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American Journal of Clinical Nutrition, Vol. 75, No. 5, 944-947, May 2002
© 2002 American Society for Clinical Nutrition

Original Research Communication

Effect of liquid dietary supplements on energy intake in the elderly1,2

Margaret-Mary G Wilson, Raj Purushothaman and John E Morley

1 From the Division of Geriatric Medicine, St Louis University Health Sciences Center (M-MGW, RP, and JEM), and the Geriatric Research, Education, and Clinical Center, Veterans Administration Medical Center, St Louis (M-MGW and JEM).

2 Address reprint requests to M-MG Wilson, Division of Geriatric Medicine, St Louis University Health Sciences Center, 1402 South Grand Boulevard, Room M238, St Louis, MO 63104. E-mail: wilsonmg{at}slu.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Undernutrition is a risk factor for increased mortality in older adults. Therapeutic intervention includes the administration of liquid dietary supplements.

Objective: We investigated the effect of liquid dietary supplements on satiation, satiety, and energy intake in older adults.

Design: This study had 2 phases in a within-subject, repeated-measures design. The energy intake of 15 elderly (aged >70 y) and 15 younger (aged 20–40 y) healthy subjects was measured after 4 liquid preloads: water, high fat, high carbohydrate, and high protein. The preloads were administered within 5 min of a test meal in phase 1 and >=60 min before the test meal in phase 2. Palatability, fullness, and hunger were assessed by using visual analogue scales.

Results: Mean energy consumption of the test meals was significantly lower in the older than in the younger subjects (P = 0.001), as was mean macronutrient consumption of fat and carbohydrate (P = 0.002 and 0.001, respectively). Mean energy intake and macronutrient consumption were higher in phase 2 than in phase 1 in both older and younger subjects (P < 0.05). Satiety lasted longer in older than in younger subjects after the high-protein and high-fat preloads (P = 0.001).

Conclusion: In the elderly, administration of dietary supplements between meals instead of with meals may be more effective in increasing energy consumption.

Key Words: Undernutrition • nutritional supplements • dietary supplements • anorexia • energy intake • liquid supplements • macronutrients • elderly


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Unintentional weight loss and undernutrition are common problems in the elderly (1–4). The resultant increase in morbidity and mortality associated with these syndromes is well documented (5–8). Anorexia is a major cause of undernutrition in the elderly. The etiology of anorexia in older adults is often multifactorial, encompassing systemic disease, iatrogenesis, and psychosocial factors. In addition, the olfactory and gustatory receptors are blunted with aging, which may compromise the hedonic qualities of food and limit intake (9).

Age-related anorexia is well documented (10–13). Available data suggest that aging leads to dysregulation of the physiologic processes that control food intake. This may explain the failure of the elderly to adjust their food intake to compensate for deviations in their body weight from baseline (14). Consequently, negative energy balance in older adults increases the risk of undernutrition, underscoring the importance of early nutritional intervention. Studies have also found slower gastric emptying times and greater satiation and satiety with meals in older than in younger adults (11). Satiation is defined as the appetite-regulating process that occurs while eating that inhibits further food intake and terminates the meal. Satiety describes the state following a meal during which hunger is dampened and the urge to consume food is inhibited (15). Thus, satiation determines meal size and satiety determines the intervals between meals (16). Both processes ultimately determine cumulative food intake.

The age-related physiologic changes described may further compromise nutritional intake in the elderly. Despite the complex interplay of multiple factors in the etiology of anorexia and undernutrition in the elderly, nutritional intervention often relies solely on the empirical administration of a wide variety of liquid dietary supplements. We designed this study to determine the effect of liquid dietary supplements on satiation, satiety, and subsequent energy intake. The results obtained in healthy elderly subjects were compared with the findings in healthy younger adults.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Thirty healthy research volunteers were recruited from the community around St Louis University Health Sciences Center through advertisements, health fairs, and posters. Fifteen subjects were >70 y of age and 15 subjects were 20–40 y of age. The elderly subjects were recruited from "well-person" visits to St Louis University Health Sciences Center Outpatient Clinics and by advertisement within neighboring senior citizen centers. No evidence of high dietary restraint, eating abnormalities, or depression in any of the subjects was shown by self-reported scoring (17–19). Elderly subjects were screened for dementia by using the Mini Mental State Examination to ensure normal cognitive function (20). All subjects ate >=3 regularly spaced meals daily and had no history of food allergies or aversions. None of the subjects had a history of gastrointestinal surgery or hepatic or renal dysfunction. None were taking prescribed medications at the time of the study. All subjects received a complete physical examination before entry into the study and gave written informed consent. The study was reviewed and approved by the Institutional Review Board of the St Louis University Health Sciences Center. All procedures complied with the ethical standards of the St Louis University Institutional Review Board policies regarding human experimentation. These are in accord with the 1983 revision of the Helsinki Declaration of 1975.

Procedure
Each subject was required to eat 3 regularly spaced meals/d on the 3 d before the study began. The subjects were instructed to keep a food diary over this 3-d period; the diary was reviewed to ensure compliance with regular meal intake. The study had a within-subject, repeated-measures design, with each subject serving as his or her own control. The study was carried out in 2 phases comprising 4 sessions each. All subjects were outpatients and were driven from their homes to the study site by one of the investigators (M-MGW) on the morning of each session. Each subject was assigned a separate room and allowed to rest for 30 min before administration of the preload. All sessions were conducted in identical rooms housed within the authors' group medical practice in the outpatient office building of the St Louis University Health Sciences Center.

Phase 1
All subjects were required to fast from midnight to 0800 on the morning the study began. At 0800, each subject was required to drink 300 mL of a liquid preparation as a preload. This was followed within 5 min by a test meal comprising sandwich quarters, which subjects were required to eat until satiation. Each subject repeated this procedure 3 times at biweekly intervals. Before each session, the subjects were again required to fast from midnight to 0800. A food diary for the previous 3 d was also requested. At each session, a different preload was administered, although the volume was unchanged. Each subject therefore received 4 different preloads in phase 1: 1) a high-carbohydrate drink, 2) a high-protein drink, 3) a high-fat drink, and 4) water, which served as a control. Each preload, except water, contained 1255 kJ energy. The sequence order of the preloads was randomly assigned. Palatability, hunger, and satiation were assessed with the use of a 10-cm horizontal visual analogue scale, immediately before each session began and at 5 min intervals until the end. The 0-cm mark on the visual analogue scale was labeled "not hungry" and the 10-cm mark was labeled "very hungry." Subjects were asked to mark a vertical line on the scale to indicate their degree of hunger. A similar scale was used to assess their degree of fullness (21).

Phase 2
Identical preloads and test meals were used in phase 2. Each subject was again required to fast from midnight to 0800 before each session. After the preload was administered, the subject was not allowed to eat for 60 min. Thereafter, the test meal was offered to the subject on request. The subject was then encouraged to continue eating until satiation was achieved. Palatability, hunger, and satiety ratings were obtained immediately before the test meal and at 5-min intervals for 1 h. Subsequent readings were at 30 min intervals until completion of the session. Each subject participated in 4 sessions. Random assignment of preloads was repeated in phase 2.

Foods and macronutrients
The high-carbohydrate preload was a fruit juice–based drink containing 88.25 g carbohydrate, 0 g protein, and 0 g fat. The high-protein drink was a reconstituted commercial liquid nutritional supplement containing 4 g fat, 47 g carbohydrate, and 26 g protein. The high-fat drink was a fortified milk-based drink containing 25.5 g fat, 11.5 g carbohydrate, and 8 g protein.

The test meal was composed of sandwich quarters prepared by one of the investigators (M-MGW). The subjects had unrestricted access to a variety of sandwiches at each session. They could choose from white or wheat bread and 3 different fillings: peanut butter, jelly, and tuna fish. All sandwiches were of known energy and macronutrient content. Immediately after the session, the energy and macronutrient content of the sandwich quarters consumed by each subject was determined by another investigator (RP), who was unaware of which type of preload was consumed by each subject.

Statistical analysis
Energy intake, including the energy content of the preload, was analyzed with the use of three-factor repeated-measures analysis of variance. STATISTICA for WINDOWS (version 5.1; StatSoft Inc, Tulsa, OK) was used for the statistical analyses. The factors used were age, phase, and preload. Any statistically significant effects were further analyzed using Tukey's honestly significant difference test for post hoc comparisons of means. The satiety period in phase 2 and the palatability, hunger, and satiation ratings were also compared with the use of three-factor repeated-measures analysis of variance. Data are presented as means ± SEM. P values < 0.05 were considered significant in all analyses.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographics
The demographic data for both groups of subjects are shown in Table 1Go. There was no significant difference in body mass index between the elderly and the younger subjects. There was also no significant difference in ratings of palatability, hunger, or fullness between the older and younger subjects in either phase 1 or 2.


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  		TABLE 1 Demographic data of healthy elderly and younger subjects1
 
Satiety, satiation, and energy consumption
The satiety period was defined as the time from the administration of the preload to the request for the test meal in phase 2. The interval between the preload and the request for the test meal in phase 2 was significantly longer in the older subjects than in the younger subjects after the high-fat and high-protein preloads (Table 2Go). After administration of the preloads, older subjects consumed less energy than did younger subjects. Energy intake was higher in both groups when the supplement was administered >=60 min before the meal than when the supplement and the meal were given together.


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  		TABLE 2 Interval between administration of the preload and consumption of the test meal in phase 2 in elderly and younger subjects1
 
Analysis of variance
The three-factor interaction between age, preload, and phase was not significant. Two-factor interactions between age and phase, phase and preload, and age and preload were also not significant. The main effects of age and phase on total energy and macronutrient consumption of the test meal are shown in Table 3Go.


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  		TABLE 3 Main effects of age and phase on total energy intake and macronutrient consumption of the test meal1
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The 2-phase paradigm used in this study allowed for observations during satiation (phase 1) and satiety (phase 2). The administration of liquid supplements with meals appeared to induce premature satiation in our elderly subjects. The pathophysiologic consequences of aging on positive allisthesia may account for this observation. Positive allisthesia refers to the positive feedback effect that the hedonic qualities of food have on further food intake during a meal (22). Pleasant sensory information obtained from gustatory, olfactory, and visual receptors serves to encourage continued meal consumption (23). Thus, during the first 15–20 min of a meal, the sensory properties of foods are the main influence on food intake. Thereafter, energy consumption is largely determined by the limitation of satiety induced by the postabsorptive effect of meals (24). In the elderly, age-related decreases in taste and olfactory receptors may negate the effect of positive allisthesia, thereby increasing the likelihood of premature satiation (9). Administration of supplements between meals in such persons may counter the effect of premature satiation on food intake by allowing postabsorptive appetite-regulatory processes to predominate. Theoretically, this should result in relatively weaker and shorter satiety signals, thereby encouraging increased energy intake at the next meal.

Previous studies showed a decline with aging in the rate of gastric emptying and adaptive fundal relaxation (25–27). The reduction in fundal relaxation results in food passing more rapidly into the antrum; consequently, antral distension occurs earlier and persists longer. These changes are associated with increased satiation in older adults (21,28–30). In addition, the findings of Cook et al (11) show that intraduodenal infusion of nutrients produces a smaller decrease in hunger and less satiety in older than in younger subjects. These findings suggest that meal consumption and satiation in the elderly are more dependent on gastric reservoir function and less dependent on postabsorptive regulatory signals. Administration of supplements between meals instead of with meals may avoid further compromising the reservoir function of the stomach by limiting the degree of antral distension during the main meal.

In our study, the elderly subjects had longer periods of satiety than did the younger subjects after consuming the high-fat and high-protein supplements. Although this finding agrees with the results of several previous studies, the administration of equal preloads to all subjects may constitute a relatively higher load in older adults because of their lower daily energy requirements. This may confound objective interpretation of our results (11,30,31). Our findings are at variance with the results of some studies that showed that fat has low satiating efficiency compared with carbohydrate and protein (32–34). However, other studies showed that jejunal and ileal infusion of lipid into healthy subjects reduces the amount of subsequent energy consumption, possibly as a result of delayed gastric emptying (35,36). It is plausible that this effect of lipid on gastric emptying further exaggerated by the age-related physiologic delay in gastric emptying may contribute to decreased energy intake after a high-fat preload in older adults. Nevertheless, more recent data indicate that the energy density of foods, and not the macronutrient content, is the critical determinant of the satiety response. Rolls et al (37,38) showed that preloads that were identical in energy and macronutrient content exerted a greater effect on satiety when their volume and weight were increased by the addition of water. There is also evidence that when the macronutrient content of preloads that are equal in energy density is varied, the effects of fat and carbohydrate on satiety are similar (37–39). Thus, although our findings indicate that high-fat nutritional supplements may have a suppressant effect on appetite in older adults, our study design precludes objective comment on the effect of specific macronutrients on satiety. The formulation of the preloads used in our study was intended only to produce identical energy content and volume; thus, their weights and energy density may have differed. Further studies using concurrent evaluation and mononutrient supplements of equal energy density may more accurately define the effect of high-fat liquid supplements on appetite in the elderly.

Our findings—that energy intake is higher in both younger and older subjects when the nutritional supplement is administered >=1 h before meals and that energy intake is lower in older than in younger subjects after they consume identical supplements—were obtained in discrete sessions. Additional studies conducted over a continuous period of several days will be required to confirm these observations.

Dietary supplementation with liquid preparations is used frequently to increase energy intake in undernourished older adults in both institutionalized and community-dwelling populations (40). In nursing home residents, these supplements are often used as an intervention for weight loss, without regard to dose, timing of administration, or outcomes (41). We suggest that when such supplements are used, they should be given between meals and >=1 h before the next meal. Constant monitoring of both energy and macronutrient intake is crucial to ensure the efficacy of nutritional intervention when liquid supplements are prescribed. The fat content of nutritional liquid supplements is also relevant, as this may have an unpredictable effect on appetite. Patients who continue to have low energy intakes after liquid dietary supplementation may increase their food consumption if supplements with a lower fat content are substituted.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication October 2, 2000. Accepted for publication June 15, 2001.




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