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a Division of Geriatric Medicine, Saint Louis University Health Sciences Center and the Geriatric Research, Education, and Clinical Center, Veteran's Administration Medical Center, Saint Louis, Missouri
Between good sense and good taste, there lies the difference between cause and its effect.
—Jean de la Bruyere cHANGING trends in the attitudes of health professionals toward geriatric medicine can be attributed in part to the painstaking repetition of basic, yet frequently ignored, geriatric principles. Nevertheless, as gerontology evolves and advances into the new millennium, clinical and academic geriatrics must move beyond the realms of mere syndrome definition. The syndromes of undernutrition and "anorexia of aging" are now firmly entrenched as bona fide geriatric problems (1)(2). The current challenge lies in the precise identification of the pathogenesis of these conditions. Critical appraisal of nutritional therapeutic modalities, utilizing objective outcome measures, is a crucial component of this process.
In this issue of the journal, Mathey and others address compelling issues regarding the theories of satiety in the elderly population (3). In their study, repeated consumption of flavor-enhanced meals by nursing home residents over a 16-week period led to an increase in the intensity of their daily perception of hunger. Although the documented daily dietary energy intake of the test subjects remained unchanged, they demonstrated significant weight gain over the course of the study. In contrast, subjects in the control group did not gain weight and demonstrated a progressive decrease in daily energy intake during the study.
These findings warrant a reappraisal of the roles of sensory-specific satiety and allisthesia on food consumption in elderly persons. Sensory-specific satiety describes the reduction in the positive hedonic response to the sensory qualities of a food item that occurs concurrent with consumption (4). This is believed to be the mechanism that prompts a person to switch from one food item to another during the course of a meal. Allisthesia, a closely aligned concept, describes the alteration in food intake that occurs in response to changes in macronutrient homeostasis (5). Earlier studies demonstrate that 1 hour after intragastric glucose loads, sweet solutions are perceived as less palatable. A similar reduction in the palatability of salty solutions occurs after intragastric salt loads (5)(6). These findings suggest that postabsorptive physiological processes elicit allisthesia, whereas sensory-specific satiety is probably generated by impulses stemming from the gustatory and olfactory receptors. Conceptually, sensory-specific satiety appears to be an inbuilt mechanism designed to preempt and oppose the effect of allisthesia by encouraging variation between food items before postabsorptive palatability wanes. Several studies have identified a reduction in sensory-specific satiety in older adults (7). This may explain the tendency for the diet to become increasingly monotonous and less varied with aging (8). It would be reasonable to hypothesize that blunted sensory-specific satiety acting in concert with allisthesia in the older adult may markedly limit both the quality and quantity of food intake.
An earlier study by Schiffman and colleagues also shows that nutrient-dense food intake in elderly persons may be increased by flavor enhancers. Additionally, they caution that flavor enhancement should be reserved for persons with reduced chemosensory functioning because enhanced flavors may reduce energy intake in persons with normal taste perception (9). However, this valid recommendation creates a paradox because the progressive blunting of taste and smell perception with aging is often not appreciated by the affected older adult (10)(11).
Nevertheless, one may theorize that there is a threshold for sensory-specific satiety determined by taste perception. It is conceivable that, with added flavors, the afferent gustatory stimulus may be enhanced to the point at which taste perception is normalized. Sensory-specific satiety may thus be restored to normal, exerting a permissive effect on increasing the variety of meals and negating the effect of allisthesia. Quantitative studies utilizing graded flavors and preferably a within-subject repeated-measures design may provide more precise and objective data on the use of enhanced flavors as a therapeutic option to combat anorexia in the older adult.
Bathalon and colleagues examine yet another aspect of the diverse spectrum of geriatric nutrition (12). As ageism becomes increasingly politically incorrect, widely propagated, though unfounded, concepts regarding age-related issues are often challenged. However, objective evidence frequently proves that the truth may lie somewhere in the middle. The diminution of appetite with aging has been recognized for centuries. The error is in its qualification as a normal physiological event. Researchers now attempt to provide firm evidence that anorexia of aging is a disease. Hence, the concept of dietary restraint in the older adult may be overshadowed. Additionally, the stereotypical impression that the older adult lacks interest in body image issues may propagate this trend. Consequently, health professionals often overlook the possibility of intentional dietary restraint in the evaluation of anorexia in the elderly population. Bathalon and colleagues bring this issue to the forefront in their cross-sectional study of healthy, postmenopausal women, in which they compared women with evidence of dietary restraint with unrestrained eaters (12). They failed to identify any difference in cardiopulmonary function, bone mass, immune function, or self-perceived health. On the surface, these findings constitute a cause for concern, when viewed in the context of the potentially devastating consequences of undernutrition in older persons. However, closer scrutiny of the results of this study study reveal no difference between macronutrient and micronutrient intake between both populations. The major health impact of dietary restraint results from the limitation of food intake and, hence, an increase in the risk of undernutrition. Thus, the argument can be made that the hiatus between the intent to restrict intake and the actual reduction in energy and micronutrient intake may explain the lack of adverse effects noted by Bathalon and colleagues (12).
An earlier study by Lindroos and colleagues examined dietary intake in relation to restrained eating, disinhibition, and hunger in obese and non-obese subjects. This study demonstrated similar findings in non-obese subjects in that they failed to identify any association between food intake and dietary restraint. However, there was a negative association between restrained eating and energy intake in the obese subjects (13). The mean body mass index (BMI) in both restrained and unrestrained eaters was reported as lower than that of the general population by Bathalon and colleagues. Furthermore, there was no difference in BMI between restrained and unrestrained eaters. The latter characteristic may explain not only the lack of reduction in energy intake but also the absence of negative changes in mood and self-perceived health among the restrained eaters (12). A dominant input to one's sense of body image is derived from societal acceptance. Currently, most western cultures base the accepted norms for body image in women on media-driven images of thin women (14)(15). It is doubtful that the results of Bathalon and colleagues will be replicated among obese women with dietary restraint who may perceive themselves as socially unacceptable. Dietary restraint in this group of women could conceivably reinforce the perception of failed therapy if weight loss is neither achieved nor sustained. This has been shown to evoke feelings of marked inadequacy and low self-esteem (16).
Bathalon and colleagues also identified a higher prevalence of repeated dietary attempts among women who exercised dietary restraint (12). Interpretation of this finding is subject to multiple confounding factors. Repeated dieting attempts may indicate repeated failure to comply with long-term dietary weight reduction regimens, or it may indicate the use of dieting as a rescue procedure in the face of weight gain, be it real or imagined. Nevertheless, the issue of recurrent dieting and consequent weight cycling is a critical consideration in evaluating the long-term effect of dietary restraint on the health of older adults. Several epidemiological studies have identified an increase in coronary artery disease and cardiovascular deaths in persons with a history of repeated dieting and weight cycling (17). Lee and Paffenbarger identified an increased risk of death among male Harvard University graduates who repeatedly lost or gained more than 11 lb when compared with controls who maintained a stable weight (18). Similarly, in the Framingham Heart study, a 32-year analysis of 3130 adults identified an increased risk of cardiovascular morbidity and mortality among persons with significant fluctuations in body weight (19). Animal studies demonstrate a preferential reduction in the adipose content of linoleate-enriched triacylglycerol in rats subjected to weight cycling by caloric restriction. This results in a proportional increase in palmitate-enriched triacylglycerol. The subsequent alteration in the ratio of polyunsaturated acids to fatty acids has been proffered as the explanation for the increase in cardiovascular morbidity and mortality (20). However, caution should be exercised in extrapolating the results of these studies to the older adult, especially in the light of other studies that do not identify an association between weight cycling and adverse outcomes (21)(22). Furthermore, there is evidence to show that the older adult who diets in an attempt to control weight may constitute a distinct subset from younger women who diet for the same reason. A notable proportion of older women who diet start dieting in the fifth decade of life and had never dieted in their teens (23). It is unclear if this subset is defined by age-related physiological changes or spawned by cultural pressures, the latter being subject to changing trends over time.
Insufficient evidence exists regarding the safety or efficacy of intentional food limitation in the older adult. In contrast, there is overwhelming evidence regarding the adverse effects of undernutrition in the elderly. Bathalon and colleagues must be commended for directing our focus toward a relatively underemphasized domain of geriatric nutrition. However, in the light of the current state of knowledge it would be premature to conclude that dietary restraint is a benign characteristic in the older adult.
The frail older adult is at greatest risk of the devastating consequences of undernutrition. The attendant morbidity and mortality associated with impaired nutritional status, particularly among institutionalized older adults, has been highlighted in several studies (24)(25)(26)(27). Nevertheless, physicians often fail to recognize risk factors or clinical markers of undernutrition in such patients (28)(29). The study by Zuliani and colleagues in this issue of the journal focuses on the complex interaction between nutritional and functional status in nursing home residents (30). They conducted a longitudinal study aimed at evaluating the relationship between undernutrition and progressive functional disability. To this end, they identified 98 nursing home residents, 40 of whom had exhibited functional stability or improvement over a 2-year period. The other 58 had lost independence in at least two activities of daily living (ADL) over the same time period. Markers of nutritional status used in this study included biochemical parameters and anthropometric indices, such as BMI, waist/hip ratio, and body composition determination. They found that subjects who had lost independence in their ADL had worse parameters of nutritional status at the onset of the 2-year period. After multivariate adjustment, the extent of lean body mass reduction was significantly associated with loss of ADL at 2-year follow-up. They conclude from their findings that among functionally impaired institutionalized older adults, evidence of undernutrition may be a predictor of further functional deterioration. The apparent simplicity of the message contained in this study may cause it to be dismissed as stating the obvious. Most physicians will claim awareness of the fact that poor nutrition and weight loss enhance functional deterioration, although few will intervene (28)(29). However, there is a dearth of scientific data that has attempted to examine the parallel, synergistic effect of both functional disability and undernutrition longitudinally. Thus, this study is valuable in that it brings some objectivity to clinical geriatric practice that heretofore was often justified on the basis of intuition. Additionally, these findings highlight the dynamic relationship between undernutrition and sarcopenia, the latter being a syndrome that describes the loss of muscle mass and function that occurs with aging (31). The increasing prevalence of sarcopenia with senescence has been highlighted in several studies (26)(29)(32). This syndrome has devastating implications for the individual and at the societal level. The increase in frailty resulting from sarcopenia can lead to a marked loss of functional independence due to increasing disability. On a more global level, the increased demand for health care services constitutes an enormous drain on available resources. It is thus appropriate that current research is directed toward identifying therapeutic and preventive strategies that will reduce the ultimate impact of sarcopenia on functional status in the older adult. Various pharmacological therapeutic modalities have been studied, among which are growth hormone, insulin growth factor-1 (IGF-1), dihydroepiandosterone, and testosterone. Studies with growth hormone, IGF-1, and dihydroepiandosterone have yielded conflicting results. Furthermore, the prohibitive cost of growth hormone and the high incidence of side effects such as carpal tunnel syndrome, insulin resistance, and arthralgia notably diminish the clinical utility of this agent (33)(34). The effect of testosterone replacement on sarcopenia in hypogonadal men has been evaluated in several trials. Evidence exists to show an increase in fat-free mass and muscle strength in older hypogonadal men following testosterone replacement (35)(36). Notably, the majority of studies have focused on healthy older men. Ongoing studies will determine the utility of testosterone replacement in the treatment of sarcopenia in frail elderly men with significant comorbidity. Nonpharmacological therapeutic methods are also being explored. Exercise resistance training has been shown to reverse the effects of sarcopenia by improving muscle mass, strength, and physical function (37)(38). The findings of Zuliani and colleagues provide another potentially viable therapeutic option (30). If, indeed, as the results of the study suggest, undernutrition heralds increased progression of sarcopenia and frailty, then maintenance of optimal nutritional status may prove to be the most critical aspect of geriatric management in the prevention of age-related disability. As the authors rightly point out, there is a paucity of knowledge regarding the "trajectory of disability" in the older adult. However, the issues raised by Zuliani and colleagues provide sufficient justification for further longitudinal studies to explore this theme further (30).
There is ample justification to consider undernutrition a major scourge of aging, warranting an aggressive approach to prevention and treatment. The eradication of the threat of undernutrition to the older population, as with any other chronic disease, will more likely be achieved by prevention rather than therapy. The basic principles of therapeutic intervention are based on the simple concept of replacement therapy. In contrast, the development of preventive strategies is rendered much more complex by the imprecise definition of the pathophysiological mechanisms that underlie age-related appetite dysregulation and undernutrition. The focus of geriatric research such as those studies published in this issue is refreshing. It suggests not only an increased awareness of the significance of undernutrition but a concerted effort by physicians and health professionals to elucidate the pathophysiological mechanisms underlying a deadly disease. Conceivably, the trend of current research heralds significant advances in geriatric nutrition. Such progress bears the potential to improve the quality of life of the older adult and ease the individual and societal care-giving burden. Ultimately, the only disadvantage to this process is that practicing clinicians will be unable to plead ignorance as justification for the provision of inadequate care to the undernourished older adult.
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