In this study, the patterns shown over time in the HR and HRV indices provided a noninvasive measure of sympathovagal balance during heel stick among 14 preterm infants 30 – 32 weeks GA in KC and IC conditions. To our knowledge, the investigation reported here is the first study examining the effect of KC on heel stick pain responses measured by HRV indices in preterm infants. Consistent with previous studies [41
], HR increased from baseline to heel stick and decreased in the recovery period in both the KC and IC conditions, indicating a clear pain response caused by the heel stick procedure. The LF and HF responses were also found similar in both KC and IC with increases from BL to HS and decreases from HS to RC. In relation to painful events in preterm infants, previous studies showed that total HRV [41
], the LF [41
] and HF bands of HRV [59
] were reduced during heel lance, but other studies did not show the correlation of HRV to pain [38
]. Our sample differed in the LF and HF responses with increases at heel stick instead of decreases as reported in these previous studies. The reason for this difference is not clear as our infants' positions and behavioral responses were similar to those in other studies. It may be that the length of the data collection period during Heel Stick varied among the studies so that the intervals are not comparable. In our study, data were collected across the HS period which ranged from 3.5 – 4.5 minutes; the length of data collection was not reported in the two Oberlander studies. The LF/HF ratio response in our sample was the same as that reported by Oberlander and colleagues [59
] with a decrease in the LF/HF ratio at heel stick. In both KC and IC, the LF/HF ratio decreased from BL to HS, and increased in RC, reflecting an increase in parasympathetic influence in order to balance sympathetic response to the heel stick.
When comparing infants' pain responses between KC and IC conditions, HR was significantly lower in KC than IC for the BL and HS periods. LF and HF were higher in the BL period and LF was also increased in the HS period in KC compared to the IC condition with a medium effect size (). The results are consistent with Schrod and Walter's [62
] findings, in which LF and HF increased when infants were tilted into the KC position. Another study by Begum and associates [63
] found that LF was significantly increase while HF was decreased during KC in low birth weight infants. However, none of these previous studies tested the effect of KC on HRV in a procedural pain condition. Increases in LF (predominately sympathetic tone) and HF (parasympathetic tone) may be explained by several factors, i.e., maturation (gestational age and postnatal age), change in body position, sleep state, and maternal presence and body temperature [44
]. In the present cross-over design study, infants in both KC and IC condition have equivalent GA and postnatal age, similarly inclined 30 – 40 degree prone position, and no difference in behavioral states during the study periods. One explanation for higher LF and HF in KC than in IC may be maternal presence and touch. Changes in LF have been found in response to thermoregulation influences and stimulation in preterm infants. Infant sympathetic activity is increased in a mother-infant bed-sharing environment compared to solitary-sleeping, which might be partly explained by thermal stimulation and thermoregulation when mothers are present [66
]. Increased environmental air temperature due to the mother's body temperature also causes LF to rise in KC. The most likely explanation is that increased environmental temperature in KC increased infants' central temperature, thus causing a concurrent increase in LF compared to IC. KC also activates pressure receptors that can increase parasympathetic activity. Studies of moderate-pressure massage therapy show that parasympathetic activity peaks during massage and remains significantly higher throughout the 15-minute post-massage period compared with infants who receive sham, light-pressure massage [67
]. Animal studies also indicate that tactile interactions between rat pups and their mother, a type of pressure receptor stimulation, activates pups' parasympathetic responses and prevents all the changes associated with maternal deprivation [69
]. Increased HF in KC may be due to KC's stimulating infants' pressure receptors, because the pressure receptors located in an infant's chest, abdomen, and extremities are activated by the full body touch between the infant and mother in KC, and the intensity of pressure in KC may be similar to moderate pressure.
For LF/HF ratio, there was more stability in KC and greater fluctuations in IC across BL, HW, HS, and RC periods (). The ratio was significantly lower in KC than in IC condition during the RC period with a medium effect size. A more mature, balanced response (lower LF/HF ratio) to the painful heel stick during recovery was present in KC compared to that in IC. Balance between parasympathetic and sympathetic tone is associated with maturation and the ability to react effectively to stress, such as heel stick pain. Sympathetic tone is dominant in preterm infants, whereas parasympathetic tone increases with maturation [64
]. A lower LF/HF ratio indicates more maturity and a greater balance between the two systems [73
]. The findings suggest a more balanced, and stable autonomic response to a painful heel stick in KC compared to that in IC. The fluctuations in autonomic response in IC were due to greater swings in sympathetic activity, suggesting that KC has a stabilizing, or balancing, effect during a painful procedure such as heel stick.
The central underlying mechanisms of KC as an analgesic and comforting experience on reducing infant pain may be through multi-sensory stimulation inputs and modulation of the stress-regulation system involved in pain. Mother-infant physical contact has been found to trigger release of beta-endorphins that are critically involved in mediation of the pain signal by blocking the perception of pain in rat pups [74
] and in human newborns [76
]. Dieter [77
] and Harrison [78
] suggested that systematic gentle human touch may stimulate peripheral nerves that activate the vagus nerve, thus promoting infant comfort and reducing stress, resulting in positive immediate and long term outcomes. In addition, KC compared to the incubator condition provides stimulation through the infant's prone positioning [79
], maternal warmth [84
], containment and swaddling [85
], maternal heart sounds [88
], vestibular movement (mother's chest respiratory movement) [90
], maternal body odor [91
], and mother's voice [94
]. Infants are apparently familiar with their mothers' odor, voice, respiratory and heart beat rhythm from the uterine environment [92
] and these have soothing effects on infants. Following KC, preterm infants showed a more rapid maturation of vagal tone as compared to controls, underscoring the effect of KC on the autonomic and circadian systems in preterm infants [19
]. These findings support the premise that maternal effects reduce infant pain by blunting sympathetic responses, accelerating parasympathetic recovery of autonomic activation, and activating the endogenous opioid system.
These HRV findings of better balance and autonomic stability in the Kangaroo Care condition during heel stick for preterm infants lend further support the findings about KC decreasing HR, crying, and grimacing during painful procedures [16
]. Our study's findings add to the continuing evidence for KC as a non-pharmacologic intervention to alleviate preterm infant pain responses related to the heel stick.