National Academies Press: OpenBook
« Previous: 9. Heat as a Factor in the Perception of Taste, Smell, and Oral Sensation
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

10
Effects of Heat on Appetite

C. Peter Herman1

INTRODUCTION

Hot environments induce efforts to stay cool. This chapter addresses the issue of how one's food intake is adjusted to compensate for environmental heat. Common knowledge suggests that people eat less when it is hot, and that they eat ''lighter'' and "cooler" foods. (This impression is reinforced by a casual survey of newspaper and magazine suggestions for summer meal planning.) As with most impressions derived from common knowledge, systematic evidence is needed to support these assertions. What does the scientific literature have to say about the effects of heat on food intake and food selection? What follows is a review of the available scientific literature on the effects of heat on appetite. This literature has been supplemented by a survey designed specifically for this chapter (consumer survey, University of Toronto, unpublished data, 1991). Because of the anticipation that the scientific literature, especially on humans, might be skimpy, a questionnaire was sent to a number of restaurant and grocery chains in the metropolitan Toronto area asking about shifts in customer purchasing behavior as a function of environmental heat. This survey is by no means scientific, but it reflects the accumulated experience of merchants whose livelihood depends to some extent on accurately assessing how people's food purchases vary with the heat.

1  

C. Peter Herman, The Department of Psychology, University of Toronto, 100 St. George Street, Toronto, Ontario, CANADA M5S 1A5

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

Before examining the available data on the effects of heat on appetite, some preliminary considerations require attention, including a definition of terms. Heat can be defined in number of ways. Environmental temperature varies seasonally in the moderate climates in which most of the research is done, so one may ask whether appetite differs in summer and winter. Even within the seasons, of course, there may be considerable variability in temperature; does appetite suffer during a summer heat wave as compared to normal summer weather? Even more acute variations in temperature are available for examination, owing to the prevalence of air-conditioning. If, during a summer heat wave, one eats in an air-conditioned dining room, is appetite controlled by the outdoor or indoor temperature? Aside from temperature changes in the normal environment, one might also want to look at changes of environment. A winter trip to the tropics probably represents a greater short-term shift in temperature than might be encountered if one stayed put; how does it affect appetite?

To further complicate matters, how hot one feels is not simply a matter of the environment; one's own activity may generate heat, so that being active may be functionally equivalent to raising the environmental temperature. Indeed, eating itself has thermogenic effects, so that not only does heat affect appetite, but appetite may affect heat.

The meaning of appetite should also be clarified. There is tremendous variability in what scientists mean when they use the term (Herman and Vaccarino, 1992). Ordinarily, to achieve some clarity, one must distinguish among three terms that are often used interchangeably and confusingly. Appetite refers to the subjective desire to eat, whereas hunger usually refers to a more objective deprivation state. These terms are not unrelated, but it is preferable to think of hunger as a true need that often produces a felt desire (appetite). Distinguishing between hunger and appetite becomes useful when considering the possibility that one may desire to eat something even in the absence of a need for it. Conceivably, one might also be hungry without recognizing it or feeling a desire to eat, as is allegedly the case with some anorexia nervosa patients.

The third appetite-related term requiring attention is intake. In the scientific literature, food intake is often taken to be an operationalization of appetite, especially in nonhuman species where the animal's desires must be inferred from its behavior. In humans, it is quite possible to distinguish between what the person wants (appetite) or needs (hunger), on the one hand, and what the person eats (intake), on the other. People sometimes eat when they experience neither hunger nor appetite. Conversely, people sometimes refrain from eating despite experiencing hunger or appetite or both. For instance, Rolls et al. (1990) found, in a study related to temperature that is reviewed below, almost no relationship between how hungry or sated people claimed to be, on the one hand, and how much they subsequently ate, on the

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

other. In this chapter, owing to the fact that the literature largely ignores the distinctions just suggested, the effect of heat on appetite, hunger, and intake is considered collectively, with the awareness that heat may affect one of these without affecting the others. Use of the term appetite in a general or unqualified sense should be understood to refer to all three constructs.

One final preliminary caution. The mandate here was to examine the effect of heat on appetite in humans. For perhaps understandable reasons, a high proportion of the scientific research on appetite and on heat effects has been conducted on nonhumans. In what follows, preference will be given to human studies. Caution is urged in extrapolating from rats and other species to humans, but the paucity of human data requires reference to animal studies for clues as to how human appetite is affected by heat.

ENVIRONMENTAL TEMPERATURE, EATING, AND THERMOREGULATION

Any discussion of the effects of heat on eating must begin with a recognition that eating represents the basic means of securing energy for humans. Most analyses of heat and eating go one step further and point out that a major physiological concern of humans is thermoregulation—the maintenance of an appropriate body temperature—and that eating provides a major contribution to maintaining body heat (Brobeck, 1948). Indeed, it may be that "the important factor in regulation of food intake is not its energy value, but rather the amount of extra heat released in its assimilation" (Strominger and Brobeck, 1953). Thus, this "thermostatic hypothesis" of feeding argues that the total energy content of the food is not the determining factor in regulation. Energy that becomes stored as fat does not control feeding; rather, it is the direct heating effect of food intake that is monitored and that provides a regulatory mechanism.

According to this view, if the environment is cold, the resultant heat loss demands compensatory strategies, including notably increased food intake for its thermic effect. By extension, if the ambient temperature is warm, and heat loss is not an issue, there ought to be a reduced caloric demand. And should the environment become significantly hot—which changes the concern from how to obtain energy to how to dissipate it—a suppression of caloric intake should be expected. "At a high temperature where loss of heat is difficult, food intake should be low, lest by eating and assimilating food the body acquire more heat than it can dispose of" (Brobeck, 1948). This temperature-dependent variation in energy needs should, in principle, be reflected in appetite. Brobeck (1948) claims that "everyone knows ... that appetite fails in hot weather."

The inverse relation of appetite to environmental temperature may be examined in a number of different ways. Clearly, one might manipulate (or

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

exploit naturally occurring variations in) ambient temperature and examine indices of appetite. One might manipulate (or exploit naturally occurring variations in) body temperature independent of environmental temperature—as in fever—and determine whether this form of hyperthermia suppresses appetite. Alternatively, one might manipulate the need to acquire or dissipate energy more indirectly, through exercise; exercise, by providing a short-term boost in internal heat, ought to reduce the need for further energy—in short, appetite should be suppressed. In the long-term, by depleting short-term energy stores, exercise should increase the cumulative demand for energy repletion.

A final research strategy involves examining the influence of eating itself. Food intake itself creates heat, in addition to providing stored energy for future use. The heat attendant on eating and digestion (the thermic effect of food) as well as the heat produced through the processes of postprandial thermogenesis, which is experienced when humans perspire or become flushed after overeating, ought to reduce appetite acutely. Eating-induced thermogenesis presumably combines with environmental heat, so that appetite will be more suppressed after a given mean in a hot environment than in a cold environment, all things being equal.

An inferential caution: Considerable research has been devoted to the effects of cold environments on physiology and behavior, including appetite. If cold exposure increases appetite compared to appetite under normal conditions, one might be tempted to conclude that heat exposure above normal levels should have the opposite effect. For example, if people eat more than normal when the ambient temperature drops from 70° to 55°F, one might be inclined to infer that appetite would be reduced below normal if the temperature were raised to 85°F. This temptation might be justified by the data, but in the absence of specific research on heat exposure, one should be cautious about extrapolating from research on cold exposure. Does unusual heat have the opposite effect from unusual cold? That is an empirical question.

Another inferential caution: The immediately foregoing analysis assumes that body temperature is regulated and that the heat generated by eating represents a major element in the regulatory equation. But temperature may not be the only important regulated variable. It is now widely believed that body weight or body fat or some associated variable is also regulated (for a review see Mrosovsky, 1990). Moreover, there is reason to believe that the level at which body weight/fat (hereafter BW) is regulated may shift in response to various inputs, perhaps including environmental temperature. What if the set-point for BW drops in the heat? (This would be a reasonable adaptive strategy physiologically, because humans require less insulation when the environmental temperature is high in order to maintain a comfortable body temperature. Note that the supposition of a BW set-point

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

is not an alternative to the supposition of thermoregulation, but rather a complementary assumption.) If it is assumed that BW set-point drops in the summer or in response to elevated temperature in general, then the explanation for the finding that humans eat less in the heat becomes slightly more complicated. The more complicated interpretation is that heat lowers BW set-point and that appetite subsides because the animal's current weight is now excessive relative to set-point. Hyperthermia following excessive eating may contribute to the decline in intake, but increased heat dissipation and decreased intake may both be understood as mechanisms in the service of attaining a lowered level of BW, which in turn may be a mechanism in the service of more efficient thermoregulation in the heat. These regulatory adaptations, then, would seem to operate in concert. Mapping these causes and effects in a simple linear way is difficult at best and may not do justice to the mutual accommodations of physiological and behavioral systems.

The elegance and apparent prevalence of such regulatory adaptations in nature should not lead to the assumption without question that any change observed is necessarily perfectly functional. It is eminently possible that adaptation to one sort of challenge may prove to be contra-adaptive in some other sense (see Mrosovsky [1990], for numerous examples of regulatory conflict). In the present example, it is certainly possible that a decline in appetite in response to heat—should it occur—will not be mediated by a lowering of BW set-point; rather, the set-point may remain where it began, and lowered BW may represent a departure from the regulated value. The consequence would be that people who eat less and lose weight or fat in a hot climate will become underweight relative to set-point. This relative underweight may apply even to obese individuals, whose BW set-point and/ or thermoregulatory set-point may be inordinately high (Wilson and Sinha, 1985). The consequences may be stressful, both physiologically and psychologically. Animals and people who maintain a BW below set-point show aberrant eating patterns, hyperemotionality (including irritability), distractibility, and a reduced sex drive (Nisbett, 1972). If heat does indeed drive appetite and BW downward, it would be important to know whether it does so in conjunction with a shift in BW set-point or in defiance of a stable set-point. It has been argued (Pénicaud et al., 1986) that temperature control has primacy over food intake control, albeit perhaps only in the short term. As long as such primacy is evident, it should not be surprising to discover disorder in the feeding system and perhaps further disorders at the psychological (emotional) and behavioral (performance) level.

Because analyzing the effects of heat on appetite presupposes an appreciation of the effects of appetite on thermoregulation, the latter question will be addressed first. Having gained a sense of the effects of appetite on heat, readers may then be in a better position to comprehend the effects of heat on appetite.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

EFFECTS OF EATING ON THERMOREGULATION

Owing to the thermic effect of eating and metabolism, eating should be expected to provide warmth. This is certainly the case. "Food has a marked effect on body temperature; the temperature difference between a fed animal and an unfed one in the same cage, in the same room, at the same time can vary as much as one full degree F. This difference is due to the specific dynamic action of food" (Beller, 1977). This effect extends fully to humans; for example, Dallosso and James (1984) found that a 50 percent increase in caloric intake by the addition of fat to the diet produced a 47 percent increase in the thermic effects of eating. Eating ground beefsteak and stewed tomatoes to satiety raised skin temperature an average of 2°C about 1 hour after the meal (Booth and Strang, 1936).

Experimental demonstrations of increased metabolic rate, oxygen consumption, and thermogenesis are now so well established that research focuses mainly on subtleties of the response. For instance, LeBlanc and Cabanac (1989) recently demonstrated that the postprandial thermogenic effect has both a cephalic and a gastrointestinal phase; remarkably, the cephalic effect—which was evident in subjects who did not even swallow the food but who merely chewed and spit it out—was even stronger than was the subsequent gastrointestinal effect in subjects who consumed the food. In dogs, a large thermic effect was obtained when the animals were exposed only to the sight and smell of food for 3 minutes (LeBlanc and Diamond, 1986). Thus, eating produces heat, as was known all along; and even sensory exposure to food may produce conditioned or anticipatory thermogenesis or both. One possibly remote implication of this research is that in order to prevent thermogenetic increases in body heat, one may be required to avoid not only eating but all the sensory trappings of food.

Hypothalamic disturbances that produce substantial weight gain may do so at least partially by suppressing the heat dissipation by brown adipose tissue (BAT) that normally follows a meal (Hogan et al., 1986), although medially lesioned rats continue to show BAT activation during cold exposure (Hogan et al., 1982). This finding suggests that the lesioned rat, in defending an artificially higher BW set-point, will store whatever additional calories it can but not if its thermoregulation is threatened. Numerous studies (for example, Booth and Strang, 1936; Segal et al., 1987) have found a blunted thermogenic response to eating in obese humans.

If the suppression of appetite observed during heat exposure drives BW levels below set-point, this heat-induced appetite suppression might be expected to be accompanied by greater metabolic efficiency. A reduced intake, accordingly, should not be cause for concern. And if heat-induced appetite suppression is accompanied or caused by a lowering of the BW set-point, then there is all the more reason to avoid forced feeding, because such

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

hyperphagia would probably lead to hyperthermia. (At 40°C, rats will stop feeding altogether, and if force fed by intubation, they suffer heat stress and occasionally die [Hamilton, 1967].) Either way, reduced intake in the heat would seem to be adaptive. The only issue concerns activity, which, if intensified, ought to place extra demands on energy stores. The prudent recommendation for heat exposure would seem to be to allow for reduced intake but to avoid, as much as possible, strenuous activity, which not only requires more energy but also generates more undesirable heat, and which also puts fluid balance in jeopardy. Reduced activity is a natural response to heat exposure. If bursts of activity are unavoidable, care should be taken to allow, as much as possible, for longer than normal metabolic recovery periods.

Although eating causes thermogenesis, it does not follow automatically that all thermogenesis will feed back as a regulator of eating. Glick et al. (1989) abolished the thermogenic response of brown adipose tissue during and after feeding in rats but found no indication that meal size was augmented, as would be expected under, say, Brobeck's (1948) theory, if heat provided a satiety signal. It remains true that "increases in body and brain temperature do not coincide exactly with the cessation of feeding" (Balagura, 1973). Of course, the apparent unimportance of BAT thermogenesis in the control of appetite does not mean that endogenous heat in general is irrelevant to the regulatory control of appetite. Rampone and Reynolds (1991) have recently outlined a proposal—a "fine-tuning" of Brobeck's (1948) proposal—in which diet-induced thermogenesis feeds back to activate temperature-sensitive neurons in the rostral hypothalamus, which in turn activate the ventromedial hypothalamus to induce satiety. They explain hyperphagia and weight gain as the result of inadequate diet-induced thermogenesis and consequent inadequate satiety, with the result that the animal takes in more energy than it expends. Consistent with this notion is the finding that animals with rostral lesions both overeat and become hyperthermic (Hamilton and Brobeck, 1964).

It should be noted that even if the abolition of all thermogenesis failed to affect satiety or the duration and/or size of a meal, it would not follow logically that thermogenesis is unimportant in the control of appetite. Conceivably, feeding might be responsive to the lack of energy/heat in the "system." Meal-induced thermogenesis might not act as a satiety signal, but still serve to delay the onset of a drop in heat below some threshold that serves as a hunger signal. In other words, the focus in this chapter on heat as a satiety signal fails to address the initiation of eating. Perhaps energy depletions as hunger signals ought to be considered, in which case heat might well remain an important determinant of feeding but more at the onset end than at the offset end. The unwarranted but prevalent assumption that the same types of signals control both meal termination and meal initiation—as in Rampone and Reynolds' (1991) hypothesis that heat induces

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

satiety and cold induces hunger—adds to the confusion in this area. In general, more attention should be paid to whether the effect of heat on appetite suppression is expressed in terms of smaller meals (presumptive satiety effects) or less frequent meals (presumptive hunger effects); of course, these alternatives are not perfectly independent of one another. The frustratingly speculative nature of the foregoing discussion, in fact, is a reflection of the fact that "in most cases the measurement of postprandial heat [has been] undertaken with a totally different objective than that of assessing its effects on food intake" (Rampone and Reynolds, 1991). Thus, the call for more research may be extended to all aspects of endogenous heat production as a moderator of appetite.

Lack of adequate food induces cold. Keys et al. (1950) found that their semistarved volunteers complained of the cold even in warm summer weather. One might be tempted to suggest underfeeding troops in hot climates in order to minimize their problems with heat. Although a somewhat reduced intake is probably desirable and inevitable, given the various regulatory pressures that are activated automatically, deliberate food restriction below what the troops naturally desire would probably not be desirable, owing to all the negative effects of maintaining a suboptimal body weight. Metabolism is, if anything, speeded up in the heat and intake is reduced; the net effect is likely to be significant weight loss, and if that weight loss occurs in the absence of a resetting of the BW set-point, the result is likely to be a substantial energy deficit.

Most humans are not built to operate optimally in extremes of temperature. If faced with severe heat, people may reduce their intake and rely on metabolic processes to dissipate as much heat as possible, but this ultimately represents a loss of energy that might well interfere with other demands placed on them (for example, demands for intense activity). The solution, it would seem, is to avoid severe heat and function in a climate where thermoregulation is not a difficult challenge. Hot environments by definition provide such a challenge, but the best solution may be to find ways to keep cool, or at least thermoneutral, other than—or in addition to—reducing intake.

Climatic Adaptation
Physique

The ability to dissipate heat depends on various factors, not the least of which is physique. Bergmann's rule states that a bulkier shape minimizes heat loss, because the bulkier animal has a relatively smaller ratio of skin surface to metabolically active bulk, and skin surface determines heat dissipation (Beller, 1977). Allen's corollary to Bergmann's rule gives a heat-

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

dissipating advantage to those with longer appendages. Accordingly, people with rounded physiques (endomorphs) should have more difficulty with heat dissipation than will those with linear physiques (ectomorphs). Presumably, a given meal will produce greater thermic overload for the endomorph, who ought to learn, eventually, to eat less in the interests of thermoregulatory comfort.

There is substantial evidence that people adapt to a hot climate. Of course, eating less may be construed as an adaptation par excellence; but other related adaptations have been proposed. It is suggested above that heat can drive one's set-point for BW downward. Physical anthropologists (see Beller, 1977 for a fascinating review) have long noted a correspondence between physique and climate (Bergmann's rule, noted above). That linear physiques generally do better in the heat may be seen as an evolutionary selection principle, with races adapting to hot environments by altering their physique in an ectomorphic direction. One strong implication of this adaptational point of view is that certain people will do better in a hot environment than will others. Presumably, an individual who is genetically preadapted to a hot climate will have less trouble adapting to such a climate; such a displacement ought to disrupt his or her eating patterns less.

More pertinent to this discussion, perhaps, is the question of individual rather than evolutionary adaptation. Does, or can, an individual's set-point shift in response to heat exposure? If so, then the individual should feel uncomfortably overweight on initial exposure and cut back on eating; with a reduced set-point, the individual would eventually maintain a lower BW, and show a continued suppression of appetite appropriate for his or her more svelte physique.

Adaptation to Heat or Cold?

Interestingly, the endomorphy of a population is not correlated with mean annual temperature so much as with mean January temperature in northern latitudes (Beller, 1977). This finding has a number of implications, foremost among which is that normative BW depends more on extremes of cold than on heat. As an adaptation, this makes sense, because in these northern or temperate latitudes—and even in some tropical latitudes where the temperature occasionally plummets—the risk of insufficient fat/energy is greater than the risk of an excess of fat/energy. When one focuses on adaptation to hot climates, the implications are confusing. The main threat facing an individual in the hot climate would seem to be a failure of thermoregulation: heat dissipation is the main concern. Yet if the nighttime temperature drops precipitously, as may happen in the desert, then heat adaptation during the day may be more than cancelled out by cold adaptation at night. Conceivably, cold desert nights could lead to a continuing

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

high BW set-point, with dire implications for heat dissipation during the day. Even excessive use of air-conditioning might make heat adaptation and successful thermoregulation difficult.

It's Not the Heat, It's the Humidity

We think of high humidity as impairing our ability to perspire; humidity ought to impair heat dissipation and render the "functional temperature" even higher (for an overview see Burse, 1979). Heat combined with humidity should have a greater suppressive effect on appetite than dry heat. The anthropological evidence is confusing on this point. In Africa, humidity tends to be associated with a shorter, fatter physique in the native people, whereas in more northern climates (for example, Scandinavia), the wetter west coast breeds taller, thinner people than does the drier interior (Beller, 1977).

Gender Differences

There is reason to believe that men may be less heat tolerant than women. Beller (1977) notes that men have more, and a higher proportion of, metabolically active tissue than do women, who have a higher proportion of fat, and suggests that women's relative metabolic inactivity buffers them from heat stress. Beller goes even further and argues that women's extra fat tissue literally buffers them, by insulating them, from the external heat. It makes sense that a layer of fat might insulate one's internal core temperature from external heat sources; but such insulation should also make it more difficult to dissipate whatever heat is generated internally, through metabolism. Beller's conclusion is disputed, although not cited, by Burse (1979), who enumerates the physiological disadvantages of women working in the heat and urges that extreme caution be taken to prevent heat exhaustion in unacclimatized women.

Stress

Under acute stress, body temperature may rise. For example, boxers before a bout have a higher body temperature than they do before a routine practice. Mrosovsky (1990) refers to this temperature shift as psychogenic hyperthermia and attributes to it an enhancement of muscular activity. "The psychogenic contribution to such warming up may be to shift the thermoregulatory set-point" upward (Mrosovsky, 1990). To the extent that stress elevates the thermoregulatory set-point—or simply adds metabolic heat even without raising the thermoregulatory set-point—it should exacerbate what-

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

ever heat dissipation threats are encountered in hot climates. On balance, stress should further suppress appetite. Previous research concurs with this expectation, in that normal eaters in both laboratory and field settings have responded to stress by decreasing their food intake (Herman and Vaccarino, 1992). The major exception to this rule is provided by dieters, who often overeat in response to distress; presumably most military personnel would not fall into this category. Military personnel, however, are quite likely to experience stress independent of heat, and the suppressive effect on appetite must be taken into account. Such stress may have debilitating effects on its own, to which may be added whatever stress stems from long-term hunger, such as may occur if stress suppresses appetite without a corresponding suppression of BW set-point.

Activity

One effective short-term technique for achieving thermoregulation is activity, because strenuous activity has a thermogenic effect (Bellward and Dauncey, 1988). Animals who are energy-deficient (either cold or hungry) become more likely to move around; such activity both provides endogenous heat directly and makes it more likely that exogenous energy sources may be encountered. Eventually, this strategy may backfire, if the extra expenditure of energy is not repleted; but in the short-term, the animal will be closer to a thermal optimum. Lassitude in the heat, conversely, probably serves a useful physiological purpose and should not be countermanded as assiduously as it might be in a temperate climate.

Food Temperature

If food contains energy, and its thermic effect depends on the amount of that energy pius the assimilative cost of consuming and digesting it, then it should follow that adding energy to the food by heating it ought to have a relatively straightforward additive effect on the food's thermic value. Conversely, cold food ought to minimize the thermic effect of eating. Indeed, one gets the impression that if the food is served at a temperature significantly below body temperature it will have a cooling effect; this cooling effect should be more reinforcing for people who are hyperthermic.

Eating tends to add energy in the form of heat to the body; if the heat-exposed individual must eat, he or she should presumably prefer a cool version of a food to a hot version, on thermic grounds. But the hot version may in general be perceived as more palatable, insofar as warming brings out the presumably pleasant flavor of the food (Trant and Pangborn, 1983). Cabanac (1971) might argue that the enhanced palatability of warmed food

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

might be a conditional preference, based on the thermic effect of the food. Negative alliesthesia effects (that is, decreased acceptability) might be expected for warm food as the internal environment heats up. In other words, warm food may not be intrinsically more palatable; rather, its palatability may depend directly on the state of the organism (in this case, whether the organism is hypo-or hyperthermic). For Cabanac, it is not that the hot food is rejected by the heat-exposed individual despite its greater palatability but because heat exposure detracts from the food's palatability.

That heat exposure might shift one's preferences away from hot food and toward cool food is understandable. But another question arises: Should heat exposure increase one's attraction to cool foods rather than to no food at all? Cooling food produces a peculiar condition: the food still contains latent calories and is likely on those grounds to raise body temperature; but the cool physical state of the food is likely to have an immediately cooling effect in the mouth and perhaps even further down the alimentary canal. From a thermoregulatory point of view, is the hyperthermic individual better off consuming a cool food or none at all?

Type of Food

It is widely accepted that ''the amount of ... added heat, of course, varies with the type ... of food consumed'' (Rampone and Reynolds, 1991). Yet there appears to be only a small variation in the thermic effect of food depending on the type of food ingested. "Eating proteins, which are somewhat more complicated to break down inside the body than carbohydrates or fats are, tends to raise body temperature very slightly more than these other two basic food components do" (Beller, 1977). Beller goes on to note (pages 157 to 158) that "this difference has probably received more attention than it deserves in the popular literature about nutrition," an allusion to the allegedly weight-reducing properties of a high-protein diet. Balagura (1973), in discussing this issue, notes that in general, animals prefer carbohydrate diets and especially prefer fat diets over protein diets, so the fact that eating terminates sooner on protein diets may be more a function of the diets' limited palatability than of their greater thermic effect. Of course, in nonhumans, palatability is often difficult to disentangle from eating itself; but in humans, the expressed preference for fats and sweets is well known (Drewnowski et al., 1989), so that if less of a high protein diet is consumed, it may well be due to taste and texture factors rather than to thermal satiety feedback. Whether in making diet prescriptions we ought to consider the thermic effect of macronutrients—or confine ourselves to a consideration of basic nutritional balance—is difficult to assess at present.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

EFFECTS OF HEAT ON APPETITE

Effects of Environmental Temperature Variations on Amount Eaten
Acute Variations
Humans

One of the earliest systematic reports of the effect of heat on appetite was Johnson and Kark's (1947) summary of ad lib intakes by soldiers in various geographic areas ranging from the mobile force "Musk Ox," stationed in the Canadian Arctic, to infantry troops on Luzon in the Philippines. Troops stationed in the tropics ate on average 3100 calories, whereas arctic troops ate 4900 calories; in both cases, troops were allegedly offered as much food as they wanted, although the skeptical reader might be able to imagine some interpretive confoundings in these results. Whether the size of the heat effect on appetite is as profound as suggested by Johnson and Kark is debatable, but the direction of the effect has not been disputed. Edholm et al. (1964) confirmed this pattern, observing a 25 percent decrease in food intake by soldiers in Aden compared to the United Kingdom (see also Collins and Weiner, 1968). More parochially, one Toronto restaurateur (unpublished data from consumer survey, 1991) conceded that "sales plunge during a heat wave .... People do not have the appetite for a large heavy meal when it is hot." Beller (1977) neatly summarized the effect of heat on appetite, explaining it on the basis of the thermic effect of food:

The ability to raise body temperature through feeding is one that is shared by all warm-blooded animals. Cattle, swine, rats, goats, and U.S. Army men all eat more when the temperature is low than when it is high, and the reverse is equally true: at environmental temperatures of 90°F feeding begins to slow down in all these animals, and by the time rectal temperatures reach 104° (which is not an unheard-of reading, incidentally, for a man doing strenuous exercise for more than a few minutes at a time) virtually all species stop feeding entirely. This state of affairs is true not only for man and other homeotherms but for such disparate creatures as toads, single-celled paramecia, and honeybees (although the critical temperature maximum for a honeybee may not be quite the same as it is for a toad—or, of course, a man).

Logue (1986) makes the same point more colloquially: "An easy way to quell appetites at a summer dinner party is to turn off the air-conditioning." These generalizations suggest that acute temperature variations have a strong effect on appetite: specifically, heat impairs appetite. (And note that the implication of the turned-off air-conditioning scenario is that had the air-conditioning stayed on, appetite would have remained unquelled, despite it being summer. This suggests that acute temperature variations

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

may have a significant effect over and above seasonal variations. The consumer survey (unpublished, 1991) yielded a strong consensus about the effect of air-conditioning on customer behavior. In the summer, "air-conditioning attracts customers and after sitting in the restaurant, many order 'normally'.... If we have an air-conditioning breakdown, sales drop dramatically." The summer peak in ice cream sales is much more noticeable in street outlets than in mall outlets, although it is unclear whether this is because the malls are air-conditioned in the summer or because they are heated in the winter. One ice cream chain blamed the increasing prevalence of air-conditioning for its slower gain in sales in recent years. It is worth noting here that there is some lingering confusion about whether the effect of air-conditioning on appetite (countering heat-induced appetite changes) depends on acute effects (that is, air-conditioning at the eating site) or more chronic effects (that is, exposure to air-conditioning through much of the day). Presumably the answer to this question depends on whether chronic exposure to air-conditioning counteracts a heat-induced drop in BW set-point.

It is not clear what happens in an environment that is naturally hot much of the time but which cools off dramatically at other times. Such dramatic cooling may occur naturally at nighttime, or even during the day, with the advent of air-conditioning. How responsive is appetite to abrupt shifts in environmental temperature? Does one's appetite pick up when leaving the broiling heat to enter an air-conditioned dining room? Or does the pressure to dissipate heat carry over even in the air-conditioned environment? The same questions can be asked when substituting "cool nights" for "air-conditioning." One study, albeit on rats, speaks at least indirectly to this question. Refinetti (1988) examined feeding in rats that were housed in normal (29°C) or cold (19°C) conditions and fed in a separate chamber that was either normal temperature or cold. Both housing and feeding environment temperatures additively affected appetite; thus, the temperature that obtains when eating occurs does affect eating, but there is also some carryover from the external environment. One possibly significant finding in this study is that animals who went to a cold environment to feed gained much more weight than did animals who remained in a warm environment to feed. The finding suggests that if one spends most of one's time in the heat but eats in an artificially cooled environment, one might end up eating more than needed, with potential problems for heat dissipation when one returns to the hot environment.

Nonhumans

Research on the effects of variations in environmental temperature on feeding was stimulated by Brobeck's (1948) hypothesis. He found that rats' food intake dropped precipitously as the environmental temperature rose from 18° to 36°C; these rats, acclimated to a temperature

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

of 28° to 29°C, began to lose weight when the environmental temperature during feeding rose above 32°C. Numerous other investigators have found equivalent results with rats (Fletcher, 1986; Hamilton and Brobeck, 1964; Jakubczak, 1976; Leon and Woodside, 1983) and with other species, such as goats (Appleman and Delouche, 1959) that eat less and hoard less (Fantino and Cabanac, 1984) and frequently lose weight in hotter ambient temperatures. Kraly and Blass (1976) found that rats will work harder for food and consume more unpalatable food in the cold. Mice eat 43 percent less in an ambient temperature of 33°C than at 17°C (Thurlby, 1979; see also Donhoffer and Vonotzky, 1947), and pigs that were maintained at 32° to 35°C ate only half as much as pigs maintained at 10° to 12°C (Heath, 1980; Macari et al., 1986). Note that Swiergiel and Ingram (1986) found that piglets maintained at 35°C gained more weight than did piglets maintained at 10°C, but the intake levels appeared to have been controlled in this study; the higher BW of the 35°C piglets may have represented their attempt to store energy rather than bum it. Cafeteria-fed rats maintained at 29°C ate less, but if anything gained more weight than did those maintained at 24°C, presumably because in the hotter environment the rats became much more energy efficient, storing their excess calories rather than burning them and risking hyperthermia (Rothwell and Stock, 1986). Presumably in severe heat, thermogenic disposal of calories would pose enough of a threat so that the animal would quickly learn to cut back on its intake.

More proximal heating (that is, in the preoptic and anterior hypothalamic regions) serves to inhibit feeding in much the same way as does distal heating (that is, in the external environment) (Andersson and Larsson, 1961). This simply indicates that the effects of environmental heat must be registered somewhere in the central nervous system if they are to affect feeding; the hypothalamic tracts remain the prime candidates for the coordination of heat-and-feeding regulation. Other loci, such as the liver (DiBella et al., 1981) and even the skin (Booth and Strang, 1936), have also been nominated as crucial in producing regulatory thermal feedback in the control of eating.

In general, "reduced intake in warm environments [has] been shown in several endothermic animals" (Refinetti, 1988). One exception to the rule that animals eat less when it is hot is contained in a study by Bellward and Dauncey (1988); in this study, mice ate more at above-normal temperatures than at below-normal temperatures. The explanation for this contrary effect supports the general approach here: mice had to choose between heat (exposure to a heat lamp) and food. When it was cold, they tended to choose heat, at the expense of food. Presumably if they had been allowed access to food but not the heat lamp, they would have eaten less as the temperature rose.

One mechanism possibly contributing to increased intake in animals

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

exposed to the cold is faster gastric emptying (Logue, 1986). Logue notes that rats exposed to the cold initiate more meals but do not eat more at a given meal. Presumably, gastric emptying rate does not affect the initial repletion rate of the stomach, and consequently the size of the meal, but does affect the length of time until the stomach again "demands" repletion, and consequently the frequency of meals. The faster the stomach empties, the sooner the next meal must begin. To extrapolate to the presumably reduced gastric emptying rate in animals exposed to the heat, one might speculate that the slowing of the digestive process is a means of muting the thermic effect of food.

Seasonal Effects

Casual inquiry yields a broad consensus that BW declines in the summer and rises in the winter. This seasonal variation is sometimes thought to be accompanied by a corresponding variation in appetite, although interestingly, people appear to be less cognizant of how much they eat than of how much they weigh. The thermoregulatory viewpoint considered above would seem to predict a decline in appetite in the summer heat as a means of ensuring that endogenous heat does not threaten one's thermoregulatory capacity. What remains uncertain—even if the appetitive shift occurs—is whether the shift in body weight is regulated or not. That is, does BW set-point shift downward in the hot months, dragging appetite with it? Or does appetite decline on its own, as a thermoregulatory tactic, while BW set-point remains high?

The need for less internal heat in the summer seems to be an adequate physiological rationale for lowered summer appetite. Other reasons may be suggested, however—notably, that people wear less clothing in the summer for thermoregulatory reasons and therefore become more concerned with their physical appearance. A bathing suit demands a slim physique, and perusal of popular magazines suggests that much of the springtime is devoted to shaping up for summer.

Among those who are exposed to summer heat involuntarily, reduced appetite would be expected. Solid evidence in support of this expectation is not abundant, if only because it has not been systematically collected. We know that the farmed polecat reduces its intake and weight during the summer months (Korhonen and Harri, 1986).

The most salient outcome of this literature search—other than consensual agreement with the general proposition that heat impairs appetite—is the dearth of actual experimental research on human consummatory response to variations in heat. It is somewhat reassuring, then, to note that retailers corroborate the consensual impression, often with hard data (sales

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

figures). A number of restaurant chains in the Toronto area report decreased sales during the summer—not only fewer customers, as might be expected because of vacations, but also a decline in the average purchase per customer (range of decrease: 2 to 20 percent). The only exceptions to this rule were a chain of restaurants specializing in salads and two chains specializing in ice cream desserts.

Fever

Fever, of course, is not an exogenous source of heat, but it may be considered as a means of inducing heat in the internal environment. Fever is usually associated with decreased appetite, which follows from most analyses of feeding in which thermoregulation is a consideration. Raising the internal temperature ought to trigger compensatory decreases in feeding if feeding threatens to raise the internal temperature even further. This conclusion is premised on the notion that fever represents a state of hyperthermia relative to some internal optimum. Note that it does not follow that if hyperthermia suppresses voluntary appetite, then voluntary appetite suppression necessarily indicates hyperthermia. Appetite suppression and indications of hypothermia coexist, for instance, in anorexia nervosa (Garfinkel and Gamer, 1982).

The possibility remains, of course, that fever might not represent true hyperthermia but rather a resetting of the thermoregulatory set-point at a higher level (Mrosovsky, 1990); in this case, the body might "want" to maintain a higher temperature, and a decline in feeding would not be expected. Intraperitoneal injection of interleukin-1, normally released in the presence of pathogens, raises body temperature and ordinarily is associated with appetite suppression; but when injected intracerebroventricularly, interleukin-1 raises body temperature in rats without affecting intake (McCarthy et al., 1986). This suggests that fever-induced anorexia may not be mediated by thermic mechanisms. Conversely, injecting endotoxin substantially lowers intake even when temperature elevation is prevented by administration of sodium salicylate (Baile et al., 1981; McCarthy et al., 1984), although the suppression may be less than when fever is not prevented (Baile et al., 1981). Another study, in which rats' body weights were lowered before the administration of interleukin-1, found that despite elevated body temperature, the animals were initially hyperphagic in defense of an albeit subnormal body weight (Mrosovsky et al., 1989); in other words, it may be that pathogens—or the interleukin-1 stimulated by them—produce a lowered BW set-point, pulling appetite down, independent of heat compensation (see also O'Reilly et al., 1989). There are plausible adaptive reasons why maintaining a lowered BW might help to fight or "starve" pathogens (Murray and Murray, 1977).

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Food Temperature

One consensual belief, at least among nonscientists, is that hot foods have a greater thermogenic effect. Accordingly, people seek hot foods when they are cold, and cold foods, if any, when they are hot. Turning this prescription around, the conclusion emerges that hot foods ought to have a greater suppressive effect on appetite than cold foods.

Humans

Because warming a food tends to enhance its flavor and aroma (Trant and Pangborn, 1983), one might expect that hotter, more palatable food will generate increased intake initially, with perhaps a subsequent caloric compensation—or perhaps not, depending on the strength of compensatory pressures. Actually, one should be careful about assuming that accentuating the flavor will make the food more palatable; some things—notably beverages such as water—are more palatable when cool (Szlyk et al., 1989). And if the food is unpalatable to begin with, warming it may make it taste worse! Holding intake constant, one might expect hot food to suppress appetite by suppressing gastric emptying rate, just as exposure to cold environments speeds gastric emptying, as shown above. Or hot food might suppress appetite by raising body temperature and inducing satiety.

No significant effect on subsequent intake of cheese sandwiches or on sensations of hunger or fullness was observed when experimental subjects were given a fixed portion of V8 juice served at 1°C or 60° to 62°C (Rolls et al., 1990). The cold juice, while not affecting intake, did reduce reported desire to eat, in male subjects only, and reduced thirst as well. No clear explanation is available for the ambiguously suppressive effect of a cold beverage on mens' appetites.

Notwithstanding these sparse and nondefinitive data, there is a strong consensus among retailers and their customers that cold foods are preferred when the ambient temperature is high (unpublished data from consumer survey, 1991). The summer sales peak for ice cream would seem to depend more on the "ice" than on the "cream." In the words of one restaurateur, ''cold menu items make them [the customers] feel even cooler.'' Soup and bakery item sales are slow in the summer.

Nonhumans

The effect of food temperature on eating in humans may be powerful, if as yet undemonstrated; in other species, it appears to be negligible. Rats who were served cold (12°C), normal (29°C), or hot (48°C) pellets showed only a weak and insignificant tendency to eat more of the hotter food. As with humans, one is entitled to wonder whether hotter food might smell or taste better, enhancing appetite, while also providing more energy and suppressing appetite. Intriguing studies in ruminants (Bhattacharya and Warner, 1968; Gengler et al., 1970) indicate that if the rumen is heated by the addition of warm water or by heating coils, intake may decline by as

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

much as 45 percent. One is tempted to imagine studies in humans where the effect of heating on flavor is separated from its direct thermic effect. Heating a basically unpalatable food would presumably suppress intake substantially if it brought out the aversive flavor as well as added unwanted heat to the system. Presumably a study in which the animal or person was offered a choice between hot and cold versions of the same food might help to disambiguate these results.

Effects of Light on Appetite

Although there is obviously not an invariant connection between environmental heat and environmental light, some of the hottest environments, especially desert areas, are notable for the intensity of the light. This fact becomes relevant, perhaps, in conjunction with recent work on seasonal affective disorder (SAD), a variant of clinical depression that is seasonal in nature and, more specifically, responsive to "light therapy" (for example, exposure for a period of hours to a bright [2500 lux] full-spectrum fluorescent light). The connection between SAD and appetitive disorders has been remarked on repeatedly (for example, Rosenthal et al., 1986; Wurtman, 1988). Specifically, the depressive phase is associated with overeating, carbohydrate craving, and weight gain. Periodic exposure to bright light produced weight loss in SAD patients, although this effect was accompanied by a decrease in their surprisingly high resting metabolic rate (Gaist et al., 1990). It is tantalizing to imagine that bright sunlight might contribute to the appetite suppression observed in hot environments; however, there is essentially no evidence that normal control subjects' appetites are affected by light exposure. Rats show a transient decline in appetite when exposed to constant light (Dark et al., 1980); but rats are nocturnal feeders, so the extended presence of light would be expected to disrupt feeding briefly, independent of profound physiological changes. The relevance to humans of studies of rats' reactions to extra light is probably negligible.

Effects of Environmental Temperature on Food Preferences
Acute Variations

The discussion above regarding thermic effects of different macronutrients suggests that, in the heat, there should be a relative suppression of the already relatively suppressed (Drewnowski et al., 1989) protein preference/intake. Johnson and Kark (1947), in their survey of wartime military nutrition, found that "regardless of environment, the percentage of proteins voluntarily chosen from the rations was practically constant." Edholm et al. (1964) concur. In mice exposed to hot and cold environments, the only

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

substantial variation was in carbohydrate (starch) intake, which was strongly elevated by cold and suppressed by heat, but not below the level for casein-and lard-supplemented diets (Donhoffer and Vonotzky, 1947). Two restaurant chains reported a decided shift away from sandwiches toward salads in the summer (unpublished data from consumer survey, 1991). Ice cream consumption, which peaks in the summer (unpublished data from consumer survey, 1991), seems to be an exception to the rule of heat-suppressed carbohydrate consumption; however, most observers regard the summer appeal of ice cream to reside in its coldness more than its sweetness. In fact, one ice cream chain reported that while ice cream sales tended to rise with increases in environmental temperature from 72° to 82°F, above 82°F customers switch to more thirst-quenching products (for example, ices and "light" ice creams).

Rothwell and Stock's (1986) casual observations suggested that food selection of rats offered a cafeteria diet was unaffected by variations (from 24° to 29°C) in environmental temperature. As already shown, however, the ability of protein to differentially suppress appetite has probably been overstated; accordingly, it should not be surprising if heat has little observable effect on macronutrient preferences. Ashworth and Harrower (1967) reported that proportional nitrogen loss from sweating is lower than normal in acclimatized tropical workers, again suggesting no need for supplemental protein in the diet, a conclusion seconded by Collins et al. (1971) and Weiner et al. (1972). Still, it would seem a reasonable precaution to maintain protein intake at or slightly above a nutritionally desirable minimum in hot environments, especially before full acclimatization has been achieved.

Seasonal Effects

Donhoffer and Vonotzky (1947) cite well-known seasonal changes in thyroid activity as a possible mediator of the heat-induced differential suppression of carbohydrate intake. How thyroid activity might control qualitative aspects of appetite and whether humans are susceptible to such seasonal variations remain obscure.

The consumer survey yielded fairly strong data regarding shifts in food preference in the summer. As noted above, the restaurant chain specializing in salads had its sales peak during the summer. Not surprisingly, so did the ice cream parlors. Seasonal shifts in consumer preferences, however, may not be driven entirely by physiology. A number of retailers indicated that intense promotional activity of different types of foods occurs on a seasonal basis; conceivably, some of the seasonal shift in preferences actually represents conformity with expectations or financial and social pressures. One hamburger chain claimed that "consumption patterns are marketing driven";

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

that is, people eat what they are told by advertisers or induced by incentives to eat.

CONCLUSIONS AND RECOMMENDATIONS

Research Recommendations

Almost any systematic research on the effects of heat on appetite would be welcome. Beyond the general and vague conclusion that heat suppresses appetite—and possibly renders cooler foods more palatable—researchers are forced to surmise where they would prefer to know. Studies of the following sort would be most desirable, although the list is somewhat arbitrary and certainly not exhaustive:

  • Straightforward studies that examine food intake in environments in which the temperature has been artificially elevated, in comparison with food intake in normal or cooled environments. Such studies should examine (a) quantity consumed, (b) preference shifts among macronutrients and/or basic food groups, and (c) preference shifts for heated versus cooled versions of the same foods.

  • Similar studies conducted in thermoneutral, heated, and cooled environments during summer versus winter. Whether living in an air-conditioned environment mitigates the effects of environmental heat should be investigated.

  • Variations on the foregoing studies in which adaptation periods are varied: (a) short-term adaptations over the course of minutes or hours (as when one acclimates to an air-conditioned room) and (b) long-term adaptation (for example, at the beginning of a heat wave versus after a week or two of a heat wave).

  • Studies on the effects on appetite of humidity manipulations in conjunction with heat manipulations.

  • Studies of the effects of heat on appetite in situations where the subjects' ad lib consumption is monitored with a specific view to determining whether appetite suppression occurs because meal size decreases and meal frequency remains constant, or because meal frequency decreases and meal size stays constant. These studies should address whether heat enhances satiety or impairs hunger.

  • Studies of the thermic effect of different diets. Do different macronutrients have different thermic effects? Enough to bother about?

  • Studies of the thermic effects of food at different temperatures.

  • Studies of the palatability of foods at different temperatures while manipulating environmental temperature and, if possible, body temperature.

  • Alliesthesia studies like that of Cabanac (1971) to determine whether

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

heat suppression of appetite occurs in conjunction with a lowered BW set-point—in which case preference for sweets following a glucose load should decline—or whether heat suppression of appetite occurs in defiance of an unchanged BW set-point—in which case preference for sweet after a glucose load should remain high.

Practical Recommendations for Working in Hot Environments

In general, work in a hot environment demands close attention to factors that might threaten either thermoregulation or BW regulation. In the absence of knowledge about whether these regulatory mechanisms act in conflict or in concert in hot environments, it is probably safest to focus on thermoregulation, which poses the most immediate physiological challenge.

  • Allow for reduced intake. Unless BW falls to dangerously low levels, if heat suppresses appetite, it should be recognized that this as an adaptive strategy in the best interest of the individual's thermoregulatory well-being.

  • Allow for some shifts in food preferences, to be determined empirically. There may be a shift in the preferred macronutrient balance; more likely, there will be a shift in the preferred temperature, toward cooler foods and, especially, beverages.

  • Ensure that protein intake is maintained at a healthy level. This is not likely to require much if any intervention.

  • Encourage adaptation to the heat through regular, graded exposure to the hot environment. During the first few days in a hot environment, exposure should be gradually increased, with care taken to provide opportunities to cool off between exposures. Excessive cooling is not advised, because it will probably interfere with heat adaptation and may conceivably interfere with the adaptive resetting of regulatory set-points.

  • Minimize activity, especially during the first few days of heat exposure. Strenuous exercise provides an additional heat challenge and may disrupt appetite in such a way as to interfere with normal regulatory adaptations. As with heat exposure, exercise may be increased gradually.

  • Women may have more difficulty than men adapting to heat, so the foregoing recommendations should be observed especially closely for women.

REFERENCES

Andersson, B., and B. Larsson 1961 Influence of local temperature changes in the preoptic area and rostral hypothalamus on the regulation of food and water intake. Acta Physiol. Scand. 52:75–89.

Appleman, R.D., and J.C. Delouche 1959 Behavioral, physiological and biochemical responses of goats to temperature 0° to 40°C. J. Anim. Sci. 17:326–335.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

Ashworth, A., and A.D.B. Harrower 1967 Protein requirements in tropical countries: Nitrogen losses in sweat and their relation to nitrogen balance. Br. J. Nutri. 21:833–843.

Baile, C.A., J. Naylot, C.L. McLaughlin, and C.A. Catanzano 1981 Endotoxin elicited fever and anorexia and elfazepam-stimulated feeding in sheep. Physiol. Behav. 27:271–277.

Balagura, S. 1973 Hunger: A Biopsychological Analysis. New York: Basic Books.

Beller, A.S. 1977 Fat and Thin: A Natural History of Obesity. New York: Farrar Straus, & Giroux. Bellward, K., and M.J. Dauncey

1988 Behavioural energy regulation in lean and genetically obese (ob/ob ) mice. Physiol. Behav. 42:433–438.

Bhattacharya, A.N., and R.G. Warner 1968 Influence of varying rumen temperature on central cooling or warming and on regulation of voluntary feed intake in dairy cattle. J. Dairy Sci. 51:1481–1489.

Booth, G., and J.M. Strang 1936 Changes in temperature of the skin following the ingestion of food. Arch. Int. Med. 57:533–543.

Brobeck, J.R. 1948 Food intake as a mechanism of temperature regulation. Yale J. Biol. Med. 20:545–552.

Burse, R.L. 1979 Sex differences in human thermoregulatory response to heat and cold stress. Hum. Factors 21:687–699.


Cabanac, M. 1971 Physiological role of pleasure. Science 17:1103–1107.

Collins, K.J., and J.S. Weiner 1968 Endocrinological aspects of exposure to high environmental temperature. Physiol. Rev. 48:785–839.

Collins, K.J., T.P. Eddy, A. Hibbs, A.L. Stock, and E.F. Wheeler 1971 Nutritional and environmental studies on an ocean-going oil tanker. 2. Heat acclimatization and nutrient balance. Br. J. Indu. Med. 28:246–258.


Dallosso, H.M., and W.P.T. James 1984 Whole-body calorimetry studies in adult men. 2. The interaction of exercise and over-feeding on the thermic effect of a meal. Br. J. Nutr. 52:65–72.

Dark, J., L.L. Rayha, I. Clark-Lane, and V. Kimler 1980 Melatonin and lighting condition: Absence of long-term effects on food intake and body weight regulation in the albino rat. Physiol. Behav. 25:855–857.

DiBella, L., G. Tarozzi, M.T. Rossi, and G. Scalera 1981 Effect of liver temperature increase on food intake. Physiol. Behav. 26:45–51. Donhoffer, S., and J. Vonotzky

1947 The effect of environmental temperature on food selection. Am. J. Physiol. 150:329–333.

Drewnowski, A., E.E. Shrager, C. Lipsky, E. Stellar, and M.R.C. Greenwood 1989 Sugar and fat: Sensory and hedonic evaluation of liquid and solid foods. Physiol. Behav. 45:177–184.


Edholm, O.G., R.H. Fox, R. Goldsmith, I.F.G. Hampton, C.R. Underwood, E.J. Ward, H.S. Wolf, J.M. Adam, and J.R. Allan 1964 Report to the Medical Research Council, No. APRC64/65. London: Army Personnel Research Committee.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

Fantino, M., and M. Cabanac 1984 Effect of a cold ambient temperature on the rat's food hoarding behavior. Physiol. Behav. 32:183–190.

Fletcher, J.M. 1986 Effects on growth and endocrine status of maintaining obese and lean Zucker rats at 22°C and 30°C from weaning. Physiol. Behav. 37:597–602.


Gaist, P.A., E. Obarzanek, R.G. Skwerer, C.C. Duncan, P.M. Shultz, and N.E. Rosenthal 1990 Effects of bright light on resting metabolic rate in patients with seasonal affective disorder and control subjects. Biol. Psychiatry 28:989–996.

Garfinkel, P.E., and D.M. Garner 1982 Anorexia Nervosa: A Multidimensional Perspective. New York: Brunner-Mazel.

Gengler, W.R., F.A. Martz, H.D. Johnson, G.F. Krause, and L. Hahn 1970 Effect of temperature on food and water intake and rumen fermentation. J. Dairy Sci. 53:434–437.

Glick, Z., A. Uncyk, J. Lupien, and L. Schmidt 1989 Meal associated changes in brown fat thermogenesis and glycogen. Physiol. Behav. 45:243–248.


Hamilton, C.L. 1967 Food and temperature. Pp. 303–317 in Handbook of Physiology: Section 6, vol. 1, C.F. Code, ed. Washington, D.C.: American Physiological Society.

Hamilton, C.L., and J.R. Brobeck 1964 Food intake and temperature regulation in rats with rostral hypothalamic lesions. Am. J. Physiol. 207:291–297.

Heath, M.E. 1980 Effects of rearing temperature on the thermoregulatory behavior of pigs. Behav. Neural. Biol. 28:193–202.

Herman, C.P., and F.J. Vaccarino 1992 Appetite. Pp. 79–86 in Encyclopedia of Food Science and Technology, Y.H. Hui, ed. New York: Wiley.

Hogan, S., D.V. Coscina, and J. Himms-Hagen 1982 Brown adipose tissue of rats with obesity-inducing ventromedial hypothalamic lesions. Am. J. Physiol. 243:E338–E344.

Hogan, S., J. Himms-Hagen, and D.V. Coscina 1986 Lack of diet-induced thermogenesis in brown adipose tissue of obese medial hypothalamic-lesioned rats. Physiol. Behav. 35:287–294.


Jakubczak, L.F. 1976 Food and water intakes of rats as a function of strain, age, temperature, and body weight. Physiol. Behav. 17:251–258.

Johnson, R.E., and R.M. Kark 1947 Environment and food intake in man. Science 105:378–379.


Keys, A., J. Brôzek, A. Henschel, O. Mickelson, and L.L. Taylor 1950 The Biology of Human Starvation. Minneapolis, Minn.: University of Minnesota Press.

Korhonen, H., and M. Harri 1986 Seasonal changes in energy economy of farmed polecat as evaluated by body weight, food intake and behavioral strategy. Physiol. Behav. 37:777–783.

Kraly, F.S., and E.M. Blass 1976 Increased feeding in rats in a low ambient temperature. Pp. 77–89 in Hunger: Basic Mechanisms and Clinical Implications, D. Novin, W. Wyrwicka and G.A. Bray, eds. New York: Raven Press.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

LeBlanc, J., and M. Cabanac 1989 Cephalic postprandial thermogenesis in human subjects. Physiol. Behav. 46:479–482.

LeBlanc, J., and P. Diamond 1986 Effects of meal size and frequency on postprandial thermogenesis in dogs. Am. J. Physiol. 250:E144–E147.

Leon, M., and B. Woodside 1983 Energetic limits on reproduction: Maternal food intake. Physiol. Behav. 30:945–957.

Logue, A.W. 1986 The Psychology of Eating and Drinking. New York: W. H. Freeman.


Macari, M., S.M.F. Zuim, E.R. Secato, and J.R. Guerreiro 1986 Effects of ambient temperature and thyroid hormones on food intake by pigs. Physiol. Behav. 36:1035–1039.

McCarthy, D.O., M.J. Kluger, and A.J. Vander 1984 The role of fever in appetite suppression after endotoxin administration. Am. J. Clin. Nutr. 40:310–316.

1986 Effect of centrally administered interleukin-1 and endotoxin on food intake of fasted rats. Physiol. Behav. 36:745–749.

Mrosovsky, N. 1990 Rheostasis: The Physiology of Change. New York: Oxford.

Mrosovsky, N., L.A. Molony, C.A. Conn, and M.J. Kluger 1989 Anorexic effects of interleukin I in the rat. Am. J. Physiol. 257:R1315–R1321.

Murray, M.J., and A.B. Murray 1977 Starvation suppression and refeeding activation of infection. Lancet 1:123–125.


Nisbett, R.E. 1972 Hunger, obesity, and the ventromedial hypothalamus. Psychol. Rev. 79:433–453.


O'Reilly, B., A.J. Vander, and M.J. Kluger 1989 Effects of chronic infusion of liposaccharide on food intake and body temperature of the rat. Physiol. Behav. 42:287–291.


Pénicaud, L., D.A. Thompson, and J. Le Magnen 1986 Effects of 2-deoxy-d-glucose on food and water intake and body temperature in rats. Physiol. Behav. 36:431–435.


Rampone, A.J., and P.J. Reynolds 1991 Food intake regulation by diet induced thermogenesis. Med. Hypotheses. 34:7–12.

Refinetti, R. 1988 Effects of food temperature and ambient temperature during a meal on food intake in the rat. Physiol. Behav. 43:245–247.

Rolls, B.J., I.C. Federoff, J.F. Guthrie, and L.J. Laster 1990 Effects of temperature and mode of presentation of juice on hunger, thirst and food intake in humans. Appetite 15:199–208.

Rosenthal, N.E., M. Genhart, F.M. Jacobsen, R.G. Skwerer, and T.A. Wehr 1986 Disturbances of appetite and weight regulation in seasonal affective disorder. Ann. N.Y. Acad. Sci. 499:216–230.

Rothwell, N.J., and M.J. Stock 1986 Influence of environmental temperature on energy balance, diet-induced thermogenesis and brown fat activity in "cafeteria"-fed rats. Br. J. Nutr. 56:123–129.


Segal, K.R., B. Gutin, J. Albu, and F.X. Pi–Sunyer 1987 Thermic effect of food and exercise in lean and obese men of similar lean body mass. Am. J. Physiol. 252:E110–E117.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

Strominger, J.L., and J.R. Brobeck 1953 A mechanism of regulation of food intake. Yale J. Biol. Med. 25:383–390.

Swiergiel, A.H., and D.I. Ingram 1986 Effect of diet and temperature acclimation on thermoregulatory behavior in piglets. Physiol. Behav. 36:637–642.

Szlyk, P., I.V. Sils, R.P. Francesconi, R.W. Hubbard, and L.E. Armstrong 1989 Effects of water temperature and flavoring on voluntary dehydration in man. Physiol. Behav. 45:639–647.

Thurlby, P.L. 1979 Ph.D. dissertation. Studies on thermoregulatory thermogenesis in relation to energy balance in genetically obese (ob/ob) mice. D35261/79 AX: Cambridge University.

Trant, A.S., and R.M. Pangborn 1983 Discrimination, intensity, and hedonic responses to color, aroma, viscosity, and sweetness of beverages. Lebens. Wissen. Technol. 16:147–152.


Weiner, J.S., J.O.C. Willson, H. EI–Neil, and E.F. Wheeler 1972 The effect of work level and dietary intake on sweat nitrogen losses in a hot climate. Br. J. Nutr. 27:543–552.

Wilson, L.M., and H.L. Sinha 1985 Thermal preference behavior of genetically obese (ob/ob) and genetically lean (+/?) mice. Physiol. Behav. 35:545–548.

Wurtman, J.J. 1988 Carbohydrate craving, mood changes, and obesity. J. Clin. Psychiatry 49:37–39.

Discussion

DR. NESHEIM: Any questions?

PARTICIPANT: Mike Sawka mentioned yesterday that discomfort is closely related to skin temperature. I wonder if you think that a feeling of discomfort in the heat would also affect appetite, and if that might be part of the appetite suppression mechanism—as opposed to solely internal body temperature?

DR. HERMAN: Certainly. I know that if you manipulate skin temperature directly, at least in nonhuman animals, that you will get a suppression of appetite. Of course we don't have subjective discomfort ratings in that situation, but I can't help but think heat discomfort would be very much a factor.

PARTICIPANT: Do you know of any studies that have tried to pinpoint whether it was blood temperature, skin temperature, a certain anatomical section, or physiological section that might be impacting on that sensation of heat discomfort?

DR. HERMAN: No, the manipulation was too crude and the measurement was just done at the skin surface. We also don't know whether there were cascading effects to the internal environment.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×

We know that heating deep core organs like the hypothalamus in animals will have the same effect. So my guess would be that almost anywhere along the chain that you apply heat, it is likely to have a suppressive effect on appetite.

Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
This page in the original is blank.
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 187
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 188
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 189
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 190
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 191
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 192
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 193
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 194
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 195
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 196
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 197
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 198
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 199
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 200
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 201
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 202
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 203
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 204
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 205
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 206
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 207
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 208
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 209
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 210
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 211
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 212
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 213
Suggested Citation:"10. Effects of Heat on Appetite." Institute of Medicine. 1993. Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. Washington, DC: The National Academies Press. doi: 10.17226/2094.
×
Page 214
Next: 11. Situational Influences on Food Intake »
Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations Get This Book
×
Buy Paperback | $100.00
MyNAP members save 10% online.
Login or Register to save!
Download Free PDF

This volume examines the current state of knowledge concerning the influence of a hot environment on nutrient requirements of military personnel. A parallel concern is ensuring that performance does not decline as a result of inadequate nutrition.

The committee provides a thorough review of the literature in this area and interprets the diverse data in terms of military applications. In addition to a focus on specific nutrient needs in hot climates, the committee considers factors that might change food intake patterns and therefore overall calories. Although concern for adequate nutrition for U.S. soldiers in Saudi Arabia prompted the initiation of this project, its scope includes the nutrient needs of individuals who may be actively working in both hot-dry and hot-moist climates.

  1. ×

    Welcome to OpenBook!

    You're looking at OpenBook, NAP.edu's online reading room since 1999. Based on feedback from you, our users, we've made some improvements that make it easier than ever to read thousands of publications on our website.

    Do you want to take a quick tour of the OpenBook's features?

    No Thanks Take a Tour »
  2. ×

    Show this book's table of contents, where you can jump to any chapter by name.

    « Back Next »
  3. ×

    ...or use these buttons to go back to the previous chapter or skip to the next one.

    « Back Next »
  4. ×

    Jump up to the previous page or down to the next one. Also, you can type in a page number and press Enter to go directly to that page in the book.

    « Back Next »
  5. ×

    Switch between the Original Pages, where you can read the report as it appeared in print, and Text Pages for the web version, where you can highlight and search the text.

    « Back Next »
  6. ×

    To search the entire text of this book, type in your search term here and press Enter.

    « Back Next »
  7. ×

    Share a link to this book page on your preferred social network or via email.

    « Back Next »
  8. ×

    View our suggested citation for this chapter.

    « Back Next »
  9. ×

    Ready to take your reading offline? Click here to buy this book in print or download it as a free PDF, if available.

    « Back Next »
Stay Connected!