malnutrition is a consequence of inadequate diet and frequent infections , leading to deficiencies in calories , protein , vitamins , and minerals . malnutrition remains a pervasive problem in developing countries , where poverty is a strong underlying determinant . all ages are at risk , but malnutrition is most prevalent among children under five years of age , especially in the weaning and postweaning period of six to twenty - four months . the world health organization ( who ) has estimated that approximately 27% ( 168 million ) of children under the age of five years are underweight . underweight children are at increased risk of mortality from infectious illnesses such as diarrhea and pneumonia . in malnourished children , stunted growth and a lower amount of spontaneous physical activity are adaptations to reduced energy intake in an attempt to preserve vital functions . furthermore , other effects of malnutrition include poor brain development   possibly leading to poor cognition . finally , children with untreated malnutrition suffer from repeated episodes of acute diarrhea resulting in dehydration . only in our previous study has there ever been a long - duration study ( 22 hours ) where energy expenditure was measured continuously in healthy infants utilizing indirect calorimetry . due to the length of the metabolic measurements , we determined that healthy infants display a metabolic circadian rhythm by four months of age . at the time of this study we were the only research group in the world conducting these types of long - term energy expenditure measurements utilizing this technology . now , we have taken our perfected methodology and applied it to infants suffering from malnutrition . this might reveal differences in the energy expenditure profile not detectable with short - duration indirect calorimetric measurements . these longer duration metabolic measurements might lead to new and improved nutrition rehabilitation regimes fine - tuned for malnourished or infants suffering from various metabolic disorders . ten chronically malnourished full term infants ( 7.7  5.0 months , 4.1  1.2  kg , 58.1  5.9  cm , 7 males and 3 females ) , with a birth weight of 2.7  0.6  kg were recruited from the inpatient metabolic ward of the department of pediatrics , federal university of bahia school of medicine , hospital universitario professor edgar stantos , salvador , brazil . six were classified as primary and four as suffering from secondary malnutrition as determined by a pediatrician familiar with our study . the data from these infants were compared to 10 healthy formula - fed ( carnation good start with iron ) counterparts ( 7.3  0.8  kg , 68.8  2.8  cm , 5.0  0.7 months ) from a prior similar metabolic study in miami , florida , usa . only infants that were admitted for severe malnutrition with a diagnosis of marasmus or kwashiorkor were studied . no healthy infants were recruited for this study since we already had data from such a group from a prior metabolic study . in our group of 10 infants , moreover , there was no presence of concurrent secondary infection in those infants that were classified as having secondary malnutrition when they underwent metabolic testing . furthermore , all infants who participated in the study were less than the 5th percentile for weight - for - length , length - for - age and weight - for - age according to the nchs growth charts . moreover , all infants were classified as being malnourished according to weight - for - age and length - for - age z - scores being less than or equal to 2 upon admission . once identified , they were studied after they showed appropriate recovery from infectious illness as determined by the attending pediatrician . moreover , there was no indication or presence of edema at the time of the metabolic test as verified by the pediatrician familiar with the study . this was also verified by the 0.36  0.22  kg of weight gained between admission and the time of the metabolic test . moreover , infants had to have a normal body temperature , as determined by the measurement of the rectal temperature , just prior to metabolic testing . finally , infants had to be consuming the prescribed amount of formula with no presence of acute diarrhea or vomiting for at least 24 hours prior to metabolic testing . infants were excluded if they were exclusively breastfed or presented with renal , hepatic , respiratory , and/or cardiac chronic diseases . moreover , those with serious infections ( pneumonia , meningitis , septicemia , etc . ) requiring intensive care were also excluded . all infants studied were of african descent and from improvised families   where there were 4.5  0.5 persons living within the household . biological parents were provided with a complete explanation regarding the purpose , procedure , risks , and benefits of the study and informed consent was obtained from at least one parent of each infant . the study was approved by the institutional review board of the hospital universitario professor edgar stantos , federal university of bahia school of medicine , and by the institute review board of lehman college , bronx , ny . length was measured in duplicate with a horizontal stadiometer ( perspective enterprises , kalamazoo , mi ) and body weight was the average of two measurements obtained with an infant scale ( cardinal detecto , webb city , mo ) . body composition was determined through the mean of triplicate measurements of triceps skin - fold thickness on the right side of the body using a lange skin - fold caliper ( lange , beta technology , cambridge md ) according to a standard procedure . calculation of the body fat was based on siri 's equation [ body fat  % of weight  = ( 4.95/body density   4.5 )   100 ] , where body density is calculated from age and sex adjusted regression equations designed for malnourished infants according to laditan and ayeni . infant bmi ( kg / m ) was calculated and all anthropometric measurements were made by a trained registered dietitian . length - for - age , weight - for - age , and weight - for - length z - scores were calculated with epi info software ( version 3.5.1 ) utilizing the 1978 who / cdc growth reference . total energy intake , and the percentage of carbohydrate , fat , and protein consumed , were determined by utilizing the formula manufacturer 's proximate analysis ( nestle good start with dha & ara ) and by the amount consumed by the infant though out the 22-hour metabolic test using calibrated infant feeding bottles . the recording of energy intake started one - hour prior to and ended one - hour before the conclusion of the 22-hour metabolic testing period . the one - hour off - set was necessary to include or exclude energy consumed before and after the metabolic testing period due to the gut transient time for formula in this age infant . furthermore , none of these infants consumed energy from other sources such as solid foods or other liquid supplements during the study . all infants were formula fed for at least three months prior to metabolic measurements . prior to each metabolic measurement , the enhanced metabolic testing activity chamber ( emtac ) instrumentation was calibrated with standard gases with a known concentration of oxygen and carbon dioxide . furthermore , parents were given instruction on how to interact with their infants and were given time to practice using the hand access ports prior to metabolic testing [ 8 , 1517 ] . once all of the instruction and calibrations were complete each infant was placed in the emtac for 22 hours from 11:30 am till 9:30 am the following day for continuous measurements of energy expenditure ( ee ; kcal / min ) , physical activity ( pa ; oscillations in weight / min / kg body weight ) , and the respiratory quotient ( rq ; vco2/vo2 ) . two hours were allowed for instrument calibrations , parental instruction and practice using the hand - access ports . any supplies such as diapers , formula , or toys were placed in the emtac in hanging bags before the start of the test . breast fed infants were not studied due to the difficulty of having pumped breast milk available for the infant during the long duration metabolic testing period . moreover , we did not have the ability to keep breast milk cool within the emtac enclosure for the 22-hour metabolic test . the family of the infant was provided lodging within the laboratory during the entire testing period . the investigator , pediatric research fellows , and attending pediatricians that were familiar with the study acted as observers on rotating eight - hour shifts and recorded all infant activities such as infant feedings , crying , periods of observed sleep , and amount of parental interaction during the entire 22-hour testing period . energy expenditure , sleeping metabolic rate , physical activity , and the respiratory quotient were continuously calculated as described in a previous infant 24-hour metabolic study . the emtac , methodology for measurement and calculation of each component of 24-hour extrapolated ee , and correction for parental interaction have been described in previous studies [ 8 , 1517 ] . to correct the continuous metabolic data for differences in body weight , each five - minute data summary period ( kcal / min ) was divided by kg body weight and expressed as kcal / min / kg . next , the corrected continuous metabolic data for each infant were than divided into three separate periods consisting of 12 , eight , and two hours each , respectively . the daytime period ranged from 11:30 am till 11:29 pm , the night time period ranged from 11:30 pm till 7:29 am the next day and the morning period ranged from 7:30 am till the completion of the metabolic test at 9:30 am . the criteria used for the division of the metabolic data into the specific time periods are similar to that used in previous metabolic studies in infants [ 8 , 1517 ] and in adults [ 18 , 19 ] . the sample size in this study was determined in advance , based on data obtained from short and long - term metabolic measurements in the emtac in previous studies [ 8 , 1517 ] . moreover , the number of infants needed to detect a 5% difference in metabolic and anthropometric parameters , were then calculated according to the formula of kuzma . all data were analyzed utilizing spss ( version 13 , chicago , il ) and expressed as mean  standard deviation . significance ( p < finally , the shapiro - wilk test of normality was utilized to determine whether the distribution was normal for both the malnourished and healthy infants . the test suggests that both the malnourished ( p < .68 ) and healthy infants ( p < .15 ) were found to be normally distributed . comparisons for 24-hour extrapolated metabolic rate and anthropometric data between malnourished and healthy infants were determined by independent t - test ( p < .05 ) . furthermore , within each group ( malnourished and healthy ) one - way anova with least significant difference was utilized to determine differences between each of the three time periods ( day time , night time , and morning ) for continuous energy expenditure ( kcal / kg / min ) , respiratory quotients ( vco2/vo2 ) , and physical activity ( oscillations in weight / min / kg body weight ) . in comparison to similarly aged healthy controls , the malnourished infants in this study were shorter , lighter , and had less body fat and fat - free mass , along with a lower bmi . moreover , the malnourished infants had lower z - scores for length - for - age ( p < .05 ) and weight - for - age ( p < .05 ) , in comparison to their healthy counterparts while no differences were found between the two groups for weight - for - length ( table 1 ) . however , no differences were found between the two groups in terms of maternal bmi ( table 1 ) which was within the normal weight range of 2025  kg / m . finally , the malnourished infants were living below the poverty line as shown by the monthly income of $ 230.00    $ 133.00 and number of persons residing in the household ( 4.5  0.5 ) . according to table 2 , the malnourished infants consumed more energy ( p < .05 ) during the metabolic test than their healthy counterparts , with a greater proportion of energy as carbohydrate ( p < .05 ) . twenty - four - hour extrapolated energy expenditure ( 24-hour ee ) and sleeping metabolic rates ( smr ) , along with the respiratory quotient ( rq ) , were greater ( p < .05 ) in the malnourished infants in comparison to their healthy counterparts ( table 2 ) . however , the malnourished infants were less physically active ( p < .05 , table 2 ) . moreover , the malnourished infants cried ( p < .05 ) and slept ( p < .05 ) longer during metabolic testing ( p , there were no differences between the two groups in the amount of time parents spent interacting with their infants ( table 2 ) . the metabolic pattern for both groups of infants throughout the 22-hour measurement period is shown in figure 1 . the malnourished infants appeared to have greater energy expenditure during the day and morning periods in comparison to their healthy counterparts . however , during the night time period ( 11:30 pm till 7:30 am ) the healthy infants showed a significant ( p < .05 ) decrease in energy expenditure as opposed to the lack of a similar decrease in the malnourished infants . similar results were obtained for physical activity where the malnourished infants showed no significant changes in this parameter throughout the 22-hour metabolic test ( figure 2 ) . however , even though not significant , the healthy infants showed greater amounts of physical activity during the day and morning periods in comparison to the night time period ( figure 2 ) . the respiratory quotient ranged from 0.83 to 1.13 across all the malnourished infants over the course of the metabolic test . this is in comparison to the range of 0.70 to 0.99 in the healthy infants undergoing a similar study ( figure 3 ) . during metabolic testing the respiratory quotient remained higher in the malnourished infants in comparison to their healthy counterparts . this is the first study of its kind where a direct comparison was made between similarly aged chronically malnourished and healthy full term infants in regards to their continuous 22-hour metabolic profiles utilizing an established accurate technology [ 8 , 16 , 17 ] . moreover , at the time of the metabolic test , none of the infants had edema or were febrile which might have affected their 22-hour energy expenditure profile . in regards to anthropometrics , we found that malnourished infants had lower body weight and length , less body fat and fat - free mass , along with a lower bmi . however , the biological parents of both groups of infants had bmi 's within the normal weight range ( 19.1 to 27.3  kg / m ) . moreover , the malnourished infants were from improvised families [ 11 , 12 ] . in regards to energy metabolism , malnourished infants consumed and expended more energy , had higher respiratory quotients , greater sleeping metabolic rates , and were less physically active . moreover , they slept and cried more . finally , they consumed a greater portion of their energy as carbohydrate . the higher proportion of energy intake as carbohydrate in the malnourished infants might explain the higher respiratory quotients found during the 22-hour metabolic test . this is similar to the findings in one study where low birth - weight infants on total parenteral nutrition had greater lipid synthesis on a high carbohydrate intake of 12  g / kg / day . it is possible that increased carbohydrate intake in the malnourished infants could lead to altered energy metabolism later in life . this might be due to altered insulin sensitivity created during the time of malnutrition . in one study children who were born prematurely it is possible that the additional carbohydrate intake in our malnourished infants might lead to the possibility of insulin resistance and a greater possibility of excess body weight gain after their recovery from malnutrition during later childhood . during the 22-hour metabolic test , the malnourished infants did not display any kind of a metabolic circadian rhythm . in a previous study , it is possible that the lack of a metabolic circadian rhythm in the malnourished infants is the result of a lack of sympathetic nervous system stimulation . reducing or eliminating circadian hormonal stimulation of the sympathetic nervous system may allow more energy to be diverted to rapid growth . the suprachiasmatic nuclei , the site of the circadian clock , are present by mid gestation . after birth there are pronounced rhythms in the sleep - wake cycle and hormone secretion by two months of age . furthermore , fetal heart rate has been found to be synchronized with maternal activity , heart rate , cortisol , maelatonin , and body temperature [ 25 , 26 ] . furthermore , the nocturnal trough of body temperature is already present in 6- to 12-week - old full term infants and is a good indicator of the presence of circadian rhythms . all of these studies [ 2527 ] suggest that a metabolic circadian rhythm is present in healthy infants almost from the time of birth . another possible explanation for the greater energy intake and expenditure in the malnourished infants during this study may be due to their rapid growth rate . it is estimated that it costs 3.96.0  kcal / gram of body weight gain during the first year of life in malnourished infants , representing a 70% energetic efficiency for energy disposition . considering they have less than half the body fat content and are half the weight of their similarly aged healthy counter parts , this suggests that they are displaying rapid catch - up growth in order to replace their fat - free and fat mass stores back to their genetically predetermined levels . the lack of a metabolic circadian rhythm may also reflect that they are laying down new tissue throughout the day and night . it is possible that their metabolic circadian rhythm might reappear once they reach their normal body weight and composition for their ages . the emtac is the first instrument of its kind to conduct continuous metabolic measurements in infants suffering from primary / secondary malnutrition . previously , metabolic evaluations in malnourished infants were made utilizing a 20-minute measurement of resting metabolic rate with a deltatrac metabolic monitor . however , short - term measurements do not encompass the true metabolic needs in these infants due to their unique metabolic profile . in this study where energy expenditure was measured continuously for 22 hours , we found the apparent lack of a metabolic circadian rhythm in the malnourished infants . moreover , the measurement could be repeated and the reappearance of the metabolic circadian rhythm could be possibly used as a sign of recovery . we found differences in the metabolic profiles between malnourished and healthy infants of similar age . these results will possibly affect determination of future energy requirements and application of nutritional rehabilitation regimes in infants suffering from malnutrition . we also found that they appear to conserve energy , possibly for catch - up growth , though a reduction in physical activity , increased sleep , and the lack of a metabolic circadian rhythm . moreover , the greater respiratory quotient possibly reflects greater lipid synthesis in order to replace depleted body fat .
background . 
 malnourished infants are small for age and weight . objectives . determine profiles in 24-hour energy metabolism in recovering malnourished infants and compare to similarly aged healthy controls . 
 methods . 10 malnourished infants ( 58.1  5.9  cm , 7.7  5.6 months ) were healthy prior to spending 22 hours in the enhanced metabolic testing activity chamber for measurement of ee ( kcal / min ) , sleeping metabolic rate ( smr ; kcal / min ) , respiratory quotient ( rq ; vco2/vo2 ) , and physical activity ( pa ; oscillations in wt / min / kg body weight ) . 
 metabolic data were extrapolated to 24 hours ( kcal / kg / d ) . 
 energy intake ( kcal / kg / d ) and the proportions ( % ) of carbohydrate , protein , and fat were calculated . 
 anthropometrics for malnourished infants were obtained . statistical differences ( p < .05 ) between groups were determined ( spss , version 13 ) . results . in comparison to controls , 
 malnourished infants were lighter ( 4.1  1.2 versus 7.3  0.8  kg ; p < .05 ) , had less body fat % ( 10.3  7.6 versus 25.7  2.5 ) , and lower bmi ( 12.0  1.7 versus 15.5  1.5 ; p < .05 ) . 
 in contrast , they had greater energy intake ( 142.7  14.6 versus 85.1  25.8 ; p 
 < .05 ) with a greater percentage of carbohydrates ( 55.1  3.9 versus 47.2  5.2 ; p < .05 ) . however , 
 malnourished infants had greater 24-hour ee ( 101.3  20.1 versus 78.6  8.4 ; p < .05 ) , smr ( 92.6  17.1 versus 65.0  3.9 ; p < .05 ) , and rq ( 1.00  0.13 versus 0.86  0.08 ; p < .05 ) along with a lower amount of pa ( 2.3  0.94 versus 4.0  1.5 ; p < .05 ) . conclusions . malnourished infants require more energy , possibly for growth .