Journal of Pediatric Surgery VOL. XI, NO. 4

A U G U S T 1976

Changes of the Postoperative Minimal Oxygen Consumption of the Newborn By Takahiro Ito, YStaro lyomasa, and Taro Inoue

N E R G Y METABOLISM following trauma or operation has been studied in adults by many investigators and has offered valuable information for better management of such surgical patients. On the other hand, studies on newborns and infants are usually limited to the balance studies of water, electrolytes, and nitrogen. ~ There are only a few reports available in literatures on the postoperative or posttraumatic metabolism of the newborn and infant. 5 The purpose of this study is to evaluate the effect of operation and pre- and postoperative starvation on energy metabolism by observing the changes of minimal oxygen consumption of the newborn.

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MATERIALS AND METHODS An open indirect calorimetry system consisting of a hood, an airpump, and oxygen and carbon dioxide analyzers was used (Fig. 1). Mixture of expired and room air was aspirated by an airpurnp at a constant flow rate during the investigation from a hood applied over the head and chest of a newborn. A part of the mixed air flow was led to the analyzers and its oxygen and carbon dioxide were quantitated continuously. Oxygen content was measured with a ToshibaBeckman F-3 paramagnetic oxygen analyzer and carbon dioxide content, with a ToshibaBeckman infrared absorption carbon dioxide analyzer. Calibrations of the analyzers were performed with a standard tank mixture of oxygen (19.1 vol %), carbon dioxide (1.92 vol %), and nitrogen before and after each measurement. The ambient temperature in a nursing incubator was maintained within the neutral thermal range 6 and was confirmed by continuous measurement of the cutaneous, rectal, and ambient temperature. Physical activity of the newborn w a s continuously observed and recorded. The study was performed during postprandial sleep over a period of about 3 hr. The smallest value between two feedings was expressed as minimal oxygen consumption (mVO 2) and minimal carbon dioxide production (mVCO2) of the newborn.

Materials The measurements were performed on total 47 newborns (Table 1). The newborns were divided into two groups based on magnitude of operation and nutritional status. Group 1 had 18 newborns without operation or with minor operation. Seven had repair of myelomeningocele, five had cutback operation for low imperforate anus and one had sacrococcygeal teratoma removed. Group 2 consisted of 24 newborns with major operation. Six had primary anastomosis

From the First Department of Surgery, University of Nagoya School of Medicine, and the Institute for Developmental Research, A ichi Prefecture Colony, Japan. Address for reprint requests: Takahiro Ito, M.D., First Department of Surgery, University of Nagoya School of Medicine, Tsurumai-cho65, Showa-ku, Nagoya, Japan. 9 1976 by Grune & Stratton, Inc. Journal of Pediatric Surgery, Vol, 11, No. 4 (August), 1976

495

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Table 1. Clinical Materials Diagnosis

Myelomeningocele Esophageal atresia with TEF Intestinal obstruction (not operated) Intestinal obstruction (operated) Congenital pyloric stenosis Hirschsprung's disease Imperforate anus Gastroschisis Others

Number of Cases

8 6 2 9 1 2 10 2 7 47

Total Treatment

Number of Cases

Without operation Primary anastomosis for esophageal atresia Anoplasty or cut back operation Removal of sacrococcygeol teratoma Repair of myelomeningocele Resection and anastomosis for intestinal atresia Resection of the membranous atresia Colostomy Repair of gastroschisis Removal of retroperitoneal teratoma Ladd-Bill's procedure for malrotation Rarnstedt's operation

9 6 6 1 8 6 2 3 2 1 2 1

Total

47

POSTOPERATIVE OXYGEN CONSUMPTION

497

8 7 6

g E Fig. 2. Changes in minimal oxygen consumption of 18 newborns without operation or with minor operation. The dotted lines indicate 2 SD of the mean (used for deciding whether or not an individual observation is within the normal range). Minimal oxygen consumption increases with increasing age in the first and second weeks of life.

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for esophageal atresia with tracheoesophageal fistula. Seventeen had major abdominal operations for neonatal intestinal obstruction, gastroschisis, and retroperitoneal teratoma.

RESU LTS

Group

1:

Eighteen Newborns Without Operation or With Minor Operation

The minimal oxygen consumption increased with advancing days after birth. Seventeen out of 18 full-term newborns weighing over 2500 g showed a large increase in mVO2 during the first 2-4 days of life and then slower but steady increase during the first and second weeks of life. Postnatal increase in mVO2 became almost minimal during the third week of life. As there was no or a very short period of starvation in these newborns, the average mVO2 of these newborns was regarded as the normal value by our method. The average mVO2 was 5.96 • 0.24 ml/kg/min during the first week of life, 6.73 • 0.25 ml/kg/min during the second week of life and 7.15 • 0.64 ml/kg/min during the third week of life (Table 2). Figure 3 shows the change of mVO2, body weight, and calorie balance of the typical newborn in the first group.

Group 2: Twenty-four Newborns With Major Operations Change in m VO 2 With Advancing Age Following Major Operation The average mVOz was 5.73 • 0.16 ml/kg/min during the first week of life and 5.62 • 0.18 ml/kg/min during the second week of life. The difference was not statistically significant. The average mVO2 increased from 5.62 • 0.18 ml/ kg/min during the second week of life to 6.39 • 0.15 ml/kg/min during the Table 2. Effect of Operation on Minimal Oxygen Consumption Newborns Without Operation and With Minor Operation

Age

Numberof

(wk)

Studies

1 2 3 4

39 25 6 .

Newborns With Major Operation

Min 02 Consumption (ml/kg/min) Mean SD SEM

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5.96 6.73 7.15 .

SD: standard deviation. SEM: standard error of the mean,

0.77 0.60 0.62 .

O. 12 O. 12 0.25

Number of studies 18 32 32 10

Min 02 Consumption (ml/kg/rnin) Mean SD SEM 5.73 5.62 6.39 7.12

0.66 0.99 0.82 0.87

O. 16 O. 18 O. 15 0.29

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Fig. 3. (Left) Postnatal increase in minimal oxygen consumption of a normal newborn. K. A., a male, 3186 g at birth with a lumbosacral myelomeningocele, was admitted on the first day of life and operated on the 15th day of life. There was no period of starvation. Minimal oxygen consumption increased with age during the first and second weeks of life. The postnatal increase was normal. Fig. 4. (Right) Postnatal increase in minimal oxygen consumption of a newborn with primary esophageal anastomosis for TEF. S. M., a male, 3460 g at birth, was admitted on the fourth day of life. Extrapleural division of the fistula and esophageal anastomosis were performed on the fifth day. Feeding was started through a transanastomotic feeding tube on the second postoperative day and increased slowly until the eighth postoperative day. Thereafter, total caloric intake of more than 80 cal/kg/day was maintained. Minimal oxygen consumption remained low during the first week after operation and increased rapidly with increasing caloric intake.

third week of life. The change was statistically significant (p < 0.005). Increase in mVO2 continued during the third and fourth week of life until 7.12 • 0.29 ml/kg/min, the value of mVO2 of the normally fed newborns without operation or with minor operation, was reached. The difference of the average mVO2 between the third and fourth week of life was statistically significant (p < 0.02). Thus, postnatal increase in mVO2 tends to be delayed in the newborn during the second and third weeks of life, who underwent major operation.

Effect of Major Operation on Minimal Oxygen Consumption The average mVO2 of the newborn with major operation was 5.73 • 0.16 ml/kg/min during the first week of life, 5.62 -4- 0.18 ml/kg/min during the second week of life, and 6.39 • 0.15 ml/kg/min during the third week of life and these were smaller than the average mVO2 in group 1 (Table 2). The difference of mVO2 between two groups was not statistically significant during the first week of life, but was statistically significant during the second and third week of

POSTOPERATIVE O X Y G E N

CONSUMPTION

499

life (p < 0.01 during the second week and p < 0.05 during the third week of life, respectively). Sixteen out of 24 newborns with m a j o r operation had been operated during the first week of life. Thus the effect of operation seemed to become apparent during the second week and to last even during the third week of life. N o n e of the newborns in group 2 showed a postoperative increase in mVO2, suggesting hypermetabolic state. Change in m VOe of the newborn with primary anastomosis for TEF. Serial measurement of mVO2 was done on three newborns with T E F and serial measurement of mVCO2 on three other newborns with T E F . The curves of the postnatal increase in mVCO2 were similar to the curves in mVO2. All three newborns showed normal mVO2 after 13 days of life. T w o newborns showed normal mVO2 during the first and the second weeks of life in spite of operation, and one had lower mVO2 than the average until 13 days of life, when he increased mVO2 to normal level for age (Fig. 4). Thus, these newborns had lower mVO2 or mVCO2 than the average for a b o u t 10 days after birth. Change in m VOe of the newborn with major abdominal operation. Serial measurements of mVO2 were made in six newborns with m a j o r abdominal operation. No a b n o r m a l change in the curve of mVO2 was observed in three new+10

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Fig. 5. (Left) Postnatal change in minimal oxygen consumption of a newborn with intestinal obstruction. K. I., a male, 3470 g at birth and 2619 g at admission, was admitted on the 7th day of life. Ladd's procedure was carried out on the 8th day of life. Oral intake was not successful until the 11th postoperative day, so he starved for about 19 days after birth. Minimal oxygen consumption remained low during this periocL Fig. 6. (Right) Postnatal change in minimal oxygen consumption of a newborn with resection and anastomosis of the small intestine. M. K., a male, 3220 g at birth, was operated on the second day of life because of ileal atresia. The dilated intestine proximal to the atresia was removed and continuity of the intestine was established. Oral feeding was started on lOth postoperative day and increased slowly. The starvation lasted more than 2 wk after birth and he had lost 2 0 % of body weight postoperatively. Minimal oxygen consumption remained low for 17 postoperative days.

500

ITO, IYOMASA, AND INOUE

borns, one of whom had removal of retroperitoneal teratoma and two of whom had colostomy for Hirschsprung's disease. Three other newborns showed a longer period of low mVO2 postoperatively. One of them with Ladd-Bill's procedure for malrotation showed low mVO2 for about 27 days following operation as illustrated in Fig. 5. Another newborn with Ladd-Bill's procedure for malrotation showed a similar change in m V O 2 . On a newborn with resection and anastomosis of the gut for ileal atresia on the second day of life, a considerably lower value of mVO2 was observed during the second and third week of life (Fig. 6). The above mentioned three newborns had been starved for 14 19 days pre- and postoperatively because of intestinal obstruction.

Minimal Oxygen Consumption of the Starved Newborn A comparison of mVO2 was made between two groups of the newborns classified according to the amount of caloric intake on the day of observation; group A was during starvation and group B during no starvation. Being calculated from m V O 2 by using a figure of 4.83 cal/liter of oxygen consumed, the average minimal caloric expenditure of the normal newborn in this study group was 41 c a l / k g / d a y during the first week of life, 47 c a l / k g / d a y during the second week of life, and 50 c a l / k g / d a y during the third week of life. The newborns whose calorie intake was below this average were regarded as the starved (group A) and the newborns whose calorie intake was above this average as group B. Differences of the average mVO2 between two groups were 0.89 ml/ kg/min, 1.34 m l / k g / m i n , and 1.30 m l / k g / m i n for the first, second, and third weeks of life, respectively (Table 3). These differences were highly significant statistically for each week of life (p < 0.001). Therefore, this study showed that starvation had a significant influence on mVO2 of the newborn, resulting in lowering the postnatal normal rise of mVO2.

DISCUSSION The results of our studies on average mVO2 of the newborn and its postnatal increase are in agreement with those of other investigators. 6 10 The results confirmed that a full-term normally fed newborn increases mVO2 with advancing age until the postnatal increase of mVO2 is completed, usually the second and third weeks of life. Many investigators IH4 reported that the adult patients or the experimental adult animals showed an increase in metabolic rate o r m V O 2 after trauma or operation, except for a short period of depressed metabolic rate immediately following trauma and operation, called " E b b " period. In our Table 3. Effect of Calorie Intake on Minimal Oxygen Consumption NewbornsWith Starvation

NewbornsWithout Starvation

Min 02 Consumption Age (wk)

Number of Studies

1 2 3

32 43 34

Mean

(ml/kg/min) SD

6.42 6.70 6.80

0.48 0.85 0.40

SD: standard deviation. SEM: standard error of the mean.

Min 02 Consumption

SEM

Number of Studies

Mean

(ml/kg/min) SD

SEM

0.08 0.13 0.07

28 14 8

5.53 5.36 5.50

0.65 0.75 0.41

0.12 0.15 0.06

POSTOPERATIVE OXYGEN CONSUMPTION

501

study, there was no such postoperative increase in mVO2 in the newborn more than the expected for a normal newborn for age as in the adult. In other words, operation does not cause an increase in metabolic rate. On the contrary, there were some newborns, particularly in the group of m a j o r abdominal operation, who maintained lower postoperative mVO2 than the expected mVO2 for a normal newborn of the same age. Varga 5 also found low VO2 in the first 3 days after operation on four out of eight infants with congenital pyloric stenosis. Our results suggest that the effect of operation on mVO2 differs in the newborn from it in the adult, but may be interpreted that the effect of operation is masked by the effect of coexistent starvation. On most of the newborns whose m V O 2 remained lower than the average regardless the types of operation, oral calorie intake could not be increased during the pre- and postoperative period due to the p o o r function of their gastrointestinal tract. It is, therefore, concluded that the mVO2 of the newborn is influenced significantly by starvation. This p o o r calorie intake was considered as the cause of their low mVO2 in our study. Oxygen consumption or B M R in semistarvation or undernutrition were extensively studied on adults after the World War II by G r a n d e et al., ~5 Keys, 16 and Taylor et al., 17 who reported that restriction of calorie intake resulted in lowering oxygen consumption or BMR. The findings studied on the infants in m a r a s m u s or K w a s h i o r k o r by M o n t g o m e r y ~8 were that B M R or oxygen consumption per kilogram of body weight was normal and increased above the normal with the recovery of food intake. Talbot et al., 19 however, observed a fall in B M R on infants after several days' fasting. A m o r e recent study by Bhakoo and Scopes 2~ on the small-for-date babies who were fed early and whose milk intake was increased m o r e that 120 c a l / k g / d a y within the first 3 days of life indicated that the postnatal increase in mVO2 was similar to that of the full-term normal babies. The previous study by the same authors showed lower mVO2 of the smallfor-date who was fed smaller amounts of milk than the small-for-date in the recent study. The mVO2 or B M R of the pediatric age group was diverse a m o n g these workers. The possible reasons for these controversial results seem to be related to the differences in the age of the studied patients (there were a very few studies on the newborns), in the duration and the severity of starvation, and in the undermined or complicated pathologic conditions. The studies on the adults were m o r e uniform in these respects, although most of the adult studies were done in chronic undernutrition or semistarvation of less severity.~5 17 In our study on the newborn, the decrease in mVO2 took place in most of the patients within a week of starvation, when calorie intake ranged from less than the normal estimated basal metabolic rate to the absolute fasting, and a rapid return of mVO2 to the normal level was observed within few days after the adequate a m o u n t of calorie was supplied. The time interval for the recovery of m V O 2 to the normal level seemed to be dependent upon the duration and the severity of starvation and the a m o u n t of calories supplied, though the limited n u m b e r of our newborns studied did not allow us to give a statistical analysis a m o n g these factors. It is very difficult to elucidate why or how the newborn decreases mVO2 during the postoperative period of starvation. Explanations for the decrease in B M R or in VO2 of the adult during semi-

502

ITO, IYOMASA, AND INOUE

s t a r v a t i o n are partly due to a decrease o f the m e t a b o l i c activity of the b o d y cells ( 3 5 ~ of the total decrease in B M R ) a n d partly due to the loss of active tissues (65~o). ~7 The m a r k e d decrease in B M R of the active b o d y cells takes place in the early phase of s t a r v a t i o n ( d u r i n g the first 2 3 wk). 15 These e x p l a n a tions o f the a d u l t studies m a y be applied to our results o n the n e w b o r n ; the decrease in mVO2 in o u r n e w b o r n s m a y be m a i n l y due to the decreased m e t a b o l i c activity of the b o d y cells in a s s o c i a t i o n with s t a r v a t i o n . A r a p i d recovery of low mVO2 with increased calorie i n t a k e is u n d e r s t o o d . It seems that the n e w b o r n s have m o r e a d a p t a t i o n m e c h a n i s m s to s t a r v a t i o n in order to c o n s e r v e the limited reserve of the energy for longer m a i n t e n a n c e of life. So the findings in o u r study m a y e x p l a i n the clinical i m p r e s s i o n t h a t some of the newb o r n s can tolerate s t a r v a t i o n s u r p r i s i n g l y well as described by R i c k h a m . 2 SUMMARY

M i n i m a l oxygen c o n s u m p t i o n a n d c a r b o n dioxide p r o d u c t i o n were studied in n e w b o r n s w i t h o u t o p e r a t i o n a n d with m i n o r or m a j o r o p e r a t i o n by m e a n s of o p e n indirect c a l o r i m e t r y . (1) A p o s t n a t a l increase in the m V O 2 was observed in most of the full-term n e w b o r n s w i t h o u t o p e r a t i o n or with m i n o r o p e r a t i o n . ( 2 ) A p o s t o p e r a t i v e increase in the mVO2, as observed in the adult, was n o t f o u n d in all n e w b o r n s with a m a j o r o p e r a t i o n . (3) This finding was p a r t i c u l a r l y o b v i o u s in the n e w b o r n with a m a j o r a b d o m i n a l o p e r a t i o n a n d with a long pre- a n d p o s t o p e r a t i v e periods of s t a r v a t i o n . (4) T h e m o s t i m p o r t a n t factor d e t e r m i n i n g the p o s t o p e r a t i v e decrease in the mVO2 is n o t the intensity of operative stress b u t the a m o u n t of caloric intake. REFERENCES

1. Knutrud O: The water and electrolyte metabolism in the newborn child after major surgery. Norweigian monographs on medical science, Oslo, Scand. University Books, Universitets Forlaget, 1965 2. Rickham PP: The metabolic response to neonatal surgery. Cambridge, Mass, Harvard Univ Press, 1959, p 74 3. Wilkinson AW, Stevens LH, Hughes EA: Metabolic changes in the newborn. Lancet 1: 983, 1962 4. Colle E, Paulsen EP: Response of the newborn infant to major surgery. Pediatrics 23: 1063, 1959 5. Varga F: The respective effects of starvation and changed body composition on energy metabolism in malnourished infants. Pediatrics 23:1085, 1959 6. Brtick K: Heat production and temperature regulation. Physiology of the perinatal period, vol 1. New York, Appleton-CenturyCrofts, 1970, p 499 7. Smith CA: The physiology of the newborn infant (third ed.). Springfield, Ill., Thomas, 1959, p 205

8. Hill JR, RahimtuUa KA: Heat balance and the metabolic rate of newborn babies in relation to environmental temperature; and the effect of age and of weight on basal metabolic rate. J Physiol 180:239, 1965 9. Hill JR, Robinson DC: Oxygen consumption in normally grown, small-for-dates and large-for-dates newborn infants. J Physiol 199: 685, 1968 10. Hey EN: The relation between environmental temperature and oxygen consumption in the new-born baby. J Physiol 200:589, 1969 11. Cuthbertson DP: Post-shock metabolic response. Lancet 1:433, 1942 12. Cuthbertson DP: Protein metabolism in relation to energy needs. Metabolism 8:787, 1959 13. Tilstone WJ, Cuthbertson DP: The protein component of the disturbance of energy metabolism in trauma. Energy metabolism in trauma. London, Churchill, 1970, p 44 14. Stoner HB: The acute effects of trauma on heat production. Energy metabolism in trauma. London, Churchill, 1970, p 14

POSTOPERATIVE OXYGEN CONSUMPTION

15. Grande FG, Anderson JT, Keys A: Changes of basal metabolic rate in man in semistarvation and refeeding. J Appl Physiol 12:230, 1958 16. Keys A: Caloric undernutrition and starvation, with notes on protein deficiency. JAMA 138:500, 1948 17. Taylor HL, Keys A: Adaptation to caloric restriction. Science 112:215, 1950 18. Montgomery RD: Changes in the basal

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metabolic rate of the malnourished infant and their relation to body composition. J Clin Invest 41:1653, 1962 19. Talbot FB, Dalrymple AJ, Hendry MF: Skin temperature and basal metabolism during fasting. Am J Dis Child 30:491, 1925 20. Bhakoo ON, Scopes JW: Minimal rates of oxygen consumption in small-for-dates babies during the first week of life. Arch Dis Child 49:583, 1974