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In a case study, two sets of premature twins were held in Shared Kangaroo Care (KC) while maternal breast and infant body temperatures were recorded. Infant temperatures remained warm and increased during KC and each breast appeared to respond to the thermal needs of the infant on that breast. Physiologic explanations for thermal synchrony exist. The data suggests that twins can be simultaneously held in KC without physiologic compromise.
As the use of Kangaroo Care (KC) spreads in the neonatal intensive care unit (Engler et al., 2002), twins and triplets are also being placed in KC (Kambarami, 2002; Wallis, 2000). Previous studies of KC with twins focused on parental confidence and comfort related to infant care, both of which increased as a result of KC (Dombrowski et al., 2000; Swinth et al., 2000). Swinth and associates (2000) measured triplet infant temperatures when all three infant were simultaneously held by their mother. At the end of the first KC session which lasted three hours, infant axillary temperature ranged between 36.8°C and 37.1°C. At the end of the second session (45 min long) that evening, infant temperatures ranged between 37.0°C and 37.3°C. Though twins have been included in other KC investigations (Kambarami, 2002) twin data has not been separately reported, so thermal condition of twins throughout KC could not be found. The ability of a single infant to stay warm while in KC has been well established (Bystrova et al., 2003; Chwo et al., 2002; Conde-Agudelo, Diaz-Rossello, & Belizan, 2003, Ludington-Hoe, Nguyen, Swinth, & Satyshur, 2000; Ludington-Hoe & Dorsey, 1998; Sontheimer, Ludington-Hoe, Fischer, Kaempf, & Linderkamp, 2004), but the ability of the mother to thermally accommodate multiple infants in Shared KC has only been suggested to date (Dombrowski et al., 2000). Thus, we conducted two case studies to determine if maternal breasts respond similarly or differently to the skin temperatures of twins when both infants are held in Shared KC. We wanted to answer the following questions:
Question #1: What are the skin temperatures of both breasts as infants lie on them in KC?
Question #2: Is there a relationship between each breast's temperature and the infant's temperature while lying on that breast during KC?
Question #3: Are there differences between the breasts' temperatures during Shared KC?
Question #4: Are there differences between the infants' temperatures during Shared KC?
The setting for the case studies was in a tertiary care, University-based NICU. Informed consent was obtained from two mothers. Both KC sessions were 1.5 hours, beginning immediately after care giving and feeding of both infants. The mothers reclined in a LaFuma lounger (LaFuma, Anneyron, France) behind privacy screens. Infants were transferred by the nurse to the mother's chest after she was seated between the incubators. Baby A was placed on the right breast (called Breast A), and Baby B was placed on the left breast (called Breast B). Infants were positioned midline over each breast so that they were facing each other and their heads were above the nipple. Positioning guidelines for co-bedding of twins were followed (DellaPorta, Aforismo, & Butler-O'Hara, 1998). Abdominal skin temperature probes (Mallinckrodt Inc, St. Louis, MO) were secured 1 cm below the right costal margin of each baby and covered by an Accutemp Plus temperature probe cover (Irvine, CA) to prevent ambient air and light influences. The temperature probes were connected to their incubators (Ohmeda Ohio Care Plus incubator, Columbia, MD) for temperature readings. Maternal breast temperature probes (YSI 409a, Yuma, AZ) were attached to Fisher Thermistors (Model 500, Friendswood, TX) and secured to the skin three inches above the nipple at the mid-clavicular line and covered with a Accutemp Plus temperature probe cover (Irvine, CA) to minimize ambient light and air influences. Thermistors were warmed-up for five min before baseline data was collected. Baseline breast and infant temperatures were obtained prior to placing the infants in KC and were recorded every 30 sec for five min. After transfer into KC, two researchers monitored breast and infant temperatures, with each researcher recording the temperatures for one breast-infant pair. Both researchers recorded data simultaneously, using one watch to signal time for data collection. The staff nurse monitored maternal and infant status every 15 min during the KC session.
This case study describes KC as given by a 33 year old white married woman who had a normal spontaneous vaginal delivery of 29 week gestational age twin boys after a history of chorioamnionitis accompanied by artificial rupture of her membranes 8 days prior to delivery. Baby A was placed on the mother's right breast (Breast A); Baby B was placed on the mother's left breast (Breast B). Breast and infant temperatures were manually recorded every 15 sec for the first 7 min and every 30 seconds thereafter.
The birth weight of Baby A was 1388 grams and he had APGAR scores of 9 and 9 at l and 5 min respectively. His weight on the day of study (9 days post-birth) was 1336 grams and he was 30 2/7 weeks corrected age. He had been on Nasal CPAP for 7 days, starting within 24 hours of birth when he developed respiratory distress and ending two days before the study. His medical course was otherwise uncomplicated and he was in stable medical condition at the time of study.
The temperature patterns of Breast A and Baby A are depicted in Table I. The mother's right breast baseline temperature ranged between 35.2°C-35.3°C (M=35.24; SD = 0.05). While the infant was being transferred into KC, Breast A temperature went up 0.2 C and was 35.5°C the first min of Baby A's presence on the breast. Breast A temperature continued to rise for 5 min (up to 36.4°C) and then started dropping when Baby A temperature rose from 37.0°C to 37.1°C. Breast temperature continued dropping over the first 18 min of KC until it was 35.4°C and then vacillated between 35.5°C and 36.1°C over the remaining 71 min of KC. During this time the infant's temperature steadily rose to 37.5°C.
Baby A baseline skin temperature in the incubator over the five min prior to transfer was stable at 37.2°C (Incubator temp was 31.5°C-31.7°C and Baby A wore no t-shirt nor blanket in the incubator). During transfer, Baby A temperature dropped to 37.0° and stayed at this temperature for the first 5 min of KC. Thereafter, Baby A temperature gradually and consistently rose from 37.0° to 37.5°C.
In summary, Baby A entered KC warm at 37.0°C, and his temperature continued to rise very slowly over the next 90 min, ending KC at 37.5°C. Breast A temperature initially rose, and then quickly dropped to 35.6°C around which it vacillated slightly until the last few min of KC. Baby A temperature began warm and was sustained in the presence of a low breast temperature. Baby A oxygen saturation level varied between 92.0% and 100.0% at all times.
The birth weight of Baby B was 1248 grams, he was the second child born, and he had APGAR scores of 4 and 7 at 1 and 5 min respectively. Respiratory distress emerged shortly after birth and was treated by nasal CPAP which was discontinued one day before the study. He too, was in stable condition at the time of study.
The temperature pattern of Breast B and Baby B is depicted in Table I. Breast B baseline temperature ranged between 36.1°C and 36.2°C (M= 36.14; SD =− 0.05) and increased by 0.1° C to 36.3° C during transfer. Breast B remained at 36.3°C for the first 8 min of KC and then fluctuated by 0.2°C over the next 12 min, reaching a peak temperature of 36.5°C before it started to fluctuate downward. Twenty min after KC began; Breast B temperature began a gradual, linear rise to 37.1°C over the next 11 min. The temperature stayed at 37.1°C for an additional 11 min and then started a gradual drop to 36.4°C by the end of the KC session. This pattern was very different from the pattern of Breast A.
Baby B had a stable baseline temperature of 36.3°C in the incubator (with the incubator temperature at 29.2°-29.4°C and with Baby B wearing a t-shirt and swaddled in one blanket). Baby B temperature dropped 0.1°C to 36.2°C during transfer and remained at 36.2°C for 11 min. His temperature then began a steady, gradual increase to 37.1°C, which was achieved in the last 3 min of KC.
In summary, Baby B entered KC much colder than Baby A, and Breast B baseline temperature was nearly one full degree warmer than Breast A. Following an initial fluctuation in breast temperature, Breast B began a steady rise to 37.1°C. This rise was accompanied by a linear rise in Baby B temperature from 36.2°C to 36.9°C. When Baby B temperature reached 36.9°C, Breast B temperature began a gradual fall which continued as Baby B temperature resumed rising and rose to 37.1°C. Baby B experienced two separate oxygen saturation readings below 88.0% (87.0% and 85.0%) from which the infant recovered spontaneously and immediately. The duration of the desaturations was one reading only and they did not appear to be due to artifact.
The second mother of twins was a 33 year old white unmarried woman who had twin girls at 33 5/7 weeks gestational age. Her pregnancy was complicated by premature rupture of membranes at 26 weeks and an abnormal Triple Screen which lead to an ultrasound showing intrauterine growth retardation for Baby A. For the case study, Baby A was placed on the right breast (Breast A) and Baby B was placed on the left breast (Breast B.) Temperatures of both breasts and both babies were recorded every min for 104 min.
The birth weight of Baby A was 1535 grams and her APGAR scores were 8 and 9 at one and five min respectively. She was medically stable at eight days old on the day of the study. The temperature patterns of Breast A and Baby A are depicted in Table I. Breast A was noted to generally have more milk than Breast B. Breast A temperature prior to KC ranged between 35.3°C and 35.5°C. For the first 16 min, Breast A temperature dropped to 33.8°C at which point the researcher noted that the deeply sleeping infant had slid down below the mother's nipple. The infant was repositioned so that his head was above the nipple and then breast temperature began to increase, continuing to do so until min 41 when the temperature was 36.8°C. Breast temperature then vacillated between 36.8°C and 35.8 C for 50 min. During the last 14 min of the study, Breast A temperature dropped precipitously as the thermistor's probe became dislodged and Baby A awoke and moved about. Thus, the last 4 min of data were invalid and not used in analyses.
Baby A baseline temperature was 36.2°-36.7° C. Her temperature rose to 37.4°C over the first 70 min and then vacillated between 37.5° and 37.1°C for the remainder of the study.
In summary, Baby A temperature continually rose and Baby A stayed warm throughout KC. Breast A temperature dropped when the head of Baby A slid beneath the nipple and rose rapidly when the infant's head was repositioned above the nipple and over the thermistor. Baby A oxygen saturation varied between 88.0%-96.0%, usually recording in the low 90s.
Baby B birth weight was 2090 grams and APGAR scores were 9 and 9 at 1 and 5 min respectively. She had a history of hyperbilirubinemia but was medically stable at the time of the study. The temperature patterns of Breast B and Baby B are depicted in Table I. Breast B temperature started at 35.8°C and rose to 36.2°C over the first 4 min and maintained that temperature for 5 more min. Breast temperature then decreased to 35.5°C over 26 min. For the next 51 min, breast temperature vacillated between 35.9°C and 35.2°C and for the last 13 min of the study, breast temperature dropped to 34.7°C.
Baby B began with a temperature of 36.5°C and it gradually and steadily rose over the duration of the study to 37.8°C. In spite of a continually decreasing breast temperature, Baby B temperature continued to rise to 37.7°C where it remained for 17 min before increasing to 37.8°C, for two readings one min apart, and then returned to 37.7°C for another 27 min. When her temperature reached 37.8°C the blanket over her was reduced from four layers to two layers, but her temperature did not drop below 37.7°C.
In summary, both Baby A and Baby B temperatures gradually increased during their time in KC. Breast A temperature decreased in the beginning of the study and then gradually increased. This increased temperature was maintained throughout the KC session vacillating only slightly until the baby's temperature increased to 37.4°C. At that time, the breast temperature began to decrease. Breast B temperature initially increased and then decreased over the duration of the study, as Baby B temperature continued to rise. Baby B oxygen saturation never dropped below 89.0% and was in the high 90s in the first half hour of KC and then in the low 90s during the remainder of KC.
To answer the research questions we posed, the means, standard deviations and ranges were computed to describe the temperatures presented by the breasts and the babies. In addition to the descriptions of temperature patterns discussed above, statistics related to temperature data are presented in Table I. To determine if a relationship existed between each breast and its baby, Pearson Product Moment Correlation coefficients were calculated (Table II). Breast temperatures were highly and significantly related to infant temperatures in both sets of subjects, but the direction of the relationship differed. In Mother #1, Breast A temperature was inversely related to Baby A temperature and Breast B temperature was positively related to Baby B temperature. In Mother #2, the pattern was reversed: Breast A temperature was positively related to Baby A temperature, and Breast B temperature was inversely related to Baby B temperature, indicating that each breast responded differently and independently of the other breast. Table III reveals significant differences (p<0.01) between Breast A and Breast B temperatures in both subjects and between Baby A and Baby B temperatures in both subjects.
We learned that both sets of infants were able to be in Kangaroo Care at the same time without any thermal compromise. All four infants had increased temperatures during KC, remained warm throughout KC and had temperatures that stayed above 36.5° C. In both mothers, the left breast demonstrated significantly different temperature patterns than the right breast. The temperature patterns of each twin differed significantly, too. In both mothers, Breast B temperature dropped when the infants' temperatures rose to 36.9C. These data showed that breasts do perform independently of each other, but not independently of the infant, as confirmed by highly significant correlation coefficients. The direction of the relationship between Breast and Baby temperatures depended upon the infant's temperature. When the infant's temperature was high, breast temperature was decreasing, perhaps to prevent overheating. When the infant's temperature was low, breast temperature was rising, perhaps to warm the infant. When babies are placed in KC, breast temperatures rise for both preterm (Ludington-Hoe et al., 2000) and full term dyads (Richardson, 1997). Meta-analysis has shown that infant skin temperature rises (Dorsey & Ludington-Hoe, 1998), usually about 0.5-1.0°C in the first hour of KC and sometimes more in the second hour of Kangaroo Care(Smith, 2001). Rising body temperature during KC has not been associated with increased oxygen or energy consumption in either preterm (Bauer et al., 1997) or full term (Karlsson 1996) infants, but has been associated with slight decreases in oxygen saturation as the duration of KC increases (Bohnhorst et al., 2001; Smith, 2001). We noted in one baby (subject 2, Baby B) that oxygen saturation level had a definite pattern of decreasing value as KC continued, suggesting that oxygen saturation be monitored in KC sessions of an hour or more.
The dyads observed for this report demonstrated a temperature pattern that has been observed before: breast temperatures move in a direction that is most physiologically supportive to the infant (Ludington, 1990; Ludington-Hoe et al., 2000). When infant temperatures were below 36.9° C breast temperatures were rising; when infant temperatures reached 36.9°C or higher, breast temperatures started to drop, leading us to speculate that breast temperatures may regulate infant body temperatures to prevent hypo- and hyperthermia. The beginning breast temperatures reported here were warmer than the temperatures of the incubators from which the infants came, but hyperthermia in the infant's did not occur. Hyperthermia is detrimental as preterm infants experience an increase in apnea of prematurity when their body temperatures reach 37.5°C (Daily, Klaus, Belton, & Meyer, 1969). Hyperthermia in Kangaroo Care is rare as only one of 374 studies to date has reported infant hyperthermia (WHO-INK, 2004). The study was a descriptive investigation of paternal kangaroo care's effects on temperature of preterm infants in a tropical area of South America. During the second hour of paternal Kangaroo Care, five of eleven healthy preterm infants experienced skin temperatures above 37.5° C (Ludington-Hoe et al., 1992) and the trend was for infant skin temperature to continue rising as long as paternal KC continued. In that study, the fathers' breast temperatures did not drop as maternal breast temperatures do when the infant's temperature reaches 36.9° C.
Baseline and KC breast temperatures reported here were slightly higher than those reported by Bauer and associates in their investigation of non-lactating women's breast temperatures (Bauer, Pasel, & Versmold, 1996) and higher than those in previous KC studies of longer duration (Ludington-Hoe et al., 2000). Being held in KC creates a very different thermal environment for the infant than the incubator. The heat source is the mother whose breast temperature quickly becomes sufficient to maintain the infant's body heat (Karlsson, 1996). In KC, a microclimate is formed around the infant's body that is draft free, contained, and heat shielding. In this microclimate, “the neonate is at thermal comfort at approximately the same temperature as his/her mother” (Le Blanc, 1991).
We were not surprised to find that maternal breasts were warm. First, both women were more than 5 days post-birth, and preterm mothers' breast temperatures increase with increasing postnatal age (Bauer et al. 1997). Second, both mothers were breastfeeding; breastfeeding stimulation increases prolactin production. Increased prolactin supports milk production and mammary gland development after delivery. Milk production and mammary gland development require considerable growth and blood flow through mammary vessels, increasing breast skin temperature (Linzell, 1974). Third, mammary blood vessels are exquisitively sensitive to parasympathetic influences (Linzell), suggesting that the relaxation mothers experience during KC (Ludington-Hoe et al., 1994; Ludington-Hoe & Swinth, 1996; Feldman 2002) promotes vasodilatation of the abundant mammary blood vessels, contributing to the increase in breast temperature evident in our results. One of the mothers wrote in a note to the researchers that “my experience with KC was heartwarming. I could actually feel differences in temperature between my two breasts.”
Physiologic events may explain why maternal breasts are able to respond differentially to each infant. First, skin-to-skin contact is a form of touch that stimulates the slow conducting unmyelinated (C) afferents in the human hairy skin. Activation of C tactile afferents produces the sensation of pleasant touch as determined by the activation of the insular cortex (Limbic system) rather than the somatosensory areas of S1 and S2 by the tactile afferents (Olausson et al., 2002). Maternal and infant skin responds to pleasant touch by releasing neuropeptides including cholescytokinin and opioids (Weller & Feldman, 2003). As little as twenty min of KC produces an opiod mediated relaxation (Modi & Glover, 1998; Mooncey, Giannakoulopoulos, Glover, Acolet, & Modi, 1997) which can cause skin vasodilation and its concomitant warming. Second, KC increases pituitary thyroid axis activity (Weller et al., 2002) which can in turn increase metabolic rate and skin temperature in each mother and infant. Third, placement of the warm infant upon the mother's breast produces a warm sensation in the mother that is dependent on each infant's body temperature. Warm touch increases skin blood flow (Yosipovitch, Chan, Tay, & Goh , 2003), helping each breast respond individually to the infant. Fourth, the warm touch perceived when an infant is placed on the breast also causes a release in calcitonin generated peptides that elevate local skin temperature (Noguchi et al., 2003; Yuzurihara et al., 2003). Fifth, each infant has his own weight, posture, and movement pattern as he/she lies on the breast. As each infant lies on the breast, skin hair follicles in the stratum corneum of the mother are aroused, stimulating release of cutaneous corticotrophin releasing hormone, which, in turn, locally vasodilates skin vessels (Crompton, et al., 2003). And, finally, the amount of corticotrophin releasing hormone that is activated in the infant by being skin-to-skin against the breast affects his/her movements (Slominski, Pisarchik, Tobin, Mazzurkiewicz, & Wortsman, 2004) each of which further stimulates cutaneous corticotrophin releasing hormone in the mother, and, ultimately, breast skin temperature.
We also observed that mothers and infants responded to shared KC with peaceful facial expressions, relaxed postures, and motoric quiescence. One mother's note accurately summed the experience for both mothers. She wrote “As a mother of preemies in the neonatal intensive care unit, this was a wonderfully warm, emotional, and special bonding experience to have with my baby boys. This was my first opportunity to hold both boys at the same time. I truly believe that my babies enjoyed the experience of being skin-to-skin with me, and also enjoyed being close to one another for the first time since birth.”
In conclusion, the data suggest that twins can be simultaneously held in KC without temperature or physiologic compromise. Right and left breast temperatures differed in both mothers, but because of the small sample size the difference needs to be confirmed before one can confidently deduce that each breast responded independently of the other. In the four infant/breast pairs studied here, each breast appeared to respond in a manner that correlated with the thermal needs of the infant who was on that breast. Infant temperatures remained warm and increased during KC while staying within neutral thermal zone. The temperatures of each twin in a pair were different as they lay on their respective breast. Further investigation with a larger sample size and more detailed information on baseline breast temperatures is merited. The value of shared KC with multiples for maternal bonding and relaxation should also be empirically studied using more rigorous design than the case study.
This study was supported in part by 5RO1-NR04926 and 1RO3-NR08587 to the first author.
We learned that both sets of twins were able to be in Kangaroo Care at the same time without any thermal compromise.
When infant temperatures were below 36.9° C breast temperatures were rising; when infant temperatures reached 36.9°C or higher, breast temperatures started to drop.
These data showed that breasts do perform independently of each other, but not independently of the infant, as confirmed by highly significant correlation coefficients.