- Email: [email protected]
Body temperatures and oxygen consumption during skin-to-skin (kangaroo) care in stable preterm infants weighing less than 1500 grams
Body temperatures and oxygen consumption during skin-to-skin (kangaroo) care in stable preterm -'n g less than 1500 grams infants we ignl Karl Bauer, MD, Caroline Uhrig, Peter Sperling, Katharina Pasel, Christine Wieland, MD, a n d Hans T Versmold, MD From the Department of Paediatrics, Freie Universit6tBerlin, Klinikum Benjamin Franklin, Berlin, Germany
Background: More and progressively smaller preterm infants are taken out of the incubator and placed skin to skin on their mother's chest to promote bonding, despite concerns that the infants are exposed to cold during this intervention. Objective: To test the hypothesis that skin-to-skin care is a cold stress for preterm infants weighing less than 1500 gm, with a decrease in rectal temperature, a decrease in peripheral skin temperature, or an increase in oxygen consumption compared with conditions monitored during incubator care. Study design: We studied 22 stable, spontaneously breathing preterm infants weighing less than 1500 gm (appropriate in size for gestational age), who had their first skin-to-skin care in the first week of life. We continuously measured rectal temperature, peripheral skin temperature (foot), and oxygen consumption (indirect calorimetry) for I hour in a thermoneutral incubator, during I hour of skin-toskin care, and for another hour in the incubator. Mean values for the three periods were compared by analysis of variance. Results:During skin-to-skin care the mean rectal temperature was 0.2 ° C (p <0.0 I) and the peripheral skin temperature was 0.6 ° C (p <0.01) higher than during the preceding hour in the incubator. Back in the incubator, body temperatures returned to values recorded before skin-to-skin care. Oxygen consumption during skin-to-skin care (6. I ___0.9 ml/kg per minute)was not significantly higher than in the incubator (5.8 _ 0.8 ml/kg per minute). Conclusion: For stable preterm infants weighing less than 1500 gm and less than I week of age, I hour of skin-to-skin care is not a cold stress compared with care in a thermoneutral incubator. (J Pediatr 1997;130:240-4)
Skin-to-skin (kangaroo) care, with preterm infants' placed on their mother's chest, was started for want of incubators in Bogota, Colombia.1 The hope of promoting mother-infant bonding led to a widespread acceptance of skin-to-skin care Submitted for publication Sept. 14, 1995; accepted Aug. 1, 1996. Reprint requests: Karl Bauer, MD, Kinderklinik, Universit~tsklinikum Benjamin Franklin, Freie Universit~it Berlin, Hindenburgdamm 30, 12200 Berlin, Germany. Copyright © 1997 by Mosby-Year Book, Inc. 0022-3476/97/$5.00 + 0 9/21/77289
240
in industrialized countries. 2 Even very low birth weight infants were exposed to this intervention despite concerns that the mother's skin temperature is too low to provide a thermoneutral environment for a VLBW infant. 3 A thermoneutral environment is regarded as "the optimum thermal environment for naked babies,"4 because there is no increase in body metabolism related to excessive heat or excessive cold and body temperature is maintained normal without a thermoregulatory increase in oxygen consumption. For VLBW infants, no measurements of V02 during skin-to-skin care exist, and there are only incomplete data on body tempera-
The Journal of Pediatrics Volume 130, Number 2
AGA
VCO2 Vo2 VLBW
Appropriate [in size] for gestational age Carbon dioxide production Oxygen consumption Very low birth weight
tures.5, 6 Therefore the purpose of this study was to test the hypothesis that skin-to-skin care is a cold stress for stable preterm infants weighing less than 1500 gm, with a decrease in rectal temperature, a decrease in peripheral skin temperature, or a thermoregulatory increase in "Vo2 during skin-toskin care compared with incubator care.
METHODS Inborn preterm infants with a birth weight of less than 1500 gm were examined every morning until a postnatal age of 7 days, if they were eligible for skin-to-skin care. Eligibility criteria were (1) not undergoing mechanical ventilation, (2) birth weight appropriate for gestational age (>3rd percentile), (3) no symptomatic sepsis, (4) cardiorespiratory stability, (5) no hypothermia, and (6) parental consent. When eligibility criteria were met, the study was scheduled for the afternoon of the same day. The study protocol guaranteed that the measurement always started at the same time of day, 1 hour after the last feeding, and did not interfere with the 3-hourly nursing routine. At 3 PM the infant was fed by gavage (6.5 +_ 3.9 ml/kg per feeding; mean _+ SD) and the temperature probes were attached. Beginning at 4 PM the infants were studied for 60 minutes before skin-to-skin care, while lying prone and naked except for a diaper in a double-walled incubator (model 8000, Draeger AG, Ltibeck, Germany) with air temperature control. We chose a thermoneutral incubator temperature according to Hey and Katz, 4 adjusted for the high humidity of 80% that we were using. Incubator air temperature was not affected by gas sampling for the Vo2 and Vco2 measurements. At 5 PM the infant was then placed prone on the mother's skin between her breasts and covered with a blanket for 60 minutes of skin-to-skin care. The measurements were interrupted by the infant's transfer to the mother for 9 -+ 4 minutes. The mother was sitting in a comfortable chair, room temperature in the intensive care unit was maintained at 26 ° C, and relative room air humidity at 40%. At 6 PM, after skin-to-skin care, the infant was transferred back to the incubator and fed by gavage, and measurements were continued for 60 minutes. 4o2 and carbon dioxide production were measured with open flow-through indirect calorimetry.7 The infant's expired air was sampled in a constant flow of room air drawn through a face mask held 2 to 5 mm in front of the infant' s nose and mouth at a constant flow rate of 3 L/rain. The oxygen and carbon dioxide content of the mixed expired air was measured with a Deltatrac II metabolic monitor (Datex Di-
B a u e r et al.
241
vision Insmamentarium Corp., Helsinki, Finland). It consists of a paramagnetic oxygen analyzer with automatically compensated baseline drift, an infrared CO2 sensor, and a constant-flow generator. Stability, resolution, and linearity of gas analyzers and flow generators have been thoroughly tested. 8 From the continuous 4o2 and Vco2 measurements an average value for each minute was calculated and recorded. We validated the use of the face mask for VLBW infants by quantitative methanol combustion in a minibumer. The mean experimental error for the Vo2 measurement was 2% _+ 2%. 9 Infants who needed an increased inspired oxygen concentration were given oxygen during skin-to-skin care via a tube introduced through a side hole into the breath-sampling face mask. Under these conditions, expired air was sampled completely, but 4o2 cannot be directly measured because the inspiratory oxygen concentration is unstable. Even in the incubator, increased inspiratory oxygen concentrations are so unstable that Vo2 measurements are difficult. 1° In infants with increased inspired oxygen concentration, we therefore calculated 402 from CO2 production, estimating respiratory quotient from the composition of nutritional intake (food quotient) ll: Food quotient
( P x 0.781) + (F x 1.427) + (C x 0.746) x 0.966) + (F ~ ~ 0.746)
Intakes of protein (P), fat (F), and carbohydrates (C) are expressed in grams per day. For enteral intake we used a digestibility factor of 0.88 for protein and of 0.84 for fat to account for incomplete absorption. The constants are the volumes of CO2 produced and 02 consumed during oxidation, expressed in liters per gram. The 4o2 is then calculated as Vco2/food quotient. In a Previous study we showed that calculated Vo2 agrees closely with measured Vo2.12 The infants were started on parenteral nutrition (glucose and amino acids) and enteral bolus feedings on day 1 (mother's milk or preterm formula). Intravenously administered lipids were added on day 2. Between day 3 and day 7, caloric intake was increased from 55 to 80 kcal/kg per day, with a constant relation of carbohydrates, protein, and lipid of 65:10:25%. On the day of the study, 80% -+ 2% of the infants' nutrition was parenteral. Rectal temperature was measured with a temperature probe inserted 2 cm into the rectum, and peripheral skin temperature was measured with a probe taped to the sole of the right foot. To minimize the influence of ambient air temperature on the temperature probe, we covered the probe with an insulating tape made of polyethylene foam. Air temperature in the incubator was measured with a temperature probe hanging 10 cm above the infant, and mattress temperature with a probe taped to the mattress 3 cm away from the infant. The mother's skin temperature was mea-
242
Bauer et al.
The Journal of Pediatrics February 1997
Table. Body temperatures, oxygen consumption, and environmental temperatures before (60 minutes), during (60 minutes), and after (60 minutes) skin-to-skin care Skin-to-skin care
Body temperatures Rectal temperature (°C) Skin temperature (foot) (°C) Oxygen consumption(ml/kg per min) Environmentaltemperatures Air temperature (°C) Mattress temperature (°C) Mother's skin temperature (°C) Heart rate (beats/rain) Time in quiet sleep (% of total)
Before (incubator)
During
After (incubator)
36.9 + 0.3 35.0 -+ 0.7 5.8 -+ 0.8
37.1 + 0.4* 35.6 -+ 1.0' 6.1 -+ 0.9
36.9 -+ 0.3 35.1 -+ 0.7 5.8 -+ 1.0
34.4 -+ 0.6 34.0 -+ 0.6
34.3 -+ 1.4
34.5 -+ 0.8 33.9 -+ 0.6
151 -+ 9 93 -+7
34.3 -+ 1.0 151 -+ l0 96---7
151 -+ 11 91 -+9
Valuesare meansof minute-by-minutemeasurements.Airtemperatureduringskin-to-skincarewas measuredbetweeninfantandblanket,and mother'sskintemperature was measuredon the right upper aspect of her chest, closeto the infant. *p <0.01 versusbefore.
sured with a temperature probe taped to the skin with insulating tape in the mid-clavicular line 2 cm below the right clavicle. Air temperature under the towel was measured with a probe housed in the center of a short paper tube to prevent direct contact with the skin. The outer surface of the tube was reflecting aluminum foil. Temperatures, heart rate, and hemoglobin oxygen saturation (pulse oximeter) were measured continuously (patient monitor CMS 5000, Hewlett Packard GmbH, Bad Homburg, Germany). The infant's activity was graded every minute from +5 (crying) to - 4 (eyes closed, no movement) by a bedside observer using a modified Brueck score. 13 The time spent in sleep was the observation time with a Bmeck score of -3 (eyes closed, facial movements) or - 4 (eyes closed, no movement). Written parental consent was obtained for each infant, and the study was approved by the hospital' s institutionalreview board. Data were analyzed with the SPSS statistical software (SPSS Inc., Chicago, Ill.). Mean values of the three study periods were compared by analysis of variance with repeated measures. Sample size was calculated to detect a more than 10% change in ) o 2 with an alpha error of 0.05 and a beta error of 0.1.
RESULTS In the 9-month recruiting period, 44 preterm infants weighing less than 1500 gm were born at our hospital; 22 infants were included in this study, 16 were excluded because they were still undergoing mechanical ventilation at the age of 7 days, and 6 were excluded because birth weight was at less than the 3rd percentile. The 22 eligible infants (median birth weight, 1200 gm [range, 772 to 1380]; median gestational age, 29 weeks [range, 25 to 31]) were studied
during their first skin-to-skin care at a median postnatal age of 4 days (range, 3 to 7) and a median body weight of 1080 gm (range, 702 to 1400). Four of the infants weighed less than 1000 gm on the day of the study. Six of the infants had increased inspired oxygen concentrations up to 30%. Before skin-to-skin care, body temperatures in the incubator were normal and the mean ) o 2 was 5.8 ml/kg per minute. During skin-to-skin care the mean ) o 2 was not increased. The mean rectal temperature was 0.2 ° C (p <0.01) and peripheral skin temperature was 0.6 ° C (p <0.01) higher during skin-to-skincare than during the preceding hour in the incubator (Table). The temperature gradient between rectal and peripheral skin temperature was significantly narrower during skin-to-skin care (1.5°_ + 0.9 ° C) than before (1.9 ° + 0.6 ° C) or afterward (1.9 ° _+ 0.6 ° C) (p = 0.044). The temperature gradient became significantly narrower, from a mean value of 2.2 ° -+ 1.1 ° C in the first 15 minutes to a mean of 1.1 ° -+ 0.7 ° C in the last 15 minutes of skinto-skin care (p <0.001) (Figure). Changes in body temperatures and ) o 2 were not related to birth weight, gestational age, postnatal weight, or age. After the skin-to-skin care period, body temperatures with the infant back in the incubator returned to values recorded before skin-to-skin care. Mean temperatures to which the infant was exposed during skin-to-skin care (air temperature between infant and blanket, and mother's skin temperature) were not lower than the respective temperatures in the incubator (incubator air and mattress temperature) (Table). There was no change in heart rate. The infants spent the same amount of time in sleep in all three study periods (Table).
The Journal of Pediatrics Volume 130, Number 2
Bauer et al.
DISCUSSION
Contrary to our hypothesis, we found that during 60 minutes of skin-to-skin care in spontaneously breathing, clinicaily stable preterm infants weighing less than 1500 gm the mean rectal temperature and the peripheral skin temperature were higher than during care in a thermoneutral incubator, and Vo2 was not increased. Our findings imply that these infants experienced no cold stress during skin-to-skin care. Nevertheless, this intervention should be used with caution in preterm infants weighing less than 1000 gin, because we studied only four such infants. Cold exposure is harmful to preterm infants. 14 Therefore they are cared for in a thermoneutral environment in which they can maintain a normal body temperature without an increase in heat production and 402 and without thermoregulatory peripheral vasoconstriction. Thermoneutral conditions in incubators are well established.4'15 Skin-to-skin care, however, was introduced for VLBW infants despite concerns that they are exposed to subthermoneutral temperatures during this type of intervention. 3 In previous studies of physiologic effects of skin-to-skin care in preterm infants, 5, 6 402 was not measured and environmental and body temperatures were not measured continuously. In our study we measured rectal temperature continuously. Rectal temperature was normal before skin-to-skin care and then slowly increased so that mean rectal temperature during skin-to-skin care was 0.2 ° C higher than in the incubator. We continuously measured peripheral skin temperature at the sole of the right foot. In a thermoneutral environment the skin temperature of the foot is 34 ° to 35 ° C and decreases to 32 ° to 34 ° C because of thermoregulatory constriction of skin blood vessels if temperatures are below the thermoneutral zone. 15, 16 We found that skin temperature of the foot increased during skin-to-skin care. We continuously measured 402. The mean 4o2 was 5.8 ml/kg per minute in the incubator before skin-to-skin care. This was in the range reported for infants in a thermoneutral environment.15, 17,18 There was no increase in 4o2 during skin-to-skin care or after transfer back to the incubator. Vo2 is influenced by many factors other than thermoregulation19: by postnatal age, by bolus feedings, by diurnal variations, by activity, and by the method of measurement. To ensure that these did not influence our results, we considered the following aspects in our study protocol: We studied a homogeneous group of spontaneously breathing, clinically stable A G A preterm infants. Each infant was studied when skin-to-skin care was done for the first time, and the age at study ranged from 3 to 7 days. We found no influence of birth weight, gestational age, postnatal weight, or age on our results. 402 increases postprandially in infants receiving full oral feedings.2° The infants in our study
243
m_2L
tO
kgmin
8-
E ffl ¢0
0¢-
4-
×
2-
0
Incubator
Skin-to-Skin
Incubator
Skin-to-Skin
Incubator
(°C)~
:~'~
Q.
38t ~rectal temperature 36
,
skin temperature (foot)
>, 34 0
Incubator
m 0
i 20
J 40
i 60
80
100
120
i
i
i
140
160
180
200
Time (minutes)
Figure. Five-minute averages of oxygen consumption, rectal temperature, and skin temperature of the foot before, during, and after skin-to-skin care (mean _+ SD). received nutrition mainly by constant intravenous infusion, supplemented with only small oral feedings; therefore a relevant postprandial increase in V02 was unlikely. Nevertheless, to minimize potential interference by feedings, we started the study I hour after the last feeding, and there was no feeding before the beginning of skin-to-skin care. We observed no increase in V02 after the feeding given after skin-to-skin care. To exclude interference of diurnal variations on V02, we started all studies at the same time of day. Activity levels were continuously monitored and scored, and the infants spent the same amount of time in quiet sleep in all three study periods. Breath sampling with a hood covering the infant's entire head changes the thermal environment. 21 Therefore we used a small face mask, which covered only the infant's mouth and nose. We have validated this face mask for 402 measurements by quantitative methanol burning. 9 The face mask did not increase the infant's activity because it was held by hand in front of the face without actually touching it. In conclusion, the infants studied maintained and even slightly increased their rectal and their peripheral skin temperature during skin-to-skin care without an increase in heat production. We conclude from these results that a period of 60 minutes of skin-to-skin care was not a cold stress
244
Bauer et al.
for spontaneously breathing, clinically stable preterm infants weighing less than 1500 grn and less than 1 week of age. REFERENCES 1. Whitelaw A, Sleath K. Myth of the marsupial mother: home care of very low birth weight babies in Bogota, Colombia. Lancet 1985;1:1206-8. 2. Anderson GC. Sldn-to-skin (kangaroo) care for preterm infants: review of the literature. J Perinatol 1991;11:216-26. 3. Sinclair JC. Management of the thermal environment. In: Sinclair JC; Bracken MB, editors. Effective care of the newborn infant. Oxford: Oxford University Press, 1992:40-58. 4. Hey EN, Katz G. The optimum thermal environment for naked babies. Arch Dis Child 1970;45:328-34. 5. De Leeuw R, Colin EM, Dnnnebier EA, Mirmiran M. Physiological effects of kangaroo care in very small preterm infants. Biol Neonate 1991;59:149-55. 6. Acolet D, Sleath K, Whitelaw A. Oxygenation, heart rate and temperature in very low birthweight infants during skin-to-skin contact with their mothers. Acta Paediatr Scand 1989;78:189-93. 7. Lister G, Hoffman JIE, Rudolph AM. Oxygen uptake in infants and children: a simple method for measurement. Pediatrics 1974;53:656-621 8. Takala J, Kein~nen O, VRis~nen P, Karl A. Measurement of gas exchange :in intensive care: laboratory and clinical validation of a new device. Crit Care Med 1989;17:1041-7. 9. Bauer K, Uhrig C, Sperling P, Versmold HT. Development of an "artificial preterm infant" to validate gas sampling devices for open flow through indirect calorimetry systems [abstract]. Pediatr Res 1995;37:302A. 10. Kalhan SC, Denne SC. Energy consumption in infants with bronchopulmonary dysplasia. J Pediatr 1990;116:662-4.
The Journal of Pediatrics February 1997
11. Black AE, Prentice AM, Coward WA. Use of food quotient to predict respiratory quotients for the doubly labeled water method of measuring energy expenditure. Hum Nutr Clin Nutr 1986;40C:381-91. 12. Bauer K, Dieckmann A, Versmold H. The calculation of energy expenditure from CO2-production in preterm infants is improved by estimating respiratory quotient from nutritional intake (food quotient) [abstract]. Pediatr Res 1994;36: 5A. 13. Brueck K, Parrnalee AH Jr, Brick M. Neutral temperature range and range of thermal comfort in premature infants. Biol Neonate 1962;4:32-8. 14. BuetowKC, Klein W. Effect of maintenance of "normal" skin temperature on survival of infants of low birth weight. Pediatrics 1964;34:163-70. 15. Bell EF, Gray JC, Weinstein MR, Oh W. The effects of thermal environment on heat balance and insensible water loss in low-birth-weight infants. J Pediatr 1980;96:452-9. 16. Matin SW, Baumgart S. Optimal thermal management for low birth weight infants nursed under high-powered radiant warmers. Pediatrics 1987;79:47-54. 17. Hey EN. The relation between environmental temperature and Vo2 in the newborn baby. J Physiol 1969;200:589-603. 18. LeBlanc MH. Relative efficacy of an incubator and an open warmer in producing thermoneutrality for the small premature infant. Pediatrics 1982;69:439-45. 19. Brooke OG. Energy expenditure in the fetus and neonate: sources of variability. Acta Paediatr Scand 1985;Suppl 319:12834. 20. Stothers JK, Warner RM. Effect of feeding on neonatal Vo2. Arch Dis Child 1979;54:415-20. 21. Stothers JK. Head insulation and heat loss in the newborn. Arch Dis Child 1981;56:530-4.
Background: More and progressively smaller preterm infants are taken out of the incubator and placed skin to skin on their mother's chest to promote bonding, despite concerns that the infants are exposed to cold during this intervention. Objective: To test the hypothesis that skin-to-skin care is a cold stress for preterm infants weighing less than 1500 gm, with a decrease in rectal temperature, a decrease in peripheral skin temperature, or an increase in oxygen consumption compared with conditions monitored during incubator care. Study design: We studied 22 stable, spontaneously breathing preterm infants weighing less than 1500 gm (appropriate in size for gestational age), who had their first skin-to-skin care in the first week of life. We continuously measured rectal temperature, peripheral skin temperature (foot), and oxygen consumption (indirect calorimetry) for I hour in a thermoneutral incubator, during I hour of skin-toskin care, and for another hour in the incubator. Mean values for the three periods were compared by analysis of variance. Results:During skin-to-skin care the mean rectal temperature was 0.2 ° C (p <0.0 I) and the peripheral skin temperature was 0.6 ° C (p <0.01) higher than during the preceding hour in the incubator. Back in the incubator, body temperatures returned to values recorded before skin-to-skin care. Oxygen consumption during skin-to-skin care (6. I ___0.9 ml/kg per minute)was not significantly higher than in the incubator (5.8 _ 0.8 ml/kg per minute). Conclusion: For stable preterm infants weighing less than 1500 gm and less than I week of age, I hour of skin-to-skin care is not a cold stress compared with care in a thermoneutral incubator. (J Pediatr 1997;130:240-4)
Skin-to-skin (kangaroo) care, with preterm infants' placed on their mother's chest, was started for want of incubators in Bogota, Colombia.1 The hope of promoting mother-infant bonding led to a widespread acceptance of skin-to-skin care Submitted for publication Sept. 14, 1995; accepted Aug. 1, 1996. Reprint requests: Karl Bauer, MD, Kinderklinik, Universit~tsklinikum Benjamin Franklin, Freie Universit~it Berlin, Hindenburgdamm 30, 12200 Berlin, Germany. Copyright © 1997 by Mosby-Year Book, Inc. 0022-3476/97/$5.00 + 0 9/21/77289
240
in industrialized countries. 2 Even very low birth weight infants were exposed to this intervention despite concerns that the mother's skin temperature is too low to provide a thermoneutral environment for a VLBW infant. 3 A thermoneutral environment is regarded as "the optimum thermal environment for naked babies,"4 because there is no increase in body metabolism related to excessive heat or excessive cold and body temperature is maintained normal without a thermoregulatory increase in oxygen consumption. For VLBW infants, no measurements of V02 during skin-to-skin care exist, and there are only incomplete data on body tempera-
The Journal of Pediatrics Volume 130, Number 2
AGA
VCO2 Vo2 VLBW
Appropriate [in size] for gestational age Carbon dioxide production Oxygen consumption Very low birth weight
tures.5, 6 Therefore the purpose of this study was to test the hypothesis that skin-to-skin care is a cold stress for stable preterm infants weighing less than 1500 gm, with a decrease in rectal temperature, a decrease in peripheral skin temperature, or a thermoregulatory increase in "Vo2 during skin-toskin care compared with incubator care.
METHODS Inborn preterm infants with a birth weight of less than 1500 gm were examined every morning until a postnatal age of 7 days, if they were eligible for skin-to-skin care. Eligibility criteria were (1) not undergoing mechanical ventilation, (2) birth weight appropriate for gestational age (>3rd percentile), (3) no symptomatic sepsis, (4) cardiorespiratory stability, (5) no hypothermia, and (6) parental consent. When eligibility criteria were met, the study was scheduled for the afternoon of the same day. The study protocol guaranteed that the measurement always started at the same time of day, 1 hour after the last feeding, and did not interfere with the 3-hourly nursing routine. At 3 PM the infant was fed by gavage (6.5 +_ 3.9 ml/kg per feeding; mean _+ SD) and the temperature probes were attached. Beginning at 4 PM the infants were studied for 60 minutes before skin-to-skin care, while lying prone and naked except for a diaper in a double-walled incubator (model 8000, Draeger AG, Ltibeck, Germany) with air temperature control. We chose a thermoneutral incubator temperature according to Hey and Katz, 4 adjusted for the high humidity of 80% that we were using. Incubator air temperature was not affected by gas sampling for the Vo2 and Vco2 measurements. At 5 PM the infant was then placed prone on the mother's skin between her breasts and covered with a blanket for 60 minutes of skin-to-skin care. The measurements were interrupted by the infant's transfer to the mother for 9 -+ 4 minutes. The mother was sitting in a comfortable chair, room temperature in the intensive care unit was maintained at 26 ° C, and relative room air humidity at 40%. At 6 PM, after skin-to-skin care, the infant was transferred back to the incubator and fed by gavage, and measurements were continued for 60 minutes. 4o2 and carbon dioxide production were measured with open flow-through indirect calorimetry.7 The infant's expired air was sampled in a constant flow of room air drawn through a face mask held 2 to 5 mm in front of the infant' s nose and mouth at a constant flow rate of 3 L/rain. The oxygen and carbon dioxide content of the mixed expired air was measured with a Deltatrac II metabolic monitor (Datex Di-
B a u e r et al.
241
vision Insmamentarium Corp., Helsinki, Finland). It consists of a paramagnetic oxygen analyzer with automatically compensated baseline drift, an infrared CO2 sensor, and a constant-flow generator. Stability, resolution, and linearity of gas analyzers and flow generators have been thoroughly tested. 8 From the continuous 4o2 and Vco2 measurements an average value for each minute was calculated and recorded. We validated the use of the face mask for VLBW infants by quantitative methanol combustion in a minibumer. The mean experimental error for the Vo2 measurement was 2% _+ 2%. 9 Infants who needed an increased inspired oxygen concentration were given oxygen during skin-to-skin care via a tube introduced through a side hole into the breath-sampling face mask. Under these conditions, expired air was sampled completely, but 4o2 cannot be directly measured because the inspiratory oxygen concentration is unstable. Even in the incubator, increased inspiratory oxygen concentrations are so unstable that Vo2 measurements are difficult. 1° In infants with increased inspired oxygen concentration, we therefore calculated 402 from CO2 production, estimating respiratory quotient from the composition of nutritional intake (food quotient) ll: Food quotient
( P x 0.781) + (F x 1.427) + (C x 0.746) x 0.966) + (F ~ ~ 0.746)
Intakes of protein (P), fat (F), and carbohydrates (C) are expressed in grams per day. For enteral intake we used a digestibility factor of 0.88 for protein and of 0.84 for fat to account for incomplete absorption. The constants are the volumes of CO2 produced and 02 consumed during oxidation, expressed in liters per gram. The 4o2 is then calculated as Vco2/food quotient. In a Previous study we showed that calculated Vo2 agrees closely with measured Vo2.12 The infants were started on parenteral nutrition (glucose and amino acids) and enteral bolus feedings on day 1 (mother's milk or preterm formula). Intravenously administered lipids were added on day 2. Between day 3 and day 7, caloric intake was increased from 55 to 80 kcal/kg per day, with a constant relation of carbohydrates, protein, and lipid of 65:10:25%. On the day of the study, 80% -+ 2% of the infants' nutrition was parenteral. Rectal temperature was measured with a temperature probe inserted 2 cm into the rectum, and peripheral skin temperature was measured with a probe taped to the sole of the right foot. To minimize the influence of ambient air temperature on the temperature probe, we covered the probe with an insulating tape made of polyethylene foam. Air temperature in the incubator was measured with a temperature probe hanging 10 cm above the infant, and mattress temperature with a probe taped to the mattress 3 cm away from the infant. The mother's skin temperature was mea-
242
Bauer et al.
The Journal of Pediatrics February 1997
Table. Body temperatures, oxygen consumption, and environmental temperatures before (60 minutes), during (60 minutes), and after (60 minutes) skin-to-skin care Skin-to-skin care
Body temperatures Rectal temperature (°C) Skin temperature (foot) (°C) Oxygen consumption(ml/kg per min) Environmentaltemperatures Air temperature (°C) Mattress temperature (°C) Mother's skin temperature (°C) Heart rate (beats/rain) Time in quiet sleep (% of total)
Before (incubator)
During
After (incubator)
36.9 + 0.3 35.0 -+ 0.7 5.8 -+ 0.8
37.1 + 0.4* 35.6 -+ 1.0' 6.1 -+ 0.9
36.9 -+ 0.3 35.1 -+ 0.7 5.8 -+ 1.0
34.4 -+ 0.6 34.0 -+ 0.6
34.3 -+ 1.4
34.5 -+ 0.8 33.9 -+ 0.6
151 -+ 9 93 -+7
34.3 -+ 1.0 151 -+ l0 96---7
151 -+ 11 91 -+9
Valuesare meansof minute-by-minutemeasurements.Airtemperatureduringskin-to-skincarewas measuredbetweeninfantandblanket,and mother'sskintemperature was measuredon the right upper aspect of her chest, closeto the infant. *p <0.01 versusbefore.
sured with a temperature probe taped to the skin with insulating tape in the mid-clavicular line 2 cm below the right clavicle. Air temperature under the towel was measured with a probe housed in the center of a short paper tube to prevent direct contact with the skin. The outer surface of the tube was reflecting aluminum foil. Temperatures, heart rate, and hemoglobin oxygen saturation (pulse oximeter) were measured continuously (patient monitor CMS 5000, Hewlett Packard GmbH, Bad Homburg, Germany). The infant's activity was graded every minute from +5 (crying) to - 4 (eyes closed, no movement) by a bedside observer using a modified Brueck score. 13 The time spent in sleep was the observation time with a Bmeck score of -3 (eyes closed, facial movements) or - 4 (eyes closed, no movement). Written parental consent was obtained for each infant, and the study was approved by the hospital' s institutionalreview board. Data were analyzed with the SPSS statistical software (SPSS Inc., Chicago, Ill.). Mean values of the three study periods were compared by analysis of variance with repeated measures. Sample size was calculated to detect a more than 10% change in ) o 2 with an alpha error of 0.05 and a beta error of 0.1.
RESULTS In the 9-month recruiting period, 44 preterm infants weighing less than 1500 gm were born at our hospital; 22 infants were included in this study, 16 were excluded because they were still undergoing mechanical ventilation at the age of 7 days, and 6 were excluded because birth weight was at less than the 3rd percentile. The 22 eligible infants (median birth weight, 1200 gm [range, 772 to 1380]; median gestational age, 29 weeks [range, 25 to 31]) were studied
during their first skin-to-skin care at a median postnatal age of 4 days (range, 3 to 7) and a median body weight of 1080 gm (range, 702 to 1400). Four of the infants weighed less than 1000 gm on the day of the study. Six of the infants had increased inspired oxygen concentrations up to 30%. Before skin-to-skin care, body temperatures in the incubator were normal and the mean ) o 2 was 5.8 ml/kg per minute. During skin-to-skin care the mean ) o 2 was not increased. The mean rectal temperature was 0.2 ° C (p <0.01) and peripheral skin temperature was 0.6 ° C (p <0.01) higher during skin-to-skincare than during the preceding hour in the incubator (Table). The temperature gradient between rectal and peripheral skin temperature was significantly narrower during skin-to-skin care (1.5°_ + 0.9 ° C) than before (1.9 ° + 0.6 ° C) or afterward (1.9 ° _+ 0.6 ° C) (p = 0.044). The temperature gradient became significantly narrower, from a mean value of 2.2 ° -+ 1.1 ° C in the first 15 minutes to a mean of 1.1 ° -+ 0.7 ° C in the last 15 minutes of skinto-skin care (p <0.001) (Figure). Changes in body temperatures and ) o 2 were not related to birth weight, gestational age, postnatal weight, or age. After the skin-to-skin care period, body temperatures with the infant back in the incubator returned to values recorded before skin-to-skin care. Mean temperatures to which the infant was exposed during skin-to-skin care (air temperature between infant and blanket, and mother's skin temperature) were not lower than the respective temperatures in the incubator (incubator air and mattress temperature) (Table). There was no change in heart rate. The infants spent the same amount of time in sleep in all three study periods (Table).
The Journal of Pediatrics Volume 130, Number 2
Bauer et al.
DISCUSSION
Contrary to our hypothesis, we found that during 60 minutes of skin-to-skin care in spontaneously breathing, clinicaily stable preterm infants weighing less than 1500 gm the mean rectal temperature and the peripheral skin temperature were higher than during care in a thermoneutral incubator, and Vo2 was not increased. Our findings imply that these infants experienced no cold stress during skin-to-skin care. Nevertheless, this intervention should be used with caution in preterm infants weighing less than 1000 gin, because we studied only four such infants. Cold exposure is harmful to preterm infants. 14 Therefore they are cared for in a thermoneutral environment in which they can maintain a normal body temperature without an increase in heat production and 402 and without thermoregulatory peripheral vasoconstriction. Thermoneutral conditions in incubators are well established.4'15 Skin-to-skin care, however, was introduced for VLBW infants despite concerns that they are exposed to subthermoneutral temperatures during this type of intervention. 3 In previous studies of physiologic effects of skin-to-skin care in preterm infants, 5, 6 402 was not measured and environmental and body temperatures were not measured continuously. In our study we measured rectal temperature continuously. Rectal temperature was normal before skin-to-skin care and then slowly increased so that mean rectal temperature during skin-to-skin care was 0.2 ° C higher than in the incubator. We continuously measured peripheral skin temperature at the sole of the right foot. In a thermoneutral environment the skin temperature of the foot is 34 ° to 35 ° C and decreases to 32 ° to 34 ° C because of thermoregulatory constriction of skin blood vessels if temperatures are below the thermoneutral zone. 15, 16 We found that skin temperature of the foot increased during skin-to-skin care. We continuously measured 402. The mean 4o2 was 5.8 ml/kg per minute in the incubator before skin-to-skin care. This was in the range reported for infants in a thermoneutral environment.15, 17,18 There was no increase in 4o2 during skin-to-skin care or after transfer back to the incubator. Vo2 is influenced by many factors other than thermoregulation19: by postnatal age, by bolus feedings, by diurnal variations, by activity, and by the method of measurement. To ensure that these did not influence our results, we considered the following aspects in our study protocol: We studied a homogeneous group of spontaneously breathing, clinically stable A G A preterm infants. Each infant was studied when skin-to-skin care was done for the first time, and the age at study ranged from 3 to 7 days. We found no influence of birth weight, gestational age, postnatal weight, or age on our results. 402 increases postprandially in infants receiving full oral feedings.2° The infants in our study
243
m_2L
tO
kgmin
8-
E ffl ¢0
0¢-
4-
×
2-
0
Incubator
Skin-to-Skin
Incubator
Skin-to-Skin
Incubator
(°C)~
:~'~
Q.
38t ~rectal temperature 36
,
skin temperature (foot)
>, 34 0
Incubator
m 0
i 20
J 40
i 60
80
100
120
i
i
i
140
160
180
200
Time (minutes)
Figure. Five-minute averages of oxygen consumption, rectal temperature, and skin temperature of the foot before, during, and after skin-to-skin care (mean _+ SD). received nutrition mainly by constant intravenous infusion, supplemented with only small oral feedings; therefore a relevant postprandial increase in V02 was unlikely. Nevertheless, to minimize potential interference by feedings, we started the study I hour after the last feeding, and there was no feeding before the beginning of skin-to-skin care. We observed no increase in V02 after the feeding given after skin-to-skin care. To exclude interference of diurnal variations on V02, we started all studies at the same time of day. Activity levels were continuously monitored and scored, and the infants spent the same amount of time in quiet sleep in all three study periods. Breath sampling with a hood covering the infant's entire head changes the thermal environment. 21 Therefore we used a small face mask, which covered only the infant's mouth and nose. We have validated this face mask for 402 measurements by quantitative methanol burning. 9 The face mask did not increase the infant's activity because it was held by hand in front of the face without actually touching it. In conclusion, the infants studied maintained and even slightly increased their rectal and their peripheral skin temperature during skin-to-skin care without an increase in heat production. We conclude from these results that a period of 60 minutes of skin-to-skin care was not a cold stress
244
Bauer et al.
for spontaneously breathing, clinically stable preterm infants weighing less than 1500 grn and less than 1 week of age. REFERENCES 1. Whitelaw A, Sleath K. Myth of the marsupial mother: home care of very low birth weight babies in Bogota, Colombia. Lancet 1985;1:1206-8. 2. Anderson GC. Sldn-to-skin (kangaroo) care for preterm infants: review of the literature. J Perinatol 1991;11:216-26. 3. Sinclair JC. Management of the thermal environment. In: Sinclair JC; Bracken MB, editors. Effective care of the newborn infant. Oxford: Oxford University Press, 1992:40-58. 4. Hey EN, Katz G. The optimum thermal environment for naked babies. Arch Dis Child 1970;45:328-34. 5. De Leeuw R, Colin EM, Dnnnebier EA, Mirmiran M. Physiological effects of kangaroo care in very small preterm infants. Biol Neonate 1991;59:149-55. 6. Acolet D, Sleath K, Whitelaw A. Oxygenation, heart rate and temperature in very low birthweight infants during skin-to-skin contact with their mothers. Acta Paediatr Scand 1989;78:189-93. 7. Lister G, Hoffman JIE, Rudolph AM. Oxygen uptake in infants and children: a simple method for measurement. Pediatrics 1974;53:656-621 8. Takala J, Kein~nen O, VRis~nen P, Karl A. Measurement of gas exchange :in intensive care: laboratory and clinical validation of a new device. Crit Care Med 1989;17:1041-7. 9. Bauer K, Uhrig C, Sperling P, Versmold HT. Development of an "artificial preterm infant" to validate gas sampling devices for open flow through indirect calorimetry systems [abstract]. Pediatr Res 1995;37:302A. 10. Kalhan SC, Denne SC. Energy consumption in infants with bronchopulmonary dysplasia. J Pediatr 1990;116:662-4.
The Journal of Pediatrics February 1997
11. Black AE, Prentice AM, Coward WA. Use of food quotient to predict respiratory quotients for the doubly labeled water method of measuring energy expenditure. Hum Nutr Clin Nutr 1986;40C:381-91. 12. Bauer K, Dieckmann A, Versmold H. The calculation of energy expenditure from CO2-production in preterm infants is improved by estimating respiratory quotient from nutritional intake (food quotient) [abstract]. Pediatr Res 1994;36: 5A. 13. Brueck K, Parrnalee AH Jr, Brick M. Neutral temperature range and range of thermal comfort in premature infants. Biol Neonate 1962;4:32-8. 14. BuetowKC, Klein W. Effect of maintenance of "normal" skin temperature on survival of infants of low birth weight. Pediatrics 1964;34:163-70. 15. Bell EF, Gray JC, Weinstein MR, Oh W. The effects of thermal environment on heat balance and insensible water loss in low-birth-weight infants. J Pediatr 1980;96:452-9. 16. Matin SW, Baumgart S. Optimal thermal management for low birth weight infants nursed under high-powered radiant warmers. Pediatrics 1987;79:47-54. 17. Hey EN. The relation between environmental temperature and Vo2 in the newborn baby. J Physiol 1969;200:589-603. 18. LeBlanc MH. Relative efficacy of an incubator and an open warmer in producing thermoneutrality for the small premature infant. Pediatrics 1982;69:439-45. 19. Brooke OG. Energy expenditure in the fetus and neonate: sources of variability. Acta Paediatr Scand 1985;Suppl 319:12834. 20. Stothers JK, Warner RM. Effect of feeding on neonatal Vo2. Arch Dis Child 1979;54:415-20. 21. Stothers JK. Head insulation and heat loss in the newborn. Arch Dis Child 1981;56:530-4.