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Department of Molecular Biosciences, School of Veterinary Medicine, University of California, Davis, CA 95616
3 To whom correspondence should be addressed. E-mail: jjramsey{at}ucdavis.edu.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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KEY WORDS: • energy restriction • metabolic rate • body composition
Obesity is considered one of the most common nutritional problems in cats and dogs (1). Studies in Western Europe and the United States have indicated that >24% of dogs (1,2) and 
25% of domestic cats are obese (3). Treatment of obesity in companion animals frequently focuses on restriction of energy intake. However, successful maintenance of weight loss can be difficult, and pet owners may lose interest in weight loss programs if the rate of weight loss does not meet their expectations or if the animals show a propensity to regain weight. Unsuccessful weight loss attempts are often attributed to a failure of the owner to supply adequate control of energy intake; however, this may not be the only factor contributing to weight regain. It was proposed that weight loss induces metabolic adaptations that prevent further weight loss and promote regain of body weight during lapses in dietary energy restriction (ER)4 (4). A reduction in mass-adjusted energy expenditure (EE) is one adaptation that could oppose weight loss with dietary ER (5,6). Several studies used animals or human volunteers to determine the effects of dietary ER on EE; however, there is still considerable debate concerning whether cellular or mass-adjusted EE is altered by dietary ER. This review summarizes current information about the energetic adaptations to sustained dietary ER. Few studies investigated the effects of ER on EE in dogs and cats; therefore, this review will not be limited to studies completed in these species but focus instead on studies completed primarily in laboratory rodents or humans. Also, this review will focus primarily on diets that restrict energy intake without inducing malnutrition because these diets would be required for long-term maintenance of a healthy, reduced body weight.
Whole-body energy expenditure and dietary ER
EE (kJ/d) must be decreased if an animal is to survive a sustained dietary ER. Once weight stability is achieved, metabolizable energy intake must match EE. Therefore, the primary question is not whether total EE is altered with ER, but whether mass-adjusted EE is altered in weight-stable animals after ER. Indirect respiration calorimetry (metabolic cart with hood, respiratory chamber, or doubly labeled water methods) was used to determine whether ER induces alterations in mass-adjusted EE. Calorimetry studies, however, produced mixed results, with some studies reporting a decrease and other studies no change in mass-adjusted EE with dietary ER. Several reviews were published summarizing the results of studies using human subjects (7–9), and these reviews concluded that ER produces a decrease in EE that cannot be entirely explained by changes in body size and composition. However, complete agreement does not exist about the effect of dietary ER on EE in humans, and some investigators reported no change in mass-adjusted EE with ER [reviewed in (10)].
Similarly, studies in rats reported either a decrease or no change in EE with dietary ER. In a study with rats restricted to 60% of ad libitum intake at 6 mo of age, 24-h and resting EE expressed as a function of lean mass or body weight (g0.75) were not altered by ER (11). Another study by this same group also found that EE expressed as a function of lean mass or total mass (g0.75 or g0.67) was not altered by ER in 6-mo-old rats fed a 40% energy-restricted diet from 6 wk of age (12). In contrast to these findings, a decrease in lean mass–adjusted EE was reported in 6-mo-old rats fed a 40% ER diet for 6 wk (13). A decrease in EE expressed as a function of lean mass or total mass (g0.75 or g0.67) was also reported in 12-wk-old rats fed a 50% ER diet for 4 mo (14). Similarly, restriction of energy intake by 10 or 20% for a period of 3 mo was shown to decrease mass-adjusted EE in rats (15), and energy expenditure adjusted for fat-free mass or fat mass using ANCOVA was decreased in rats fed a 40% ER diet for 16 wk (6). Thus, studies in rats reported either a decrease or no change in mass-adjusted EE with dietary ER.
In addition to studies in rats and humans, the influence of dietary ER on EE was also studied in dogs, cats, and rhesus monkeys. Dietary ER was reported to decrease EE in dogs (16), but not in cats after adjusting for differences in body size (17). Studies in rhesus monkeys also reported either a decrease or no change in mass-adjusted energy with dietary ER. In a study in which adult rhesus monkeys were energy restricted to maintain body weight for a period of 10 y, total EE adjusted for lean mass or metabolic body size (kg0.75) was decreased in energy-restricted compared with control monkeys (18). Also, total EE adjusted for lean body mass was decreased in juvenile monkeys fed a 30% ER diet for a period of 4 mo (19). However, other studies with a 30% ER diet initiated in adult monkeys found that resting, but not total EE [adjusted for lean mass using analysis of covariance (ANCOVA)] was decreased with ER (20,21). A 30% dietary ER initiated in young adult (3- to 5-y-old) monkeys also did not alter EE adjusted for lean or total (kg or kg0.67 or kg0.75) mass after 4.5 y of ER (22). Thus, studies in a variety of species did not produce a consensus concerning whether dietary ER decreases or does not affect mass-adjusted EE.
The reason for the differences between studies in EE response to dietary ER is not entirely clear, although some of the discrepancies among previous studies may be due to the use of inappropriate statistical methods to adjust for differences in body size with ER. In particular, the use of a ratio to adjust for lean body mass (e.g., kJ/kg fat-free mass) was questioned and regression-based approaches were recommended to control more fully for the influence of body size or composition (23). Using a regression-based approach (ANCOVA) to determine whether dietary ER-induced changes in EE are independent of changes in body weight, results from multiple human, rodent, and monkey studies were combined and analyzed (21). The results of this analysis indicated that ER does induce a decrease in total EE adjusted for body weight and a decrease in resting EE adjusted for fat-free mass (21). Thus, the discrepancies in the literature over EE response to dietary ER appear to be due at least in part to the use of inappropriate statistical methods to adjust EE for alterations in body size with dietary ER.
EE comparisons between control and ER animals, however, are also hampered by the fact that methods used to normalize EE for body size differences often assume that the composition of lean mass (or body mass) is similar among groups. Previous studies showed that dietary ER does not result in uniform changes in the weights of organs and tissues (24–28). Nonuniform changes in organ and tissue mass greatly complicate comparisons of whole-animal EE, and it is possible that many of the differences among studies would be eliminated if organ mass were taken into consideration (25,29). Also, metabolic body size (kg0.75) and surface area (kg0.67) were not derived for comparisons of EE among animals consuming different levels of energy intake. EE may not be adequately adjusted for the body composition changes that occur with ER when using either kg0.75 or kg0.67 to adjust for differences in body size. Therefore, to have a true understanding of the effect of dietary ER on EE, it is imperative that measurements be made of both major energy-consuming cellular processes and body composition (organ and tissue weight) with dietary ER.
Organ mass and energy restriction
It was proposed that previous studies may have failed to report an ER-induced decrease in EE because they did not adequately adjust EE for metabolically active tissue mass (29,30). However, few ER studies either measured organ mass or attempted to adjust EE for differences in organ mass. Many studies in humans and rodents simply use lean body mass to adjust EE for differences in body weight induced by restriction of energy intake. The use of lean mass in this manner requires 2 assumptions: 1) that all components of lean mass have equivalent rates of EE; and 2) that ER induces uniform changes in all components of lean body mass. As will be discussed below, neither of these assumptions is correct. In addition to the use of lean body mass, many animal studies use an exponential function of body weight (kg0.67 or kg0.75) to adjust for the differences in body weight induced by restriction of energy intake. However, it is not known whether either of these exponential functions of body weight adequately reflects energetic changes in response to sustained dietary ER. To determine the energetic response to the restriction of energy intake with some accuracy, it is important to know how individual organ and tissue weights are altered by ER.
Internal organs are responsible for 70% of resting EE, despite the fact that they account for <10% of body weight (31,32). In contrast, skeletal muscle accounts for 40% of body weight in adult humans, but it is responsible for <30% of resting EE (31,33). The contribution of specific organs or tissues to resting EE in rats and humans is summarized in Table 1. The variability in the results obtained for the contribution of organs to total EE (Table 1) is due at least in part to the methods used to measure organ oxygen consumption. In vitro measures of oxygen consumption in tissue slices and in vivo arteriovenous difference measures of oxygen consumption were both used to determine the contribution of individual organs to whole-body EE. In vitro measures of tissue oxygen consumption, however, are very sensitive to the composition of the medium in which the tissues are suspended (40), and variability among studies may be related to differences in the composition of the assay media. Also, it was suggested that oxygen consumption is higher in tissue slices than in vivo measurements in the corresponding organ (31). A variety of methods were used to measure blood flow for in vivo arteriovenous difference assessments of oxygen consumption, and differences in the sources of error for each of these methods can also contribute to variability among studies (41). Despite some variation in the estimates of organ contribution to whole-body EE, studies using in vivo or in vitro methods both demonstrated that the internal organs (liver, brain, heart, kidneys) are the major contributors to resting EE. The rate of EE (kJ/g tissue) in these tissues is 15–40 times greater than that in skeletal muscle and 50–100 times greater than that in adipose tissue (33).
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Energy restriction and organ weights. When adjusting EE data for lean body mass or total body mass, it is assumed that ER simply produces a smaller version of the control animal. However, this assumption is not correct and several studies demonstrated that organs change mass at very different rates after the initiation of dietary ER. Starvation studies in rats showed that the liver and gastrointestinal tract are the first tissues to show significant weight loss, loss that may even precede decreases in some fat pads (45–47). Similar changes were also observed with dietary ER. It was shown that liver and gastrointestinal tract weights rapidly increase or decrease in direct proportion to dietary energy intake (48). Several studies in growing lambs showed that restricting energy intake to maintain body weight resulted in rapid decreases in liver and gastrointestinal tract weights (49–51). Also, studies completed in growing rats, in which combinations of high-, medium-, or low-energy diets were used to produce animals with the same body weight but different levels of energy intake for the preceding 3 wk, showed that liver weight was lower in animals that had recently been allowed a low-energy intake compared with animals allowed a higher-energy intake (52). Although these studies were completed in growing animals, it was also shown that feeding adult rats a diet at 70% of ad libitum energy intake produces a 30% decrease in liver weight within 10 d of initiating the ER (53).
Changes in organ mass with dietary ER, however, are not restricted to the liver and gastrointestinal tract. Several studies investigated the effect of long-term dietary ER on organ mass in adult rats (Table 2). These studies showed that liver, heart, and kidney weights were all decreased with long-term ER. Organ/tissue response to dietary ER, however, is variable with 3 patterns of response being observed: 1) weight loss that exceeds the magnitude of the ER; 2) weight loss that matches the level of ER; and 3) lack of weight change or weight loss of a lower magnitude than the level of ER. Adipose tissue is the only tissue that was shown consistently to lose weight at a magnitude that exceeded the level of ER (25,27,54,55). Because the primary purpose of a weight loss program is to lose body fat, it is reassuring that this is the tissue that shows the greatest response to dietary ER. Liver shows the next greatest weight change (as a percentage of initial weight) in response to ER. After 1 mo of a 40% ER, liver weight in rats decreased by >25% (26,28), whereas with long-term (
12 mo) consumption of a 40% energy-restricted diet, liver weight is decreased by a magnitude that approaches or slightly exceeds the 40% level of ER (24–26,55,56). All other major organs either do not change weight with dietary ER or show a weight loss that is below the level of ER. Several studies reported that long-term (12 mo) consumption of a 40% ER diet results in an 30% decrease in heart and kidney weights (25,26,56). In contrast to these organs, which show some weight loss with ER, brain weight is not significantly altered by 40% ER (25,56), and lung weight was reported to show no change with long-term ER (56). In skeletal muscle, the effect of 40% ER is variable and likely depends on the age at which ER was initiated. Initiation of ER in 1-mo-old rats produced a stunting of growth and caused a 40% decrease in skeletal muscle weight that nearly matched the level of ER (24). However, 40% ER was shown to decrease fat-free mass (primarily a measure of skeletal muscle mass) by 30% when initiated in 13-wk-old rats (25), whereas other studies indicated that long-term ER does not consistently decrease skeletal muscle mass (57,58). Together, these studies clearly show that dietary ER does not cause uniform changes in all tissues and organs. Long-term ER frequently produces a decrease in body weight that matches the level of ER (Table 2). However, this weight loss is achieved primarily by loss of adipose tissue; heart, brain, kidneys, and lungs become a proportionally greater component of body weight in energy-restricted animals, although the contribution of metabolically active organs to body weight is nearly equal between control and ER animals when liver weight is included in the calculation. With short-term ER, however, large decreases in liver weight may reflect water loss secondary to glycogen depletion, and it is not certain that a 40% decrease in liver mass with long-term ER truly reflects a 40% decrease in metabolically active tissue. The maintenance of relatively high internal organ weights with ER may be suggestive of decreases in tissue EE. However, detailed comparisons of body composition and EE data are required to determine whether the body composition changes that occur with long-term ER are indeed indicative of a decrease in tissue EE.
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A recent study used a stepwise multiple regression technique with thorough measures of organ and tissue weights to develop a best-fit equation to predict daily EE. Predicted EE was then compared with measured EE, and the authors concluded that EE in energy-restricted rats was higher than would be predicted based on body composition (58). That study, however, was completed only on either senescent animals or young animals that had been consuming energy-restricted diets only for a period of months. It is difficult to determine whether that study was truly investigating the effects of long-term dietary ER in weight-stable rats or instead investigating EE in groups of rats that were not in energy balance. It is hoped that additional studies will be completed in energy-restricted animals during periods of relative weight stability to determine whether ER alters EE after weight loss has been achieved. However, EE and organ mass provide only an estimate of EE at the cellular level, and integration of EE and organ mass measures with measures of energy metabolism at the biochemical level are required to determine more accurately whether animals adapt to sustained ER with a decrease in EE.
Energy restriction and cellular energy expenditure
Does dietary ER produce a sustained decrease in cellular EE? To answer this question, it is absolutely essential to determine the effect of dietary ER on major cellular energy-expending processes. Resting EE is the primary contributor to total EE in sedentary animals; therefore, the processes responsible for resting EE are the largest contributors to total EE in these animals. The cellular processes contributing to resting EE were reviewed (61,62) and are summarized in Table 3. Mitochondrial proton leak, Na+-K+-ATPase activity, and protein turnover are the primary processes contributing to resting EE; together, these processes may be responsible for >75% of resting EE. Therefore, these 3 processes are a good starting point for determining whether dietary ER decreases cellular EE. This section is devoted to a review of the literature on ER and these processes. Triacylglycerol turnover, calcium cycling, and other "futile" cycles may also be altered by dietary ER; however, the influence of ER on these processes was not investigated extensively.
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Studies were completed on rat liver and skeletal muscle mitochondria to determine whether dietary ER induces a change in mitochondrial proton leak. In liver, no diet-induced change in mitochondrial proton leak was observed in rats fed a 50% energy restricted diet for a period of 3 d, (67). Similarly, liver mitochondrial proton leak was not altered at 1, 6, or 12 mo of ER in rats fed a 40% energy restricted diet from 6 mo of age (28,56). However, liver proton leak was decreased in energy-restricted compared with control animals by 18 mo of ER, indicating that either very long-term ER and/or the influence of aging are required for a decrease in liver proton leak with sustained ER (56). In contrast to these findings, one study reported that liver mitochondrial proton leak is increased in rats fed an energy-restricted diet designed to maintain body weight at 55% of age-matched fully fed animals (68). However, another study by this same group found that mitochondrial proton leak was not altered by ER when studied in intact hepatocytes isolated from rats (69). Together, these results indicate that liver mitochondrial proton leak is not altered by dietary ER, except that a decrease in proton leak may occur with very long-term ER.
Skeletal muscle, however, shows very rapid changes in mitochondrial proton leak in response to dietary ER. In adult (6-mo-old) rats fed a 40% energy-restricted diet, respiration dependent upon mitochondrial proton leak was decreased in energy-restricted compared with control rats after 2 wk of ER (27). This decrease in proton leak–dependent respiration continued through 12 mo of ER (55). These results indicate that dietary ER causes rapid decreases in proton leak–dependent respiration in skeletal muscle that are maintained for a large portion of the animal's lifespan.
Thus, dietary ER causes either a decrease or no change in mitochondrial proton leak–dependent respiration in skeletal muscle and liver. These results are consistent with the idea that dietary ER may induce long-term decreases in cellular EE; however, studies in additional tissues are required for a better determination of the net effect of ER on mitochondrial proton leak.
Energy restriction and Na+-K+-ATPase activity.
Na+-K+-ATPase (EC 3.6.3.9) is the primary enzyme that functions to maintain sodium and potassium concentrations within the cell. Na+-K+-ATPase expels 3 Na+ in exchange for 2 K+ at the cost of hydrolysis of 1 molecule of ATP to ADP (70). Na+-K+-ATPase is found in all cells of the body, and it is required for proper nutrient transport, nerve function, and maintenance of cell volume (71). Na+-K+-ATPase is a major contributor to resting EE, with estimates indicating that 20–28% of resting EE is devoted to this process.
The effect of restriction of energy intake on Na+-K+-ATPase activity was investigated in several tissues. Food deprivation for a period of 4 d was shown to decrease Na+-K+-ATPase activity in the soleus muscle of rats (72). Similarly, Na+-K+-ATPase activity was decreased in intestinal epithelium (73) and liver (74) in food-deprived sheep. Although these studies involved food deprivation, it was also shown that Na+-K+-ATPase activity is decreased in jejunal mucosa obtained from sheep fed a 40% energy-restricted diet for a period of 28 d (75). Na+-K+-ATPase activity was also decreased in erythrocytes of rats fed a 40% energy-restricted diet for a period of 4 wk (76). In contrast to this finding, one study reported that erythrocyte Ca2+-ATPase activity, but not Na+-K+-ATPase activity, is decreased in rats with long-term feeding of a 40% energy-restricted diet (77). Several studies reported that Na+-K+-ATPase activity is positively correlated with the level of energy intake (70), and it appears likely that Na+-K+-ATPase (and possibly Ca2+-ATPAse) activity is decreased in at least some tissues with long-term dietary ER.
Energy restriction and protein turnover. Most cellular proteins undergo a continual cycle of synthesis and degradation. The energy cost associated with this protein turnover is considerable, and it was estimated that 20–30% of whole-animal resting EE is devoted to protein turnover. Several studies investigating the effects of dietary ER on protein turnover were completed. A series of studies with rats, fed a 50% energy-restricted diet from 21 d of age, examined protein turnover at the whole-animal and organ level. At the whole-animal level, it was found that protein turnover was higher in energy-restricted than control rats at 1 y of age, whereas protein turnover did not differ between the diet groups at either 52 d or 2 y of age (78). At the organ level, protein turnover was decreased by dietary ER in lungs (79) and soleus, tibialis anterior, and extensor digitorum longus muscles (80,81) with short-term ER (4 wk). However, protein turnover was not altered by dietary ER at the later assessments in either soleus muscle (81) or lungs (79). Also, diaphragm, tibialis anterior, and extensor digitorum longus muscles produced fluctuating changes with no clear, long-term alteration in protein turnover rate with sustained ER (80,81). These results indicate that a long-term reduction in protein turnover does not likely contribute to a decrease in EE with dietary ER. However, these studies involved initiation of dietary ER in young animals, and it remains to be determined whether similar results would be observed if ER were started in adult animals.
A few studies examined whether dietary ER in adult humans produces alterations in whole-body protein turnover. A study in obese men subjected to a 50% ER for 4 wk found a 20% decrease in whole-body protein turnover (82). Similarly, whole-body protein turnover was decreased in obese subjects consuming a very low energy diet (1.7 MJ/d) for a period of 6 wk (83). In contrast to these results, a study of obese patients who lost weight after vertical banded gastroplasty did not report a change in protein turnover adjusted for body mass between measurements presurgery and those 12 mo postsurgery (84). However, it is not possible to determine from that study whether weight loss was due entirely to voluntary dietary ER or whether physical activity also played a major role. These studies were all relatively short term, and it is not possible to determine whether these same results would be observed if ER were maintained for several years. However, a few long-term ER studies were completed in humans. Studies in 2 populations of south Asian Indian men (college students with ad libitum consumption of food or undernourished laborers who had low daily energy intakes) found no difference between the groups in protein turnover adjusted for differences in body size or composition (85,86). Although nutrient deficiencies may complicate the interpretation of these results, these studies at least suggest that long-term ER is not associated with an alteration in protein turnover in humans. Together, the results from the rodent and human studies indicate that it is unlikely that changes in protein turnover contribute to alterations in EE with long-term maintenance of dietary ER.
Energy restriction and substrate oxidation. In addition to changes in proton leak or ATP-consuming reactions, it is possible that dietary ER could influence EE through alterations in substrate oxidation pathways. A few studies in laboratory rodents do indicate that dietary ER induces a sustained decrease in central pathways of energy metabolism. In studies in which rats or mice were fed 40% energy-restricted diets, it was shown that dietary ER induced a sustained decrease in the activity of liver glycolytic enzymes (87–90). It was also shown that 40% ER in mice induces a differential regulation of the Krebs cycle, such that activities of citrate synthase, aconitase, and isocitrate dehydrogenase are decreased with ER, whereas the remaining enzymes of the cycle are increased (91). Such a change is indicative of a chronic increase in capacity for gluconeogenesis and a decrease in capacity for substrate oxidation. Although these studies were completed in liver, one study in muscle also indicated a chronic decrease in capacity for energy metabolism with sustained ER. It was shown that the activities of mitochondrial electron transport chain complexes I, III, and IV were decreased by 33–64% in mice consuming a 40% energy-restricted diet compared with controls consuming food ad libitum (92). These data indicate that sustained dietary ER produces chronic alterations in energy metabolism pathways in a manner that would limit capacity for substrate oxidation. These changes are consistent with the idea that ER produces a sustained decrease in EE.
Conclusions
The influence of dietary ER on EE is the subject of continued debate. At the whole-animal level, it was reported that mass-adjusted energy expenditure is either decreased or not changed by dietary ER. The reason for this discrepancy in results is not entirely known, although the use of inadequate methods to adjust EE for body size may contribute at least in part to differences among studies. Also, current methods to adjust EE for body size may not adequately reflect changes in the weight of metabolically active tissues. Internal organs account for >70% of resting EE, despite the fact that they compose <10% of body weight. Therefore, energetically important changes in organ mass may be missed by methods that use lean body mass or total body weight to adjust EE for body size. It was proposed that dietary ER would be associated with a decrease in EE if organ weights were taken into consideration. Thus, it would be concluded that energy-restricted animals have a decrease in cellular EE if they are able to maintain a higher proportion of their body weight as metabolically active tissues compared with controls. To test this idea, several studies investigated the effect of dietary ER on organ and tissue weights. These studies found that only adipose tissue and liver showed a magnitude of weight change that met or exceeded the level of dietary ER. Brain (and possibly lungs) showed no change in weight with dietary ER, and heart and kidneys showed a magnitude of weight change that was less than the level of ER. Attempts were made to determine whether alterations in organ mass can entirely explain changes in EE with dietary ER. Nevertheless, these studies were not conclusive and it remains to be seen whether changes in EE exceed those that would be predicted from ER-induced alterations in organ mass. However, it is necessary ultimately to determine whether dietary ER reduces EE at the cellular level. A few studies determining the effect of dietary ER on key pathways or processes in energy metabolism were completed. These studies produced evidence that in some tissues, dietary ER may cause sustained decreases in mitochondrial proton leak–dependent respiration, Na+-K+-ATPase activity, and the activity of substrate oxidation pathways (glycolysis, Krebs cycle, and the mitochondrial electron transport chain). These results are consistent with the idea that dietary ER may result in a decrease in cellular EE. Studies involving whole-animal, organ, and cellular EE measurements have increased current understanding of the factors regulating EE. However, future studies integrating measurements at the-whole animal, organ, and cellular level will ultimately be required to determine definitively whether dietary ER produces sustained decreases in tissue or cellular EE.
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FOOTNOTES |
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2 Author disclosure: no relationships to disclose.
4 Abbreviations used: ANCOVA, analysis of covariance; EE, energy expenditure; ER, energy restriction.
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