Below, we examine recent applications of doubly labeled water methodology in healthy and diseased older individuals to understand better daily energy requirements and the regulation of energy balance. We consider several diseases that are associated with negative energy balance and generalized wasting.
Heart failure is an increasing important and frequent clinical problem, with the highest prevalence observed in the elderly ( 24). The incidence of heart failure increases 50-fold between the ages of 40 and 60 years. The unexplained loss of body weight and muscle mass are hallmark clinical features of end-stage congestive heart failure (25). It is unclear whether reduction in caloric intake or elevated caloric expenditure accounts for the negative energy balance and subsequent weight loss in advanced heart failure. Furthermore, daily energy requirements in heart failure are unknown.
Several studies have examined energy expenditure in heart failure. RMR, body composition, and dietary intake were examined in 20 heart failure patients with documented systolic dysfunction and compared with an age-matched cohort of 40 healthy elderly volunteers ( 26). RMR was measured by indirect calorimetric techniques and fat mass and fat-free mass were measured by dual-energy x-ray absorptiometry. Fat-free mass (lean body mass minus skeleton) was approximately 4 kg lower in heart failure patients, despite similar amounts of fat mass. Although lower fat-free mass was noted, the RMR was 18% higher in heart failure patients than in healthy controls (Fig 5.2.). These results suggest that heart failure patients have a higher RMR (for their metabolic size), which may contribute to their propensity for unexplained weight loss and musculoskeletal wasting.
Figure 5.2. The relationship between resting metabolic rate and fat-free mass in healthy individuals and patients with heart failure. This figure shows that resting metabolic rate (per kg of fat-free mass) is higher in heart failure patients. (Adapted from Poehlman ET, Scheffers J, Gottlieb SS, et al. Ann Intern Med 1994;121:860-2).
Measurement of the RMR, however, only provides partial information on whether energy needs are indeed higher in congestive heart failure patients. Ultimately, the balance between daily energy expenditure and food intake regulates body composition in humans. Although recent work ( 26, 27 and 28) provided evidence that resting energy requirements are higher in heart failure and that the magnitude of the increase in resting energy needs increases with symptom severity ( 27), it was unclear whether daily energy needs are higher in heart failure patients in their free-living environment. Accordingly, daily energy expenditure and physical activity were measured in free-living cachectic (12) and noncachectic (13) patients with heart failure and 50 healthy control volunteers, by doubly labeled water and indirect calorimetry methodology (29) (T.a.bIe 5,3.). As expected, fat mass and fat-free mass were lower in cachectic patients than in noncachectic patients and controls. Daily energy expenditure was lower (P < .05) in cachectic patients (1870 ± 347 kcal/day) than in noncachectic patients (2349 ± 545 kcal/day) and healthy controls (2543 ± 449 kcal/day) (Table. . . .5.3). Differences in daily energy expenditure were due to lower (P < .05) free-living physical activity energy expenditure in cachectic (269 ± 307 kcal/day) and noncachectic patients (416 ± 361 kcal/day) compared with healthy controls (728 ± 374 kcal/day). Thus, the hypothesis that daily energy requirements are higher in heart failure patients is not supported by these initial studies using doubly labeled water methodology. Moreover, these findings underscore the need to measure daily energy expenditure in free-living patients accurately before drawing conclusions about the presence or absence of elevated daily energy expenditure and its relationship to weight loss. Because no evidence for an elevated daily energy expenditure in cachectic heart failure patients was found, the suggestion is that inadequate energy intake is a likely determinant of weight loss. Several factors including abdominal pain and distention, gastrointestinal hypomotility, and delayed gastric emptying have been suggested to contribute to anorexia in heart failure patients ( 25). The fact that daily energy expenditure was not elevated in noncachectic patients, however, argues against an elevated daily energy expenditure preceding weight loss.
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Table 5.3 Daily Energy Expenditure,a Its Components and Energy Intake in Cachectic and Noncachectic Heart Failure Patients and Healthy Controls
Alzheimer-type dementia, a growing health problem, is one of the leading causes of death among elderly people ( 30). The overall estimate is that more than 10% of persons over 65 suffer from senile dementia of the Alzheimer's type (31). Annual medical costs for Alzheimer's disease are estimated to be more than 40 billion dollars (32).
Unexplained weight loss is a frequent clinical finding in patients with Alzheimer's disease. The National Institute of Neurological and Communicative Disorders and Strokes Task Force on Alzheimer's Disease has included weight loss as a "clinical feature consistent with the diagnosis of Alzheimer's disease" ( 33). Moreover, it has been postulated that Alzheimer's disease may be characterized by dysfunction in body weight regulation ( 34).
Weight loss is due to a mismatch of energy intake with energy expenditure, which leads to low body weight, atrophy of muscle mass, and accelerated loss of functional independence in persons with Alzheimer's disease. Weight loss also increases the risks of decubitus ulcers, systemic infection, mortality, and greater consumption of health care resources (35, 36). Although it may not yet be possible to prevent, treat, or permanently alter the course of the underlying disease, identification and amelioration of nutritional problems may prove an ideal strategy for lessening the burden of the disease.
Is the energy imbalance associated with Alzheimer's disease caused by reduced energy intake, an elevated rate of energy expenditure, or a combination of both? Studies examining the caloric adequacy of diets of Alzheimer's patients as a potential contributor to weight loss ( 3,7, 38 and 39) have yielded inconclusive results. This is not surprising, since the recording of food intake is an unreliable method that provides little useful information on an individual's actual habitual energy intake. Therefore, investigators have focused on the possibility that elevated energy expenditure contributes to unexplained weight loss in Alzheimer's patients. Several investigators found an elevated RMR in Alzheimer's patients, which might itself result in weight loss, ( 40, 41 and 42), although these results remain controversial (43, 44, 45 and 46). A more important question, however, is whether free-living Alzheimer's patients have a higher daily energy expenditure than normal elderly persons.
Doubly labeled water methodology was used to examine the hypothesis that Alzheimer's patients are characterized by high levels of daily energy expenditure ( 47). Thirty Alzheimer's patients (73 ± 8 years of age; Mini-Mental score: 16 ± 8) and 103 healthy elderly persons (69 ± 7 years of age) were studied. Daily energy expenditure and its components (RMR and free-living physical activity) from doubly labeled water and indirect calorimetry were measured over a 10-day period. Fat-free mass tended to be lower in Alzheimer's patients (45 ± 9 kg) than in the healthy controls (49 ± 10 kg; P = .07), whereas no differences were noted in fat mass between groups. Daily energy expenditure was 14% lower in Alzheimer's patients (1901 ± 517 kcal/day) than in the controls (2213 ± 513 kcal/day; P £ .001) because of a lower RMR (1287 ± 227 vs. 1418 ± 246 kcal/day; P < .01) and physical activity-related energy expenditure (425 ± 317 vs. 574 ± 342 kcal/day; P < .05) (Table
5,4). There were no differences between groups when energy expenditure was normalized for differences in fat-free mass. Thus, the lower energy expenditure in Alzheimer's patients is primarily due to their lower fat-free mass.
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Table 5.4 Daily Energy Expenditure3 and Its Components in Alzheimer's Patients and Healthy Elderly Persons
Daily energy expenditure was also examined in a subgroup (N = 11) of Alzheimer's patients who had lost significant body weight (5.6 ± 2.3 kg) within the previous year. A lower daily energy expenditure was found in cachectic Alzheimer's patients (1799 ± 474 kcal/day) than in noncachectic Alzheimer's patients (1960 ± 544 kcal/day) and healthy elderly controls (2213 ± 513 kcal/day; P < .01). Thus, daily energy expenditure is not higher, but lower in Alzheimer's patients, because of lower levels of resting and physical-activity-related energy expenditure and fat-free mass.
Collectively, the hypothesis that an increased daily energy expenditure contributes to weight loss in heart failure or Alzheimer's diseases is not supported by these findings. These findings, again, underscore the importance of assessing daily energy expenditure in free-living individuals before drawing conclusions regarding the presence or absence of a "hypermetabolic state.
Approximately 50% of patients afflicted with Parkinson's disease experience significant weight loss during the course of the disease. The suggestion has been made that inappropriately high levels of energy expenditure contribute to their unexplained weight loss. Several studies have compared differences in RMR between Parkinson's disease patients and an age-matched control population in an attempt to address this question. Several investigators ( 48, 49 and 50) found an elevated RMR in Parkinson's disease patients, compared with healthy controls. The elevated RMR was at least partially attributed to tremor, rigidity, and a general dyskinesia in these patients.
More recently, total daily energy expenditure was assessed in Parkinson's patients to examine the hypothesis that free-living daily energy expenditure and its components (RMR and physical activity energy expenditure) are elevated (51). In contrast to the proposed hypothesis, daily energy expenditure was 15% lower in Parkinson's disease patients (2214 ± 460 kcal/day) than in healthy elderly controls (2590 ± 497 kcal/day). This was primarily due to lower physical activity energy expenditure (339 ± 366) in Parkinson's disease patients compared with that of the controls (769 ± 412 kcal/day). Thus, although excessive muscular activity in the form of rigidity and tremor may contribute to an elevated RMR (48, 49 and 50), the overall effect of Parkinson's disease is to lower daily energy expenditure by reducing the energy expenditure associated with purposeful physical activity. Impairment of gain and movement associated with the signs and symptoms of Parkinson's disease probably promotes a reduction in physical activity.
The absence of an elevated daily energy expenditure suggests that an abnormally elevated daily energy expenditure is not a likely predisposing factor to weight loss. Thus, it is likely that a lower caloric intake is implicated in the weight loss of these patients. Swallowing disorders, impaired hand-to-mouth coordination, nausea, excessive saliva production, and delayed gastric emptying time may contribute to reduced energy intake in Parkinson's disease patients ( 52).
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