Plasma Insulin Levels in Weaned Pigs Fed Protein or Energy Restricted Diets1
ABSTRACT Two experiments were conducted with pigs to investigate changes in plasma insulin levels during protein-energy malnutrition. Three or four week old pigs were fed a control diet (18% protein), an energyrestricted diet (18% protein) or a low protein diet (6% protein) for 8 weeks. Energy restriction was achieved by feeding the control diet in amounts that allowed some growth, but only to an extent equal to the low protein diet. At the end of the restriction period, all pigs were fed the control diet for another 8 weeks. Blood samples from the superior vena cava were collected at intervals throughout the experimental period. Plasma samples were analyzed for insulin by radioimmunoassay. Protein restriction after weaning resulted in persistently low insulin levels during depletion and rehabilitation periods, while high levels of plasma insulin were observed in energy-restricted pigs only during the depletion period compared to pigs fed the control diet. J. Nutr. 106: 1654-1658, 1976. INDEXING KEY WORDS postnatal malnutrition •protein restriction •energy restriction •insulin There is still incomplete information among studies from different parts of the world about insulin secretion during pro tein-energy malnutrition. It is generally believed that insulin secretion is impaired in kwashiorkor. The evidence for this con clusion is based on impairment of glucose tolerance (1) and a poor plasma insulin response to oral and intravenous glucose (2, 3). Some workers (1, 3) have found a normal glucose tolerance and rise in plasma insulin levels under marasmic con ditions, whereas others have found im paired secretion and glucose tolerance (4, 5). In Jamaica, James and Coore (6) and Milner (7) showed that plasma in sulin is low initially and that the rise in response to intravenous glucose, although significantly improved, is still much lower than in normal children. These results sug gest that a temporary nutritional insult af fecting endocrine pancreatic function could be of importance in the pathogene-
sis of diabetes in later life in those coun tries where malnutrition is endemic in children. In a more extensive study car ried out in Uganda (8), plasma insulin concentrations were significantly above normal during the initial stages of protein malnutrition in human infants, but fell to subnormal levels as the disease progressed. Biochemical changes resulting from pro tein-energy malnutrition have been re ported for the pig (9-14), and there are many similarities between biochemical changes from protein-energy malnutrition in man and swine (15). The purpose of Received for publication April 14, 1976. 1Supported in part by funds provided through the State University of New ïork and Public Health Research Grant no. HD-025S1 from the National Institute of Child Health and Human Development. « Present address : Applied Nutrition Unit, Univer sity of Ibadan. Nigeria. *Present address : Departamento de Fisiologia, Instituto de Ciencias Biomedicas, Universldade de Sao Paulo, Brasil. »Department of Animal Science, Cornell Univer sity, Ithaca, New York 14853.
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TOLA ATINMO,2 CARLOS BALDIJÄO,3 WILSON G. POND * ANDRICHARD H. BARNES Division of Nutritional Sciences and Department of Animal Science, Cornell University, Ithaca, New York 14853
MALNUTRITION AND POSTWEANING INSULIN
the present study was to further elucidate the developmental changes that occur in plasma insulin levels during proteinenergy malnutrition with the weaned pig as the animal model. It was also of interest to know whether these changes revert to normal after the pigs have been rehabili tated. Effect of protein deprivation after wean ing on plasma insulin levels of young growing pigs. Twelve 4-week-old male Yorkshire pigs weighing between 6 and 7 kg were divided equally into two groups. Group 1 was fed a control 18% protein diet while group 2 received a 3% protein diet both fed ad libitum (table 1) for 8 weeks. The pigs were kept in concrete floored pens in groups of three, and rec ords of biweekly body weight and food consumption were kept ( 16 ). After a 4 hour fast, blood samples were taken from the jugular vein at 4, 7, 10 and 12 weeks of age and plasma stored at —20°. At the end of the 8-week deprivation period, all pigs were fed the control diet for another 8-week rehabilitation period. Biweekly body weight records were kept and the blood was sampled at 16 and 20 weeks of age. Effect of protein restricted or energy re stricted diets after weaning on plasma insulin levels of young growing pigs. Twenty-four 3 week old male Yorkshire pigs were divided into three groups of eight each and fed the control 187o pro tein diet (group 1), energy-restricted diet
RESULTS AND DISCUSSION
Mean plasma insulin levels during the protein deprivation and rehabilitation pe riods are presented in figure 1. Figure 2 shows the plasma insulin levels in protein or energy restricted pigs. The pigs were fed the restricted diets from 4 weeks of age for 8 weeks and then rehabilitated by feeding a control diet for another 8 weeks. There was a greater drop in plasma in sulin levels in the low protein fed pigs at the initiation of the restriction period compared to the control or energy re stricted pigs (figures 1 and 2). More im portant is the fact that plasma insulin
TABLE 1 Composition of protein or energy restricted diet1
restricted3%84.66.0•
levelGlucose Ingredient protein %Soybean monohvdrate,
%Casein, meal (00% protein),3
%Corn %Vitamin oil, %Mineralmix, mix, %Control18%70.6—20.03.01.05.4Protein Total
100.0
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MATERIALS AND METHODS
(group 2) and 6% protein diet (group 3). Group 1 and 3 pigs were fed ad libitum (table 1) while energy restriction was achieved in group 2 by feeding the control diet in an amount that allowed this group of pigs to grow at the same rate as group 3. This amount was provided in two equal rations per day. All pigs were kept in in dividual pens and weekly records of body weight and food consumption were kept ( 16 ). After a 4 hour fast, a blood sample was obtained from the jugular vein at 3, 6, 9, and 11 weeks of age and the plasma stored at -20°. At the end of the 8-week restriction period, all pigs were fed the control diet for another 8-week rehabilita tion period. Blood samples were again ob tained at 15 and 19 weeks of age. Plasma insulin concentration was deter mined by a modified radioimmunoassay method of Hales and Rändle(18) as pre viously described (19).
—3.01.05.46%83.6—7.03.01.05.4Energyrestricted218%70.6—20.03.01.05
100.0
100.0
100.0
1For additional details. See Atinmo, et al. (17). 2Same as control except fed in amounts (two equal portions per day) that allowed pigs to grow at the same rate as protein-restricted pigs. 3Solvent extracted dehulled, 50% protein.
ATINMO, BALDIJÄO, POND AND BARNES
a3
10
13
AGE IN WEEKS
Fig. 1 Plasma insulin ( mean ±SD) in protein deprived pigs during depletion and rehabilitation periods. Four-week-old pigs were weaned to a low protein diet for 8 weeks and then adequately fed for another 8 week period. Plasma insulin levels were consistently lower in the protein de prived pigs throughout the experimental period (P
ABSTRACT Two experiments were conducted with pigs to investigate changes in plasma insulin levels during protein-energy malnutrition. Three or four week old pigs were fed a control diet (18% protein), an energyrestricted diet (18% protein) or a low protein diet (6% protein) for 8 weeks. Energy restriction was achieved by feeding the control diet in amounts that allowed some growth, but only to an extent equal to the low protein diet. At the end of the restriction period, all pigs were fed the control diet for another 8 weeks. Blood samples from the superior vena cava were collected at intervals throughout the experimental period. Plasma samples were analyzed for insulin by radioimmunoassay. Protein restriction after weaning resulted in persistently low insulin levels during depletion and rehabilitation periods, while high levels of plasma insulin were observed in energy-restricted pigs only during the depletion period compared to pigs fed the control diet. J. Nutr. 106: 1654-1658, 1976. INDEXING KEY WORDS postnatal malnutrition •protein restriction •energy restriction •insulin There is still incomplete information among studies from different parts of the world about insulin secretion during pro tein-energy malnutrition. It is generally believed that insulin secretion is impaired in kwashiorkor. The evidence for this con clusion is based on impairment of glucose tolerance (1) and a poor plasma insulin response to oral and intravenous glucose (2, 3). Some workers (1, 3) have found a normal glucose tolerance and rise in plasma insulin levels under marasmic con ditions, whereas others have found im paired secretion and glucose tolerance (4, 5). In Jamaica, James and Coore (6) and Milner (7) showed that plasma in sulin is low initially and that the rise in response to intravenous glucose, although significantly improved, is still much lower than in normal children. These results sug gest that a temporary nutritional insult af fecting endocrine pancreatic function could be of importance in the pathogene-
sis of diabetes in later life in those coun tries where malnutrition is endemic in children. In a more extensive study car ried out in Uganda (8), plasma insulin concentrations were significantly above normal during the initial stages of protein malnutrition in human infants, but fell to subnormal levels as the disease progressed. Biochemical changes resulting from pro tein-energy malnutrition have been re ported for the pig (9-14), and there are many similarities between biochemical changes from protein-energy malnutrition in man and swine (15). The purpose of Received for publication April 14, 1976. 1Supported in part by funds provided through the State University of New ïork and Public Health Research Grant no. HD-025S1 from the National Institute of Child Health and Human Development. « Present address : Applied Nutrition Unit, Univer sity of Ibadan. Nigeria. *Present address : Departamento de Fisiologia, Instituto de Ciencias Biomedicas, Universldade de Sao Paulo, Brasil. »Department of Animal Science, Cornell Univer sity, Ithaca, New York 14853.
KÌ.-.4
Downloaded from https://academic.oup.com/jn/article-abstract/106/11/1654/4768783 by guest on 24 October 2019
TOLA ATINMO,2 CARLOS BALDIJÄO,3 WILSON G. POND * ANDRICHARD H. BARNES Division of Nutritional Sciences and Department of Animal Science, Cornell University, Ithaca, New York 14853
MALNUTRITION AND POSTWEANING INSULIN
the present study was to further elucidate the developmental changes that occur in plasma insulin levels during proteinenergy malnutrition with the weaned pig as the animal model. It was also of interest to know whether these changes revert to normal after the pigs have been rehabili tated. Effect of protein deprivation after wean ing on plasma insulin levels of young growing pigs. Twelve 4-week-old male Yorkshire pigs weighing between 6 and 7 kg were divided equally into two groups. Group 1 was fed a control 18% protein diet while group 2 received a 3% protein diet both fed ad libitum (table 1) for 8 weeks. The pigs were kept in concrete floored pens in groups of three, and rec ords of biweekly body weight and food consumption were kept ( 16 ). After a 4 hour fast, blood samples were taken from the jugular vein at 4, 7, 10 and 12 weeks of age and plasma stored at —20°. At the end of the 8-week deprivation period, all pigs were fed the control diet for another 8-week rehabilitation period. Biweekly body weight records were kept and the blood was sampled at 16 and 20 weeks of age. Effect of protein restricted or energy re stricted diets after weaning on plasma insulin levels of young growing pigs. Twenty-four 3 week old male Yorkshire pigs were divided into three groups of eight each and fed the control 187o pro tein diet (group 1), energy-restricted diet
RESULTS AND DISCUSSION
Mean plasma insulin levels during the protein deprivation and rehabilitation pe riods are presented in figure 1. Figure 2 shows the plasma insulin levels in protein or energy restricted pigs. The pigs were fed the restricted diets from 4 weeks of age for 8 weeks and then rehabilitated by feeding a control diet for another 8 weeks. There was a greater drop in plasma in sulin levels in the low protein fed pigs at the initiation of the restriction period compared to the control or energy re stricted pigs (figures 1 and 2). More im portant is the fact that plasma insulin
TABLE 1 Composition of protein or energy restricted diet1
restricted3%84.66.0•
levelGlucose Ingredient protein %Soybean monohvdrate,
%Casein, meal (00% protein),3
%Corn %Vitamin oil, %Mineralmix, mix, %Control18%70.6—20.03.01.05.4Protein Total
100.0
Downloaded from https://academic.oup.com/jn/article-abstract/106/11/1654/4768783 by guest on 24 October 2019
MATERIALS AND METHODS
(group 2) and 6% protein diet (group 3). Group 1 and 3 pigs were fed ad libitum (table 1) while energy restriction was achieved in group 2 by feeding the control diet in an amount that allowed this group of pigs to grow at the same rate as group 3. This amount was provided in two equal rations per day. All pigs were kept in in dividual pens and weekly records of body weight and food consumption were kept ( 16 ). After a 4 hour fast, a blood sample was obtained from the jugular vein at 3, 6, 9, and 11 weeks of age and the plasma stored at -20°. At the end of the 8-week restriction period, all pigs were fed the control diet for another 8-week rehabilita tion period. Blood samples were again ob tained at 15 and 19 weeks of age. Plasma insulin concentration was deter mined by a modified radioimmunoassay method of Hales and Rändle(18) as pre viously described (19).
—3.01.05.46%83.6—7.03.01.05.4Energyrestricted218%70.6—20.03.01.05
100.0
100.0
100.0
1For additional details. See Atinmo, et al. (17). 2Same as control except fed in amounts (two equal portions per day) that allowed pigs to grow at the same rate as protein-restricted pigs. 3Solvent extracted dehulled, 50% protein.
ATINMO, BALDIJÄO, POND AND BARNES
a3
10
13
AGE IN WEEKS
Fig. 1 Plasma insulin ( mean ±SD) in protein deprived pigs during depletion and rehabilitation periods. Four-week-old pigs were weaned to a low protein diet for 8 weeks and then adequately fed for another 8 week period. Plasma insulin levels were consistently lower in the protein de prived pigs throughout the experimental period (P
