Skin Temperatures at the Nape in Infants at High Altitude DARNA L. DUFOUR,, MICHAEL A. LITTLE2 AND R. BROOKE THOMAS3 2 Department of Anthropology, State University of New York at Binghamton, Binghamton, New York 13901 and 3 Department of Anthropology, Cornell University, Ithaca, New York 14850
K E Y WORDS Skin temperatures . Infants . Altitude adipose tissue . Peru.
'
Brown
ABSTRACT Skin temperatures were measured on three Quechua Indian infants resident at 4,000 meters above sea level in Peru. Nape temperatures were warmer than other skin sites, suggesting that the brown adipose tissue associated with non-shivering thermogenesis is metabolically active despite the reduced oxygen availability at high altitude. The question of the role of non-shivering thermogenesis in infant thermoregulation under the covariant stresses of hypoxia and cold is still open.
Increasing attention has been focused on the mechanism and role of non-shivering thermogenesis (NST) in infant thermoregulation. When exposed to temperatures below thermoneutrality, human infants and certain newborn and adult mammals can increase heat production without shivering (Bruck, '61, '70a). The primary tissue responsible for this increase in metabolic rate has been identified as brown adipose tissue (BAT) (Bruck, '70b; Smith and Horowitz, '69). Sites of BAT deposition are the abdomen, and the cervical, interscapular, and axillary regions. Several studies demonstrated that on cold exposure, the nape and interscapular regions of infants were relatively warmer than other skin sites (Ahern and Hull, '66; Perlstein et al., '70; Perlstein et al., '72; Silverman et al., '64). The increase in oxygen consumption normally accompanying cold exposure is suppressed in some small mammals and their newborn under hypoxic conditions (Dawkins and Hull, '64; Roberts et al., '69; Blatteis and Gilbert, '74). This decreased metabolic response is thought to be due to the selective depression of NST (Roberts et al., '69; Blatteis and Gilbert, '74). Roberts et al. ('69), however, have shown for the deer mouse (Peromyscus) that after acclimatization to hypoxia, heat production under cold exposure returns to normal. This is accompanied by BAT hyperplasia and a n increase AM. J. PHYS. ANTHROP.,44: 91-94
in BAT in vitro respiration (q0,). These authors also compared deer mice native to sea level with a wild population native to 3,800 meters. Despite the slight depression of the 90, of BAT homogenate at altitude, the ratio of BAT to body weight and the estimated heat production of BAT were signficantly greater in the high altitude population naturally exposed to both hypoxia and cold ambient conditions. Human infants similarly respond to acute hypoxia with a decrease in oxygen consumption (Rylander, '69). The effects of the covariant stresses of hypoxia and cold on infant thermoregulation, however, are not well understood. In a preliminary attempt to assess thermal conditions in human infants naturally exposed to the reduced oxygen pressure and cold ambient conditions of high altitude, we measured skin temperatures on three infants native to the high Andes of southern Peru. The surface of the nape was chosen as a n indirect measure of heat production by BAT at this site. METHODS
The subjects were three infants ages 8 (Subject 1), 9 (Subject 2), and 15 (Subject 3) months whose parents were Quechua 1 Funds were provided by the Research Foumdation of the State Universityof New York (40-7225-A) and Cornell University. This work is a part of the U. S. contribution to the International Biological Program.
91
92
D. L. DUFOUR, M. A. LITTLE AND R. B. THOMAS
Indian farmer/herders resident in the town respective courtyards. Mothers of the three of Nunoa, Peru, located on the southern expended a variable amount of effort in Peruvian altiplano at an altitude of 4,000 keeping the infants in dry clothing and in meters. At this altitude, the partial pres- the warmth of direct sunshine. The infants sure of oxygen is about 60% that at sea were all dressed in customary clothing of a level. The mean annual temperature is 8 "C wool cap, one or more wool sweaters, and a with wide diurnal variation and cold stress homespun wool skirt (estuna) hanging to to infants and children is common, par- just below the knees and held in place with ticularly in the early morning and evening a woven belt. Neither undergarments, dia(Baker, '66). pers nor footwear were used. Wet clothing A disk thermistor probe was applied to of the infants was changed three to four six skin sites every hour during a 12-hour times per day, suggesting that evaporative observation period from 0700 to 1900 hours cooling of the lower body may occur periodi(13 measurements). The six skin sites were cally, especially during crawling activity. the forehead, nape at the level of the sevRESULTS enth cervical vertebra, chest over the manubrium, right lateral thigh, and the dorsal Mean skin temperatures at each surface surfaces of the right hand and foot. Field site for the three infants are presented in conditions precluded the measurement of figure 1. Nape temperatures remained the rectal temperatures. highest of all skin sites. Extremity temperThe 12-hour observation period and all atures showed the widest range of variation, temperature measurements were carried and since the infants' feet were in almost out at the respective homes of the three in- continuous contact with the ground, foot fants during days of normal activity. The in- temperatures tended to reflect most closely fants were not restrained in any manner, the daily variations in ambient temperature. except for the brief period each hour Means and standard deviations of the during which temperatures were being re- hourly skin temperature values are given corded. The infants spent approximately in table 1 for each of the subjects and for 75% of the observation period playing, sit- the three subjects combined. Differences beting and crawling on the ground in their tween nape and chest skin temperatures
35 r 0 30-
w'
5 25-
!z
U
w 20- Ao
forehead nape of the neck a chest 2 thigh W 0 hand I- 15- o foot x ambient xx'x'-/ x/x\x 10- x/ I 1 1 I
0700
0900
I
I
1100
I
1300
I
I
1500
I
1
1700
I
I
~~
1900
TIME OF DAY, hr Fig. 1 activity.
Mean skin temperatures of three Quechua Indian infants during days of normal
93
INFANT NAPE TEMPERATURE AT HIGH ALTITUDE TABLE 1
Serial means and standard deuiations of 13 hourly (0700to 1900 hours) skin temperiiture measurements ( " C ) of three Quechua Indian infiznts during normril cictivities Subject 1 (Age 8 mos) Skin site
Subject 2 (Age 9 mos)
Subject 3 (Age 15 mos)
Combined subjects
a
S.D.
a
S.D.
a
S.D.
a
Forehead Nape Chest Thigh Hand Foot
30.8 33.2 32.4 30.2 29.2 28.6
1.48 1.23 1.51 1.50 2.02 2.08
28.7 32.3 28.9 27.2 25.7 24.0
1.35 1.61 2.29 1.94 4.78 5.08
31.8 33.3 32.9 28.8 28.7 24.6
1.59 1.27 1.25 1.52 2.51 2.85
30.5 33.0 31.4 28.8 27.8 25.7
0.90 2.16 1.98
Ambient temp.
17.1
6.14
12.7
2.54
12.7
2.78
14.2
2.78
(by t-test) were statistically significant (p < 0.01) for Subject 2 and the combined subjects. Corresponding differences approached statistical significance for Subject 1 (p< 0.15) while the higher serial mean nape temperature for Subject 3 was not significantly greater than the chest value. DISCUSSION
These data confirm other observations of relatively warm nape temperatures in infants exposed to cold ambient conditions (Perlstein et al., '72; Silverman et al., '64). Since it has been established that warm nape temperatures are in fact a measure of the metabolic activity of BAT (Smith and Horowitz, '69), then this suggests that in infants native to high altitude, NST is important in thermoregulation as it is under conditions of sea lev,elatmospheric pressure. Although all infants in the present study displayed elevated nape temperatures, these results should be interpreted with some degree of caution since only three infants were tested. Sources of variation might be attributed to the higher ambient temperatures to which Subject 1 was exposed (resulting from a higher than normal proportion of time spent indoors), and the older age of Subject 3 (15 months). These two factors are important since NST activity is inversely related to ambient temperature (Briick, '70a), and although NST has been observed in cold-acclimatized adults (Davis, '63), it is most pronounced in very young infants (Briick, '70a). On the basis of these observations it would seem profitable to undertake further studies to clarify the role of NST in infants, children, and perhaps even adults living under the covariant stresses of high altitude hypoxia and cold.
S.D.
1.05 1.04 1.16
LITERATURE CITED Ahern, W., and D. Hull 1966 Brown adipose tissue and heat production in the newborn infant. J. Path. Bact., 91 : 223-234. Baker, P. T. 1966 Micro-environment cold in a high altitude Peruvian population. In: Human Adaptability and Its Methodology. H. Yoshimura and J. S. Weiner, eds. Jap. Soc. Prom. Sci., Tokyo, pp. 67-77. Blatteis, C. M., and T. M. Gilbert 1974 Hypoxia and shivering thermogenesis in cold-acclimatized miniature pigs. J. Appl. Physiol., 36:453456. Briick, K. 1961 Temperature regulation in the newborn infant. Biol. Neonat., 3:6.5119. - 1970a Heat production and thermoregulation. In: Physiology of the Neonatal Period. U. Stave, ed. Appleton-Century-Crofts, New York, pp. 49-57. 1970b Nonshivering thermogenesis and brown adipose tissue in relation to age, and their integration in the thermoregulatory system. In: Brown Adipose Tissue. 0. Lindberg, ed. American Elsevier, New York, pp. 117-154. Davis, T. R. A. 1963 Nonshivering thermogenesis. Fed. Proc., 22: 777-782. Dawkins, M. J. R., and D. Hull 1964 Brown adipose tissue and response of newborn rabbits to cold. J. Physiol. (London), 172:216238. Perlstein, P. H., N. K. Edwards, C. Courpotin and J. M. Sutherland 1970 Thermal patterns on the backs of cold stressed babies. Pediat. Res., 4:472-473 (abstract). Perlstein, P. H., N. K. Edwards and J. M. Sutherland 197!2 Age relationship to thermal patterns on the backs of cold-stressed infants. Biol. Neonat., 20:127-133. Roberts, J. C., R. J. Hock and R. Em. Smith 1969 Effects of altitude on brown fat and metabolism of the deer mouse, Peromyscus. Fed. Proc., 28: 1065-1072. Rylander, E. 1969 Brown adipose tissue and thermoregulation. Acta Obstet. Gynecol. Scand., 48 (Suppl. 3): 97-98. Silverman, W. A,, A. Zamelis, J. C. Sinclair and F. J. Agate, Jr. 1964 Warm nape of the newborn. Pediat., 33: 984-987. Smith, R. Em.,and B. A. Horowitz 1969 Brown fat and thermogenesis. Physiol. Rev., 49: 330425.
K E Y WORDS Skin temperatures . Infants . Altitude adipose tissue . Peru.
'
Brown
ABSTRACT Skin temperatures were measured on three Quechua Indian infants resident at 4,000 meters above sea level in Peru. Nape temperatures were warmer than other skin sites, suggesting that the brown adipose tissue associated with non-shivering thermogenesis is metabolically active despite the reduced oxygen availability at high altitude. The question of the role of non-shivering thermogenesis in infant thermoregulation under the covariant stresses of hypoxia and cold is still open.
Increasing attention has been focused on the mechanism and role of non-shivering thermogenesis (NST) in infant thermoregulation. When exposed to temperatures below thermoneutrality, human infants and certain newborn and adult mammals can increase heat production without shivering (Bruck, '61, '70a). The primary tissue responsible for this increase in metabolic rate has been identified as brown adipose tissue (BAT) (Bruck, '70b; Smith and Horowitz, '69). Sites of BAT deposition are the abdomen, and the cervical, interscapular, and axillary regions. Several studies demonstrated that on cold exposure, the nape and interscapular regions of infants were relatively warmer than other skin sites (Ahern and Hull, '66; Perlstein et al., '70; Perlstein et al., '72; Silverman et al., '64). The increase in oxygen consumption normally accompanying cold exposure is suppressed in some small mammals and their newborn under hypoxic conditions (Dawkins and Hull, '64; Roberts et al., '69; Blatteis and Gilbert, '74). This decreased metabolic response is thought to be due to the selective depression of NST (Roberts et al., '69; Blatteis and Gilbert, '74). Roberts et al. ('69), however, have shown for the deer mouse (Peromyscus) that after acclimatization to hypoxia, heat production under cold exposure returns to normal. This is accompanied by BAT hyperplasia and a n increase AM. J. PHYS. ANTHROP.,44: 91-94
in BAT in vitro respiration (q0,). These authors also compared deer mice native to sea level with a wild population native to 3,800 meters. Despite the slight depression of the 90, of BAT homogenate at altitude, the ratio of BAT to body weight and the estimated heat production of BAT were signficantly greater in the high altitude population naturally exposed to both hypoxia and cold ambient conditions. Human infants similarly respond to acute hypoxia with a decrease in oxygen consumption (Rylander, '69). The effects of the covariant stresses of hypoxia and cold on infant thermoregulation, however, are not well understood. In a preliminary attempt to assess thermal conditions in human infants naturally exposed to the reduced oxygen pressure and cold ambient conditions of high altitude, we measured skin temperatures on three infants native to the high Andes of southern Peru. The surface of the nape was chosen as a n indirect measure of heat production by BAT at this site. METHODS
The subjects were three infants ages 8 (Subject 1), 9 (Subject 2), and 15 (Subject 3) months whose parents were Quechua 1 Funds were provided by the Research Foumdation of the State Universityof New York (40-7225-A) and Cornell University. This work is a part of the U. S. contribution to the International Biological Program.
91
92
D. L. DUFOUR, M. A. LITTLE AND R. B. THOMAS
Indian farmer/herders resident in the town respective courtyards. Mothers of the three of Nunoa, Peru, located on the southern expended a variable amount of effort in Peruvian altiplano at an altitude of 4,000 keeping the infants in dry clothing and in meters. At this altitude, the partial pres- the warmth of direct sunshine. The infants sure of oxygen is about 60% that at sea were all dressed in customary clothing of a level. The mean annual temperature is 8 "C wool cap, one or more wool sweaters, and a with wide diurnal variation and cold stress homespun wool skirt (estuna) hanging to to infants and children is common, par- just below the knees and held in place with ticularly in the early morning and evening a woven belt. Neither undergarments, dia(Baker, '66). pers nor footwear were used. Wet clothing A disk thermistor probe was applied to of the infants was changed three to four six skin sites every hour during a 12-hour times per day, suggesting that evaporative observation period from 0700 to 1900 hours cooling of the lower body may occur periodi(13 measurements). The six skin sites were cally, especially during crawling activity. the forehead, nape at the level of the sevRESULTS enth cervical vertebra, chest over the manubrium, right lateral thigh, and the dorsal Mean skin temperatures at each surface surfaces of the right hand and foot. Field site for the three infants are presented in conditions precluded the measurement of figure 1. Nape temperatures remained the rectal temperatures. highest of all skin sites. Extremity temperThe 12-hour observation period and all atures showed the widest range of variation, temperature measurements were carried and since the infants' feet were in almost out at the respective homes of the three in- continuous contact with the ground, foot fants during days of normal activity. The in- temperatures tended to reflect most closely fants were not restrained in any manner, the daily variations in ambient temperature. except for the brief period each hour Means and standard deviations of the during which temperatures were being re- hourly skin temperature values are given corded. The infants spent approximately in table 1 for each of the subjects and for 75% of the observation period playing, sit- the three subjects combined. Differences beting and crawling on the ground in their tween nape and chest skin temperatures
35 r 0 30-
w'
5 25-
!z
U
w 20- Ao
forehead nape of the neck a chest 2 thigh W 0 hand I- 15- o foot x ambient xx'x'-/ x/x\x 10- x/ I 1 1 I
0700
0900
I
I
1100
I
1300
I
I
1500
I
1
1700
I
I
~~
1900
TIME OF DAY, hr Fig. 1 activity.
Mean skin temperatures of three Quechua Indian infants during days of normal
93
INFANT NAPE TEMPERATURE AT HIGH ALTITUDE TABLE 1
Serial means and standard deuiations of 13 hourly (0700to 1900 hours) skin temperiiture measurements ( " C ) of three Quechua Indian infiznts during normril cictivities Subject 1 (Age 8 mos) Skin site
Subject 2 (Age 9 mos)
Subject 3 (Age 15 mos)
Combined subjects
a
S.D.
a
S.D.
a
S.D.
a
Forehead Nape Chest Thigh Hand Foot
30.8 33.2 32.4 30.2 29.2 28.6
1.48 1.23 1.51 1.50 2.02 2.08
28.7 32.3 28.9 27.2 25.7 24.0
1.35 1.61 2.29 1.94 4.78 5.08
31.8 33.3 32.9 28.8 28.7 24.6
1.59 1.27 1.25 1.52 2.51 2.85
30.5 33.0 31.4 28.8 27.8 25.7
0.90 2.16 1.98
Ambient temp.
17.1
6.14
12.7
2.54
12.7
2.78
14.2
2.78
(by t-test) were statistically significant (p < 0.01) for Subject 2 and the combined subjects. Corresponding differences approached statistical significance for Subject 1 (p< 0.15) while the higher serial mean nape temperature for Subject 3 was not significantly greater than the chest value. DISCUSSION
These data confirm other observations of relatively warm nape temperatures in infants exposed to cold ambient conditions (Perlstein et al., '72; Silverman et al., '64). Since it has been established that warm nape temperatures are in fact a measure of the metabolic activity of BAT (Smith and Horowitz, '69), then this suggests that in infants native to high altitude, NST is important in thermoregulation as it is under conditions of sea lev,elatmospheric pressure. Although all infants in the present study displayed elevated nape temperatures, these results should be interpreted with some degree of caution since only three infants were tested. Sources of variation might be attributed to the higher ambient temperatures to which Subject 1 was exposed (resulting from a higher than normal proportion of time spent indoors), and the older age of Subject 3 (15 months). These two factors are important since NST activity is inversely related to ambient temperature (Briick, '70a), and although NST has been observed in cold-acclimatized adults (Davis, '63), it is most pronounced in very young infants (Briick, '70a). On the basis of these observations it would seem profitable to undertake further studies to clarify the role of NST in infants, children, and perhaps even adults living under the covariant stresses of high altitude hypoxia and cold.
S.D.
1.05 1.04 1.16
LITERATURE CITED Ahern, W., and D. Hull 1966 Brown adipose tissue and heat production in the newborn infant. J. Path. Bact., 91 : 223-234. Baker, P. T. 1966 Micro-environment cold in a high altitude Peruvian population. In: Human Adaptability and Its Methodology. H. Yoshimura and J. S. Weiner, eds. Jap. Soc. Prom. Sci., Tokyo, pp. 67-77. Blatteis, C. M., and T. M. Gilbert 1974 Hypoxia and shivering thermogenesis in cold-acclimatized miniature pigs. J. Appl. Physiol., 36:453456. Briick, K. 1961 Temperature regulation in the newborn infant. Biol. Neonat., 3:6.5119. - 1970a Heat production and thermoregulation. In: Physiology of the Neonatal Period. U. Stave, ed. Appleton-Century-Crofts, New York, pp. 49-57. 1970b Nonshivering thermogenesis and brown adipose tissue in relation to age, and their integration in the thermoregulatory system. In: Brown Adipose Tissue. 0. Lindberg, ed. American Elsevier, New York, pp. 117-154. Davis, T. R. A. 1963 Nonshivering thermogenesis. Fed. Proc., 22: 777-782. Dawkins, M. J. R., and D. Hull 1964 Brown adipose tissue and response of newborn rabbits to cold. J. Physiol. (London), 172:216238. Perlstein, P. H., N. K. Edwards, C. Courpotin and J. M. Sutherland 1970 Thermal patterns on the backs of cold stressed babies. Pediat. Res., 4:472-473 (abstract). Perlstein, P. H., N. K. Edwards and J. M. Sutherland 197!2 Age relationship to thermal patterns on the backs of cold-stressed infants. Biol. Neonat., 20:127-133. Roberts, J. C., R. J. Hock and R. Em. Smith 1969 Effects of altitude on brown fat and metabolism of the deer mouse, Peromyscus. Fed. Proc., 28: 1065-1072. Rylander, E. 1969 Brown adipose tissue and thermoregulation. Acta Obstet. Gynecol. Scand., 48 (Suppl. 3): 97-98. Silverman, W. A,, A. Zamelis, J. C. Sinclair and F. J. Agate, Jr. 1964 Warm nape of the newborn. Pediat., 33: 984-987. Smith, R. Em.,and B. A. Horowitz 1969 Brown fat and thermogenesis. Physiol. Rev., 49: 330425.
