Sensory Perception of Food and Aging

Chapter 3

Sensory Perception of Food and Aging S. Nordin Umeå University, Umeå, Sweden

3.1 INTRODUCTION Malnutrition is a common problem in the aging population, with prevalence rates of 3–10% among independently living elderly and 25–85% among institutionalized elderly (Saletti et al., 2000; Vellas et al., 2001). It may to a large extent be referred to as anorexia, for which age-related changes in sensory perception are likely to contribute considerably (MacIntosh et al., 2000). Sensory perception of food is complex and involves the sensory modalities of olfaction, gustation, chemical and nonchemical skin senses, vision, audition, and kinesthesis to provide the individual with information about the food’s flavor, temperature, color, appearance, and texture. The most important senses for food perception are the chemical senses that provide information about flavor, which are olfaction, gustation, and chemesthesis. The objectives of this chapter are to (i) provide a brief description of the functions of the chemical senses and the role they play in food intake, (ii) review documented age-related changes in chemosensory perception and their possible underlying causes, (iii) present possible consequences of these chemosensory changes for food intake and well-being in elderly, and (iv) describe the literature regarding flavor enhancement of food for the elderly population.

3.2  GENERAL FUNCTION AND ROLE OF THE CHEMICAL SENSES The following section provides a brief description of the chemical senses and their integration.

Food for the Aging Population. DOI: http://dx.doi.org/10.1016/B978-0-08-100348-0.00003-2 © 2017 Published by Elsevier Ltd. All rights reserved.

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3.2.1 Olfaction Odorous molecules, enhanced by sniffing, reach the olfactory epithelium that is located in the roof of the nasal cavity through the orthonasal passage. In addition to the orthonasal passage, and of particular importance for food perception, molecules can also reach the epithelium from the oral cavity through the retronasal passage (Bojanowski and Hummel, 2012), which is enhanced by movements of the tongue, cheek, and throat that pump the molecules through this passage (Burdach and Doty, 1987). The olfactory epithelium contains the olfactory neurons and their receptors, which are located on cilia that are embedded in mucus. The receptors have specifically shaped proteins to which the odorous molecules can bind and activate the olfactory neurons, after having penetrated the mucus (Moon and Ronnett, 2003). The neurons project through the cribiform plate to the olfactory bulb where they make contact with mitral cells (and interneurons). The mitral cells, in turn, project to higher-order olfactory areas, including the pyriform cortex, orbitofrontal cortex, amygdala, and enthorinal cortex (Zald and Pardo, 2000). The human capacity to discriminate odor qualities is particularly good. Most likely, there is an infinite number of qualities that can be distinguished, which is made possible by as many as 250–750 genes that code for olfactory receptors, of which about half are nonfunctional (Buck and Axel, 1991; Rouquier et  al., 2000). When damaged, the olfactory epithelium can be reconstituted. However, the success of the regeneration is influenced by age-related processes, such as the degree of cumulative damage from prior environmental insults, including those from pollution and viral and bacterial infections (Doty and Kamath, 2014). The most important function of human olfaction is to guide our attention toward hazards (e.g., spoiled food and poisonous fumes) and toward items that in a general sense have positive connotations (e.g., nutritious food). With a few possible exceptions, there appears to be no innate preference for odors. Instead, a prerequisite for an odorous substance to warn or attract us is that we at an earlier encounter with the substance associate its odor with a positive or negative emotion depending on the context, and that we at the later occasion recognize the odor and retrieve the association from memory (Engen, 1991). Odors have an extraordinary ability to evoke autobiographical memories, and compared to those triggered by verbal and visual information, odor-triggered memories are older, typically from childhood (Chu and Downes, 2002; Willander and Larsson, 2006). The relatively strong emotions often evoked by odors are believed to enhance the appropriate behavioral response. The hedonic dimension is the dominating aspect of odor perception (Stevenson, 2010). The pleasantness/unpleasantness of an odorous item, such as food, is to a large extent determined by an individual’s personal history with that item.

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3.2.2 Gustation Taste cells are found in groups of 30–50 in the membranes of taste buds. A pore at the top of the taste bud makes contact with the outside fluid environment in the mouth, and the taste molecules bind to taste receptors in the taste cell’s hair-like cilia at the pore. The taste cells make contact with primary taste nerves over a gap of synaptic connection and project to higher brain regions. The taste buds are contained in groups in three types of structures called papillae that are visible to the eye: fungiform (distributed over the anterior two-thirds of the tongue), foliate (along the posterolateral margins of the tongue), and circumvallate papillae (extended in a V-shaped line across the root of the tongue; Witt et al., 2003). Three cranial nerves innervate the taste system: VII innervates the fungiform papillae of the anterior tongue (chorda tympani branch) and taste buds on the palate (greater superficial petrosal branch); IX (glossopharyngal) innervates the foliate papillae on the rear edges of the tongue, and the circumvallate papillae on the back of the tongue; and X (vagus) innervates receptors in the throat (Duffy and Bartoshuk, 1996). Sweet, salty, sour, bitter, and umami tastants innervate all three cranial nerves (Bartoshuk, 1993; Sako et al., 2000) and can be perceived on any area of the tongue (Nordin et al., 2007a). The taste information is carried by the cranial nerves to the solitary tract in the medulla, and from there to the ventroposteromedial thalamic nucleus, and further to the anterior insula (primary taste cortex). Other important brain areas involved in taste processing include the orbitofrontal cortex and amygdala (Rolls and Scott, 2003). The gustatory system is also enhanced by endocrine and paracrine modulation, such that hormones that bind to receptors on taste cells alter the palatability of food and therefore also intake. For example, the hormone leptin reduces the palatability for sweet tastants, whereas insulin increases the palatability for salty tastants (Loper et al., 2015). Linda Bartoshuk has done pioneer work on individual differences in taste sensitivity due to genetic variation. Differences have been found, e.g., for the bitter compounds phenylthiocarbamide (PTC) and 6-n-propylthiouracil (PROP). Based on detection thresholds, individuals can be categorized as “tasters” (sensitive) and “nontasters” (relative insensitive; Bartoshuk et  al., 1994; Duffy, 2007; see Garcia-Bailo et al., 2009 for genes controlling the basic taste qualities). The gustatory system functions as a final gatekeeper of the internal milieu to guide ingestive and avoidance behaviors (Smith and Scott, 2003). Hedonic value is an important perceptual dimension of taste, with close ties to motivational behavior. The traditional basic taste qualities subserve signaling functions about the presence of nutrients or dangers: carbohydrate energy sources in sweetness, sodium, and other minerals in saltiness, and proteins in umami, whereas sour and bitter warn for danger from acids and toxins, respectively. As a consequence, humans are born liking sweet and disliking bitter and sour

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(Lawless, 1985). A fifth quality, called umami, is now recognized as an additional basic quality. Its sensation can be referred to as “brothy,” “savory,” or “meaty,” and it is evoked by monosodium glutamate (MSG).

3.2.3 Chemesthesis Chemesthesis refers to chemosomatosensory function (also called the common chemical sense) that is activated by chemical substances that stimulate open nerve endings, so-called nociceptors, located in the nasal cavity, oral cavity, and cornea. The neural signals are transmitted to the brain via the three branches of the trigeminal nerve. The sensations can be characterized as stinging (e.g., from carbon dioxide in soda), burning (e.g., chili pepper), cooling (e.g., peppermint), or astringent (e.g., wine). Practically all substances can evoke one of these sensations if the substance reaches a sufficiently high concentration (Doty et al., 1978), and can at high concentrations generate pain (see Viana, 2011, for a detailed description of the anatomy, histology, and physiology of the chemesthetic system). The primary function of the chemesthetic system is to act as a sentinel of the airways where it reflexively stops inspiration to prevent inhalation of potentially life-threatening substances (Silver, 1991). Thus it is to an even larger extent than olfaction a chemical warning system since substances with strong activation are likely to be potentially harmful. The warning feature is further illustrated by defense reflexes in the body in response to this type of chemical stimulation, such as sweating, coughing, tearing, and salivary flow.

3.2.4 Flavor Olfactory, gustatory, and chemesthetic perception are closely integrated (Cain and Murphy, 1980; Lawless and Stevens, 1984), and as a consequence difficult to separate when perceived simultaneously. Their blended perception, in response to food in the oral cavity, constitutes flavor. This perceptual unity can be explained by its neuroanatomy with cortical multimodal neurons that are specialized for this integration. For example, there are neurons in the orbitofrontal cortex and insula that are activated only when odorants and tastants are presented simultaneously (Rolls and Baylis, 1994; Francis et  al., 1999). Importantly, flavor is the strongest determinant of food consumption in the elderly (Rolls and McDermott, 1991). It has long been known that retronasal odor perception easily can be confused with taste and thereby increase taste perception (Murphy et al., 1977; Murphy and Cain, 1980). However, there are various other types of sensory interaction of relevance for food perception, such as sweet taste enhancing retronasal odor perception (Green et al., 2012), color enhancing flavor (Shankar et al., 2009), and retronasal odor perception enhancing activation in mechanosensory brain areas of importance for thickness perception (Iannilli et al., 2014). These interactions can be referred to as the multimodal neurons, specialized to integrate

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information for various sensory systems in brain regions (Rolls, 2005; Verhagen and Engelen, 2006; Boyle et al., 2007).

3.3  CHEMOSENSORY PERCEPTION AND FOOD INTAKE Regulation of energy balance is controlled by metabolic mechanisms and meal behavior, and both are influenced by chemosensory function. This influence can be referred to as the onset of the meal, its continuation, and its termination with consequences for when and how much we decide to eat. The chemical senses also shape human eating behavior in terms of what we decide to eat.

3.3.1  When to Eat Mechanisms that enhance the onset of the meal and that prepare the individual for the meal include food cravings and hunger, which are both emotional in character and motivate food intake. The food cravings reflect to a large extent cravings for specific chemical stimulation to satisfy somatic needs for nutrients and minerals. This is referred to as positive alliesthesia. Alliesthesia can be both positive and negative in character and described as a change in food palatability (pleasantness) caused by internal chemical signals from the food (e.g., glucose in the intestines; Cabanac, 1971; Rolls, 2005). In positive alliesthesia the flavor of a specific nutrient that the body is deficient in is perceived as particularly pleasant (Fig. 3.1). Examples include the taste of sweetness being particularly pleasant when the blood-glucose level is low, and the pleasant taste of saltiness when the body’s need of additional salt is large, which results in increased likelihood of ingesting these substances. The smell, taste, sight, and even thought of food also encourage general food intake, which is accomplished by both biological and psychological mechanisms. The biological mechanisms prepare the individual for the meal by stimulation from the food sensations to, e.g., secrete insulin (Fig. 3.1). Insulin will lower the blood-glucose level and generate a sensation of hunger to start general food intake. Odor and taste sensations from food also improve the metabolism of nutritions, carbohydrates, and fats by triggering a number of reflexes. These include secretion of saliva, gastric acids, and substances from the pancreas as well as cardiovascular and thermal responses (Fig. 3.1; Richardson et al., 1977). An important psychological mechanism is so-called learned sensory control, in which food cravings are evoked by classical conditioning (De Houwer et al., 2001) of the food sensations that have been associated with the behavior to start eating (Fig. 3.1).

3.3.2  How Much to Eat During a meal, two groups of sensory mechanisms oppose each other: one group that enhances continued eating, and another group that enhances termination of eating. The difference in strength between these two groups determines

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FIGURE 3.1  Mechanisms involving the chemical senses that enhance the onset of the meal and prepare the individual for the meal.

FIGURE 3.2  Mechanisms involving the chemical senses that enhance continued eating.

to a large extent the size of the meal (Davis and Levine, 1977). The former group includes smell and taste sensations that stimulate dopaminergic and serotonergic systems in the central nervous system (CNS; Fig. 3.2). Dopaminergic activation stimulates the “reward system,” whereas serotonergic activation evokes general well-being, encouraging continued eating (Rolls, 2015). The orbitofrontal cortex, insula, and amygdala are important regions for emotional “reward” and ”punishment” for food intake, with consequences for motivation and food behavior (Francis et al., 1999; Rolls, 2000). Opioids have long been known to play an important role in this respect by acting on the amygdala and hypothalamus, with subsequent effect on taste and gastrointestinal function to enhance appetite and food intake (Levine et al., 1985).

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The chemical senses’ role in terminating food intake includes negative alliesthesia, sensory-specific satiety, and learned sensory control. The first two mechanisms affect the individual’s relation to specific foods, and the third mechanism affects the relation to food in general. Negative alliesthesia implies, in contrast to positive alliesthesia, that the pleasantness of “superfluous” food fades as more of this specific food is consumed (Fig. 3.3). This mechanism is activated by signals from the digestive system, in particular by uptake of glucose in the blood and by increased concentration of nutrients in the intestines (Cabanac and LeFrance, 1990). This encourages consumption of a variation of different foods. In sensory-specific satiety a relatively large intake of food with the same flavor leads to decreased sensory appreciation for this particular food, more than for food with other flavors (Rolls, 2005; Fig. 3.3). Although sensoryspecific satiety, similar to negative alliesthesia, results in faded palatability, these two phenomena differ in an important aspect: alliesthesia is generated by somatic signals, whereas sensory-specific satiety is generated by external, sensory signals. Sensory-specific satiety is not directed toward food in general, but to food with sensory properties similar to the food that has been consumed (Rolls et al., 1981). As for negative alliesthesia, this encourages intake of different foods. In addition to preparing the individual for a meal, learned sensory control also contributes to the termination of the meal (Fig. 3.3). For example, Birch and Deysher (1985) have shown that calorie content can be predicted based on flavor and that the meal size can be adjusted depending on the flavor.

FIGURE 3.3  Mechanisms involving the chemical senses that enhance termination of eating.

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3.3.3  What to Eat Food preference and aversions strongly affect what we decide to eat and are to a large extent influenced by prior experiences by means of classical and instrumental conditioning, but also by genetic factors. In this respect the chemical senses, olfaction in particular, play important roles due to their ability to easily make strong associations (Baeyens et  al., 1988). We learn very early in life, primarily based on olfactory cues, to identify an item with respect to its edibility (Schaal et al., 1998). Preferences are formed throughout life, and begin even before birth by flavors in the amniotic fluid from the mother’s food intake (Mennella and Beauchamp, 1993; Mennella et al., 1995). Regarding food aversions, signals from the sense of smell to area postrema in the brainstem evoke nausea and vomiting that underlie aversions. Odor-based associations, followed by taste-based associations, appear to be the most common reason for food aversions (Nordin et al., 2004a). Although there is an innate preference for sweetness and aversion toward bitter and sour (Steiner et  al., 2001; Mennella et  al., 2005), genetic variation across individuals does partly explain both taste sensitivity and preference. Genetic factors may in fact play a larger role than environmental factors for taste preference (Törnwall et al., 2012). Extensive research has in recent years been conducted on the role of genetic variability in food intake, in particular regarding bitterness (Garcia-Bailo et al., 2009; Beckett et al., 2014). For example, tasters for bitterness, compared to nontasters, have also shown enhanced perception of other taste qualities, sensory irritation, and thickness perception, and increased preference for various sweet foods (Karrer and Bartoshuk, 1991; Prescott and Swain-Campbell, 2000; Keskitalo et al., 2007).

3.4  AGE-RELATED CHANGES IN CHEMOSENSORY PERCEPTION Changes in chemosensory perception can be both quantitative and qualitative in nature. Quantitative changes include detection sensitivity, intensity discrimination, and perceived intensity, whereas quality changes refer to quality discrimination and typically also identification.

3.4.1 Olfaction A vast number of studies have demonstrated substantial impairment in various olfactory functions in elderly people when presenting food and nonfood odorants orthonasally. Impairment in one such function is in detection sensitivity (Hummel et al., 1997; Larsson et al., 2009; Kern et al., 2014), and it seems that an age-related loss in detection sensitivity for one odor quality is accompanied by a loss in detection of other qualities (Cain and Stevens, 1989; Cain and Gent, 1991). However, there is evidence that age-related loss is more pronounced

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for heavy molecules (Sinding et al., 2014) and pleasant odors (Konstantinidis et al., 2006). Importantly, loss in olfactory detection sensitivity is not found in all elderly people. Thus in studying a group of successfully aged elderly who were carefully screened for medical and lifestyle factors that may affect olfaction, odor detection thresholds were obtained that were very similar to those for young adults (Nordin et al., 2012). Furthermore, poorer odor sensitivity has been reported in institutionalized elderly in comparison to independently living elderly (Sulmont-Rossé et al., 2015), which is possibly a sign of frailty. There is strong evidence for age-related impairment in the ability to discriminate between qualitatively different odors (Schiffman and Leffingwell, 1981; Stevens and Lawless, 1981; Choudhury et al., 2003; Hedner et al., 2010). Parosmia is a condition in which certain odors are qualitatively distorted and thus may compromise discrimination ability. Postviral upper-respiratory infection and head trauma are common causes of parosmia (Nordin et al., 1996). It has been estimated that about 4% of the general adult population suffer from parosmia, but it appears to be somewhat less common in elderly than in young adults (Nordin et al., 2007b). The ability to discriminate between odorants of different intensities has also been found to decline in normal aging (Koskinen and Tuorila, 2005). Diminished perceived odor intensity was suggested in older adults decades ago (Stevens et al., 1982; Stevens and Cain, 1985, 1987). Stevens et al. (1989) demonstrated stronger olfactory adaptation and slower recovery in this population. It is worth noting that calcium imaging and psychophysical studies suggest largely independent, parallel processing of odor intensity and quality discrimination as well as of odor detection and quality discrimination (de Wijk et al., 1994; Rawson et al., 1998; Savic et al., 2000; Cain et al., 2008). Hence, e.g., a mild-to-moderate loss in detection sensitivity may not necessarily be accompanied by a loss in quality discrimination. For general evaluation of the sense of smell, in both clinical and nonclinical settings, it is common to assess the ability to identify (name) common odorous items. This ability requires intact detection sensitivity (assumed to underlie relatively strong odor sensation), quality discrimination, and recognition memory, which all are important olfactory functions for human daily routines (Croy et al., 2014). As would be expected based on the review above, studies do indeed show clear impairment in odor identification in the elderly (Doty et al., 1984; Duffy et al., 1995; Olofsson et al., 2010; Schubert et al., 2011; Wehling et al., 2011). Results from population-based studies show that prevalence rates for olfactory dysfunction, by means of tests of cued odor identification, increase from 11% to 24% in middle-aged individuals to 37% to 70% at the age of 70 years (Murphy et al., 2002; Brämerson et al., 2004). The 5-year incidence for impairment in odor identification has been estimated to increase from 4.1% in ages 53–59 years to 47.1% in ages 80–97 years (Schubert et al., 2011). Age-related decline in other cognition-dependent functions of olfaction are also well documented (e.g., Larson, 1997; Nordin, 2012). Despite the fact that it is common

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among the elderly to be unaware of their compromised olfactory function (Nordin et al., 1995; White and Kurtz, 2003; Wehling et al., 2011), results from population-based studies show that self-reports of loss in olfactory dysfunction are indeed more common in elderly than in young adults (Nordin et al., 2004b; Bhattacharyya and Kepnes, 2015). Elderly have to some extent also been investigated with respect to retronasal olfaction. In accordance with orthonasal olfaction, impairment has been found with respect to detection, quality and intensity discrimination (Cain et al., 1990; Stevens and Cain, 1993; Duffy et al., 1999; Koskinen and Tuorila, 2005), perceived intensity (Stevens and Cain, 1986a), and identification (Murphy, 1985).

3.4.2 Gustation Despite limited documentation at the time, there was early recognition of the importance of age-related changes in gustatory function and its impact on food preference and consequences for nutritional status (Cowart, 1981). In more recent years, gustatory function in elderly people has been studied rather extensively. A systematic review of age-related changes in taste function published in 2012 identified 40 studies examining detection sensitivity, 2 examining discrimination, 23 examining perceived intensity, and 18 examining identification ability (Methven et al., 2012). In addition to the studies included in that review, contributions have been made regarding age-related differences in absolute detection sensitivity (Weiffenbach et al., 1982; da Silva et al., 2014), detection of a certain tastant in food (Cain et al., 1990; Stevens et al., 1991), intensity discrimination (Stevens and Lawless, 1981), perceived intensity (Schiffman and Clark, 1980; Fischer et al., 2013; Heft and Robinson, 2004), and identification (Nordin et al., 2007). Overall, the scientific literature clearly suggests that aging is associated with decline in gustatory detection sensitivity, discrimination, perceived intensity, and identification. Moreover, Mojet et  al. (2004) showed age-related differences in perception of side tastes. For example, the elderly, compared to the young, more strongly perceive sourness and bitterness as side tastes of NaCl in tomato soup. It is also of interest to note that poorer taste sensitivity has been reported in institutionalized in comparison to independently living elderly people (Spitzer, 1988; Toffanello et  al., 2013; Sulmont-Rossé et al., 2015). It has long been recognized that taste dysfunction is less common than smell dysfunction (Goodspeed et al., 1987; Deems et al., 1991). The relative robustness of gustation may be explained by the fact that as many as three cranial nerves innervate the taste system. It is therefore not surprising that age-related impairment is also less prominent for taste than for smell (Weiffenbach, 1984; Cain et  al., 1990). Nevertheless, 5.3% of the US adult population have been found to report a problem with taste in the previous 12 months (Bhattacharyya and Kepnes, 2015). Importantly, there seems to be quality-specific age-related changes in taste perception when reviewing studies of changes in detection

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sensitivity, intensity discrimination, and perceived intensity in which two or more basic taste qualities were used for the same individuals (Weiffenbach et al., 1982, Gilmore and Murphy, 1989; Murphy and Gilmore, 1989; Nordin et  al., 2003). Although the results are not fully consistent, bitter sensitivity seems to be most affected by age and sweet sensitivity least affected (see also Methven et al., 2012).

3.4.3 Chemesthesis Although age-related effects have been studied considerably less regarding chemesthesis compared to olfaction and gustation, data suggest that aging also takes its toll on this chemical sense. Using predominantly CO2 as a trigeminal intranasal stimulus, but also other stimuli with irritating properties, results from investigations suggest poorer detection sensitivity in elderly than in young adults. This has been demonstrated when expressing detection sensitivity as the traditional threshold and the reflex apnea threshold (Murphy, 1983; Stevens and Cain, 1986b; Shusterman et al., 2003), and as the trigeminal lateralization threshold (Hummel et al., 2003; Wysocki et al., 2003). In line with these threshold data, aging also appears to suppress perceived intensity of irritating stimuli (Stevens et al., 1982; Murphy, 1983). Laska (2001) compared young and elderly people in their ability to discriminate between chemical stimuli with trigeminal properties, and found a modest decline with age. Further support for age-related effects on chemesthesis is provided by electrophysiological data. Compared to young adults, elderly people have been shown to require a stronger concentration to elicit a negative mucosal potential, which reflects activation of the nociceptors in the nasal cavity (Frasnelli and Hummel, 2003). Hummel et al. (1998) also demonstrated smaller chemosomatosensory amplitudes of event-related potentials (ERPs) in elderly than in young adults.

3.4.4  Pleasantness and Preference Pleasantness mediated by sensory characteristics of food is a strong determinant of food choice (Clark, 1998). Loss in chemosensory sensitivity is therefore likely to affect pleasantness and preferred concentration of food components since intensity is a powerful predictor of hedonic tone. Indeed, compared to young adults, diminished perception of saltiness and sweetness in the elderly has been reported to lead to increased pleasantness and preference for these tastants at a given concentration (Murphy and Withee, 1986; Zallen et al., 1990; Drewnowski, 1997). Murphy and Withee (1987) also showed that elderly people, particularly those with low nutritional blood values, perceive amino acids (common food flavors) in an amino-acid-deficient soup base as less strong than did young participants and preferred higher concentrations. Furthermore, de Graaf et al. (1994) reported that elderly people, on average, perceive high

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concentrations of food flavors to be less intense than do younger adults, and that optimal pleasantness concentrations of the flavors are higher in the elderly. The authors also argue that olfaction contributed more than gustation to this age-related effect on flavor perception.

3.4.5  Causes of Age-Related Changes in Chemosensory Perception 3.4.5.1 Olfaction Doty (2015) listed over 200 etiologies that, irrespective of age, can cause an olfactory disorder. The mechanisms underlying these disorders can be classified as conductive (e.g., caused by nasal polyposis), sensorineural (e.g., postviral upper-respiratory infection), or impairment in the olfactory CNS (e.g., tumor). The most common etiologies of olfactory disorders among patients seeking medical attention at ear, nose, and throat clinics include upper respiratory infection, chronic sinusitis, nasal polyposis, allergic rhinitis, and head trauma (Temmel et al., 2002; Brämerson et al., 2007). Given this, it is not surprising that a large number of anatomical and histological changes can take place in the elderly individual that may compromise the ability to process olfactory information. In a review, Doty and Kamath (2014) describe age-related changes such as pathology in the nasal cavity (e.g., chronic rhinosinusitis and nasal polyposis), occlusion of patent foramina of the cribiform plate leading to pinching off of olfactory receptor cell axons, decreased number of olfactory receptor cells and consequently replacement of olfactory epithelia with respiratory epithelia, and broader electrophysiological tuning curves for receptor cells. Considerable age-related anatomical changes in the brain have been documented regarding the olfactory bulb (e.g., decline in the size and presence of neurofibrillary tangles), decrement in the volume of amygdala, piriform cortex, anterior olfactory nucleus, and frontal poles of the brain. Physiological changes in the aging individual are typically manifested when recording olfactory ERPs, which reflect electrophysiological brain activity in response to odorous stimuli. Results show diminished neuronal allocation (reflected by the amplitudes) and decreased processing speed (reflected by the latencies) in normal aging for both sensory and cognitive components (Murphy et al., 1994; Hummel et al., 1998; Murphy et al., 2000; Morgan and Murphy, 2010). Results from functional neuroimaging suggest age-related decrease in activity in the enthorinal cortex, piriform cortex, amygdala and periamygloid cortex, hippocampus and parahippocampal gyrus, orbitofrontal cortex, insula, and perisylvian zones when conducting tasks requiring low-cognitive olfactory functioning (Yousem et al., 1998; Suzuki et al., 2001; Cerf-Ducastel and Murphy, 2003; Wang et al., 2005). Regarding age-related neurochemical changes, acetylcholine is of particular interest since it is a neurotransmitter critical for the olfactory system, and has

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shown deficiency in the aging brain (Doty and Kamath, 2014). Furthermore, nigrostriatal dopaminergic degeneration has been reported to be associated with poor performance in olfactory function in elderly (Wong et al., 2010). Due to very early and extensive neuropathology in both peripheral and central olfactory areas, patients with Alzheimer’s disease are likely to constitute a special-risk group regarding olfactory impairment and its consequences for food perception. Thus this population shows severely impaired sensory- and memory-based olfactory functions (Nordin and Murphy, 2002; Ottaviano et al., 2015). Impaired olfactory function is also common in other neurodegenerative diseases, such as Parkinson’s and Huntington’s diseases (Barresi et al., 2012; Doty, 2012). Attention has also been directed to genes related to olfactory function and aging. The human apolipoprotein E (ApoE) gene is of particular interest in this respect. ApoE is a plasma protein that is involved in lipid transport and located on chromosome 19, carrying the three possible alleles ε2, ε3, and ε4. This gene is expressed in the CNS, including the olfactory bulb and the olfactory epithelium (Struble et al., 1999; Nathan et al., 2007), and is believed to play a role in neuronal regenerative processes as well as in the development of Alzheimer’s disease. The combination of high age and having an ε4 allele seems to have a particular adverse effect on electrophysiological brain activity in response to odors (Green et al., 2013a,b). Although there is some inconsistency in the literature (Handley et al., 2006), impaired odor identification in the elderly has been observed in nondemented, but cognitively impaired elderly ε4-carriers (Murphy et al., 1998). Longitudinal data suggest that elderly ε4-carriers show larger than normal decline in odor identification performance (Calhoun-Haney and Murphy, 2005), and that the ApoE gene plays a role in olfactory functioning independent of dementia conversion within 5 years (Olofsson et al., 2010).

3.4.5.2 Gustation Etiologies of gustatory disorders among patients who seek medical attention at ear, nose, and throat clinics are numerous, but the most common are head trauma and upper-respiratory infections (Bartoshuk and Duffy, 1995). As for olfaction, a large variety of conditions can cause taste disorders in the elderly. In a review of such causes, Imoscopi et al. (2012) included changes in the oral cavity, oral and systemic diseases (e.g., CNS-related and endocrine), iatrogenic effects of medication and treatment, nutritional deficiencies, and lifestyle factors. Closely related to the lifestyle factors, it has been suggested that sociodemographic and cultural factors should also be taken into account when considering taste acuity in older people (Simpson et al., 2012). Adults over 65 years of age take on average 3–4 medications, and institutionalized elderly take about twice as many (Finkelstein and Schiffman, 1999). It has been suggested that more than 250 drugs may alter taste and smell sensations. These include antihistamines, lipid-lowering drugs, antimicrobial medications,

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antineoplastic medications, asthma medications, antihypertensives, muscle relaxants, and antidepressants (Schiffman, 1991). Nutritional deficits, such as reduced levels of zinc and vitamins A and B, are known to affect sensitivity and hedonics of taste and smell (Friedman and Mattes, 1991; Schiffman, 1997; Aliani et  al., 2013). The effects of malnutrition on chemosensory perception may, in turn, affect food intake and aggravate the state of malnutrition. Poor oral health in elderly, such as tooth loss and caries, may affect retronasal smell and taste perception (Ship, 1999; Seiberling and Conley, 2004; Solemdal et al., 2012), and dentures have been suggested to increase the risk of impaired flavor perception (Duffy et al., 1999). Saliva plays an important role in taste function by carrying sapid molecules to the receptors and by containing substances capable of modulating taste responses. Although salivary function appears to be relatively unimpaired in healthy aging, dry mouth is a common complaint among elderly who take medication (Bradley and Beidler, 2003). Chewing problems associated with tooth loss and dentures can also interfere with taste sensations, along with the reduction in saliva production (Boyce and Shone, 2006). Neuroanatomical degeneration is likely, at least partly, to explain the agerelated changes in taste perception. It was very early demonstrated that aging typically is accompanied by reduction in receptor-cell, taste-bud, and papilla density (Arey et  al., 1935; Miller, 1989). Although less is known about agerelated changes in the gustatory CNS, functional brain imaging with exposure to sucrose and caffeine has shown decreased activity in the anterior cingulate, lentiform nucleus, putamen, caudate and precentral gyrus in middle-aged adults in comparison with young adults (Green et al., 2013a,b). The same research group has also demonstrated that aging is associated with increased activation in brain regions not commonly associated with taste processing. They discuss the results in terms of a compensation hypothesis due to decreased processing resources and inefficiency in certain brain regions, but also a possible age-related difference in strategy use (Jacobson et al., 2010).

3.5  CONSEQUENCES OF AGE-RELATED CHEMOSENSORY CHANGES FOR FOOD INTAKE AND HEALTH Patients with olfactory loss commonly complain of diminished quality of life, affected interpersonal relations, worry about not perceiving toxic substances, poor control over personal hygiene, difficulties with daily routines, and depression (Croy et  al., 2014). The importance of olfaction in health in general is highlighted by results from longitudinal data indicating increased mortality risk in nondemented elderly who show poor performance on odor identification (Wilson et al., 2011). Given the importance of smell and taste for food intake, it would be expected that impairment in the chemical senses would be accompanied by considerable impact on food intake and health. This is indeed the case, with poor food

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appreciation and decreased appetite, resulting in decrease in body weight (Croy et  al., 2014). Aging individuals, and in particular the institutionalized, can be considered as very vulnerable in this respect. Thus data from elderly with changes in chemosensory perception suggest associated poor food appreciation and appetite, change in food choice such as decreased dietary variation, poor nutritional status, change in body weight, and increased risk for chronic disease (Stevens and Lawless, 1981; Mattes and Cowart, 1994; Duffy et al., 1995; Griep et al., 1995; Schiffman and Zervakis, 2002). Although it is likely that the change in chemosensory perception is the cause in this cause-effect relation, lack of longitudinal data evokes the question as to whether poor nutritional status may contribute to the change in perception. Furthermore, Rolls and McDermott (1991) have demonstrated that elderly people do not show as strong sensoryspecific satiety as young adults, which may contribute to the decreased dietary variation with age. However, not all studies have shown a relation between chemosensory impairment and nutritional problems (e.g., Ferris and Duffy, 1989), and lack of sensory feedback from eating may in some cases actually leads the individual to eat more and become obese. This may be explained by the need to compensate for diminished sensations when eating. Certain elderly subgroups are likely to constitute particular risk groups due to age-related chemosensory loss. For example, the effect of age-related changes in saltiness and sweet perception on food choice may have considerable consequences for elderly people with hypertension and diabetes (Murphy, 1992). Since diminished taste perception appears to lead to increased preference for relatively strong concentrations of the tastant (Murphy and Withee, 1986; Zallen et  al., 1990; Drewnowski, 1997), it becomes difficult for these individuals to adhere to a low-salt and low-sugar diet. There is also considerable risk among elderly to ingest spoiled food. It has, e.g., been suggested that elderly adults are less likely than young adults to reject foods with unpleasant odors (Pelchat, 2000). The unawareness of the olfactory loss, which is common in aging (e.g., Nordin et al., 1995), may aggravate the risk of ingesting spoiled food since these people are less likely to take precautions to avoid eating such food. It can be assumed that the risk among the elderly of ingesting spoiled food is also elevated due to age-related impairments in bitter-taste sensitivity and chemesthesis.

3.6  EFFECTS OF FLAVOR ENHANCEMENT OF FOOD FOR THE ELDERLY The impact of age-related changes in chemosensory perception on food intake, nutritional status, and health is an important issue for the fields of gerontology and food science to address. Schiffman and her research group have done pioneer work and have obtained encouraging results, which suggest that anorexia in the elderly often remits when foods are amplified by additional flavoring (e.g., artificial chicken flavor to a chicken dish) to compensate for diminished

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chemosensory function (Schiffman and Warwick, 1988). More specifically, results from their research suggest that additional flavoring will increase institutionalized elderly people’s preference for and intake of food, increase salivation, and improve immunological status and grip strength (Schiffman and Warwick, 1993; Schiffman, 1998; Schiffman and Miletic, 1999). Despite somewhat mixed results, subsequent research shows continued promise for the approach of flavor enhancement for elderly. A number of investigations have studied enhancement with umami taste of MSG. Essed et  al. (2009) reported an optimal preferred concentration of MSG in mashed potatoes, but not in spinach or ground beef, and no difference in intake of these dishes with or without MSG among institutionalized elderly. By supplementing regular meals with MSG to hospitalized elderly patients, certain aspects of the patients’ daily performance (e.g., clear speech and cheery facial expression) was found to improve and the immune function to be facilitated (Toyama et al., 2008). From a follow-up study the same research group reported improved behavior (e.g., response when called and facial expressions) and nutritional status (Tomoe et  al., 2009). However, although umami taste may improve appreciation and intake of food (Schiffman, 1998), the effects of MSG were in these two studies not due to increased nutritional intake. In a recent study, repeated exposure to a novel flavor combined with MSG in healthy elderly showed increased consumption of soup (Dermiki et al., 2015). Regarding enhancement with flavors other than MSG, institutionalized elderly patients have shown increased food enjoyment when the flavor of first courses (e.g., sage and rosemary added in rice with butter) and juice (sucrose and peach aroma added in peach juice) had been amplified (Laureati et  al., 2008). Having perceived custard dessert as less intense in flavor (cherry/vanilla), and with sensitivity loss to olfactory, gustatory, and trigeminal stimuli, elderly patients showed increased food enjoyment after the compensatory strategies of flavor enrichment, textural change, and irritant addition (Kremer et al., 2007). Amplification with vegetable flavor in soup and with cherry flavor in yogurt resulted in increased consumption of the soup and yogurt in geriatric patients (Griep et al., 1997). A significant correlation has also been observed between BMI and preference for flavor-amplified yogurt, but no correlation was found between BMI and neither odor perception nor relative consumption of highly flavored yogurt (Griep et al., 2000). A number of studies have shown either no effect or only very weak beneficial effects of flavor enhancement. In one study, despite impaired olfactory functioning in the elderly, no clear indication of benefit of enhanced flavor of yogurt-like snack products with strawberry, red currant, lingonberry, and chokeberry was found for either pleasantness or intake (Koskinen et al., 2003). De Graaf et al. (1996) found a higher preferred concentration of food flavors in elderly than for young adults in orange lemonade, but not in bouillon, tomato soup, or chocolate custard. Tuorila et al. (2001) reported only a very slight improvement in hedonic quality of cream cheese in elderly by adding vanilla aroma.

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3.7  CONCLUSIONS AND FUTURE TRENDS As discussed above, it is well documented that the chemical senses influence when, how much, and what the human individual ingests. A considerable volume of research has also been conducted over the past several decades to investigate perceptual, anatomical, histological, and physiological changes in olfaction and gustation in normal and pathological aging. From this research it is clear that various aspects of the sense of smell are impaired in the aging individual. Although the gustatory system may be less affected than the olfactory system by the aging process, taste function does clearly decline with age. However, there is still limited knowledge of age-related pathological changes in the gustatory CNS that can account for the perceptual changes. Future research may target this issue. It is obvious that genetic variation plays a crucial role in taste sensitivity and food preference. However, there appears to be a lack of documentation of the interaction effects of genetic variation and aging, which may be a promising route for study in order to understand the large variability in taste sensitivity and food preference between elderly people. Research in chemesthesis has grown rapidly in the past decade, and a large number of laboratories are today focusing on this sensory system. The need for further understanding of perceptual changes in chemesthesis in aging and its consequences for food intake has therefore good potential to be met within a near future. In particular, there is a need for better documentation of anatomical, histological, and physiological pathology underlying age-related changes in chemesthesis. Another question to be approached is the relative degree to which the alterations in the chemical senses are caused by normal aging processes or rather by diseases, medications, cognitive status, or environmental factors. Finally, flavor enhancement, in particular among institutionalized elderly, appears to be a fruitful approach. The combination of promising but also somewhat inconsistent results calls for further investigation of this intervention to improve nutritional intake in the growing elderly population in which chemosensory impairment is common.

ACKNOWLEDGMENT This work was supported by grants from the Swedish Foundation for Humanities and Social Sciences (M14–0375:1).

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