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Part II

Invited Papers

IN PART II THE EXPERT PAPERS that formed the basis for the development of the basic science summary and recommendations in Part I are included here in the order they were presented at the workshop. A sub-committee of the CMNR worked with the Army Grant Officer Representative, COL E. Wayne Askew to define the focus for the workshop and the report. Speakers were selected who were active senior investigators and well known for their research in the specific area. Each speaker was asked to carefully review the literature in their own field of expertise in preparation for their presentation. In their presentation and in their chapter, the invited experts were requested to make critical comments on the relevant research and conclude with their personal recommendations. After the workshop, each author was given the opportunity to revise or add to their papers based on committee questions. The final papers were used by the committee in the development of Part I. Although the conclusions of the following chapters focussed on fluid replacement and heat stress in a military setting, these chapters provide a state-of-the art review of fluid and carbohydrate-electrolyte beverage intake during any type of outdoor activity whether heavy work, sports, or recreation.



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FLUID REPLACEMENT AND HEAT STRESS Part II Invited Papers IN PART II THE EXPERT PAPERS that formed the basis for the development of the basic science summary and recommendations in Part I are included here in the order they were presented at the workshop. A sub-committee of the CMNR worked with the Army Grant Officer Representative, COL E. Wayne Askew to define the focus for the workshop and the report. Speakers were selected who were active senior investigators and well known for their research in the specific area. Each speaker was asked to carefully review the literature in their own field of expertise in preparation for their presentation. In their presentation and in their chapter, the invited experts were requested to make critical comments on the relevant research and conclude with their personal recommendations. After the workshop, each author was given the opportunity to revise or add to their papers based on committee questions. The final papers were used by the committee in the development of Part I. Although the conclusions of the following chapters focussed on fluid replacement and heat stress in a military setting, these chapters provide a state-of-the art review of fluid and carbohydrate-electrolyte beverage intake during any type of outdoor activity whether heavy work, sports, or recreation.

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FLUID REPLACEMENT AND HEAT STRESS Fluid Replacement and Heat Stress, 1993 Pp. 11-21. Washington, D.C. National Academy Press 2 Use of Electrolytes in Fluid Replacement Solutions: What Have We Learned From Intestinal Absorption Studies? Carl V. Gisolfi1 INTRODUCTION There is abundant evidence to indicate that fluid replacement during exercise, especially in the heat, is essential to prevent hyperthermia and improve work capacity (Adolph and Associates, 1947). It is also well established that the inclusion of carbohydrates in oral hydration solutions (OHSs) can prolong exercise and improve performance (Christensen and Hansen, 1939; Coyle et al., 1983; Lamb and Brodowicz, 1964; Murray, 1987). It is considerably less clear what role electrolytes play when they are added to these solutions. Are electrolytes lost in sufficient quantities to warrant their replacement in OHSs? If not, is there any other reason to include them 1   Carl V. Gisolfi, Department of Exercise Science, University of Iowa, Iowa City, IA 52242

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FLUID REPLACEMENT AND HEAT STRESS in such beverages? For example, does their inclusion in OHSs enhance the absorption of water and other solutes? Do they contribute to beverage palatability, osmoregulation, or maintenance of plasma volume? The purpose of this paper is to review the effects of Na+on the intestinal absorption of water and carbohydrates during rest and exercise. It begins with a brief review of the methods employed in such studies and is followed by a discussion of the interactions among sodium, water, and glucose absorption. The emphasis will be on in vivo experiments on human subjects. METHODS Although there are several different methods of studying absorption (Leiper and Maughan, 1988; Modigliani et al., 1973), the segmental perfusion technique provides the most quantitative assessment of water and solute absorption in humans (Fordtran et al., 1961; Schedl and Clifton, 1963). This technique requires the subject to pass a multilumen catheter into the small intestine under fluoroscopic guidance. A mercury ball enclosed by an inflatable balloon is attached to the distal end to facilitate movement through the intestine. The test solution is infused at a constant rate (usually 8 to 20 ml/min) and contains a water-soluble nonabsorbable marker (usually polyethylene glycol). When this technique was first introduced, it employed only a double-lumen tube with a mercury bag attached to its distal end. One lumen was used for infusion and the other was used to sample the perfusate at the end of the test segment. The drawbacks of the double-lumen tube are (1) reflux of the perfused solution proximally, and (2) contamination of the perfused solution by proximal endogenous secretions (Modigliani et al., 1973). To eliminate these problems, (1) an occlusive balloon proximal to the infusion port was included to prevent reflux and contamination of intestinal secretions, or (2) a third lumen was added to the catheter. The disadvantage of the occlusive balloon is that it may interfere with intestinal motility. Most investigators who use the segmental perfusion technique employ a triple-lumen tube. By this technique, the test solution is perfused through the most proximal port and is sampled from the two more distal sites. The distance (10-15 cm) between the perfusion port and the first sampling site is called the mixing segment. It allows the marker to form a homogeneous solution with the intestinal contents before a sample is drawn (1 ml/min) from the proximal sampling site. The fluid then traverses the test segment (usually 20-40 cm) and is collected continuously by siphonage at the distal sampling site. It is not necessary to collect all of the solution, because the

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FLUID REPLACEMENT AND HEAT STRESS flux calculations depend only on changes in concentration of the marker and the test solution. Accuracy of the technique depends on two assumptions: (1) that the marker is not absorbed appreciably, and (2) that complete mixing has occurred. It is important to realize that the composition of the solution under study is not the composition of the solution perfused, but rather is the composition of the fluid collected from the proximal sampling site before it enters the test segment. It is also important to understand that the results from such studies apply only to the portion of gut represented by the test segment. Different results could be obtained by perfusing a larger segment or a different segment of the intestine. WATER AND ELECTROLYTE ABSORPTION Electrolyte and nonelectrolyte absorption involve both active and passive transport along the entire length of the intestine. Water is primarily absorbed in the proximal small intestine (duodenum and jejunum), but it is absorbed more efficiently in the colon (American Gastroenterological Association, 1989); it is a passive process dependent upon net solute absorption (Curran, 1968). Water transport and fluid homeostasis are highly dependent upon Na + absorption. This is a two-step process involving (1) passive Na+ entry across the brush border membrane via simple diffusion or cotransport with electrolytes or nonelectrolytes, and (2) active Na+extrusion across the basolateral membrane via the Na+ - K+ pump (Powell et al., 1985). Na+ - sugar coupling stoichiometry across the brush border is 2:1 (Kimmich and Randles, 1984). Na+ may also move passively across the cell via bulk flow through the intercellular (paracellular) pathway. Glucose-Stimulated Na+ Absorption This phenomenon was first observed in the guinea pig small intestine by Riklis and Quastel (1958), and it is now a firmly entrenched biological concept (Powell et al., 1985; Schultz and Curran, 1970). It occurs in the small intestine but not in the colon (Binder and Sandle, 1987) and is attributed to either glucose-Na+ cotransport (an active process) or to glucose-stimulated Na+ absorption secondary to solvent drag (a passive process). Fordtran (1975) has presented convincing evidence that up to 85% of the glucose-stimulated Na+ absorption in the human jejunum is due to passive transport.

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FLUID REPLACEMENT AND HEAT STRESS The concentration of Na+ in the jejunal lumen plays a crucial role in determining the rate of sugar enhancement of Na+ absorption, but not in the ileum. Using the double-lumen technique with a proximal occlusive balloon, Spiller et al. (1987) reported that perfusing solutions with less than 90 meq Na+ per liter resulted in net Na+ secretion into the jejunum of normal human subjects. Fordtran (1975) found that when the luminal Na+ concentration in the human jejunum was 120 meq/liter, Na+ absorption was virtually doubled compared with a luminal concentration of 80 meq/liter. Water absorption followed net solute absorption and was therefore highly dependent upon Na+ transport. Olsen and Ingelfinger (1968) perfused different segments of the intestine with isotonic solutions containing various concentrations of glucose and either 0 or 140 meq of Na+ per liter. When the glucose concentration was between 1 and 3 mmol/liter, and was therefore moving against a concentration gradient, glucose transport was inhibited with Na+-free perfusions. On the other hand, when the glucose concentration ranged from 6 to 20 mmol/liter in the perfusion solution, glucose transport was not affected by the absence of Na+ in the perfusion solution. In the human, rat, and dog ileum, Saltzman et al. (1972) were unable to show an important role for intraluminal Na+ in the active absorption of glucose. Glucose absorption was virtually unaffected when the luminal Na+ concentration was reduced from 140 to 2.5 meq/liter; however, in the in vivo preparation, Na+ could be trapped in the negatively charged mucous gel adjacent to the apical membrane, making it impossible to reduce Na+ to very low levels (Smithson et al., 1981). Although Na+ appears to be required to maximize glucose and water absorption in the small intestine, is it necessary to include Na+ in fluid replacement beverages or will intestinal secretions suffice in supplying the needed electrolytes? In a recent study by Wheeler and Banwell (1986), there was no difference in water absorption from carbohydrate-electrolyte solutions perfused into the jejunum of normal human subjects compared with that when plain water was perfused. They concluded that the limiting factor in rehydration was gastric emptying. In a similar study, Gisolfi et al. (1990) found significantly greater water absorption from a 6% carbohydrate-electrolyte solution than from distilled water. The difference between studies could be attributed to differences in the intestinal segment perfused, the form of carbohydrate used, or the electrolyte concentration of the solutions. Wheeler and Banwell (1986) perfused the jejunum with solutions containing complex carbohydrates and 10 meq of Na+ per liter, whereas Gisolfi et al. (1990) perfused the duodenojejunum with more simple sugars and 20 meq of Na+ per liter. What is the optimal ratio of Na+ to glucose required to maximize water absorption, and what form of carbohydrate best facilitates net Na+ and

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FLUID REPLACEMENT AND HEAT STRESS water transport? Schedl and Clifton (1963) were the first investigators to demonstrate that glucose markedly enhances water absorption from the human small intestine; 56 mmol glucose (1% solution) made isotonic with Ringer's solution increased water absorption fivefold over Ringer 's solution alone. Water absorption was the greatest in the duodenojejunum. Jones et al. (1987) found that glucose absorption was significantly faster from maltotriose and a glucose oligomer mixture than from isocaloric 140 mmol glucose. Water and sodium absorption were not measured. Wheeler and Banwell (1986) found that water and mineral absorption from solutions containing glucose polymers and fructose or glucose polymers, fructose, and sucrose were not different from absorption from solutions containing only water. Malawer et al. (1965) systematically varied sodium:glucose ratios of isotonic solutions perfused through the jejunum and concluded that water absorption was directly proportional to net solute movement and was maximal with 140 mmol glucose. The ratio of sodium to glucose absorbed depended upon the ratio of sodium to glucose perfused. Similar in vivo studies by Sladen and Dawson (1969) with isotonic glucose-saline solutions showed that water absorption correlated well with total solute absorption and was maximal with 56-84 mmol glucose. Fordtran (1975) found maximal water absorption when glucose in the test solution was 130 mmol and Na+ was 80 meq/liter, with Cl− as the major anion. None of these studies identified the optimal form of carbohydrate or the optimal glucose : sodium molar ratio that maximizes water absorption. In the rat duodenojejunum, Saunders and Sillery (1985) found the greatest water absorption when 10 mmol polycose (equivalent to 56 mmol glucose oligosaccharides) was added to 120 mmol NaCl and 20 mmol KCl. Thus, the optimal glucose : sodium molar ratio was approximately 1:2. Using the same animal model, Lifshitz and Wapnir (1984) found that a solution containing 60 mmol Na+ and 111 mmol glucose (2% solution) optimized both water and Na+ absorption and concluded that the optimal molar glucose:sodium ratio of an oral hydration solution was 2:1. Interestingly, intestinal fluid absorption is not only enhanced by the presence of glucose in luminal fluid but is also enhanced by elevating the glucose concentration in plasma (Lee, 1987). The mechanism of this increase in fluid absorption is not clear. It is not due to an increase in luminal glucose concentration and infusing NaCl to produce a similar rise in plasma osmolality reduced fluid absorption. Thus, the increase in fluid absorption during glucose infusion is attributed primarily to an increase in plasma glucose concentration and in part to glucose stimulated vasodilation and to glucose increasing intestinal blood flow (Bohlen, 1980).

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FLUID REPLACEMENT AND HEAT STRESS Fructose Versus Glucose The mechanism of intestinal fructose absorption is controversial. In humans, it is slower than glucose absorption and is thought to occur by energy-independent, facilitated diffusion (Holdsworth and Dawson, 1965). The absorption capacity of orally ingested fructose taken alone ranges from approximately 5 to 50 g, but when consumed in equal quantities with glucose or given as sucrose, absorption capacity (based on breath hydrogen analysis) is significantly increased. The latter observation led Rumessen and Gudmand-Hoyer (1986) to suggest that glucose enhances fructose absorption in a dose-dependent fashion. This second mechanism of fructose absorption is thought to occur in addition to the transport of a saturating level of free fructose. Fructose at 1 mmol (0.018%) is almost as efficient as 1 mmol (0.018%) glucose in stimulating water and Na+ absorption compared with the effects of perfusing mannitol, but glucose causes K+ secretion, whereas fructose causes K+ absorption (Fordtran, 1975). In the rat, fructose is absorbed by an active carrier-mediated mechanism (Gracey et al., 1972; Macrae and Neudoerffer, 1972), but infusing 60 mmol (2%) sucrose with 120 mmol NaCl and 20 mmol KCl did not promote water or Na+ absorption (Saunders and Sillery, 1985). The inhibitory influence of sucrose on water absorption has been observed in both animal and human studies (Fordtran, 1975; Newton et al., 1985; Patra et al., 1982; Wheeler and Banwell, 1986). ANION TRANSPORT The major anion included in the perfusion solution can have a significant effect on water and salt absorption. Fordtran (1975) maintained Na + and glucose concentrations constant at 80 meq/liter and 65 mmol/liter, respectively, and varied the anion composition of test solutions. Maximal water and Na+ absorption was found with Cl− followed by HCO3− and then SO4−2. Combining Cl− and HCO3− was not as effective as Cl− alone. EFFECTS OF EXERCISE Intestinal absorption during exercise is not well understood. Using an indirect method (3-O-methyl glucose), Williams et al. (1964) found that prolonged (4.5 h) moderate exercise in the heat reduced active sugar transport. Using the direct method of segmental perfusion with a triple-lumen catheter, Fordtran and Saltin (1967) found that a 1-h cycle of exercise at 64%-78% had no consistent effect on jejunal or ileal absorption of water, Na+, Cl−, K+, glucose, L-xylose, urea, or tritiated water. Although

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FLUID REPLACEMENT AND HEAT STRESS exercise has been shown to markedly reduce splanchnic blood flow (Rowell et al., 1964), Fordtran and Saltin (1967) concluded that severe exercise did not reduce intestinal blood flow enough to reduce the rate of either active or passive absorption. In that study, however, five different solutions were perfused through the intestine and most were perfused in only one or two subjects. Thus, it is difficult to generalize about the effects of exercise on intestinal absorption from that investigation. In a more recent study, Barclay and Turnberg (1988) used the triple-lumen perfusion technique to evaluate the effects of cycle exercise at a pulse rate of 40%-50% above the mean resting heart rate on jejunal absorption of an electrolyte solution (Na+, 136 mmol; Cl−, 105 mmol; K+, 5 mmol; SO4−2, 18 mmol). During exercise, the heart rate increased from 68 ± 4 beats per minute to 103 ± 7 beats per minute; and the absorption of water, Na+, K+, and Cl− fell significantly. They attributed this reduction in absorption to a parasympathetic effect on mucosal transport, but acknowledged other possible explanations. Among these were (1) a reduction in splanchnic blood flow secondary to increased sympathetic drive, (2) release of some humoral mediator, or (3) changes in intestinal motility and transit. Although increased sympathetic activity can reduce splanchnic blood flow (Rowell et al., 1964), the effect of intestinal blood flow on absorption is controversial (Brunsson et al., 1979; Varro et al., 1965; Williams et al., 1964). Changes in motility and transit are also controversial (Morris and Turnberg, 1980). Cammack et al. (1982) reported that moderate exercise had no effect on small bowel transit of a solid meal, whereas Keeling and Martin (1987) reported a significant decrease in small bowel transit of a liquid meal. SUMMARY AND NEEDED RESEARCH The inclusion of electrolytes in fluid replacement beverages is important to offset the losses in sweat and urine during prolonged exercise in the heat; but, perhaps more importantly, electrolytes should be incorporated into these beverages because they play a pivotal role in glucose, water, and salt absorption, which, in turn, is essential for the maintenance of plasma volume and osmoregulation. Glucose-stimulated Na+ absorption is a well-accepted biological phenomenon in the human intestine. The ratio of carbohydrate to salt and the form of carbohydrate that maximizes water absorption is controversial and warrants further investigation. The effects of exercise, hydration state, and ambient conditions on intestinal absorption have not been studied systematically and require investigation.

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FLUID REPLACEMENT AND HEAT STRESS RECOMMENDATIONS The following recommendations are based on current understanding of the interactions between water, electrolyte, and carbohydrate transport. It must also be recognized that the composition of a solution can be altered before it reaches the intestine. Thus, recommendations based solely on intestinal absorption data must be taken with a note of caution. Furthermore, it is possible that the segmental perfusion technique itself could alter the normal absorptive properties of the intestine. Much research is required in this field before we can understand how to formulate a rehydration beverage that maximizes water and carbohydrate absorption. Whether this same beverage can also serve as an oral hydration solution in the treatment of diarrheal disease also requires more research. Include Na+ in the amount of 20-30 meq/liter in the formulation of an oral hydration beverage. Include glucose in the beverage in the concentration of at least 50 mmol (0.9%). Maximal water absorption has been observed with values as high as 140 mmol (2.5%). Most drinks provided for use after sports and other activities contain 5%-10% carbohydrate, and these higher concentrations must be evaluated to determine the optimal amount that can be absorbed without reducing water transport. Include 5-10 meq of K+ per liter to offset the potential loss of K+ in sweat, the K+-secretory effect of glucose, and the potential loss of K+ in diarrheal disease. The primary (or only) anion should be Cl−. By comparison, all other anions tend to reduce water absorption. Consider the inclusion of a small amount of fructose, because glucose causes K+ secretion in the jejunum, while fructose causes K+ absorption. Determine the effectiveness of glucose polymers instead of glucose to reduce osmolality and provide for more Na+ without reducing the glucose concentration below a minimal level. REFERENCES Adolph, E.F., and Associates. 1947 Physiology of Man in the Desert. Interscience Publishers, New York. 357 pp. American Gastroenterological Association. 1989 AGA Teaching Projects in Gastroenterology and Liver Disease. Milner-Fenwick, Timonium, Md.

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FLUID REPLACEMENT AND HEAT STRESS Barclay, G.R., and L.A. Turnberg. 1988Effect of moderate exercise on salt and water transport in the human jejunum. Gut 29:816-820. Binder, H.J., and G.I. Sandle. 1987Electrolyte absorption and secretion in the mammalian colon. Pp. 1389-1418 in Physiology of the Gastrointestinal Tract, 2nd edition, vol 2, L.R. Johnson, ed. Raven, New York. Bohlen, H.G. 1980Intestinal tissue PO2 and microvascular responses during glucose exposure. Am. J. Physiol. 238 (Heart Circ. Physiol. 7):H164-H171. Brunsson, I., S. Eklund, M. Odal, O. Lundgreon, and H. Sjovall. 1979The effect of vasodilation and sympathetic nerve action on net water absorption in the cat's small intestine. Acta Physiol. Scand. 106:61-68. Cammack, J., N.W. Read, P.A. Cann, B. Greenwood, and A.M. Holgate. 1982Effect of prolonged exercise on the passage of a solid meal through the stomach and small intestine. Gut 23:957-961. Christensen, E.H., and O. Hansen. 1939Arbeitsfahigkeit und Ehrnahrung. Skand. Arch. Physiol. 81:160-171. Coyle, E.F., J.M. Hagberg, B.F. Hurley, W.H. Martin, A.A. Ehsani, and J.O. Holloszy. 1983Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J. Appl. Physiol. 55:230-235. Curran, P.F. 1968Coupling between transport process in intestine. Physiologist 11:3-23. Fordtran, J.S. 1975Stimulation of active and passive sodium absorption by sugars in the human jejunum. J. Clin. Invest. 55:728-737. Fordtran, J.S., and B. Saltin. 1967Gastric emptying and intestinal absorption during prolonged severe exercise. J. Appl. Physiol. 23:331-335. Fordtran, J.S., R. Levitan, V. BikermanS.B.A. Burrow, and F.J. Ingelfinger. 1961 The kinetics of water absorption in the human intestine. Trans. Assoc. Am. Physicians 74:195-205. Gisolfi, C.V., R.W. Summers, H.P. Schedl, T.L. Bleiler, and R.A. Oppliger. 1990Human intestinal water absorption: direct vs. indirect measurements Am. J. Physiol. 258:G216-G222 Gracey, M., V. Burke, and A. Oshin. 1972Active intestinal transport of D-fructose. Biochim. Biophys. Acta 266:397-406. Holdsworth, C.D., and A.M. Dawson. 1965Absorption of fructose in man. Proc. Soc. Exp. Biol. Med. 118:142-145. Jones, B.J.,B.E. Higgins, and D.B. Silk. 1987Glucose absorption from maltotriose and glucose oligomers in the human jejunum. Clin. Sci. 72:409-414. Keeling, W.F., and B.J. Martin. 1987Gastrointestinal transit during mild exercise. J. Appl. Physiol. 63:978-981. Kimmich, G.A., and J. Randles. 1984Sodium-sugar coupling stoichiometry in chick intestinal cells. Am. J. Physiol. 247:C74-C82. Lamb, D.R., and G.R. Brodowicz. 1964Optimal use of fluids of varyingformulations to minimize exercise-induced disturbances in homeostasis. Sports Med. 3:247-274.

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FLUID REPLACEMENT AND HEAT STRESS Stage 3 The rapid decrease in plasma volume during stage 2 compromises cardiac filling, stimulating cardiopulmonary volume receptors, which attenuate the vasodilatory reflex and inhibit sweating (Nadel, 1985). Stimulation of the cardiopulmonary receptors also stimulates secretion of antidiuretic hormone (ADH) (Moore, 1971; Segar and Moore, 1968), which reduces free-water clearance and conserves plasma water (Khokhar et al., 1976). ADH may also affect the sweat glands directly, to inhibit sweating (Nadel, 1985). When central blood volume is decreased, arterial blood pressure may fall, stimulating the sinoaortic baroreceptors and thereby causing a redistribution of blood flow away from splanchnic vascular beds (Abboud et al., 1979). This reduction in splanchnic blood volume may be important in conserving plasma water. Horowitz (1984) has demonstrated the importance of restricting splanchnic perfusion for conserving body fluids by comparing the heat stress responses of various species of rats. Since the splanchnic capillaries are among the most porous capillaries of the body to proteins and fluids, a species that can significantly reduce splanchnic blood flow will be most successful in conserving plasma volume and surviving during severe water restriction. Horowitz (1984) reported that the desert rat species Psammomys obesus withstood dehydration for over 48 h at least partly because of its ability to almost completely reduce splanchnic vascular permeability. If such findings can be extrapolated to man, then, reducing splanchnic blood flow during heat exposure is a positive step toward conserving plasma proteins and water. The increase in plasma osmolality also reduces the rate of plasma volume loss during heat exposure. Sweat is a hypotonic secretion, and therefore, as sweat production continues, the plasma becomes more and more hypertonic. This increase in plasma osmolality inhibits sweating (Fortney et al., 1984) and attenuates the rate of water loss from the vascular compartment. EFFECT OF AGE ON BODY FLUIDS Aging has been defined as an inability to adapt to changing environmental conditions (Piscopo, 1985). Several investigators (Leaf, 1984; Miller, 1987; Phillips et al., 1984) have observed that elderly individuals have difficulty maintaining body fluid balance. Physiological alterations in water and sodium regulation result in an increased danger of both dehydration and overhydration in the elderly (Crowe et al., 1987). Leaf (1984) observed that nursing home patients have an increased susceptibility to dehydration, and

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FLUID REPLACEMENT AND HEAT STRESS Spangler et al. (1984) reported that as many as 25% of nursing home patients may be chronically dehydrated. However, these findings do not prove that there is an age-related change in fluid regulation, since the results may have been complicated by a restricted access to fluids or by the prevalent use of medications that alter body fluids. The extent of dehydration in healthy, active older individuals has been debated. One study by Phillips et al. (1984) reported normal hydration in elderly subjects, while another study by the same group found elevated baseline sodium concentrations and plasma osmolalities in healthy older subjects (Crowe et al., 1987). Miller (1987) recently reviewed potential mechanisms for the occurrence of body fluid disturbances during the normal aging process. Lindeman et al. (1960) found that renal concentrating capacity in response to dehydration decreases with age, becoming evident between approximately 45 and 50 years of age. Rowe et al. (1976) substantiated this observation in men after 12 h of dehydration. The regulation of plasma sodium also appears to be affected by the normal aging process. Epstein and Hollenberg (1976) studied the renal response to sodium restriction in individuals from 18 to 76 years of age. Renal sodium excretion decreased by 50% after 18 h in subjects younger than 30 years, after 24 h in subjects between 30 and 60 years of age, and after 31 h in subjects older than 60. Impaired fluid and electrolyte balance in the elderly also may be due to an inability to detect changes in body hydration. Phillips et al. (1984) compared thirst perception between a group of young men and a group of men 67 to 75 years of age. The subjects were dehydrated for approximately 24 h, until both groups had a similar decrease in body weight. Following dehydration, the older subjects were not as thirsty as the younger subjects, based on their responses to a visual analog thirst scale, despite a greater increase in plasma osmolality. Increased secretion of ADH in response to osmotic stimuli and decreased secretion in response to hypovolemic stimuli occur with aging (Bevilacqua et al., 1987; Ledingham et al., 1987). During water restriction, Phillips et al. (1984) found a greater increase in ADH in older subjects, despite a similar loss of plasma volume. Helderman et al. (1978) infused hypertonic saline into young and older individuals and found a greater release of ADH into the plasma of older subjects compared with that in the plasma of the young subjects. This increased responsiveness of ADH is believed to compensate for the reduced sensitivity of the kidneys of older subjects to ADH. Baseline concentrations of atrial natriuretic factor (ANF) increase with increasing age (Wambach and Kaufmann, 1988; Yamasaki et al., 1988). The consequences of these changes in ANF regulation on body fluid responses

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FLUID REPLACEMENT AND HEAT STRESS are not known. Specific high-affinity binding sites for ANF have been found in many areas of the body, including the kidneys, the adrenal gland, smooth muscles of blood vessels, and the hypothalamus. Increases in plasma ANF have been shown to inhibit aldosterone production in the adrenal zona glomerulosa (Laragh and Atlas, 1988) and thus might contribute to the altered sodium regulation that occurs with aging. ANF also has an antagonist role to many of the actions of angiotensin II. It inhibits water intake induced by the administration of angiotensin II to the central nervous system. It has the potential to block the formation and secretion of both ADH and angiotensin II (Kramer, 1988; Laragh and Atlas, 1988), and it modulates sympathetic activity by inhibiting epinephrine release and reducing baroreceptor responsiveness. We are just beginning to understand the role of ANF in the regulation of body fluids and electrolytes. HYPOTHESIS On the basis of two facts, that (1) acute heat exposure provokes rapid changes in body fluids and (2) older individuals have an impaired ability to regulate body fluids, we hypothesized that older subjects would have difficulty maintaining plasma volume and osmolality during prolonged heat exposure. By comparing the time courses of body fluid responses to heat exposure of young and older individuals, the mechanisms for altered body fluid regulation in older healthy men may become apparent. Study Description The experiment outlined below is described in more detail in Miescher and Fortney (1989). The plasma volume, protein, and osmolality responses of six young men (age, 24-29 years) were compared with those of five older men (age, 61-67 years). The subjects were normotensive, non-smokers who were not taking any medications. The subjects had an average level of aerobic fitness for their age (Astrand, 1960). Each subject had an active life-style but did not participate in routine exercise training or sports. The two groups were matched for height, body surface area, and surface area/weight ratio (Table 16-1). The tests were performed in the winter months in Baltimore. The subjects reported to our laboratory at 8 a.m. after a light breakfast and after

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FLUID REPLACEMENT AND HEAT STRESS Table 16-1 Age and anthropometric characteristics of older and younger mena Subjects Age (yr) Weight (kg) SAb (m2) SA/Wt (m2/kg) VO2maxc (ml/kg/min) Older men (n = 5) 64.0d 73.0 1.9 0.026 38.8e ±SEM ± 1.0 ± 2.3 ± 0.04 ± 0.000 ± 2.3 Younger men (n = 6) 26.0 69.3 1.8 0.027 52.1 ±SEM ± 0.7 ± 3.1 ± 0.05 ± 0.000 ± 2.2 a All values are mean ±SEM. b Surface area. c maximal oxygen consumption. d p < 0.05, older versus younger. e p < 0.01, older versus younger. abstaining from caffeine beverages for at least 10 h. They were given 200 ml of water to drink when they arrived. They changed into shorts and were provided with a rectal thermistor, an Exersentry heart rate monitor, and venous catheter. They rested for 30 min in a cool room (25°C) before moving to a hot, dry heat chamber (45°C, 25%) for 180 min of heat exposure without fluid replacement. The subjects reclined to a sitting position in a webbed chair, and blood samples were drawn by a free-flowing technique just before they entered the heat chamber and every 30 min during the heat exposure. From each blood sample, hematocrit (microhematocrit technique), hemoglobin concentration (cyanomethemoglobin method), and total protein concentration (refractometry) were determined. Also, measurements of body weight, rectal temperature, and heart rate were obtained at 30-min intervals. Following 30 min of baseline rest, the older men had significantly lower rectal temperatures (Figure 16-2) and higher plasma osmolalities, despite similar hematocrits, hemoglobin concentrations, and plasma protein concentrations (Figure 16-3). During the 180-min heat challenge, rectal temperatures rose in both groups, but the rise was significantly greater in the older men ( Figure 16-2). The decreases in body mean weight were similar in both groups (1.52% in the older subjects and 1.55% in the younger subjects), yet the change in xxxxxx

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 16-2 Rectal temperature responses and changes in rectal temperature for young (n = 6) and older (n = 5) men during a 3-h passive heat exposure. Values are the means ± standard errors of the mean.

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 16-3 Plasma osmolality, percent changes in plasma volume, and absolute changes in plasma proteins in young (n = 6) and older (n = 5) men during a passive 3-h heat exposure. Values shown are the means ± standard errors of the mean.

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FLUID REPLACEMENT AND HEAT STRESS plasma volume in the older subjects was significantly greater during the heat exposure (Figure 16-3). Every young subject hemodiluted during the first 30 min of heat exposure, while only one older subject hemodiluted. The increases in plasma osmolality were similar in both groups during the heat exposure, although the older group maintained significantly higher plasma values. The total protein concentration increased or remained the same during the initial 90 min of heat exposure; it then stabilized in the younger men and decreased in the older men. DISCUSSION Compared with the younger men, the older men in this study showed an impaired ability to maintain their core temperature and plasma volume during a passive heat challenge. By carefully examining the time course of the changes in body fluids during the 180-min heat exposure, we may be able to identify potential causes for these age-related differences. The most striking difference in the plasma responses of the two groups was the lack of hemodilution during the first 30 min of heat exposure in the older men. Since hemodilution is thought to be due to a transient imbalance of venous and arteriolar tone (Harrison, 1986), this finding suggests that with increasing age, the veins become less responsive to environmental changes. Changes in the structure of cutaneous veins might increase wall stiffness or increased sympathetic tone might prevent venous relaxation in response to body heating as part of an overall change in the autonomic nervous function. Differences in the fitness levels of the two groups may have contributed to the heat response differences. The maximum oxygen consumption of the older men was significantly lower than that of the younger men, as would be expected in an older population with a similar life-style (Astrand, 1960). Although we did not specifically assess daily energy requirements, neither group participated in regular exercise or had jobs that required hard physical labor. If a significant training effect had been present, then a more sensitive sweating response would have maintained lower temperatures in the trained group. The absolute rectal temperatures were not significantly different after the first 30 min of heat exposure, and the total body weight loss of the two groups was similar. Therefore it is unlikely that the differences in body fluids in this study were due to a training difference. Our finding of elevated plasma osmolality in healthy older subjects under resting conditions agrees with the findings of Crowe et al. (1987). However, it is unclear whether the higher osmolalities indicate that the older men were dehydrated or whether they resulted from an age-related

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FLUID REPLACEMENT AND HEAT STRESS difference in sodium regulation. Baseline dehydration could explain the failure of the older men to hemodilute during acute heat exposure (Sawka et al., 1984). However, if the older men were dehydrated, then they should have had higher resting hematocrits and plasma protein concentrations. The similar rate of loss of plasma volume during the final 2 h of heat exposure suggests that the mechanisms responsible for fluid shifts during these stages of heat exposure were not altered by age. The total body sweat loss was similar for the two groups and, therefore, probably contributed equally to the hemoconcentration response. However, the greater loss of plasma proteins in the older men during the final hour of heat exposure suggests that older men may have greater difficulty restricting splanchnic blood flow during prolonged heat exposure (Horowitz, 1984). If the heat exposure had been extended in this study, greater differences in plasma volume might have occurred. We conclude that a difference exists in the ability of young and older healthy men to maintain plasma volume during passive heat exposure. This difference may contribute to the greater rate of rise in core temperature in the older group and, therefore, might affect heat tolerance. Our findings suggest that future studies should focus on age-related changes in vascular responsiveness to uncover mechanisms of greater heat strain in the elderly. REFERENCES Abboud, F.M., D.L. Eckberg, U.J. Johannsen, and A.L. Mark. 1979 Carotid and cardiopulmonary baroreceptor control of splanchnic and forearm vascular resistance during venous pooling in man. J. Physiol. 286:173-184. Astrand, I. 1960 Aerobic work capacity in men and women with special reference to age. Acta Physiol. Scand. 49 Suppl. 169:92. Barcroft, J., J.C. Meahins, H.W. Davis, J. Scott, and W.J. Fetter. 1922 The relation of the external temperature to blood volume. Phi Trans. R. Soc. London, Ser. B 211:455-464. Bass, D.E., and A. Henschel. 1956 Responses of body fluid compartments to heat and cold. Physiol. Rev. 3:128-144. Bass, D.E., C.R. Kleeman, M. Quinn, A. Henschel, and A.H. Hegnauer. 1955 Mechanisms of acclimatization to heat in man. Medicine 34:323-380. Bevilacqua, M., G. Norbiato, E. Chebat, U. Raggi, P. Cavaiani, R. Guzzetti, and P. Bertora. 1987 Osmotic and nonosmotic control of vasopressin release in the elderly: effect of metoclopramide. J. Clin. Endocrinol. Metab. 65:1243-1247. Crowe, M.J., M.L. Forsling, B.J. Rolls, P.A. Phillips, J.G.G. Ledingham, and R.F. Smith. 1987 Altered water excretion in healthy elderly men. Age and Aging 16:285-293. Epstein, M., and N.K. Hollenberg. 1976 Age as a determinant of renal sodium conservation in normal man. J. Lab. Clin. Med. 87:411-417.

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