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Effects of chronic energy deficiency on stature, work capacity and productivity

G.B. SPURR*

* Department of Physiology, Medical College of Wisconsin, 8701 Watertown Plank Road Milwaukee, WI 53226, U.S.A.

1. Studies in adults
2. Studies in children
3. Men and boys
4. Productivity, earning and nutrition in developing countries
5. Summary
Acknowledgements
References

In general, there is an association between economic development and adult body size. The small adult stature of people in developing countries is a common feature of many nutritional surveys (Interdepartmental Committee on Nutrition for National Defense, 1959-63). In Figure 1, the adult height in several Latin American nations is compared with that of adults in the United States (SPURR, BARAC-NIETO and MAKSUD, 1978). The division of the Colombian data into upper and lower socioeconomic groups demonstrates that the ethnic component contributes little to the observed differences, as has been emphasized by HABICHT et al. (1974). MARTORELL (1985) has pointed out that the cause of the small stature of adults in developing countries, where nutritional deficiencies are prevalent (BERG, 1973; 1981), is the result of chronic undernutrition and infection during the period of growth. In general, differences are related to socioeconomic level with manual workers being shorter than non-manual workers and university students being the tallest in all countries (EVELETH, 1985).

The present paper will discuss the effects of chronic energy deficiency and associated small body size on physical work capacity (PWC) and productivity in heavy physical work. The concern with PWC and its relation to hard physical work is valid only if both hard physical work and malnutrition are associated. In the less developed areas of the world, where the incidence of protein-calorie undernutrition is high and mechanization is at a minimum, human labor provides much of the power for economic productivity (SMIL, 1979). Using data published by the United Nations (e.g., United Nations Demographic Year Book, 1979), it is possible to estimate for six South American countries that about 54% of the actively employed male population is engaged in work which can be classified as moderate to heavy (agriculture, forestry, mining, construction, etc.). ARTEAGA (1976), using the same source of data for 1972, concluded that in all of Latin America, about 54% of employed men were engaged in heavy work, 20% in medium intensity work and 26% in sedentary occupations. The data in Table 1 extend these observations. Consequently, hard physical work is a reality for the majority of adult males in the work force of poor countries, and factors which affect it will have a bearing on economic development (MARTORELL, 1 985).

In what follows, our own studies in adults and those of others which relate physical work capacity, as measured by the maximum oxygen consumption (VO₂ max), to productivity and nutritional status will be presented. The data show a strong relationship between body size and VO₂ max. The physiological relationship between body size and VO₂ max. on the one hand, and productivity in hard physical work on the other, is an indirect one, but nevertheless real.

MARGEN (1984) has stated that, while it is obvious that a larger individual can perform heavier work than a small one, this may not be the proper interpretation since, if expressed per unit of lean body mass (LBM), the work which can be performed by a small person is as great as that of a large one. Others have also suggested that because the rate of energy expenditure is proportional to body size (weight), smaller individuals will be disadvantaged in hard work only when VO₂ max per kg of body weight is also reduced (FERRO-LUZZI, 1985; WATERLOW, 1986). This presentation will attempt to show that mild to moderate malnutrition is accompanied by functional decrements in work capacity which have particular importance when it occurs during the period of growth, and that it is the total work capacity which matters, not the physical work capacity normalized for weight or LBM.

Table 1. Percentage of economically active populations engaged in moderate to heavy physical work (agriculture, hunting, fishing, forestry, mining and construction) of some countries (United Nations, New York, 1980).

1. Studies in adults

1.1. Malnutrition and VO₂ max
1.2. Endurance
1.3. Productivity and physical work capacity

The studies from our laboratory were carried out in Cali, Colombia, and its rural environs. Colombia is a country considered to be at a middle level of development. Cali is an industrial city of 1.7 million inhabitants, the third largest in Colombia, located 3°22' north of the equator at an altitude of 976 meters. In common with other Latin American cities, during the past 20-25 years, it has undergone rapid growth due, in part, to an influx of population from rural areas. It enjoys a year-round average temperature of some 24°C (high 29°C, low 1 8°C) which varies little throughout the year, so that wide seasonal differences in ambient temperature were not a factor in the studies to be described. There are two "rainy" seasons (March to June and October to December) during which average monthly rainfall may reach a maximum of 18 cm, while maximum rainfall during the "dry" seasons is 6-7 cm per month (CVC).

Since the malnourished individual is usually not working (a reason for his malnourished state), particularly not in moderate or heavy work tasks, it has not been possible to relate malnourished states directly to productivity. Rather, the attempt has been made to relate both nutritional status and productivity (measured in nutritionally normal employed subjects) to a common measurement (VO₂ max), and from these relationships to infer the association between nutritional status and productivity in moderate to heavy work.

1.1. Malnutrition and VO₂ max

VITERI (1971) and VITERI and TORÚN (1975) compared the PWC of several groups of young Guatemalan adults, one of which, the subjects from San Antonio La Paz, can probably be considered at least marginally malnourished, on the basis of their adiposity, lean body mass (LBM), and muscle cell mass (calculated from daily creatinine excretion). The San Antonio La Paz group, another group of recent inductees into the army who were from a similar rural socioeconomic background, and 10 nutritionally supplemented agricultural workers all had significantly lower VO₂ max and maximal aerobic power (expressed per kg of body weight and of LBM) than army cadets from middle or upper socioeconomic levels who had never been exposed to nutritional deprivation. When compared on the basis of "cell residue" (body weight less fat, water and bone mineral), all differences in maximal aerobic power between groups disappeared. VITERI (1971) observed that the differences in maximal aerobic power were due to differences in body composition and not to differences in cell function.

We have studied three groups of chronically malnourished adult males who were selected for their existing degree of undernutrition (BARAC-NIETO et al., 1978). The most severely malnourished of these subjects were also studied during a 45-day basal period in the hospital and during 79 days of dietary repletion regime (BARAC-NIETO et al., 1980). Subjects were classified into those with mild (M), intermediate (I) and severe (S) malnutrition based on their weight/height ratios, serum albumin concentrations and daily creatinine excretions per meter of height, as detailed in Table 2. Each group was significantly different (p<0.001) from the other two in regard to each variable used in the classification.

Detailed body composition and biochemical measurements of the three groups were made shortly after admission to the hospital metabolic ward (BARAC-NIETO et al., 1978) and during the dietary repletion regime of Group S (BARAC-NIETO et al., 1979). Upon entry into the hospital, the subjects were placed on an energy intake (2240 kcal/d; 9.4 MJ/d) adequate for the sedentary conditions of the metabolic ward. They continued the same protein intake (27 g/d) as before.

Table 2. Criteria of mild (M), intermediate (I) and severe (S) malnutrition in adult males; means ± SD

From SPURR, 1983.

Studies of work capacity and endurance in the severely malnourished men were made at the beginning and end of the 45-day basal period on this diet. The protein intake was then increased to 100 g/d for the 79-day repletion regime; the increased caloric intake from proteins was balanced by reducing carbohydrate intake to maintain the diets isocaloric. Measurements of VO₂ max and endurance were repeated at 90 and 124 hospital days. The results for the three groups and the changes in the severely malnourished men during dietary repletion are presented in Figures 2 and 3 and compared with data from 107 nutritionally normal control subjects who were sugar-cane cutters (SPURR, BARAC-NIETO and MAKSUD, 1975), loaders (SPURR, MAKSUD and BARAC-NIETO, 1977) or general farm laborers (MAKSUD, SPURR and BARAC-NIETO, 1976).

There were progressive differences in body weight, weight/height ratio, serum albumin concentrations and total proteins in the control (C), M, I and S groups (Figure 2). Groups C and M were not significantly different in regard to hematocrit and blood hemoglobin, but I and S were significantly and progressively depressed in these measurements. There was a slight gain in body weight of Group S during the basal period, but otherwise the variables did not change. Weight, weight/height ratio and the serum proteins showed progressive improvement during the repletion regime, but the hematological values did not show improvement until the final round of measurements (Figure 2).

Figure 3 presents the results for maximal heart rate, maximal aerobic power VO₂ mL/min/kg body weight) and VO₂ max (L/min) for the control and malnourished subjects. Average maximal heart rate values were not different in the various groups, nor did they change during dietary repletion. However, VO₂ max and maximal aerobic power were progressively less in C, M, I and S subjects, did not change in the S subjects during the basal period, and then progressively improved during dietary repletion, although they did not return even to the level of Group M during the period of study. Figure 3 also expresses a theoretical submaximal workload of 0.75 L/min VO₂ in terms of % VO₂ max for each of the groups. From Figure 3, it is clear that VO₂ max and maximal aerobic power are markedly depressed in chronic malnutrition and that the degree of reduction is related to the severity of depression in nutritional status.

Using the three groups of malnourished subjects, a stepwise multiple regression analysis (BARAC-NIETO et al., 1980) revealed that the weight/height ratio (kg/m), log of the sum of triceps and subscapular skinfolds in mm (SK), total body Hb (TotHb) obtained as the product of blood Hb and blood volume (g/kg body weight), and daily creatinine (Cr) excretion (g/d/kg) contributed significantly to the variation in VO₂ max (L/min):

VO₂ max = 0.095 W/H - 0.152 SK + 0.087 TotHb + 0.031 Cr - 2.550 (1)
(r = 0.931; S.E.E. = 0.21)

All of the variables in the equation are related to nutritional status.

Figure 3. Maximum heart rates (f_H), aerobic power, and VO2 max in control, undernourished, and severely malnourished subjects and during dietary repletion of the latter. Lower panel shows a fixed submaximal workload (0.75 L/min) in terms of % VO2 max (SPURR, 1983).

Figure 4 expresses the data for the three malnourished groups and for Group S during recovery, in terms of various body compartments. It was not possible to do detailed body composition studies on the control subjects. The salient feature of Figure 4 is that over 80% of the difference in VO₂ max between M and S subjects is accounted for by difference in muscle cell mass. The remaining difference might be ascribed to reduced capacity for oxygen transport either because of low blood Hb (Figure 2) or reduced maximum cardiac output. There do not seem to be any reports of studies on maximum cardiac output in malnourished subjects.

Another possibility is that the skeletal muscle cells have reduced maximal aerobic power because of reduced oxidative enzyme content. TASKER and TULPULE (1964) found a marked decrease in the activities of oxidative enzymes in skeletal muscle of protein-deficient rats and RAJU (1974) reported that after recovery from 13 weeks of reduced protein intake, rat skeletal muscle had an increase in glycolytic and a decrease in oxidative enzymes and activity. However, there appear to be no studies which have measured similar biochemical changes in humans, although LOPES et al. (1982) have recently shown that malnourished patients exhibited marked impairment in muscle function.

There were both an increased muscle fatigability in static muscular contraction and a changed pattern of muscle contraction and relaxation which were reversed in patients undergoing nutritional supplementation. Their data indicate the possibility of a decreased content of ATP and phosphocreatine in the skeletal muscle tissue of malnourished subjects. The data of HEYMSFIELD et al. (1982) indicate changes in the biochemical composition of skeletal muscle in both acute and chronic semistarvation, particularly in glycogen and total energy contents. In any event, it should be emphasized that the VO₂ max not accounted for by differences in muscle cell mass is small (Figure 4). After 2 1/2 months of recovery, the VO₂ max increased significantly in L/min and when expressed in terms of body weight and LBM but, although mean values were elevated in terms of body and muscle cell mass, the increases were not statistically significant. However, at the termination of the experiment, PWC had not returned to values comparable to those seen in mild malnutrition (Figures 3 and 4), which indicates that the recovery process is a long one, particularly when carried out under the sedentary conditions of the hospital metabolic ward.

It is interesting to note that the VO₂ max was increased 45 days after beginning of the repletion diet (90 hospital days), when blood Hb concentration had not yet increased (Figure 2), but muscle cell mass was significantly increased over basal values (BARAC-NIETO et al., 1979). This also points to a primary dependence of VO₂ max on muscle cell mass (Figure 4). Furthermore, it appears that supplying adequate calories alone was not sufficient to bring about an increase in VO₂ max or muscle cell mass and that only after increasing the protein intake to 100 g/d was there improvement in these two variables (BARAC-NIETO et al., 1979; 1980).

Figure 4. VO₂ max expressed in terms of various body compartments for the undernourished subjects and during dietary repletion of the most severely malnourished (SPURR, 1983).

ANGELI et al. (1983) recently reported the results of a lunch supplementation program on physical work performance. The latter was measured by submaximal bicycle ergometry before and after three months of supplementation which increased the daily intake by 355 kcal and 20 g protein of mixed quality. The workload required to reach a target submaximal heart rate (195 minus age) increased significantly, indicating an improvement in overall physical work capacity. It would seem then that it does not require very much supplementation to register an improved physical work capacity in marginally undernourished groups.

1.2. Endurance

An endurance test is carried out on a treadmill or bicycle ergometer at a workload (VO₂) of 70-80% of the subject's maximum until exhaustion supervenes, usually with the heart rate within about five beats of the maximum. Because of the difficulty in performing this test, only a few laboratories have attempted measurement of endurance times in normal individuals and, to our knowledge, none except our own, in malnourished subjects.

From a number of sources, it is known that the maximum relative workload that can be sustained for an 8-hour workday usually does not exceed about 35-40% VO₂ max. Thus, MICHAEL et al. (1961) found in laboratory treadmill work that 8 hours could be tolerated without undue fatigue when the relative load did not exceed 35% VO₂ max. Subjects rested for 10 minutes each hour and for one half-hour between the 4th and 5th hours of work. In the building industry, ÅSTRAND (1967) reported that about 40% VO₂ max was the upper limit that could be tolerated for an 8-hour workday, and we have estimated that sugar-cane cutters worked at an average of about 35% of their VO₂ max during an 8-hour day (SPURR, BARCO-NIETO and MAKSUD, 1975). These studies were performed in physically fit subjects. Sedentary individuals can be expected to have lower upper limits for 8 hours of work (ÅSTRAND and RODAHL, 1970, p. 292).

We have measured maximum endurance times at 80% VO₂ max (T₈₀) in the groups of malnourished subjects described above (BARAC-NIETO et al., 1978; 1980). We did not find any significant differences between the three groups (M, I and S) of malnourished men; T₈₀ averaged 97 ± 12 min (mean ± SE) in all subjects (BARAC-NIETO et al., 1978). However, it might be assumed that the VO₂ max of Group S subjects would be about 2.4 L/min had they not been malnourished, and that about 35% (0.84 L/min) could be sustained for an 8-hour workday. The value of 0.84 L/min is 80% of the VO₂ max (1.05 L/min) for these subjects who had maximum endurance times at this relative workload of a little over 1.5 hours, a loss of about 6.5 hours of daily working time or about an 80% reduction in productive potential (BARAC-NIETO et al., 1978). Using a similar method of estimation, BARAC-NIETO (1984) has calculated a 16% reduction in work output of the M subjects, a 35% decrease in I and a 78% reduction in S men.

In the case of Group S during dietary repletion, an interesting change in T₈₀ was observed. Endurance times were significantly reduced from 113 minutes at the first measurement of the basal period to 42 minutes at the end of the dietary repletion (BARAC-NIETO et al., 1980). The explanation for this surprising reduction is still not clear. HANSON-SMITH et al. (1977) reported decreased work-endurance times in rats on high-protein diets compared to animals ingesting an isocaloric carbohydrate diet, and BERGSTRÖM et al. (1967) and GOLLNICK et al. (1972) have shown that diets in which the energy value of carbohydrate has been replaced with fat and/or protein lead to reduced stores of muscle glycogen. Furthermore, BERGSTRÖM et al. (1967) demonstrated that the maximum endurance time in humans is directly related to the initial glycogen content of skeletal muscle.

During the dietary repletion period of the Group S subjects, carbohydrate intake was reduced from 64 to 50% of calories. In a normal individual this amount of carbohydrate should be sufficient to maintain muscle glycogen stores, but definitive studies seem not to have been done (DURNIN, 1982). The rebuilt muscle tissue of Group S subjects may not store glycogen normally and, together with the lack of regular exercise in the protracted sedentary existence in the metabolic ward, may lead to reduced muscle glycogen and shorter endurance times. Nutritive supply to muscles, and the metabolic and endocrine responses which regulate it during both short term and prolonged exercise, have not been investigated in malnourished individuals. Even though there is little reason at the moment to suspect abnormal muscle function in acute exercise testing to maximum levels, the responses to prolonged exercise may be worth investigating.

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