fed Insoluble Dietary Fiber J. Nutr., October 1, 2006; 136(10): 2486 - 2491. [Abstract] [Full Text] [PDF]
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