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Effects of mouth dryness on drinking behavior and beverage acceptability
Physiology & Behavior 76 (2002) 423 – 429
Effects of mouth dryness on drinking behavior and beverage acceptability Jeffrey M. Brunstrom* Department of Human Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, UK Accepted 28 March 2002
Abstract In humans, the association between mouth dryness and thirst has been examined in a variety of contexts. Typically, drinking behavior produces a concomitant reduction in unpleasant dry mouth sensations. Evidence is reviewed for a mechanism that influences the termination of drinking behavior by metering this change. Drinking behavior causes a progressive increase in parotid saliva flow. Thus, one possibility is that satiety results from a decrease in the reward associated with mouth wetting during a drinking episode. Beverages can differ in their satiating ability. This variability may be related to their mouth-wetting characteristic, and may be reflected in a shift in their acceptability when the mouth becomes dry. Physically drying the mouth appears to increase the acceptability of beverages that are either cold or acidic. It may be significant that two important determinants of mouth wetting are temperature and acidity. Cold or acidic beverages are also likely to be regarded as ‘thirst-quenching.’ Thus, shifts in acceptability, ‘thirst quenching’ and satiety may all be related to the mouth-wetting properties of a beverage. The extent to which this coincidence is meaningful warrants further investigation. However, if a common underlying process exists, then this may help to elucidate reasons for voluntary dehydration and aberrant drinking behavior in the elderly. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Human thirst; Review; Saliva; Flavor preference; Mouth dryness
1. Introduction Thirst and the feeling of dryness in the mouth covary. This observation led to early speculation about the mechanism governing thirst [1]. This ‘dry mouth theory’ proposed that the functioning of the salivary glands becomes impaired over time and that thirst constitutes a need to alleviate the unpleasant symptoms that result when they fail to moisten the mouth adequately. Experientially, this is an appealing idea. It is simple, and there is good supporting evidence. Thirst can be alleviated, albeit temporarily, by rinsing the mouth with water. Moreover, this mouth-wetting effect can be evoked by manipulating salivary gland activity directly. Mastication and other mouth movements can increase the volume of parotid saliva in the main oral cavity. Thus, in desert conditions, thirst can be alleviated by placing insoluble objects in the mouth [2]. Despite the close relationship between mouth state and thirst, establishing causality has proved more difficult. Early
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studies explored drinking behavior following injections of pilocarpine or atropine, both of which are known to increase saliva flow. Unfortunately, these studies yielded inconsistent findings [3 –6]. One explanation is that their animals were forced into a ‘depressed malaise’ as a result of drug administration [7]. Moreover, the effects of drugs such as atropine and pilocarpine are likely to be confounded by their more central effects on the central cholinergic system, which may influence drinking behavior. For this reason, some dry mouth theorists examined water-seeking activity after mechanically impairing natural saliva production. Experiments with salivarectomized dogs show that this procedure can increase drinking behavior [8,9]. However, an alternative explanation is that drinking behavior is otherwise aimed at maintaining moisture over the surface of the tongue, the purpose of which is to promote evaporation to maintain thermoregulation [10]. A major problem for the dry mouth theory is that sham drinking appears to have little effect on suppressing future drinking [11]. This was found to be the case despite the fact that the mouth was held constantly moist, implying that drinking was rewarding for reasons other than mouth wetting. The dry mouth theory was finally superseded by
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the discovery of osmoreceptors and a role for the lateral hypothalamus [12]. This discovery, and others since, has shown that thirst can be generated more centrally. Specifically, it appears to be mediated by at least two processes. Osmometric thirst is associated with a change in the solute concentration of the interstitial fluid [13], and volumetric thirst is associated with depletion of intravascular volume (hypovolemia), arising from vomiting, diarrhea, or a hemorrhage [14]. Integration of signals from osmometric and volumetric thirst appears to be governed by the median preoptic nucleus [15]. In recent years, our understanding of the nature and interaction of the mechanisms that initiate and terminate animal drinking behavior has increased considerably [16]. Despite this, it is unclear whether or not these models can account for much of the fluid intake that is observed in humans. This is because most drinking behaviors are nonhomeostatic, and do not occur in response to a specific deficit. This point is illustrated in one study in which subjects were given free access to water over a 24-h period [17]. Subjects felt thirsty and drank mainly in association with eating. This was the case despite the fact that they remained euhydrated throughout. (There were no concomitant changes in body fluid variables—haematocrit, plasma osmolality, sodium, potassium, protein, and angiotensin II.) Why then is thirst experienced? One possibility is that when water is readily available, humans experience thirst in order to anticipate future fluid deficit [17]. It is noteworthy that the subjects in this study attributed part, if not all, of their thirst to oral sensations, such as a dry unpleasant taste or to viscid saliva in the mouth. This is important because it implies that while mouth dryness is not exclusively the ‘seat’ of thirst (as previously proposed [1]), it may still influence aspects of normal everyday drinking behavior. This possibility is considered here.
2. Effects of mouth dryness on human drinking behavior After the onset of a drinking episode, a set of inhibitory mechanisms operates to meter and then terminate drinking behavior. The signals that are generated can be described as oropharyngeal, gastrointestinal, or postabsorptive in origin. Oropharyngeal stimulation may act to inhibit AVP release [18 – 20] and gastrointestinal inhibition appears, in the first instance, to result from mechanical gastric distension [21]. Together, these signals are generated in an overlapping temporal sequence that combines to produce a continuous inhibitory signal that limits further ingestion [22]. These preabsorptive satiety signals can account for the finding that dehydrated humans experience a marked reduction in thirst within minutes of drinking, long before absorption begins [2]. As drinking behavior terminates, changes also occur in the mouth. After 24 h of water deprivation, the most salient sensation reported is that of a dry ‘tacky’ mouth [23]. However, after an initial bout of drinking, subjects report
a marked attenuation of mouth dryness. Interestingly, smaller bouts of drinking, during a 1-h period following water access, are attributed to fluctuations in unpleasant oral sensation [23]. To explore the relationship between thirst and mouth dryness in more detail, one study explored changes in visual ratings of thirst and mouth dryness in thirsty males and females [24]. Measures were taken before and 0, 2.5, and 5 min after the participants ingested either 150 or 400 ml of water. This study reports a relationship between thirst reduction and changes in mouth dryness, in the measures taken at 2.5 and 5 min. Furthermore, the reduction in thirst and mouth dryness appears to be volume-dependent. A 400-ml sample reduces both thirst and mouth dryness to a greater extent than a 150-ml sample. This observation led to speculation that if saliva production increases monotonically with drinking behavior, then increasing mouth wetness will produce an attenuating incentive to continue to drink. This is because an increase in saliva production will remove mouth dryness, thereby reducing the reward offered by the mouth-wetting effect of drinking behavior [24]. In a related study, this hypothesis was tested explicitly by physically manipulating the state of the mouth [25]. Subjects were tested in both a dry mouth and a control condition. In the dry mouth condition, they exercised intensively for 20 min. Afterwards, the participants placed two absorbent cotton wool dental rolls in each cheek, adjacent to the upper and the lower teeth with the mouth closed. They were then instructed to drink water freely through a straw, and were told to do so until they no longer wished to continue. During this drinking episode, the subjects were free to take pauses in their drinking activity. Measures were taken of the duration of each bout and interbout interval. The control condition was identical except that the participants placed only a single roll in each cheek, adjacent to the lower teeth. The tactile experience of one roll was much like that of having two rolls in each cheek. Despite this, pilot testing confirmed that two rolls in each cheek reduced saliva volume in the main oral cavity much more effectively than one roll. Drinking in the dry mouth and control condition differed significantly. In the dry mouth condition, participants drank for longer, drank with a greater number of bouts, and drank a greater volume of water (see Table 1).
Table 1 Mean (S.D.) drinking episode, number of bouts of drinking, and volume ingested in the dry mouth and the control condition (data from Brunstrom et al. [25]) Condition
Drinking episode (s)*
Number of bouts**
Volume ingested (ml)**
Control Dry mouth
69.3 (53.8) 93.8 (72.5)
4.7 (3.2) 7.0 (3.5)
300 (147.7) 428 (204.7)
The superscripts * and ** refer to the statistical reliability of the withinsubject difference between each condition. * P<.015. ** P<.001.
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Since water was ingested freely in both conditions, it is unlikely that the effect of the saliva barrier should be attributed to the inhibition of AVP that is associated with swallowing [19,20], or to other satiety cues generated further down the gastric tract. An analysis of the microstructure of each drinking episode indicated that the pattern of drinking behavior did not differ greatly across conditions. Instead, it appears that the size of the saliva barrier served only to modulate the duration of natural drinking behavior. Augmented drinking activity was attributed to a difference in the effectiveness of the saliva barrier during the interbout intervals. More specifically, across successive interbout intervals, the barrier may extend the period during which continued drinking behavior is rewarded by relief from mouth dryness. Consistent with this theorizing, the pleasantness of a water sample is found to decrease throughout a drinking episode when it is used to rehydrate following a period of water deprivation [2]. If restricting the free movement of saliva around the mouth can influence drinking behavior, then under normal circumstances, natural changes in mouth dryness may help to meter fluid intake. At present, the extent to which this process acts as a useful satiety cue is unclear. Likewise, the time course of this cue relative to satiety signals generated further down the gastric tract remains to be determined. However, we do know that beverages differ in the extent to which they elicit a salivary response. Thus, one indication that mouth state changes are important to human drinking behavior would be evidence that mouth-wetting beverages are selected to alleviate thirst. Section 3 reviews evidence of this kind.
3. Thirst quenching and flavor preference The diversity of human drinking behavior can be attributed largely to the efficiency of our kidneys. When fluid is freely available, we have the luxury to consume a variety of different beverages, often at different times of the day, and in different contexts. Drinking caffeinated or alcoholic drinks can account for a major proportion of daily fluid intake [26]. However, there are considerable individual and cultural differences in the preferred flavor of beverages that contain these drugs. Much of our drinking behavior occurs during meal times [27,28]. This activity might serve to anticipate future fluid deficits, or possibly it occurs out of habit to aid the mastication process. Either way, the nature and the flavor of the beverage are likely to vary considerably across cultures, and are quite likely to be chosen to complement the meal itself. Despite this diversity in flavor preferences and drinking habits, beverages that are used to slake thirst have characteristics that appear to be selected almost universally. Here, the origin of two attributes, temperature and acidity, will be considered. Both are associated with the mouth-wetting characteristics of a beverage.
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3.1. The role of beverage temperature Very hot and very cold substances elicit production of watery parotid saliva. This reflex may serve as a ‘saliva buffer,’ acting to mitigate the temperature of the object in the mouth [29,30]. The close relationship between temperature and saliva production was explored in one study in which saliva was collected over a 6-min period, using a vacuum cap [31]. Every 30 s, assessors swilled their mouths with distilled water for 5 s and then expectorated. Water samples at 0 and 55 °C were found to induce significantly higher flow rates than intermediate samples at 22 and 37 °C. The question of whether or not we are able to distinguish between the effects of warm and cold temperatures has only recently been explored systematically. In one study, thirsty subjects completed visual ratings of mouth dryness before and after drinking a water sample served at either 5 or 22 °C [24]. After ingesting the 5 °C sample, ratings were reduced relative to those for the warmer sample. If the termination of drinking behavior is influenced by the extent to which changes occur in mouth dryness, then two predictions follow. First, cooler beverages may offer greater immediate relief from thirst. Second, a cold beverage will be regarded as more acceptable when it is used to slake thirst. This is because cold temperatures offer greater reward in terms of a reduction of the unpleasant dry mouth symptoms that are associated with thirst. These predictions are considered in turn. 3.1.1. Temperature and thirst reduction An association between beverage temperature and drinking behavior has been reported extensively, both in animals and in humans. In dehydrated rats, cold water availability has a suppressive effect on water consumption relative to warmer samples served near body temperature [32,33]. In contrast, humans may drink more cold water than warm water during prolonged periods of exercise [34,35]. However, when thirsty humans are offered a very short period of time to rehydrate, cold (0 °C) water is ingested less than water at 16 °C [36]. This implies that cold water is particularly satiating during the period immediately following a bout of drinking. It is also consistent with recent speculation that the cooling effect of menthol can offer immediate reduction from thirst [37]. However, an alternative interpretation is that the cold (0 °C) water sample was ingested to a lesser extent because water has aversive properties when served at this extreme temperature. The problem with intake measures is that they only reflect a person’s predilection for a particular fluid. They do not necessarily reveal the potential of a water sample to reduce motivation to continue drinking. In humans, the best way to explore changes in thirst is to use some form of analogue rating scale. One study found that during ad libitum drinking over 6 h of 30/30 min work/rest, cold water produced lower thirst ratings than warm water [38]. Unfortunately, interpreting this result is difficult because intake differences
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confound conclusions regarding the satiating ability of water at different temperatures. Moreover, this study was concerned with postabsorptive rather than preabsorptive effects of temperature on thirst. Only two studies have systematically examined the short-term effects of beverage temperature on thirst satiety (i.e., observed the reduction in thirst that results from the ingestion of equal-volume drinks served at different temperatures). The effect of temperature on thirst ratings was explored after lunchtime drinking of vegetable juice, served at either 1 or 61 –62 °C [39]. This study found that in male subjects, a cold 400-ml sample reduced thirst ratings more effectively than a warm sample. However, this was not the case in a female group that received 300-ml samples. The authors of this study acknowledge that the volume of the test sample was confounded with the assessor’s gender, making it difficult to attribute differences unequivocally either to gender or to volume. This issue was addressed in a subsequent study in which thirsty males and females were provided water samples both at different temperatures and at different volumes [24]. In both males and females, 5 °C water reduced thirst ratings more than 22 °C water, although in each case, this effect was dependent on the volume of water ingested and the specific method of assessing thirst. 3.1.2. Temperature and acceptability The sparse research exploring the effects of temperature on short-term reductions in thirst contrasts with the abundance of studies exploring its effect on beverage acceptability. When thirsty, both humans and laboratory animals tend to choose water served at lower temperatures [32,35,38, 40,41]. In rats, the advantage gained by this predisposition remains unclear. However, some studies suggest that the reward offered by drinking cool water results directly from cooling the mouth rather than from a reduction in core temperature or thirst [33]. Thus, rats appear to be rewarded by licking cool air streams [42] or cold metal [43]. However, in humans, the relationship between cool water preference and thirst is less equivocal. In one study, exercise-induced thirst increased the palatability of 16 °C water more than that of warmer water (22 and 38 °C) [34]. Water at 5 °C also increased in palatability more than these warmer samples. However, reliable effects of exercise were found only for the 16 °C sample. In a similar study, hydrated and dehydrated groups rated 10 °C water as being most pleasant [36]. However, dehydrated assessors found the 0 °C sample to be as pleasant as the 10 °C sample, whereas the control group found it significantly less pleasant than the 10 °C sample. One possibility is that these hydration-dependent shifts in preference are governed by mouth state changes rather than by any of the other physiological consequences of dehydration. In other words, we prefer cold water when we become thirsty because it offers greater relief from mouth dryness than water served at warmer temperatures. One way to test this hypothesis is to determine whether hydration-
dependent shifts in cold water preference can be replicated by manipulating only mouth state. In a recent study, this possibility was explored by testing subjects both in a dry mouth and a control condition [44]. In the dry mouth condition, subjects placed two cotton wool dental rolls in each cheek. This inhibits movement of parotid saliva into the main oral cavity, causing the mouth to become dry. After 2 min, the dental rolls were removed and the subjects then immediately tasted and rated a water sample served at 3, 13, 23, or 33 °C. Measures taken earlier confirmed that the 3 °C sample elicits significantly more salivation that the warmer samples. Since this sample will offer the greatest reward in terms of mouth wetting, the mouth-drying procedure was expected to increase preference for samples served at that temperature. This is exactly what happened. Artificial mouth drying selectively increased preference for the cold water (3 °C) and no significant shifts in preference were found for the warmer samples. The authors of this study concede that the origin of thirst-induced cold water preference is probably complex. Nevertheless, their account does offer a logical explanation for our universal preference for cold rather than tepid beverages when we are thirsty. Finally, one type of beverage that is commonly regarded as thirst quenching is hot tea. One explanation for this is that tea is preferred for much the same reason as cold water. As with cold water, hot tea will elicit a strong salivary response [31]. Thus, hot tea and cold water may both offer greater alleviation of dry mouth symptoms than beverages served at intermediate temperatures. To date, this hypothesis remains unexplored. 3.2. The role of beverage acidity If the acceptability of cold water is modulated by the extent to which it alleviates mouth dryness, then it follows that any mouth-wetting beverage may be susceptible to similar shifts in hedonic value. In addition to hot and cold substances, acids found in foods and beverages also elicit a marked increase in saliva production [45]. This reflex helps to dilute the harmful effects of acids or alkalis that can lead to tooth decay [46]. In one study [47], this hypothesis was investigated using the same mouth-drying procedure that was used to explore the interaction between mouth state and temperature preference (see Section 3.1.2) [44]. In a preliminary experiment, measures were taken of the volume of saliva in the mouth following ingestion of a lime drink served with one of three different citric acid concentrations (0, 1.75, and 3.5 g/1000 ml). As expected, acid concentration and saliva volume were related monotonically. Next, flavor preference was assessed in a dry mouth condition and a control condition. The results from this study indicate that mouth drying does increase flavor preference, but only in the lime drink having the highest citric acid concentration (3.5 g/1000 ml). This finding is important because it implies that shifts in hedonic value are not exclusive to cold water, but may be more commonplace, such that any mouth-
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wetting drink will increase in acceptance when the mouth becomes dry. Few studies have explored which features of a beverage contribute to whether or not it is labeled as ‘thirst-quenching.’ In one study, this issue was explored using focus group and sensory testing methods [48]. A focus group of consumers regarded the attributes—acidity, stringency, carbonation, fruitiness, flavor strength, sweetness, and thickness—to be all characteristics that are likely to influence a drink’s thirstquenching properties. Using correspondence analysis to relate consumer assessments of thirst-quenching character and acceptability to descriptive ratings by a trained panel, acidity was found to be the characteristic most associated with ‘thirst quenching,’ while sweetness and thickness were least associated. Unfortunately, temperature was not included in this analysis. Nevertheless, it seems highly likely that cold temperatures are better associated with ‘thirst quenching’ than tepid or warm temperatures. Thus, there appears to be a correspondence between characteristics that contribute to use of the term ‘thirst quenching’ and those that have the capacity to alleviate mouth dryness. If normal drinking behavior and beverage selection are influenced by mouth state changes, then it is plausible that this process also plays some role in situations where aberrant drinking behavior occurs. This possibility is considered briefly in Section 4.
4. Mouth state and adequate fluid replacement The term ‘voluntary dehydration’ is used to describe a situation in which fluid intake fails to match water losses, even under conditions where there is ample water freely available [40]. Flavoring is important because it can prevent, or at least reduce the risk of, voluntary dehydration [41]. The interactive effect of flavoring and beverage temperature has also been explored [35,38]. In one study, subjects were given free access to liquids during a period of exercise in a climatic chamber [35]. Flavoring and cooling effects on ad libitum intake were additive and increased by over 100% relative to a group who received warm (ambient temperature) disinfected (unpalatable) water. Flavoring water will increase its overall acceptance, and it may be this fact alone that is responsible for an increase in intake [49]. However, it is noteworthy that it is often acidic fruit flavorants that are added to samples used in these studies [50,51]. In particular, ‘grape’ flavor has been found to be particularly good at promoting adequate fluid intake [50,51]. Thus, one possibility is that, among other things, acidic flavorants increase the reward that is experienced by the act of drinking and, hence, beverages with this characteristic are ingested in greater quantities over time for this reason. In relation to this hypothesis, it would be interesting to compare the extent to which voluntary dehydration occurs when wetting and nonwetting beverages are readily available during exercise.
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Problems with thirst and hydration are not limited to situations were humans engage in rigorous exercise. There is now reasonable evidence that thirst declines as age increases [52,53]. Elderly people also appear to have a diminished renal capacity, making it difficult to produce urine with a high osmolality [54]. Consequently, after 24 h of complete water deprivation, healthy elderly men consume insufficient water to rehydrate themselves to predeprivation levels [52]. There are several reasons why thirst may be impaired. For example, thirst may be associated with changes in central levels of dopamine, which reduces with age [55], and may facilitate drinking behavior [56]. Alternatively, attenuated thirst may be related to diminished functioning of central volume receptors [57,58]. Although it is commonly believed that salivary function decreases with age, recent evidence suggests that there is no significant decrease in major salivary gland function [59 – 61]. Nevertheless, elderly people report fewer oropharyngeal symptoms such as mouth dryness compared with healthy young control subjects [59,62]. The reason for this difference is unclear, but may be attributed to age-dependent differences in taste sensitivity or salivary constituents. Either way, one possibility is that age-dependent deficits in thirst may be related to differences in sensitivity to changes in mouth feel. To test this, one might examine whether or not the drinking behavior and flavor preferences of elderly people can be modulated by a saliva barrier of the kind used in recent studies [25,44,47] and described elsewhere in this review.
5. Concluding remarks Since the rejection of the dry mouth theory of thirst [1], very little attention has been paid to the possibility that mouth dryness influences everyday ingestion of fluids. This is probably because research activity has focused primarily on more central homeostatic mechanisms and because, until recently, we have lacked appropriate techniques to manipulate mouth state directly. The evidence presented here suggests that changes in mouth state are not simply a byproduct of drinking activity. Rather, they may have subtle yet cogent effects on flavour acceptability and thirst satiety. In this regard, it is noteworthy that those beverage characteristics that elicit saliva production (acidity and a cold temperature) are (a) likely to be labelled ‘thirst-quenching,’ (b) are likely to be chosen and ingested in greater quantities when we are thirsty, and (c) are most sensitive to hedonic shifts caused by increases in mouth dryness. Further research is now warranted in order to determine whether this is mere coincidence, or whether a common mechanism underlies these findings. Once this is established, we may be better placed to understand whether or not this process contributes to voluntary dehydration and age-related problems associated with attenuated levels of thirst.
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avp secretion in dehydrated elderly men. Ann NY Acad Sci 1993; 689:651 – 5. Phillips PA, Johnston CI, Gray L. Disturbed fluid and electrolyte homeostasis following dehydration in elderly people. Age Ageing 1993;22(1):s26 – 33. Morgan DG, Finch CE. Dopaminergic changes in the basal ganglia. A generalized phenomenon of aging in mammals. Ann NY Acad Sci 1988;515:145 – 60. Zabik JE, Sprague JE, Odio M. Interactive dopaminergic and noradrenergic systems in the regulation of thirst in the rat. Physiol Behav 1993;54:29 – 33. Stachenfeld NS, DiPietro L, Nadel ER, Mack GW. Mechanism of attenuated thirst in aging: role of central volume receptors. Am J Physiol 1997;272:R148 – 57.
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[58] Kenny W, Chiu P. Influence of age on thirst and fluid intake. Med Sci Sport Exercise 2000;33(9):1524 – 32. [59] Ship JA, Fischer DJ. The relationship between dehydration and parotid salivary gland function in young and older healthy adults. J Gerontol, Ser A 1997;52(5):M310 – 9. [60] Ghezzi EM, Lange LA, Ship JA. Determination of variation of stimulated salivary flow rates. J Dent Res 2000;79(11):1874 – 8. [61] Ship JA, Nolan NE, Puckett SA. Longitudinal analysis of parotid and submandibular salivary flow-rates in healthy, different-aged adults. J Gerontol, Ser A 1995;50(5):m285 – 9. [62] Rolls BJ, Phillips PA. Aging and disturbances of thirst and fluid balance. Nutr Rev 1990;48(3):137 – 44.
Effects of mouth dryness on drinking behavior and beverage acceptability Jeffrey M. Brunstrom* Department of Human Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, UK Accepted 28 March 2002
Abstract In humans, the association between mouth dryness and thirst has been examined in a variety of contexts. Typically, drinking behavior produces a concomitant reduction in unpleasant dry mouth sensations. Evidence is reviewed for a mechanism that influences the termination of drinking behavior by metering this change. Drinking behavior causes a progressive increase in parotid saliva flow. Thus, one possibility is that satiety results from a decrease in the reward associated with mouth wetting during a drinking episode. Beverages can differ in their satiating ability. This variability may be related to their mouth-wetting characteristic, and may be reflected in a shift in their acceptability when the mouth becomes dry. Physically drying the mouth appears to increase the acceptability of beverages that are either cold or acidic. It may be significant that two important determinants of mouth wetting are temperature and acidity. Cold or acidic beverages are also likely to be regarded as ‘thirst-quenching.’ Thus, shifts in acceptability, ‘thirst quenching’ and satiety may all be related to the mouth-wetting properties of a beverage. The extent to which this coincidence is meaningful warrants further investigation. However, if a common underlying process exists, then this may help to elucidate reasons for voluntary dehydration and aberrant drinking behavior in the elderly. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Human thirst; Review; Saliva; Flavor preference; Mouth dryness
1. Introduction Thirst and the feeling of dryness in the mouth covary. This observation led to early speculation about the mechanism governing thirst [1]. This ‘dry mouth theory’ proposed that the functioning of the salivary glands becomes impaired over time and that thirst constitutes a need to alleviate the unpleasant symptoms that result when they fail to moisten the mouth adequately. Experientially, this is an appealing idea. It is simple, and there is good supporting evidence. Thirst can be alleviated, albeit temporarily, by rinsing the mouth with water. Moreover, this mouth-wetting effect can be evoked by manipulating salivary gland activity directly. Mastication and other mouth movements can increase the volume of parotid saliva in the main oral cavity. Thus, in desert conditions, thirst can be alleviated by placing insoluble objects in the mouth [2]. Despite the close relationship between mouth state and thirst, establishing causality has proved more difficult. Early
* Tel.: +44-1509-223048; fax: +44-1509-223940. E-mail address: [email protected] (J.M. Brunstrom).
studies explored drinking behavior following injections of pilocarpine or atropine, both of which are known to increase saliva flow. Unfortunately, these studies yielded inconsistent findings [3 –6]. One explanation is that their animals were forced into a ‘depressed malaise’ as a result of drug administration [7]. Moreover, the effects of drugs such as atropine and pilocarpine are likely to be confounded by their more central effects on the central cholinergic system, which may influence drinking behavior. For this reason, some dry mouth theorists examined water-seeking activity after mechanically impairing natural saliva production. Experiments with salivarectomized dogs show that this procedure can increase drinking behavior [8,9]. However, an alternative explanation is that drinking behavior is otherwise aimed at maintaining moisture over the surface of the tongue, the purpose of which is to promote evaporation to maintain thermoregulation [10]. A major problem for the dry mouth theory is that sham drinking appears to have little effect on suppressing future drinking [11]. This was found to be the case despite the fact that the mouth was held constantly moist, implying that drinking was rewarding for reasons other than mouth wetting. The dry mouth theory was finally superseded by
0031-9384/02/$ – see front matter D 2002 Elsevier Science Inc. All rights reserved. PII: S 0 0 3 1 - 9 3 8 4 ( 0 2 ) 0 0 7 6 2 - X
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the discovery of osmoreceptors and a role for the lateral hypothalamus [12]. This discovery, and others since, has shown that thirst can be generated more centrally. Specifically, it appears to be mediated by at least two processes. Osmometric thirst is associated with a change in the solute concentration of the interstitial fluid [13], and volumetric thirst is associated with depletion of intravascular volume (hypovolemia), arising from vomiting, diarrhea, or a hemorrhage [14]. Integration of signals from osmometric and volumetric thirst appears to be governed by the median preoptic nucleus [15]. In recent years, our understanding of the nature and interaction of the mechanisms that initiate and terminate animal drinking behavior has increased considerably [16]. Despite this, it is unclear whether or not these models can account for much of the fluid intake that is observed in humans. This is because most drinking behaviors are nonhomeostatic, and do not occur in response to a specific deficit. This point is illustrated in one study in which subjects were given free access to water over a 24-h period [17]. Subjects felt thirsty and drank mainly in association with eating. This was the case despite the fact that they remained euhydrated throughout. (There were no concomitant changes in body fluid variables—haematocrit, plasma osmolality, sodium, potassium, protein, and angiotensin II.) Why then is thirst experienced? One possibility is that when water is readily available, humans experience thirst in order to anticipate future fluid deficit [17]. It is noteworthy that the subjects in this study attributed part, if not all, of their thirst to oral sensations, such as a dry unpleasant taste or to viscid saliva in the mouth. This is important because it implies that while mouth dryness is not exclusively the ‘seat’ of thirst (as previously proposed [1]), it may still influence aspects of normal everyday drinking behavior. This possibility is considered here.
2. Effects of mouth dryness on human drinking behavior After the onset of a drinking episode, a set of inhibitory mechanisms operates to meter and then terminate drinking behavior. The signals that are generated can be described as oropharyngeal, gastrointestinal, or postabsorptive in origin. Oropharyngeal stimulation may act to inhibit AVP release [18 – 20] and gastrointestinal inhibition appears, in the first instance, to result from mechanical gastric distension [21]. Together, these signals are generated in an overlapping temporal sequence that combines to produce a continuous inhibitory signal that limits further ingestion [22]. These preabsorptive satiety signals can account for the finding that dehydrated humans experience a marked reduction in thirst within minutes of drinking, long before absorption begins [2]. As drinking behavior terminates, changes also occur in the mouth. After 24 h of water deprivation, the most salient sensation reported is that of a dry ‘tacky’ mouth [23]. However, after an initial bout of drinking, subjects report
a marked attenuation of mouth dryness. Interestingly, smaller bouts of drinking, during a 1-h period following water access, are attributed to fluctuations in unpleasant oral sensation [23]. To explore the relationship between thirst and mouth dryness in more detail, one study explored changes in visual ratings of thirst and mouth dryness in thirsty males and females [24]. Measures were taken before and 0, 2.5, and 5 min after the participants ingested either 150 or 400 ml of water. This study reports a relationship between thirst reduction and changes in mouth dryness, in the measures taken at 2.5 and 5 min. Furthermore, the reduction in thirst and mouth dryness appears to be volume-dependent. A 400-ml sample reduces both thirst and mouth dryness to a greater extent than a 150-ml sample. This observation led to speculation that if saliva production increases monotonically with drinking behavior, then increasing mouth wetness will produce an attenuating incentive to continue to drink. This is because an increase in saliva production will remove mouth dryness, thereby reducing the reward offered by the mouth-wetting effect of drinking behavior [24]. In a related study, this hypothesis was tested explicitly by physically manipulating the state of the mouth [25]. Subjects were tested in both a dry mouth and a control condition. In the dry mouth condition, they exercised intensively for 20 min. Afterwards, the participants placed two absorbent cotton wool dental rolls in each cheek, adjacent to the upper and the lower teeth with the mouth closed. They were then instructed to drink water freely through a straw, and were told to do so until they no longer wished to continue. During this drinking episode, the subjects were free to take pauses in their drinking activity. Measures were taken of the duration of each bout and interbout interval. The control condition was identical except that the participants placed only a single roll in each cheek, adjacent to the lower teeth. The tactile experience of one roll was much like that of having two rolls in each cheek. Despite this, pilot testing confirmed that two rolls in each cheek reduced saliva volume in the main oral cavity much more effectively than one roll. Drinking in the dry mouth and control condition differed significantly. In the dry mouth condition, participants drank for longer, drank with a greater number of bouts, and drank a greater volume of water (see Table 1).
Table 1 Mean (S.D.) drinking episode, number of bouts of drinking, and volume ingested in the dry mouth and the control condition (data from Brunstrom et al. [25]) Condition
Drinking episode (s)*
Number of bouts**
Volume ingested (ml)**
Control Dry mouth
69.3 (53.8) 93.8 (72.5)
4.7 (3.2) 7.0 (3.5)
300 (147.7) 428 (204.7)
The superscripts * and ** refer to the statistical reliability of the withinsubject difference between each condition. * P<.015. ** P<.001.
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Since water was ingested freely in both conditions, it is unlikely that the effect of the saliva barrier should be attributed to the inhibition of AVP that is associated with swallowing [19,20], or to other satiety cues generated further down the gastric tract. An analysis of the microstructure of each drinking episode indicated that the pattern of drinking behavior did not differ greatly across conditions. Instead, it appears that the size of the saliva barrier served only to modulate the duration of natural drinking behavior. Augmented drinking activity was attributed to a difference in the effectiveness of the saliva barrier during the interbout intervals. More specifically, across successive interbout intervals, the barrier may extend the period during which continued drinking behavior is rewarded by relief from mouth dryness. Consistent with this theorizing, the pleasantness of a water sample is found to decrease throughout a drinking episode when it is used to rehydrate following a period of water deprivation [2]. If restricting the free movement of saliva around the mouth can influence drinking behavior, then under normal circumstances, natural changes in mouth dryness may help to meter fluid intake. At present, the extent to which this process acts as a useful satiety cue is unclear. Likewise, the time course of this cue relative to satiety signals generated further down the gastric tract remains to be determined. However, we do know that beverages differ in the extent to which they elicit a salivary response. Thus, one indication that mouth state changes are important to human drinking behavior would be evidence that mouth-wetting beverages are selected to alleviate thirst. Section 3 reviews evidence of this kind.
3. Thirst quenching and flavor preference The diversity of human drinking behavior can be attributed largely to the efficiency of our kidneys. When fluid is freely available, we have the luxury to consume a variety of different beverages, often at different times of the day, and in different contexts. Drinking caffeinated or alcoholic drinks can account for a major proportion of daily fluid intake [26]. However, there are considerable individual and cultural differences in the preferred flavor of beverages that contain these drugs. Much of our drinking behavior occurs during meal times [27,28]. This activity might serve to anticipate future fluid deficits, or possibly it occurs out of habit to aid the mastication process. Either way, the nature and the flavor of the beverage are likely to vary considerably across cultures, and are quite likely to be chosen to complement the meal itself. Despite this diversity in flavor preferences and drinking habits, beverages that are used to slake thirst have characteristics that appear to be selected almost universally. Here, the origin of two attributes, temperature and acidity, will be considered. Both are associated with the mouth-wetting characteristics of a beverage.
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3.1. The role of beverage temperature Very hot and very cold substances elicit production of watery parotid saliva. This reflex may serve as a ‘saliva buffer,’ acting to mitigate the temperature of the object in the mouth [29,30]. The close relationship between temperature and saliva production was explored in one study in which saliva was collected over a 6-min period, using a vacuum cap [31]. Every 30 s, assessors swilled their mouths with distilled water for 5 s and then expectorated. Water samples at 0 and 55 °C were found to induce significantly higher flow rates than intermediate samples at 22 and 37 °C. The question of whether or not we are able to distinguish between the effects of warm and cold temperatures has only recently been explored systematically. In one study, thirsty subjects completed visual ratings of mouth dryness before and after drinking a water sample served at either 5 or 22 °C [24]. After ingesting the 5 °C sample, ratings were reduced relative to those for the warmer sample. If the termination of drinking behavior is influenced by the extent to which changes occur in mouth dryness, then two predictions follow. First, cooler beverages may offer greater immediate relief from thirst. Second, a cold beverage will be regarded as more acceptable when it is used to slake thirst. This is because cold temperatures offer greater reward in terms of a reduction of the unpleasant dry mouth symptoms that are associated with thirst. These predictions are considered in turn. 3.1.1. Temperature and thirst reduction An association between beverage temperature and drinking behavior has been reported extensively, both in animals and in humans. In dehydrated rats, cold water availability has a suppressive effect on water consumption relative to warmer samples served near body temperature [32,33]. In contrast, humans may drink more cold water than warm water during prolonged periods of exercise [34,35]. However, when thirsty humans are offered a very short period of time to rehydrate, cold (0 °C) water is ingested less than water at 16 °C [36]. This implies that cold water is particularly satiating during the period immediately following a bout of drinking. It is also consistent with recent speculation that the cooling effect of menthol can offer immediate reduction from thirst [37]. However, an alternative interpretation is that the cold (0 °C) water sample was ingested to a lesser extent because water has aversive properties when served at this extreme temperature. The problem with intake measures is that they only reflect a person’s predilection for a particular fluid. They do not necessarily reveal the potential of a water sample to reduce motivation to continue drinking. In humans, the best way to explore changes in thirst is to use some form of analogue rating scale. One study found that during ad libitum drinking over 6 h of 30/30 min work/rest, cold water produced lower thirst ratings than warm water [38]. Unfortunately, interpreting this result is difficult because intake differences
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confound conclusions regarding the satiating ability of water at different temperatures. Moreover, this study was concerned with postabsorptive rather than preabsorptive effects of temperature on thirst. Only two studies have systematically examined the short-term effects of beverage temperature on thirst satiety (i.e., observed the reduction in thirst that results from the ingestion of equal-volume drinks served at different temperatures). The effect of temperature on thirst ratings was explored after lunchtime drinking of vegetable juice, served at either 1 or 61 –62 °C [39]. This study found that in male subjects, a cold 400-ml sample reduced thirst ratings more effectively than a warm sample. However, this was not the case in a female group that received 300-ml samples. The authors of this study acknowledge that the volume of the test sample was confounded with the assessor’s gender, making it difficult to attribute differences unequivocally either to gender or to volume. This issue was addressed in a subsequent study in which thirsty males and females were provided water samples both at different temperatures and at different volumes [24]. In both males and females, 5 °C water reduced thirst ratings more than 22 °C water, although in each case, this effect was dependent on the volume of water ingested and the specific method of assessing thirst. 3.1.2. Temperature and acceptability The sparse research exploring the effects of temperature on short-term reductions in thirst contrasts with the abundance of studies exploring its effect on beverage acceptability. When thirsty, both humans and laboratory animals tend to choose water served at lower temperatures [32,35,38, 40,41]. In rats, the advantage gained by this predisposition remains unclear. However, some studies suggest that the reward offered by drinking cool water results directly from cooling the mouth rather than from a reduction in core temperature or thirst [33]. Thus, rats appear to be rewarded by licking cool air streams [42] or cold metal [43]. However, in humans, the relationship between cool water preference and thirst is less equivocal. In one study, exercise-induced thirst increased the palatability of 16 °C water more than that of warmer water (22 and 38 °C) [34]. Water at 5 °C also increased in palatability more than these warmer samples. However, reliable effects of exercise were found only for the 16 °C sample. In a similar study, hydrated and dehydrated groups rated 10 °C water as being most pleasant [36]. However, dehydrated assessors found the 0 °C sample to be as pleasant as the 10 °C sample, whereas the control group found it significantly less pleasant than the 10 °C sample. One possibility is that these hydration-dependent shifts in preference are governed by mouth state changes rather than by any of the other physiological consequences of dehydration. In other words, we prefer cold water when we become thirsty because it offers greater relief from mouth dryness than water served at warmer temperatures. One way to test this hypothesis is to determine whether hydration-
dependent shifts in cold water preference can be replicated by manipulating only mouth state. In a recent study, this possibility was explored by testing subjects both in a dry mouth and a control condition [44]. In the dry mouth condition, subjects placed two cotton wool dental rolls in each cheek. This inhibits movement of parotid saliva into the main oral cavity, causing the mouth to become dry. After 2 min, the dental rolls were removed and the subjects then immediately tasted and rated a water sample served at 3, 13, 23, or 33 °C. Measures taken earlier confirmed that the 3 °C sample elicits significantly more salivation that the warmer samples. Since this sample will offer the greatest reward in terms of mouth wetting, the mouth-drying procedure was expected to increase preference for samples served at that temperature. This is exactly what happened. Artificial mouth drying selectively increased preference for the cold water (3 °C) and no significant shifts in preference were found for the warmer samples. The authors of this study concede that the origin of thirst-induced cold water preference is probably complex. Nevertheless, their account does offer a logical explanation for our universal preference for cold rather than tepid beverages when we are thirsty. Finally, one type of beverage that is commonly regarded as thirst quenching is hot tea. One explanation for this is that tea is preferred for much the same reason as cold water. As with cold water, hot tea will elicit a strong salivary response [31]. Thus, hot tea and cold water may both offer greater alleviation of dry mouth symptoms than beverages served at intermediate temperatures. To date, this hypothesis remains unexplored. 3.2. The role of beverage acidity If the acceptability of cold water is modulated by the extent to which it alleviates mouth dryness, then it follows that any mouth-wetting beverage may be susceptible to similar shifts in hedonic value. In addition to hot and cold substances, acids found in foods and beverages also elicit a marked increase in saliva production [45]. This reflex helps to dilute the harmful effects of acids or alkalis that can lead to tooth decay [46]. In one study [47], this hypothesis was investigated using the same mouth-drying procedure that was used to explore the interaction between mouth state and temperature preference (see Section 3.1.2) [44]. In a preliminary experiment, measures were taken of the volume of saliva in the mouth following ingestion of a lime drink served with one of three different citric acid concentrations (0, 1.75, and 3.5 g/1000 ml). As expected, acid concentration and saliva volume were related monotonically. Next, flavor preference was assessed in a dry mouth condition and a control condition. The results from this study indicate that mouth drying does increase flavor preference, but only in the lime drink having the highest citric acid concentration (3.5 g/1000 ml). This finding is important because it implies that shifts in hedonic value are not exclusive to cold water, but may be more commonplace, such that any mouth-
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wetting drink will increase in acceptance when the mouth becomes dry. Few studies have explored which features of a beverage contribute to whether or not it is labeled as ‘thirst-quenching.’ In one study, this issue was explored using focus group and sensory testing methods [48]. A focus group of consumers regarded the attributes—acidity, stringency, carbonation, fruitiness, flavor strength, sweetness, and thickness—to be all characteristics that are likely to influence a drink’s thirstquenching properties. Using correspondence analysis to relate consumer assessments of thirst-quenching character and acceptability to descriptive ratings by a trained panel, acidity was found to be the characteristic most associated with ‘thirst quenching,’ while sweetness and thickness were least associated. Unfortunately, temperature was not included in this analysis. Nevertheless, it seems highly likely that cold temperatures are better associated with ‘thirst quenching’ than tepid or warm temperatures. Thus, there appears to be a correspondence between characteristics that contribute to use of the term ‘thirst quenching’ and those that have the capacity to alleviate mouth dryness. If normal drinking behavior and beverage selection are influenced by mouth state changes, then it is plausible that this process also plays some role in situations where aberrant drinking behavior occurs. This possibility is considered briefly in Section 4.
4. Mouth state and adequate fluid replacement The term ‘voluntary dehydration’ is used to describe a situation in which fluid intake fails to match water losses, even under conditions where there is ample water freely available [40]. Flavoring is important because it can prevent, or at least reduce the risk of, voluntary dehydration [41]. The interactive effect of flavoring and beverage temperature has also been explored [35,38]. In one study, subjects were given free access to liquids during a period of exercise in a climatic chamber [35]. Flavoring and cooling effects on ad libitum intake were additive and increased by over 100% relative to a group who received warm (ambient temperature) disinfected (unpalatable) water. Flavoring water will increase its overall acceptance, and it may be this fact alone that is responsible for an increase in intake [49]. However, it is noteworthy that it is often acidic fruit flavorants that are added to samples used in these studies [50,51]. In particular, ‘grape’ flavor has been found to be particularly good at promoting adequate fluid intake [50,51]. Thus, one possibility is that, among other things, acidic flavorants increase the reward that is experienced by the act of drinking and, hence, beverages with this characteristic are ingested in greater quantities over time for this reason. In relation to this hypothesis, it would be interesting to compare the extent to which voluntary dehydration occurs when wetting and nonwetting beverages are readily available during exercise.
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Problems with thirst and hydration are not limited to situations were humans engage in rigorous exercise. There is now reasonable evidence that thirst declines as age increases [52,53]. Elderly people also appear to have a diminished renal capacity, making it difficult to produce urine with a high osmolality [54]. Consequently, after 24 h of complete water deprivation, healthy elderly men consume insufficient water to rehydrate themselves to predeprivation levels [52]. There are several reasons why thirst may be impaired. For example, thirst may be associated with changes in central levels of dopamine, which reduces with age [55], and may facilitate drinking behavior [56]. Alternatively, attenuated thirst may be related to diminished functioning of central volume receptors [57,58]. Although it is commonly believed that salivary function decreases with age, recent evidence suggests that there is no significant decrease in major salivary gland function [59 – 61]. Nevertheless, elderly people report fewer oropharyngeal symptoms such as mouth dryness compared with healthy young control subjects [59,62]. The reason for this difference is unclear, but may be attributed to age-dependent differences in taste sensitivity or salivary constituents. Either way, one possibility is that age-dependent deficits in thirst may be related to differences in sensitivity to changes in mouth feel. To test this, one might examine whether or not the drinking behavior and flavor preferences of elderly people can be modulated by a saliva barrier of the kind used in recent studies [25,44,47] and described elsewhere in this review.
5. Concluding remarks Since the rejection of the dry mouth theory of thirst [1], very little attention has been paid to the possibility that mouth dryness influences everyday ingestion of fluids. This is probably because research activity has focused primarily on more central homeostatic mechanisms and because, until recently, we have lacked appropriate techniques to manipulate mouth state directly. The evidence presented here suggests that changes in mouth state are not simply a byproduct of drinking activity. Rather, they may have subtle yet cogent effects on flavour acceptability and thirst satiety. In this regard, it is noteworthy that those beverage characteristics that elicit saliva production (acidity and a cold temperature) are (a) likely to be labelled ‘thirst-quenching,’ (b) are likely to be chosen and ingested in greater quantities when we are thirsty, and (c) are most sensitive to hedonic shifts caused by increases in mouth dryness. Further research is now warranted in order to determine whether this is mere coincidence, or whether a common mechanism underlies these findings. Once this is established, we may be better placed to understand whether or not this process contributes to voluntary dehydration and age-related problems associated with attenuated levels of thirst.
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