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Laboratory of Animal Nutrition, Faculty of Agriculture, Okayama University, Tsushimanaka 1–1-1, Okayama, 700-8530 Japan and * Department of Basic Sciences, Ishinomaki Senshu University, Ishinomaki, 986-8580 Japan
3To whom correspondence should be addressed. E-mail: takashi_sakata{at}nifty.com.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • viscosity • cecum • large particles • pigs • yield stress
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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–4
). The viscosity of intestinal contents has been measured only after the removal of solid particles by centrifugation (5
,6
), under the assumption that particles or insoluble fibers in the diet do not affect the viscosity of gut contents (7
). However, the complete removal of solid particles considerably reduced the coefficient of viscosity of pig cecal contents and changed the contents from a non-Newtonian to a Newtonian fluid in our recent study (8
). In other words, solid particles elevate the viscosity of gut contents and are responsible for their basic rheological characteristics, suggesting the considerable contribution of solid particles to the viscoelastic property of gut contents. Sources of such particles would be the diet, host epithelial cells and gut bacteria. However, we do not know whether large particles (>1 mm in size) mainly of dietary origin or small particles such as bacteria and finely ground dietary particles provide the basic viscoelastic character to gut contents. Accordingly, the purpose of the present study was to examine the contribution of large solid particles, the major fraction of solid particles in the gut, to the viscoelastic properties of gut contents by measuring such properties after the removal and readdition of different levels of large solid particles to pig cecal contents. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We collected cecal contents of commercially produced pigs slaughtered by bleeding after electric shock and inspected by veterinary officers at a local slaughterhouse (Senpoku Meat Center, Yoneyama-machi, Miyagi, Japan) under strict monitoring by a local authority. The pigs were for commercial meat production and were not killed for the present study.
Within 5 min of slaughtering, we sampled 
2000 mL of cecal contents each time from 8 to 12 healthy pigs weighing 110 kg and fed commercial diets for growing pigs. Pigs were deprived of food overnight before slaughtering. The cecal contents were filtered through two layers of surgical gauze (1 mm mesh size) to remove large particles from the filtrate but not the fine particles such as bacteria and finely ground dietary particles. Then, we reconstructed the cecal contents by returning the all (100%), one half (50%) or none (0%) of the original wet weight of large particles to the filtrate. The reconstructed cecal contents with 100, 50 or 0% of the original weight of large particles included 13.4 ± 7.4, 6.4 ± 3.1 or 0.0 ± 0.0% (mean ± SD, wet mass basis) of large particles in the total contents, respectively.
We measured the dry matter content of samples and that of large particles as the weight difference before and after drying the cecal contents in a vacuum desiccator (IUCHI, Osaka, Japan) at 600 mm Hg at room temperature for 72 h. The content of large particles was calculated by subtracting the mass of dry matter of each sample from that of pig cecal contents without large particles.
We measured the viscosity of the reconstructed cecal contents as described below, based on the law of Hagen-Poiseuill (2
), at 37 ± 1°C assuming that the contents were incompressible. We employed a self-made tube-flow viscometer using glass tubes for this purpose (8
) (Fig. 1
).
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). Therefore, we measured the coefficient of viscosity at various shear rates. For this purpose, we set various levels of pressure drop to obtain different shear rates. We controlled the pressure drop by changing the difference in height between the upper level of cecal contents in the reservoir and the lower exit of the glass tube. Although the viscosity theoretically is not affected by the inner diameter of the glass tube (2
), we chose the inner diameter for measuring the viscosity of gut contents so that the gut contents would not form a plug in the glass tube or slip on the wall of the glass tube, but would fill in the glass tube. Diameter of glass tubes and the difference in height.
We used a glass tube of 10 mm i.d. and 1.0 m length to measure the viscosity of cecal contents with 100 or 50% original large particles. We set the difference in height at 0.30, 0.50, 0.60 or 0.70 m, or at 0.18, 0.23, 0.28 or 0.33 m to measure the viscosity of cecal contents with 100 or 50% original large particles, respectively. We used a glass tube of 4.0 mm i.d. and 1.0 m length and set the difference in height at 0.40, 0.60, 0.80 or 1.0 m for the contents without large particles.
Measurement of the density of contents and calculation of pressure drop.
We measured the volume and weight of cecal contents at 37°C after each series of viscometry to calculate their densities and pressure drops.
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Calculation of viscosity, shear stress and shear rate.
We calculated shear stress, shear rate and coefficient of viscosity as follows (3
):
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where N was the slope of the least-square linear regression equation between log[pressure drop (Pa)] (dependent variable) and log[10-3 ·volume flow rate (L · s-1)] (independent variable).
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Viscosities of fluids such as suspensions and viscous fluids depend on their flow rates (9
). The local flow rate shows a velocity gradient in the flow (9
). This velocity gradient is defined as shear rate. Generally, high flow rate accompanies high shear rate in the flow through a tube (9
). Shear stress is the pressure that makes a fluid move and is expressed as force per unit area (9
).
Results were expressed as means ± SD, n = 3, unless stated otherwise. The coefficient of viscosity of cecal contents did not differ among replications (P > 0.8) in our recent study (8
). We therefore calculated the above regression equations using data pooled for three replicates.
The relationship between shear stress and shear rate, or that between the coefficient of viscosity and shear rate was analyzed by linear and power regression analysis, respectively (10
). We calculated the constants of the power regression equations between the coefficient of viscosity and shear rate, and the slope and y-intercept of the linear regression equation between shear stress and shear rate both after jackknife resampling (11
). The relationship between the large-particle content (independent variables) and the constants of power or linear equations (dependent variables) was analyzed using general linear models (SAS system, SAS Institute Japan, Tokyo, Japan) after log-transformation of data.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The pressure drops used to measure the viscosity of reconstructed cecal contents with 100 or 50% original large particles were 3900, 5900, 7900 and 9800 Pa, or 1900, 2400, 2800 and 3300 Pa, respectively. The pressure drops used to measure the viscosity of cecal contents with 0% large particles were 3100, 5100, 6100 and 7100 Pa.
We calculated the coefficients of viscosity of the above samples over wide ranges of shear rate. The coefficient of viscosity and shear rate of the cecal contents showed negative power correlation in all samples (P < 0.01 by power regression analysis; Fig. 2
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The linear regression equation relating shear stress and shear rate of the fully reconstructed cecal contents in the present study (Fig. 4)
was similar to that of intact cecal contents in our previous study [y = (0.13 ± 0.01)x + (11 ± 1)] (8
), because no materials except for a small amount of absorbed water in the surgical gauze were subtracted. Thus, reconstructed cecal contents with 100% original large-particle content in the present study should have represented intact cecal contents. At the same time, this would support the reproducibility of viscosity measurements using the present method.
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60% [ (22 - 8.7)/22 x 100] of the total dry mass in the contents.
The coefficient of viscosity of the cecal contents was not constant and depended on their shear rate in all three samples (Fig. 2)
. Such a dependency is typical of non-Newtonian fluids (12
), consistent with our previous results using intact pig cecal contents (8
). In other words, the viscosity of cecal contents should decrease with an increase in flow rate of cecal contents, irrespective of large particle content. Non-Newtonian fluids include emulsions, paints, pulps, molten chocolate and blood (3
,9
,13
), all of which are suspensions of particles in the fluid. The significant power regression for all samples between the coefficient of viscosity and shear rate (Fig. 2)
indicated that cecal contents were very viscous at low flow rates.
The constant (a) of the power regression equation (y = a · xb) between the coefficient of viscosity (y) and shear rate (x) increased with an increase in large particle content (P < 0.01; Fig. 3
). The constant (a) (Pa · s) is a parameter proportional to the viscosity of power law fluids. The viscosity and shear rate of a power law fluid can be described with a power equation (14
). Therefore, the addition of large particles should have elevated the coefficient of viscosity of cecal contents over a wide range of shear rates, as in studies using non-Newtonian fluids other than gut contents (15
–18
). In other words, the viscosity of the cecal contents should increase with an increase in large particle content at any flow rate that can be found in the large intestine.
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). The exponent (b) indicates flow properties of the power law fluid (19
). Therefore, we conclude that the content of large particles did not alter the basic flow behavior of pig cecal contents as a non-Newtonian fluid.
The plot of shear stress (ordinate) vs. shear rate (abscissa) represents the viscous properties of a fluid (9
). Shear stress and shear rate of the cecal contents showed a positive linear correlation in all samples (P < 0.05 by linear regression analysis; Fig. 4
). The shear stress of the cecal contents positively and linearly correlated with shear rate, and had a positive value when we extrapolated the regression line to a shear rate of zero (Fig. 4)
. These are characteristic properties of a Bingham plastic (3
) and agree with our previous study using intact pig cecal contents (8
). Bingham plastic shows the linear relationship between shear stress and shear rate, and has the restoring force for strain, elasticity, at low shear stress below the y-intercept of the regression equation between shear stress and shear rate (3
).
This was the case even for the contents without large particles (Fig. 4)
. Accordingly, the Bingham plastic nature of pig cecal contents should be independent of the large particle content. Interestingly, the complete removal of solid particles by centrifugation made the cecal contents into a typical Newtonian fluid (no influence of shear rate on the coefficient of viscosity) without any characteristics of a Bingham plastic (8
). A Newtonian fluid should move in the intestine even at very low shear stress, i.e., with very little pressure. Accordingly, we conclude that fine particles, including bacteria and fine dietary particles, but not large particles of mainly dietary origin, are responsible for the basic viscoelastic properties of pig cecal contents.
It may be too early to conclude that the present samples as well as intact pig cecal contents (8
) were typical Bingham plastics because we did not measure the shear stress at a shear rate below 1 s-1 in either study. Therefore, these fluids may behave as yield-pseudo plastics (12
). A yield-pseudo plastic is a fluid for which shear stress becomes very small at a shear rate below 1 s-1, and has a lower yield stress than Bingham plastics (12
). If pig cecal contents are a yield-pseudo plastic, the shear stress for pig cecal contents at very low shear rate should be far lower than the above-mentioned values.
The y-intercept of the linear regression equation between shear stress and shear rate (Fig. 4)
is called the "yield stress for Bingham plastic" (3
), which is the critical pressure point between the flowing and the immovable state of a Bingham plastic. Bingham plastics behave as a solid when the shear stress is smaller than the yield stress and behave as a fluid when the shear stress is above the yield stress (3
). We adopted this parameter as an alternative measure for the ease of moving pig cecal contents because it is difficult to measure the yield stress for a yield-pseudo plastic.
The slope and y-intercept of the linear regression equation (Fig. 4)
positively correlated with the large particle content linearly and quadratically, respectively (P < 0.01; Fig. 5
). In other words, large particles elevated the "yield stress for Bingham plastic" of the cecal contents quadratically (Fig. 5)
. This suggests that the stress required to move the cecal contents increases drastically as the large particle content increases. If cecal contents are yield-pseudo plastic, the true yield stress should be less than the yield stress for Bingham plastic. However, we assume that the yield stress of the present samples should increase by the addition of large particles, even if they are yield-pseudo plastics. Therefore, the contracting force of the intestine to squeeze cecal contents should increase considerably with a modest increase in the content of large particles. The ingestion of solid particles, especially indigestible particles, should make it more difficult to move and to mix digesta. A modest change in fluid absorption or fluid secretion in the gut can also have a considerable effect on the ease of mixing or squeezing gut contents.
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). The shear stress of yield-pseudo plastics should be greater than that of Bingham plastic and lower than that of Newtonian fluids at a low shear rate, which should be found at very slow flow rates in the intestine. Accordingly, the required pressure difference along the intestine at low shear rate should be in the order of Bingham plastics > yield-pseudo plastics > Newtonian fluids. As we discussed above, large particles should elevate the yield stress even when cecal contents are yield-pseudo plastic. On the other hand, the lack of large particles in cecal contents should considerably reduce the yield stress to make the contents flow easily. This may explain why the movement of diarrheic large bowel contents is entirely different from that of normal stools.
Nutritional importance of large particles.
Large particles elevated the viscosity of cecal contents (Figs. 2
, 4)
. It is likely that large particles would elevate the viscosity of small intestinal contents, which also comprise a suspension of particles of various sizes. Large particles in cecal contents originate mainly from insoluble dietary fibers after autoenzymic digestion. Accordingly, insoluble dietary fibers should make the gut contents more "solid," more viscous, harder to move and harder to mix. This should also be the case in the small intestine because the effect of large particles on the viscosity and yield stress depends on the large particle content over a wide range. There is no reason to exclude a similar contribution of digestible solid particles before they are solubilized by digestion. This again emphasizes the importance of solid food particles in the regulation of digestion and absorption of nutrients in the small intestine. It is also probable that solid particles in small intestinal contents affect the ease of squeezing contents in the small intestine and thereby modify motility.
Considering that high viscosity generally depresses the diffusion of substances in a fluid (1
), insoluble dietary fibers should reduce the diffusion of nutrients and enzymes in gut contents. The diffusion rate of a nutrient in the gut contents should correlate positively with the reaction rate (20
) and should be positively associated with the rate of nutrient approach to the intestinal mucosa. Therefore, insoluble dietary fibers should retard the digestion and absorption in both the small and large intestine, not only by the dilution or adsorption effects (21
) but also by increasing the viscosity of the gut contents as we demonstrated in the present study. The small intestinal contents are also suspensions of dietary particles of various particle sizes. This should be taken into account when we plan to add "inert bulk" such as cellulose or plastic particles into experimental diets because they may not be entirely inert.
Results of the present and our previous (8
) studies strongly suggest that both fermentable and nonfermentable indigestible food components affect the microbial metabolism in the large intestine by changing the viscosity of the gut contents through the provision of large particles of dietary origin and by stimulating bacterial proliferation and thereby increasing the number of fine particles.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by a grant from the Iijima Memorial Foundation for the Promotion of Food Sciences and Technology and a grant from the Ministry of Education and Science (no. 13878019, 2001).
Manuscript received 5 April 2001. Initial review completed 7 July 2001. Revision accepted 11 February 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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