< back to Home page    CD Table of Contents    References

        THE DIGESTIVE SYSTEM OF VERTEBRATES: CD 

---

10. Secretion and absorption of electrolytes and water: 

Introduction:

The salivary glands, pancreas, biliary system, and gastrointestinal tract secrete large quantities of electrolytes and water, which aid in the passage of digesta through the digestive tract and provide the pH necessary for the activation of endogenous enzymes and the maintenance of its indigenous microbes. The electrolytes consist mainly of the cations Na⁺, K⁺, and H⁺, and the anions Cl^- and  HCO₃^-, and their secretion results in the passive diffusion of water into the digestive tract. The daily secretions of electrolytes and water are equivalent to about 30 to 40% of those  present in the extracellular fluid of humans and a much higher percentage in the herbivores (Table 10.1). Most of these secretions must be reabsorbed to prevent rapid dehydration and major disturbances in the electrolyte/water and acid/base balance of body fluids. Much of the energy consumed by the digestive system is utilized for the secretion and reabsorption of these electrolytes. The mechanisms involved in the secretion and absorption of electrolytes by the mammalian digestive system are reviewed in Physiology of the Gastrointestinal Tract, 3rd edition, Volume 2, Section 3 (ed. Johnson et al. 1994). The following discussion is confined mainly to the integrative and comparative physiology of electrolyte secretion and recovery.

Table 10.1.

Values for human are estimates for an individual starved 24 hours prior to measurements (Soergal & Hofmann 1972). Other values are means for sheep (Denton 1957, Harrison 1962, Hill 1965, Kay 1960, Kay & Pfeffer 1970, Magee 1961, Taylor 1962), and means for ponies (Alexander & Hickson 1970, Argenzio et al. 1974a) (from Stevens and Hume 1995)


Body Fluid Compartments:

About 70% of the weight of most vertebrates is comprised of the water distributed in the intracellular, extracellular (plasma and interstitial) and transcellular (alimentary tract, urine, synovial fluid, aqueous humor) compartments of the body. The distribution of water between the extracellular and intracellular compartments is similar in all species. However, the quantity in gut contents ranges from a small percentage of the body water of most carnivores, to about 2 to 4% in humans, and almost 30% of the body water of herbivores such as sheep (Table 10.2). 

Table 10.2.

(Stevens & Hume 1995)


Body Fluid Compartments - Intracellular and extracellular compartments:

The electrolyte concentrations and pH of intracellular and extracellular fluids are maintained at relatively constant but very different levels (Fig. 10.1). The principal cations in cellular contents are K⁺ and much smaller concentrations of Mg⁺⁺, and Na⁺. The  principal anions are organic   phosphates and proteins, with much smaller concentrations of HCO₃^-. The principal electrolytes in the extracellular fluid are Na⁺, Cl^-, and HCO₃^-, with much lower levels of K⁺. Extracellular fluid has a higher pH than the cell contents, but a similar osmotic activity. The high concentrations of  Na⁺ and Cl^- in extracellular fluid have been attributed to the origin of unicellular animals in a bathing solution of sea water that has increased its salinity and osmotic activity since that time.


Figure 10.1.  Electrolyte composition of extracellular and intracellular fluid compartments of humans. (Modified from Guyton 1986)


The differences between the electrolyte composition of intra- and extracellular fluids can be attributed largely to the active transport of Na⁺ out of the cells. Although the outer membranes of body cells are relatively impermeable to the passive diffusion of Na⁺, it is actively transported out of the cell by a Na⁺, K⁺-ATPase membrane carrier that exchanges three Na⁺ ions for 2 K⁺ ions, which can passively diffuse across back the membrane. This is responsible for most of the electrical potential gradient (inside negative) across the cellular membrane. The intracellular and extracellular concentrations of  K⁺, H⁺, Cl^-, and HCO₃^- are determined mainly by their ability to permeate the membrane and the transmembrane electrical potential gradient. 

The electrolyte composition and osmolality of extracellular fluid are controlled largely by the kidneys. Freshwater fish maintain this equilibrium by eliminating excess water by glomerular filtration of plasma and reabsorption of electrolytes by the renal tubules (Smith 1943). Marine fish drink sea water, which has an osmolality and NaCl content three times that of the body fluids of most vertebrates (Gamble 1954). The absence or intermittent function of glomerulus filtration reduces the renal excretion of water by marine fish, and excess Na⁺ and Cl^- are actively excreted by their gills and by salt glands in the rectum of some elasmobranches and the marine catfish (van Lennep and Lanzing 1967). However, the body fluids of marine hagfish, sharks, rays, coelocanths, and the marine frog Rana cancrivora are either isotonic or hypertonic to sea water (Bentley 1982) due to the retention of urea (Fig. 10.2).

The urea serum levels of marine elasmobranches ranged from 209 to 453 mmoles/l, as compared to 81 to 180 mmoles/l for the euryhaline species (which can adapt to a wide range of salinities), and 1 to 2 mmoles/l for freshwater fish (Griffiths et al 1973). Movement of euryhaline fish, such as eels and flounder, from freshwater to sea water is accompanied by replacing the stratified squamous epithelium that lines their esophagus with a columnar epithelium, which absorbs Na⁺ and Cl^-, and reduces the osmolality of gastric contents. (Hirano and Mayer-Gostan 1976; Yamamoto and Hirano 1978; Parmelee and Renfro 1983).   


Figure 10.2.  Osmotic regulation in a typical elasmobranch, the dogfish shark (Squalus acanthias). Values for NaCl, Na⁺, Cl^- and urea are given in mM or mEq per liter.  Osmotic pressures (OP) of sea water (SW), body fluids and  urine are given in mOsmoles per liter. (Modified from Kormanik 1992)


Terrestrial animals need to conserve Na⁺, Cl^-, and water. The kidneys of amphibians, reptiles and most birds are relatively limited in their ability to concentrate urine, and urinary electrolytes and water are also reabsorbed from their cloaca or hindgut (Fig. 4.5). Minnich (1970) concluded that much of the urinary electrolytes and water of desert iguanas was absorbed from the cloaca. However, the hindgut plays a major role in a number of snakes (Junqueira et al. 1966) and most birds (Skadhauge 1993). In most eutherian mammals the urinary and digestive system exit the body separately and the kidneys are much more efficient in their ability to concentrate urine, but the hindgut retains the responsibility for the final recovery of electrolytes and water secreted into the digestive tract.


Figure 4.5.  Adaptations of the nephron and hindgut in relation to habitat The nephrons of fish, amphibians, reptiles, and birds are limited in their ability to concentrate urine. Urine is excreted into the cloaca of amphibians, reptiles, and birds and refluxed into the hindgut, which aids in the recovery of electrolytes and water from the urine and digesta. Microbial digestion of uric acid also aids in the conservation of nitrogen. The majority of mammals excrete their digesta and urine separately. Recovery of urinary electrolytes is aided by the kidney’s loop of Henle. Nitrogen conservation is aided by diffusion of urea into the intestine where it is digested by hindgut microbes into ammonia and absorbed. (Modified from Smith 1943 by Stevens 1977)


Body Fluid Compartments - Gut contents:

The osmolality, electrolyte composition, and pH of gut contents vary among segments of the gastrointestinal tract and with time after feeding. Figure 10.3 shows the mean osmolality and electrolyte composition of digesta along the gastrointestinal tract of a pony, obtained from four measurements over a 12 hour period between meals. The higher osmotic activity of gastric contents is due to the release of electrolytes and other osmotically active particles from food. This is rapidly reduced to the osmolality of extracellular fluids by diffusion of water across the more permeable intestinal epithelium. The concentration of individual electrolytes in gut contents is determined by their concentrations in the food and salivary, pancreatic, biliary and gastrointestinal secretions, the rate SCFA production, and the relative rate that electrolytes and water are absorbed from the gastrointestinal tract.


Figure 10.3.  Mean digesta osmolality and concentrations of the major electrolytes along the gastrointestinal tract of the pony obtained from four measurements over a 12-h period after a meal. Segments represent the stomach (S), three equal segments of the small intestine (SI), the cecum (C), and the ventral (VC), dorsal (DC) and small (SC) colon. Hydrogen was omitted, because it is only a small component (1 mEq/L) of the cations, even in gastric contents. Concentrations of PO₄^-- were calculated on the basis of a pKa of 6.8 for NaH₂PO₄ and the mean pH of digesta in each segment.  The principal organic acids (OA) are SCFA and lactic acid. At the pH of intestinal contents, ammonia, SCFA and lactic acid exist principally in their ionized form. Concentrations of HCO₃^- were calculated as the difference in concentration of measured cations and anions. (Modified from Argenzio 1975)


The pH of digesta also varies among segments of the gastrointestinal tract and with time after feeding. The pH of digesta along the gastrointestinal tract of dogs, pigs, and ponies 2, 4, 8, and 12 hours after a meal is shown in Figure 10.4a, b, c. The pH of gastric contents showed the greatest variation with time after feeding due to secretion of HCl. Although the contents of the small and large intestine were maintained at a higher and more constant pH, this also varied among segments and with time after feeding.


Figure 10.4a.  Mean (+/- SE) values for digesta pH in the gastrointestinal tract of dogs 2 hours (closed triangle), 4 hours (open circle), 8 hours (x), and 12 hours (closed circle) after a meal. The segments of the tract are the cranial (S1) and caudal (S2) halves of the stomach, equal succeeding segments of small intestine (SI1, SI2, SI3), the cecum (Ce), and equal lengths of succeeding segments of colon (C1, C2).  (From Banta et al. 1979)



Figure 10.4b.  Mean (+/- SE) values for digesta pH in the gastrointestinal tract of pigs 2 hours (closed triangle), 4 hours (open circle), 8 hours (x), and 12 hours (closed circle) after a meal. The segments of the tract are the cranial (S1) and caudal (S2) halves of the stomach, equal succeeding segments of small intestine (SI1, SI2), the cecum (Ce), and equal lengths of succeeding segments of colon (PC, CCp, CCa, TC), plus the rectum (R). (Argenzio and Southworth 1974)



Figure 10.4c.  Mean (+/- SE) values for digesta pH in the gastrointestinal tract of ponies 2 hours (closed triangle), 4 hours (open circle), 8 hours (x), and 12 hours (closed circle) after a meal. The segments of the tract are the cranial (S1) and caudal (S2) halves of the stomach, equal succeeding segments of small intestine (SI1, SI2, SI3), the cecum (Ce), and equal lengths of succeeding segments of colon (RVC, LVC, LDC, RDC, SC1, SC2). (Argenzio et al. 1974a)


Electrolyte Transport Mechanisms:

The mechanisms of electrolyte transport across the epithelial cells lining the salivary glands, exocrine pancreatic glands, biliary system, and gastrointestinal tract are both numerous and complex. They can be transported across the opposing membranes of these cells by passive diffusion or by carrier-mediated mechanisms that are highly selective for a given ion species. The membrane carriers can transport an ion by itself, in cotransport with other ions or organic solutes, or in exchange for another ion species. The net transport of ions across these cells is due to differences in the permeabilities and transport mechanisms of their lumen and blood-facing (basolateral ) membranes. Differences in the rates of cation and anion transport set up a transepithelial electrical potential gradient. Therefore, the transport of an ion across these epithelial tissues is also dependent on its ability to permeate by passive diffusion through the intercellular junctions down its electrochemical gradient.

Electrolytes can be transported across the lumen-facing membrane of these epithelial cells by a variety of different mechanisms (Fig. 10.5).  Sodium, K⁺, Cl^-, and HCO₃^- can pass through the membranes of some cells via channels that are specifically designed for diffusion of an ion species (Fig. 10.5 A, B, C, D). They are transported across some membranes by individual carriers that exchange Na⁺ or K⁺ for H⁺, or exchange Cl^- or SCFA^- for HCO₃^- (Fig. 10.5 E, F, G, H). Sodium can also enter the midgut absorptive cells in cotransport with glucose, galactose, amino acids, or B-vitamins (Fig. 10.5 I). Cotransport of Na⁺ and Cl^- with imino and amino acids (Fig. 10.5 J) was described in the midgut of fish (Bogé et al. 1983) and rabbits (Miyamoto et al. 1989). Cotransport of Na⁺, K⁺, and 2 Cl^- (Fig. 10.5 K) was also reported in the lumen-facing membranes of the flounder midgut epithelium (Frizzell et al. 1984) and the basolateral membranes of the midgut secretory and the salivary duct cells of mammals. Rapid removal of Na⁺ from these cells by the Na⁺, K⁺- ATPase exchange pump in their basolateral membranes results in a transepithelial electrical potential gradient, with the blood-facing (basolateral) surface of these epithelial cells positive to the lumen in most vertebrates.


Figure 10.5.  Mechanisms of electrolyte transport across the lumen- or blood-facing membranes of epithelial cells lining the  gastrointestinal tract and the glandular and duct cells of salivary gland, exocrine pancreas, liver, and gallbladder. A through D demonstrate diffusion of electrolytes down their electrochemical gradient via conductance channels in the cell membrane. E through H show mechanisms for the exchange of electrolytes between cell contents and their bathing solution. The last three models show mechanisms for cotransport of electrolytes with one another or with organic solutes. (Modified from Stevens and Hume 1995)


Secretion and Absorption of Electrolytes:

The salivary glands, pancreas, biliary system, and gastrointestinal tract secrete large amounts of electrolytes and water. They are secreted continuously, even during periods of prolonged starvation. However, their rates of secretion are increased by ingestion of food and by the physical and chemical composition of food and digesta, which are monitored by receptors located along the digestive tract. Stimulation of these receptors initiates a neural and/or endocrine response that increases the rate of fluid secretion (see Section 11). Therefore, the rates of salivary, gastric, pancreatic, biliary, and intestinal secretion are associated with the passage of food and digesta through the alimentary tract, and they are higher and more constant in the more continuously-feeding herbivores. The large quantities of electrolytes and water released into the digestive tract each day cannot be completely replaced by the diet. Thus, most of these secretions must be reabsorbed. This is accomplished partly by the reabsorption of some of these secretions by the ducts of the salivary glands, pancreatic glands, and biliary system. However, most of these secretions are recovered by absorption from midgut and hindgut.


Secretion and Absorption of Electrolytes - Salivary glands:

The rate of salivary secretion is controlled mainly by the nervous system and increased by anticipation of feeding and the presence of food in the mouth. The composition and volume of salivary secretions vary among the different sets of salivary glands of a species, among different species, and with the rate of salivary secretion (Burgen 1967; Ellison 1967; Leeson 1967; Phillipson 1970; Cook et al. 1994). The parotid salivary glands generally secrete a serous (watery) fluid and electrolytes, while the submaxillary (mandibular) and sublingual glands usually secrete large amounts of mucous. The parotid glands are large in ungulates, kangaroos, beavers, manatees, and fruit bats, and approximately the same size as the submaxillary glands in the Norwegian rat. However, the submaxillary glands of insectivorous bats are larger than the parotids, and those of the giant anteater are both large and equipped with a storage bladder.

The salivary glands consist of acini (or acinotubules) and a series of ducts, that are lined with epithelial cells (Fig. 10.6). The major electrolytes in mammalian saliva are Na⁺, K⁺, Cl^-, and HCO₃^-, along with high concentrations of PO₄^{- -}  in ruminants and kangaroos. The saliva entering the oral cavity is the product of an isotonic secretion of ions by the acini of these glands adjusted by their absorption or secretion along the glandular ducts. At high rates of flow, the parotid saliva released into the mouths of humans, dogs, cats, and rats had an osmolality and a Na⁺/K⁺ ratio similar to plasma, but a higher HCO₃^-/Cl^- ratio and pH (Fig. 10.7). The Na⁺, K⁺, and Cl^- are cotransported into the acinar cell from the blood, but the HCO₃^- is produced within the these cells by hydration of CO₂ (Fig. 10.8A). The Cl^- and HCO₃^- enter the lumen via ion conductive channels. Sodium enters the lumen by diffusion down its electrochemical gradient via the extracellular space. At slower rates of flow, absorption by duct cells reduced the Na⁺/K⁺ ratio, HCO₃^-/Cl^- ratio, osmolality, and pH of the saliva that is released into the mouth.

The parotid gland of ruminants secretes much larger quantities saliva at a more continuous rate and with a different composition (Fig. 10.7B). Sheep can secrete 8-16 liters and cattle can secrete 98-190 liters of saliva per day, largely from their parotid glands (Phillipson 1970). Blair-West and coworkers (1965, 1970) showed that in the absence of stimulation the parotid saliva of sheep was isotonic to blood, with a high Na⁺/K⁺ ratio, high concentrations of HCO₃^- and PO₄^{- -}, and a high pH. Stimulation of flow rate increased the Na⁺/K⁺ and HCO₃^-/PO₄^{- -} ratios, with no change in osmolality or pH. The parotid salivary glands of camels and kangaroos appear to function in a similar manner (Engelhardt and Hőller 1982; Beal 1984, 1986). This pattern of flow provides a continuous buffer for the SCFA produced in the forestomach at the expense of the large quantities of Na⁺, HCO₃^-, and water released into the digestive tract. However, the Na⁺/K⁺ ratio of sheep saliva was reduced during sodium deficiency or following the administration of aldosterone. Furthermore, half of the 1.2 to 1.5 moles of Na⁺ that was secreted each day by the salivary glands of sheep was reabsorbed by the forestomach (Dobson 1959), and most of the HCO₃^- is titrated by SCFA and reabsorbed as CO₂, and H₂O.        


Figure 10.6.  Organization of the submaxillary gland of the rat. (from Leeson 1967)



Figure 10.7.  Concentration of major electrolytes in the saliva of humans (From Thaysen et al. 1954) and sheep (From Argenzio 1984) as a function of the rate of salivary flow.



Figure 10.8. Electrolyte transport across the acinar cells of the parotid salivary glands of humans, dogs, cats, and rats. (Modified from Cook et al. 1994)


Secretion and Absorption of Electrolytes - Stomach:

The rate of gastric secretion is under both nervous and endocrine control and influenced by the anticipation of feeding and conditions in the stomach and initial segment of the midgut. The proper gastric glands of the stomach secrete HCl and pepsinogen. Both are secreted by the same glandular cell in fish, adult amphibians, and reptiles (Stevens and Hume 1995), but the proper gastric glands of mammals contain both parietal (oxyntic) cells, which secrete HCl, and neck chief cells that secrete pepsinogen. Secretion of HCl is controlled principally by the release of the hormone gastrin from gastric epithelium in response to stimulation by nerves or the presence of end products of protein digestion in gastric contents. The mechanisms responsible for H⁺ and Cl^- secretion by the parietal cells are illustrated in Figure 10.9. Intracellular hydration of CO₂ produces H⁺, which is secreted into the lumen in exchange for K⁺, and HCO₃^-, which is exchanged for Cl^- in the blood. This results in a net loss of H⁺ and gain in HCO₃^- in the gastric blood supply. 


Figure 10.9.  A model proposed for secretion of HCl by gastric parietal cells. Intracellular production of H₂CO₃ by hydration of CO₂ produces H⁺, which is secreted into the lumen in exchange for K⁺, and HCO₃^-, which is released into the blood in exchange for Cl^-.  The lumen-facing  membrane contains conductive pathways for passive diffusion of Cl^- into the lumen. (Modified from Reenstra et al. 1987)


The surface epithelium of the proper gastric region of frogs (Flemstrőm 1977), guinea pigs (Garner and Flemstrőm 1978), and dogs (Kauffman et al. 1980) has been shown to secrete HCO₃^-. The pyloric and cardiac glandular regions of the stomach also secrete HCO₃^-. The cardiac glandular region of the pig appears to secrete HCO₃^- in exchange for Cl^- (Hőller 1970 a, b) and there is conflicting evidence for HCO₃^-/Cl^- exchange by the cardiac glandular region of the llama stomach (Eckerlin and Stevens 1973; Rübsamen and Engelhardt 1978; Engelhardt et al. 1979).

Although nonglandular, stratified squamous epithelium is found in the stomach of at least some of the species belonging to half of the mammalian orders, studies of its secretory and absorptive characteristics have been confined largely to the forestomach of ruminants. The ruminant forestomach absorbs Na⁺ in exchange for H⁺ and Cl^- in exchange for HCO₃^- (Chien and Stevens 1972; Martens and Gäbel 1988). As mentioned in the previous section, it also absorbs SCFA. A reduction in Na⁺ absorption following the replacement of SCFA with Cl^- suggests that the SCFA were absorbed partly by an SCFA^-/HCO₃^- exchange that is linked to the absorption of Na⁺ in exchange for H⁺ (Gäbel and Martens 1991, and Fig. 9.8). 


Figure 9.8. Mechanisms proposed for the transport of  SCFA transport across gut epithelium. Hydrogen ions produced by hydration of the CO₂ in the lumen or secreted by carrier-mediated Na⁺/H⁺ exchange in the lumen-facing membrane may protonate SCFA anions (Ac^-) to their undissociated form (HA_c), which passively diffuses across these membranes. The H⁺ and HCO₃^-  produced by carbonic anhydrase-catalyzed intercellular hydration of CO₂ produces both H⁺ for carrier-mediated Na⁺/H⁺ exchange and HCO₃^- for  exchanged with SCFA^- anions in the lumen.  SCFA may be transported across the basolateral membrane by either diffusion of the undissociated form or carrier-mediated exchange of SCFA^- anions with blood HCO₃^-.  (Modifications and combinations of models from Stevens et al. 1969; 1986 and Titus & Ahearn 1992.)  (From CD Chapter 9)


Secretion and Absorption of Electrolytes - Pancreas:

The rate of electrolyte secretion by the exocrine pancreas is also under neural and endocrine control and influenced by the anticipation of feeding, but the principal stimulus is the low pH of the gastric effluent that enters the proximal midgut. This initiates release of the hormone secretin, which increases the rate of pancreatic electrolyte secretion. The exocrine pancreas is an important source of fluid and buffer. The pancreas of intermittent feeders such as humans and dogs secretes chiefly during the intestinal digestive phase following a meal. Daily secretions of 2 liters were reported in humans. The Na⁺/K⁺ ratio is similar to that of extracellular fluid and the HCO₃^-/Cl^- ratio increases with an increase in the rate of flow (Fig. 10.10).


Figure 10.10.  Effects of an increase in the flow rate of the electrolyte composition of pancreatic fluid of cats. (From Argent and Case 1994)


The centroacinar cells lining the initial segment of the pancreatic ducts secrete a fluid with an osmolality and Na⁺/K⁺ ratio similar to plasma, and a much higher HCO₃^-/Cl^- ratio and pH, by mechanisms similar to those of parotid acinar cells (Fig. 10.11). This results in a net gain of H⁺ in the blood, which is opposite to and compensates for the effects of HCl secretion by gastric oxyntic cells. The more distal duct epithelial cells reduce the HCO₃^-/Cl^- ratio. However, continuous feeders, such as the herbivores, secrete much larger volumes at a more continuous rate and with a relatively constant HCO₃^-/Cl^- ratio and pH. This is especially true for horses, which can secrete 10 to 12 l of pancreatic fluid/day (Alexander and Hickson 1970).


Figure 10.11. Electrolyte transport across centroacinar cells of the exocrine pancreatic gland. (From Argent and Case 1994)


Secretion and Absorption of Electrolytes - Biliary system:

The rate of biliary secretion is also influenced by the hormone secretin, but the release of bile from the gallbladder is controlled by the hormone cholecystokinin, which is secreted by midgut epithelial cells in response to the presence of lipid. The electrolytes and water in biliary secretions are initially derived from the epithelial cells of the enterohepatic canaliculi and adjusted by passage through the bile ducts. Biliary secretions also have a high Na⁺/K⁺ and HCO₃^-/Cl^- ratio, and high pH at rapid rates of flow, and lower HCO₃^- and pH levels with a reduction in flow. Bile is stored by a gall bladder in most vertebrates for release following a meal, and can be concentrated 20- to 30-fold in some species by absorption of electrolytes and water (Hofmann 1994). This appears to be accomplished by Na⁺-H⁺ exchange and by cotransport of Na⁺, K⁺, and Cl^- in at least some species (Reuss 1991). However, the gallbladder has little absorptive ability in pigs and ruminants, and bile is released continuously into the midgut of horses and other species that lack a gall bladder.


Secretion and Absorption of Electrolytes - Midgut:

Powell (1986) and Chang and Rao (1994) reviewed information on the secretion and absorption of electrolytes by the mammalian midgut epithelium. Transport of electrolytes across midgut epithelium varies among intestinal segments and between crypt and villi cells. Crypt cells secrete electrolytes and the absorptive cells on the villi both secrete and absorb electrolytes. Some ions and most of the water are transferred via pericellular diffusion, which varies with ion species (P_K>P_Na>P_Cl) and decreases progressively between the duodenum and rectum.

The major mechanisms for Na⁺ and Cl^- absorption and K⁺ transport across human intestinal epithelium are illustrated in Figure 10.12a, b, c. Secretory cells in the crypts of the small intestine secrete Na⁺ and Cl^- into the lumen with the aid of a carrier in the basolateral membranes that cotransports Na⁺, K⁺, 2 Cl^-, in a manner similar to that of the parotid acinar cells. Much of the Na⁺ is absorbed from the small intestine in cotransport with solutes (glucose, galactose, fructose, amino acids, and B-vitamins). Cotransport of Na⁺, Cl^-, and amino or imino acids was also reported in the midgut of fish (Bogé et al. 1983). Most of the remainder is absorbed by Na⁺/H⁺ exchange, which is coupled with Cl^-/HCO₃^- exchange in the ileum. There is also evidence for carrier mediated Na⁺/NH₄⁺ exchange in the ileum of rats (Koch and Hall 1992).  Chloride is absorbed from the midgut by passive diffusion down its electrochemical gradient, and by Cl^-/HCO₃^- exchange in the ileum. Cotransport of Na⁺, K⁺, 2 Cl^- was also reported across the lumen-facing membrane of the flounder midgut absorptive cells (Fig. 10.13).


Figure 10.12a.  Pathways for the transport of sodium ions across human intestinal epithelium.  The thickness of arrow heads represents relative degree of transport.  (From Chang and Rao 1994)



Figure 10.12b.  Pathways for the transport of chlorine ions across human intestinal epithelium.  The thickness of arrow heads represents relative degree of transport. (From Chang and Rao 1994)



Figure 10.12c.  Pathways for the transport of ions across human intestinal epithelium.  The thickness of arrow heads represents relative degree of transport. (From Chang and Rao 1994)



Figure 10.13. A model that would account for Na⁺, K⁺, and Cl^- transport by flounder intestine. (From Frizzell et al. 1984)


Absorption of potassium from the midgut has been attributed to passive diffusion, and the disappearance of HCO₃^- from the lumen can be attributed to its conversion to CO₂ and water, which are readily absorbed. However, there is evidence for K⁺ - H⁺ exchange in the rat jejunum (Smith and McCabe 1984), rabbit ileum (Smith et al. 1985) and amphibian midgut (Imon and White 1984), and for electrogenic absorption of HCO₃^- in the midgut of the amphibian congo eel Amphiuma (White 1985).


Secretion and Absorption of Electrolytes - Hindgut:

Secretion and absorption of electrolytes by hindgut epithelia differ from that of the midgut and can vary among species and between its proximal and distal segments (Fig. 10.12a,b,c above). Carrier mediated, Na⁺-dependent transport of glucose and amino acids has been demonstrated in the hindgut of neonate pigs (Bentley and Smith 1975), the ceca of birds (Skadhauge 1993), and proximal colon of chickens on high Na⁺ diets (Skadhauge et al. 1983; Munck 1989; Arnason and Skadhauge 1991). However, it appears to be absent from the hindgut of postnatal mammals and other vertebrates (Potter 1989). SCFA appear to be absorbed from the large intestine by same mechanisms as those described for rumen epithelium, including its coupling with Na⁺/H⁺ exchange (Fig. 9.8). The absorption of SCFA and Na⁺ account for a major fraction of the water that is absorbed from the hindgut. 


Figure 9.8. Mechanisms proposed for the transport of  SCFA transport across gut epithelium. Hydrogen ions produced by hydration of the CO₂ in the lumen or secreted by carrier-mediated Na⁺/H⁺ exchange in the lumen-facing membrane may protonate SCFA anions (Ac^-) to their undissociated form (HA_c), which passively diffuses across these membranes. The H⁺ and HCO₃^-  produced by carbonic anhydrase-catalyzed intercellular hydration of CO₂ produces both H⁺ for carrier-mediated Na⁺/H⁺ exchange and HCO₃^- for  exchanged with SCFA^- anions in the lumen.  SCFA may be transported across the basolateral membrane by either diffusion of the undissociated form or carrier-mediated exchange of SCFA^- anions with blood HCO₃^-.  (Modifications and combinations of models from Stevens et al. 1969; 1986 and Titus & Ahearn 1992.)  (From CD Chapter 9)


Sodium is absorbed across the lumen-facing membranes of cells in the proximal colon of mammals by Na⁺/H⁺ exchange, which is coupled with Cl^-/HCO₃^-, as seen in the distal midgut (Fig. 10.12a,b,c). The same is true for the distal hindgut of normal rats. However, the distal colon of humans, rabbits, pigs, sheep, ponies, and sodium-depleted rats absorbs Na⁺ by electrogenic diffusion through sodium-permeable channels in the lumen-facing membranes (Engelhardt 1995). Depletion of dietary Na⁺ initiates the release of aldosterone, which stimulates the absorption of Na⁺ by both Na⁺/H⁺ exchange and electrogenic transport, and results in a conversion from Na⁺/H⁺ exchange to electrogenic transport of Na⁺ in the distal colon of rats. Sodium depletion also resulted in the replacement of Na⁺-dependent cotransport of glucose and amino acids with electrogenic Na⁺ transport in the colon of chickens (Skadhauge et al. 1983). This adaptation was not observed in ducks, which can excrete Na⁺ via salt glands. The distal colon also absorbs K⁺ by K⁺/H⁺ exchange, in a manner similar to that seen in the parietal cells of the stomach.


Enterocirculation of Electrolytes and Water:

Therefore, electrolytes and water are circulated through the digestive system by a limited number of transport mechanisms located in the membranes of epithelial cells lining the salivary and pancreatic glands, biliary system, and gastrointestinal tract. Most of these mechanisms are found in all vertebrates. However, their distribution varies with their location in the glands or segments of the digestive tract and, in some cases, their location in the lumen-facing versus basolateral membranes of the cells.

With the above in mind, the osmolality and composition of electrolytes recorded along the gastrointestinal tract of the pony (Fig. 10.3) can be attributed to following series of events. The high Na⁺ concentration and osmolality of gastric contents are derived from the diet and saliva. The osmotic activity is lowered by diffusion of water from the proximal small intestine down its osmotic gradient. Despite its continuous absorption along the small intestinal tract, the Na⁺ levels remained high, due to its secretion in pancreatic and biliary fluids, and the absorption of Na⁺ and water at a relatively constant ratio. The concentration of Na⁺ decreased in the distal hindgut, with a reciprocal rise in K⁺ concentration, due to absorption of Na⁺ and both the secretion of K⁺ and its release from plant material by gut microbes.


Figure 10.3.  Mean digesta osmolality and concentrations of the major electrolytes along the gastrointestinal tract of the pony obtained from four measurements over a 12-h period after a meal. Segments represent the stomach (S), three equal segments of the small intestine (SI), the cecum (C), and the ventral (VC), dorsal (DC) and small (SC) colon. Hydrogen was omitted, because it is only a small component (1 mEq/L) of the cations, even in gastric contents. Concentrations of PO₄^-- were calculated on the basis of a pKa of 6.8 for NaH₂PO₄ and the mean pH of digesta in each segment.  The principal organic acids (OA) are SCFA and lactic acid. At the pH of intestinal contents, ammonia, SCFA and lactic acid exist principally in their ionized form. Concentrations of HCO₃^- were calculated as the difference in concentration of measured cations and anions. (Modified from Argenzio 1975)


The high Cl^- concentration of gastric contents was derived from the diet and gastric secretion of HCl. Chloride levels decreased along the small intestine with a reciprocal raise in HCO₃^-, due to the addition of pancreatic and biliary secretions, and its exchange for Cl^- in the ileum. Although HCO₃^- is the predominant anion in the ileum of horses, pigs, and humans, PO₄^{- -} was the principal anion in the ileum of dogs, cats, rabbits and guinea pigs (Alexander 1965). The marked reduction of HCO₃^- in the large intestine was due mostly to its neutralization by SCFA. Therefore, the principal anions in the large intestine were the SCFA produced by microbial fermentation of carbohydrates and the PO₄^{- -} released by microbial digestion of plant material.

The more continuous feeding and larger gut capacity of herbivores require the secretion and reabsorption of much larger quantities of electrolytes and water. Table 10.1 lists the volume of daily secretions in humans, sheep and ponies. The upper digestive tract of human subjects that were starved for 24 hours secreted about 5.5 l per 100 kg of body weight per day (Soergal and Hofmann 1972). This increased to 7.7 l/ kg per day in subjects that were fed (Powell 1986). The volume of these secretions in fed patients was equivalent to about 39% their extracellular fluid volume and 11% of their total body water, with a Na⁺, K⁺, and HCO₃^- content equivalent to 30 to 45% of that in the extracellular fluid compartment  (Soergal and Hofmann 1972). However, the daily secretion of fluids into the digestive tract of the herbivorous sheep and pony were equivalent to over 200% of their extracellular fluid volume or 50% of their body water. Ninety-nine percent of this fluid was reabsorbed from the gastrointestinal tract of each species.

Table 10.1.

Values for human are estimates for an individual starved 24 hours prior to measurements (Soergal & Hofmann 1972). Other values are means for sheep (Denton 1957, Harrison 1962, Hill 1965, Kay 1960, Kay & Pfeffer 1970, Magee 1961, Taylor 1962), and means for ponies (Alexander & Hickson 1970, Argenzio et al. 1974a) (from Stevens and Hume 1995)


An uncompensated loss of 15% of the extracellular fluid volume or 20% of body water can produce clinical signs of dehydration in most species, and a 30% loss of body water is generally fatal. As mentioned in Section 9 (Microbial production of nutrients: Digestive diseases associated with diet or feeding regimes), the enterocirculation of water by herbivores can be seriously interrupted by changes in the diet or feeding schedule. However, any condition that results in a marked loss of these fluids by vomiting or diarrhea, or their entrapment due to blockage (vovulus, intususseption, or impaction) of the gastrointestinal tract requires immediate fluid therapy regardless of the cause or species.


< Top of Page     Next section:  11. Neuroendocrine control