Effects of nutritive and non-nutritive sucking on infant heart rate variability during the first 6 months of life

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Infant Behavior & Development 30 (2007) 546–556

Effects of nutritive and non-nutritive sucking on infant heart rate variability during the first 6 months of life Hanne Lappi a,∗ , Minna Valkonen-Korhonen a , Stefanos Georgiadis b , Mika P. Tarvainen b , Ina M. Tarkka c,d , Pasi A. Karjalainen b , Johannes Lehtonen a a

Department of Psychiatry, Kuopio University Hospital, Finland Department of Applied Physics, University of Kuopio, Finland Department of Clinical Neurophysiology, Kuopio University Hospital, Finland d Brain Research and Rehabilitation Center Neuron, Kuopio, Finland b

c

Received 28 June 2006; received in revised form 10 February 2007; accepted 28 April 2007

Abstract The effects of eating on heart rate variability (HRV) differ between adults and newborns. This may reflect the impact of suckling on the overall psychophysiological and autonomic nervous system maturation. The purpose of the present study was to explore whether the reactions of HRV during feeding change towards the adult pattern during the first 6 months of life. In addition, the effects of non-nutritive and nutritive sucking on heart rate (HR) and HRV were compared. The participants were 23 infants on whom recordings were performed as newborns and at 6, 12 and 24 weeks old. Nutritive sucking caused an increase in HR and a decline in HRV. The results were consistent with previous reports of a decrease in high frequency components of HRV during feeding in newborns, reflecting a decrease in parasympathetic activity. This response was apparent in all four ages studied, and remained similar throughout the 6-month period. However, age as an independent factor seemed to influence both HR and HRV. Pacifier sucking had no significant effects on HRV at any age. The results demonstrate the physical strain that sucking imposes on the baby, with a specific autonomic nervous system response involved. We consider this response an essential part of the overall psychophysiological maturation of infants. © 2007 Elsevier Inc. All rights reserved. Keywords: Suckling; Heart rate variability; Heart rate; Sucking; Pacifier; Autonomic nervous system; Feeding

1. Introduction Maturation of sucking and swallowing are essential for the survival of a newborn baby. The mechanisms controlling these functions and physiological responses during feeding have been widely studied. Fully matured nutritive sucking behaviour can be seen as a hallmark of neurological, behavioural and physiological maturity, and, on the other hand, when an infant grows up, abnormal sucking patterns seem to be associated with various neurological problems (for review, see Medoff-Cooper & Ray, 1995). Changes in heart rate (HR) associated with psychological and physiological states have been observed (Berntson et al., 1997). The applications of heart rate variability (HRV) provide methods to

∗

Corresponding author. Tel.: +358 50 3447759; fax: +358 17 173549. E-mail address: [email protected] (H. Lappi).

0163-6383/$ – see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.infbeh.2007.04.005

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explore autonomic nervous system functions (ANS), and particularly the clear equilibrium between sympathetic and parasympathetic domains. Previous research has revealed systemic vagal control of the heart rate associated with gustatory stimulation in newborns. Porges and Lipsitt (1993) introduced a gustatory-vagal hypothesis after observing that increased sweet gustatory stimulation caused a reduction in cardiac vagal tone and increased heart rate in neonates. In their study vagal tone was measured with respiratory sinus arrhythmia (RSA). They concluded that this effect might be explained by a common medullary origin of vagal innervations of sucking and heart rate. The right branch of the vagus, which innervates the sino atrial nodus, originates from the nucleus ambiguus. Furthermore, the nucleus ambiguus includes source nuclei for the structures coordinating sucking and swallowing, including the soft palatum and pharynx. Portales et al. (1997) tested this hypothesis with high-risk, low-birth-weight neonates. In agreement with the gustatory-vagal hypothesis, RSA in infants decreased during bottle-feeding when conditions before and after feeding were compared. Suess et al. (2000) used this hypothesis to test the maturity of vagal functioning in preterm infants. They found a heart rate and RSA decrement during feeding and an increase towards pre-feeding levels only in infants with a greater gestational age, suggesting that the more mature babies were better able to adjust their autonomic nervous system according to task requirements. An increase in heart rate as a response to feeding is a common finding in many newborn studies (Cohen, Brown, & Myers, 1998, 2001; Porges & Lipsitt, 1993). HR increases more in newborns while sucking a sweet liquid than in no-fluid sucking (Lipsitt, Reilly, Butcher, & Greenwood, 1976). Paradoxically, sucking occurs more slowly for sweet substances (Lipsitt et al., 1976). On the other hand, feeding with colostrum has been shown to prevent the increase in heart rate during painful procedures, despite pain reactivity and extreme crying (Blass & Miller, 2001). Although the vagal tone reduction during feeding described in infant studies has not been observed in adults during a meal (Nederkoorn, Smulders, & Jansen, 2000), very little information is available about the immediate HRV responses of adults to eating. Instead, many adult studies have focused on the long-term effects of eating on HRV and HR and the results have been somewhat contradictory. In healthy adults, HR increases after a meal (Matsumoto et al., 2001; Nederkoorn et al., 2000), which is accompanied by a decrease in LF and VLF components of HRV (Nederkoorn et al., 2000). However, a meal was found to have no significant effect on RSA (in this case 0.15–0.4 Hz), and the LF and VLF components remained low after meal, while VLF returned to the pre-fed level within about 16 min after eating (Nederkoorn et al., 2000). Lipsitz et al. (1993) compared young and elderly people and found a more delayed HR increase in young subjects (significant at 60 min after meal). In the healthy old subjects, the HR increase was already significant 15 min after the meal. The LF power of young subjects increased significantly at 80 min after a meal with no increase in HF components. The HRV reaction of elderly subjects after a meal was not significant. Non-nutritive and nutritive sucking cannot be completely separated because of their largely shared controlling mechanisms. Using a pacifier appears to reduce the time for transition from tube feeds to bottle feeds and results in better bottle feeding performance and behaviour (Cochrane, 2003). The use of a pacifier has also been associated with a reduced risk of sudden infant death syndrome (SIDS) (Hauck, Omojokun, & Siadaty, 2005). Franco, Chabanski, Scalliet, Groswasser, and Kahn (2004) showed that the use of a pacifier modifies cardiac autonomic control during both sucking and non-sucking sleep periods; when compared to infants with no pacifier, infants who slept with a pacifier displayed a significant increase in parasympathetic activity and decrease in sympathovagal heart rate control during both REM and non-REM sleep. This effect on HRV might be an explanation for the SIDS reducing effect of the pacifier. Pacifier sucking has also been noted to reduce heart rate levels after a heel-stick (Campos, 1994). However, contrary results concerning the effects of pacifier sucking have also been reported (Cohen, Witherspoon, Brown, & Myers, 1992). Morren et al. (2002) showed that non-nutritive sucking elevates HR especially during sucking bursts. On the other hand, Di Pietro, Cusson, Caughy, and Fox (1994) observed non-nutritive sucking to have no effect on HR or vagal tone in nasogastric gavage fed infants. In the present study we examined the effects of both nutritive and non-nutritive sucking on heart rate and heart rate variability during infancy. Previous studies with newborns have revealed a decrease in HRV at RSA frequencies during feeding. However, in adults there is no decrease in high frequency components of HRV during eating (Nederkoorn et al., 2000). Our aim was to examine whether sucking itself produces the difference between adult and infant patterns of autonomic nervous system (ANS) reaction, and hence whether pacifier sucking (non-nutritive sucking) causes similar changes in heart rate and heart rate variability to nutritive sucking.

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Fig. 1. The filtered unipolar EMG recording showing the sucking rhythmicity and the rest periods of a male newborn (upper figure), and the corresponding RR intervals (lower figure), illustrating how the RR interval decreases in relation to sucking.

In addition to the effects of feeding, we were interested in the maturation of HRV during the first 6 months of life, and whether HRV reaction patterns during feeding change in the course of infancy towards adult reaction pattern. We studied healthy babies with no perinatal problems and followed the babies for 6 months from the newborn phase. As our aim was to create as natural a testing situation as possible, babies were breast- or bottle-fed in the same way as at home. Heart rate variability data were examined in the time domain, frequency domain and using Poincar´e plotting. 2. Methods 2.1. HRV measurement HRV provides a non-invasive method to explore ANS during various psycho- and/or physiological tasks. In HRV studies, variations in the distances between adjacent R peaks (i.e. RR intervals) of ECG are analysed. Time domain methods of HRV determine how the RR intervals (or HR) vary over time, and typical methods include the standard deviation of RR intervals and HR. Another time domain method, also used in this study, is the RMSSD (root mean square value of differences of successive RR intervals), which is an estimate of the short-term components of HRV (Task force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996). In the frequency domain the spectrum of the RR intervals is calculated and thus the frequency content of HRV can be estimated. From the selected frequency bands, the total power of the band and peak frequencies can be calculated. Three standard bands are usually used in HRV analysis: a very low frequency band (VLF) (0.003–0.05 Hz), low frequency band (LF) (0.05–0.15 Hz) and high frequency band (0.15–0.4 Hz) (Berntson et al., 1997; Task Force, 1996). Respiratory sinus arrhythmia (RSA), describes the fluctuation in heart rate produced by respiration. It is generally thought to be predominantly mediated by fluctuations in vagal-cardiac nerve traffic and may thus provide an index of vagal activity (Berntson et al., 1997). RSA is normally thought to range from 0.15 to 0.4 Hz but may extend, especially in infants, up to 1 Hz or more (Berntson et al., 1997). Thus, RSA components are often referred to as high frequency components of heart rate variability. Some reports concerning LF components submit that these rhythms mainly reflect sympathetic outflow, but most studies support the theory that they are modulated by both sympathetic and vagal domains (Berntson et al., 1997; Lombardi, Malliani, Pagani, & Cerutti, 1996; Task Force, 1996; Zaza & Lombardi, 2001). VLF components may reflect thermoregulatory cycles (Berntson et al., 1997). One method to illustrate HRV is Poincar´e plotting, which is a graphic representation of the correlations between successive RR intervals (Fig. 1). Two variables can be calculated from the Poincar´e plot: SD1 and SD2, which respectively describe short- and long-term variability in HR. (Brennan, Palaniswami, & Kamen, 2001).

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2.2. Participants Twenty-three babies participated. Voluntary mothers were recruited from the birth unit of Kuopio University Hospital. All mothers provided a written informed consent. The study was approved by the local ethical committee. One of the babies was fed with a bottle at 6-, 12- and 24-week recordings while another was bottle-fed only at the 24-week recording. Both babies fitted well within the distribution of the group in all HRV variables. All other babies were breast-fed. Neonatal clinical details of the babies are summarised in Table 1. 2.3. Recording procedure Infants were tested at four ages (newborn and at 6, 12 and 24 weeks; Table 1) and ECGs were recorded in four situations: before feeding, during pacifier sucking, during feeding and after feeding. Pacifier sucking was recorded before or after baseline recordings in most cases, but after feeding in one recording session. Not all the babies used a pacifier and the time between recordings before and during feeding could not therefore be adjusted. Recordings during feeding started as soon as sucking had properly begun. After feeding an ECG sample was recorded immediately when the baby was satisfied and had voluntarily dispensed with the breast. Sucking was carefully monitored and doublechecked: a unipolar electromyography (EMG) electrode was placed under the jaw and the researcher observed sucking during recording and marked the onsets and breaks in sucking online in the continuous ECG signal. The unipolar EMG electrode was referenced to a midfrontal EEG electrode and thus provided a bipolar EMG measurement that displayed the sucking rhythmicity rather than muscular activation (Fig. 2). Analysed ECG epochs were selected based on the EMG and behavioural information on the sucking activity. The researcher observed the babies during the whole recording procedure and noted their state and behaviour. The single-use electrodes were placed on the chest of the babies to detect R peaks. ECG was recorded using a Neuroscan Synamps amplifier (Neuroscan Inc., Sterling, Virginia) and sampled at 500 Hz. QRS complexes were detected using an adaptive QRS detector algorithm similar to the one presented by Pan and Tompkins (1985). In addition, each R-peak detection was manually checked. The time and frequency domain analyses were performed with locally engineered HRV analysis software (Niskanen, Tarvainen, Ranta-Aho, & Karjalainen, 2004). Artefact-free epochs of 80 s in duration were selected for further analysis. Since analysed epochs should last for at least 10 times the wavelength of the lower frequency band of the investigated component (Task Force, 1996), the frequencies 0–0.15 Hz were not calculated. In addition to the common high frequency band (HF = 0.15–0.4 Hz) we analysed the band between 0.4–1 Hz (very high frequency band, VHF). The low frequencies were detrended with the smoothness priors method (Tarvainen, Ranta-Aho, & Karjalainen, 2002). The Fast Fourier transform (FFT) was used to determine the spectrum of HRV. Before spectral analysis, the RR series was transformed to evenly sampled series using a 4 Hz cubic spline interpolation. 2.4. Statistics Not all babies provided data from every situation at every age (Table 2) for the following reasons: (a) not all the babies participated in every recording, (b) some babies did not use a pacifier (non-nutritive sucking recordings were omitted), (c) some babies were already so hungry when they came to recordings that before feeding and pacifier sucking recordings were impossible, and (d) due to failures in the recording procedure (e.g. ECG artefacts). Table 1 Neonatal clinical characteristics and the infant ages at the separate recording sessions Type of delivery Sex Gestational age (week) Birth weight (g) Apgar scores after 5 min Age at recordings (days) n = 23 Means ± SD.

Vaginal: 20 Female: 14 39.6 ± 1.37 3586 ± 542 8.9 ± 0.4 2.6 ± 0.7 n = 23

Cesarean: 3 Male: 9

45.2 ± 1.9 n = 20

88.1 ± 4.8 n = 17

169.5 ± 3.0 n = 12

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Fig. 2. A Poincar´e plot of a breast-feeding male newborn. The ellipse is fitted onto the line-of-identity at 45◦ to the normal axis. The standard deviation of the points perpendicular to the line-of-identity is denoted by SD1 (describing the short-term variation in HR). The standard deviation along the line-of-identity is denoted by SD2 (describing the long-term variation in HR).

The experimental units for the repeated measures factorial design are presented in Table 2. In parenthesis are the data points for the balanced case with no missing values. Every baby was present at least one time in each situation and the resulting design is close to proportional with no empty cells. The effects of different situations and ages and their interaction for all the selected variables were tested with univariate analysis of variance. For all the data sets we applied natural logarithmic transformation to improve the Gaussianity and the homogeneity of the variance among groups. The selected linear model had two main fixed factors, AGE and SITUATION and their interaction, and a between-subjects random factor, BABY. Type III sum of squares of SPSS (Version 11.5) was used, which in this case is the weighted squares of means of Yates. This technique is commonly used for unbalanced designs with no empty cells, and is based on the sums of squares of the cell means, but the terms in the sums of squares are weighted in inverse proportion to their variance (Montgomery, 1991). To compensate for the possible violation of sphericity we also computed tests based on adjusted degrees of freedom (Vasey & Thayer, 1987). The F ratios were found significant when sphericity was assumed (under the null hypothesis the F ratios for the main effects follow approximately F(3, 217) distribution) and were further tested with adjusted degrees of freedom assuming maximum non-sphericity (F ratios for main effects follow approximately F(1, 72) distribution). Table 2 The experimental units of the repeated measures design Experimental units based on 23 subjects SITUATION

AGE

Total

1 2 3 4

Total

1

2

3

4

21 (23) 16 (23) 10 (23) 11 (23) 58 (92)

19 (23) 11 (23) 14 (23) 11 (23) 55 (92)

23 (23) 19 (23) 17 (23) 12 (23) 71 (92)

23 (23) 20 (23) 16 (23) 12 (23) 71 (92)

86 (92) 66 (92) 57 (92) 46 (92) 255 (368)

In parenthesis are the data points for the balanced case with no missing values. Data points per baby (15, 13, 14, 14, 16, 14, 14, 12, 14, 4, 9, 15, 8, 7, 13, 12, 10, 11, 11, 10, 9, 6, 4).

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Fig. 3. HR (±STD) at different ages during the feeding paradigm. Means and confidence intervals for all the levels of AGE and SITUATION are presented as error bars. The difference between newborn and other ages is clearly seen and also the significant difference between nutritive sucking and all other situations.

The univariate approach and the rather conservative assumption of maximum non-sphericity is a useful procedure to derive statistical tests for repeated measures when missing values exist and it is not possible to reliably estimate the covariance structure of the different data sets. For the main effects (AGE, SITUATION) we also used post hoc multiple comparisons to examine the individual pairs for significant differences. The selected post hoc tests for all pairs of a main effect are based on the Bonferroni adjustments for the Student’s t statistic, i.e. individual comparison level alpha/k, where the number of comparisons is k = (4 − 1)/2 = 6 and the overall significance level was chosen as alpha = 0.05. Means and confidence intervals for all the levels of AGE and SITUATION for every variable are presented in Figs. 3 and 4. ANOVA tables and the relevant statistical tests are presented in Table 3. 3. Results The pattern of cardiac responses through the different phases of the feeding paradigm was largely similar at all tested ages (Figs. 3 and 4). In all HRV variables, the interactions between age and situation were found negligible (p-values and degrees of freedom presented in Table 3). However, as age and situation independently produced significant effects, the sucking effects (i.e. situation) and the maturation effects (i.e. age) on HRV are separately described in detail. In general, feeding produced significant changes in HR and in most of the HRV variables. In addition, maturation produced significant changes in HRV when age was set as an independent factor. 3.1. Effect of nutritive and non-nutritive sucking Decreases and increases in HR related to bursts and breaks in nutritive sucking were clearly seen (Fig. 2). Feeding differed significantly from all other situations in every variable except in peak frequency of the HF band, where there was no significant difference between situations. In fact, in all variables (with this one exception) only feeding differed from other situations and no other significant differences were found. The measure was lowest during feeding in RR, STD of RR, STD of HR, RMSSD, SD1, SD2, and in the absolute power of HF and VHF bands, and highest during feeding in HR and the peak frequency of the VHF band. 3.2. Effect of age HR was lowest in newborns and highest in 6-week-old infants. After 6 weeks the HR slowly decreased with age. However, the difference was only significant between newborn and all other ages. Age had a corresponding influence on STD of RR, STD of HR, RMSSD, SD1 and the absolute power of HF and VHF bands. All these measures were highest in newborns and lowest at the age of 6 weeks. There was a trend of an

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Fig. 4. HRV variables at different ages during the feeding paradigm. Values are presented as natural logarithms (ln). Means and confidence intervals for all the levels of AGE and SITUATION are plotted. Significances are seen in ANOVA Table 3. Ages: 1: newborn, 2: 6 weeks, 3: 12 weeks, 4: 24 weeks. Situations: 1: before feeding, 2: pacifier sucking, 3: nutritive sucking, 4: after feeding.

increase at the age of 12 weeks in all these measures but not as high as in newborns. At the age of 24 weeks these measures returned to their lower level. Significant differences were detected between newborn and all other ages, and between the ages of 6 and 12 weeks. The peak frequency of the VHF band resembled the behaviour of HR, but the only significant difference was between newborns and the age of 6 weeks. Age had no significant influence in the peak frequency of the high frequency band. 4. Discussion The effects of the non-nutritive and nutritive sucking on HR and HRV were examined in the same babies from newborn to the age of 24 weeks. The results demonstrated that feeding produces changes in the cardiac response, and its influence seems to remain constant throughout the first 6 months of life. During feeding there was an increase in HR at every age compared to the non-feeding situation, and in addition a decrease in many HRV parameters describing short-term variability (e.g. HF, RMSSD and SD1) and reflecting changes

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Table 3 AGE and SITUATION and their interaction, and the between-subjects random factor BABY Analysis of variance Source of variation Error (d.f. = 217) AGE (d.f. = 3) SITUATION (d.f. = 3) Interaction (d.f. = 9) BABY (d.f. = 22) Significant differences at 0.05 Level (Bonferroni)

F p** p*** HR 68.51 <0.0001 <0.0001 15.10 <0.0001 0.0002 0.44 Not significant 3.59 <0.0001 – AGE: 1–2, 1–3, 1–4, (2–4)* SIT: 3-1, 3-2, 3-4

STD HR 17.53 <0.0001 0.0002 22.64 <0.0001 <0.0001 1.47 Not significant 4.03 <0.0001 – AGE: 1–2, 1–3, 1–4, 2–3 SIT: 3-1, 3-2, 3-4

RR 70.18 <0.0001 <0.0001 15.25 <0.0001 0.0002 0.44 Not significant 3.57 <0.0001 – AGE: 1–2, 1–3, 1–4, (2–4)* SIT: 3-1, 3-2,3-4

STD RR

RMSSD

SD1

SD2

36.93 <0.0001 <0.0001 20.95 <0.0001 <0.0001 0.70 Not significant 3.97 <0.0001 – AGE: 1–2, 1–3, 1–4, 2–3 SIT: 3-1, 3-2, 3-4

46.54 <0,0001 <0.0001 11.98 <0.0001 0.0009 0.47 Not significant 3.82 <0.0001 – AGE: 1–2, 1–3, 1–4, 2–3, (2–4)* SIT: 3-1, 3-2, 3-4

47.47 <0.0001 <0.0001 13.01 <0.0001 0.0006 0.49 Not significant 3.93 <0.0001 – 1–2, 1–3, 1–4, 2–3 3-1, 3-2, 3-4

39.57 <0.0001 <0.0001 28.14 <0.0001 <0.0001 1.513 Not significant 3.77 <0.0001 – 1–2, 1–3, 1–4 3-1, 3-2, 3-4

PHF 0.38 1.61 0.75 1.40 – –

Not significant Not significant Not significant Not significant

–

PVHF

AHF

AVHF

2.28 0.0807 0.1358 8.83 <0.0001 0.004 0.83 Not significant 0.82 Not significant – 1–2 (sig. 0.048) 3-1, 3-2 (sig. 0.05), 3-4

36.04 <0.0001 <0.0001 22.36 <0.0001 <0.0001 0.52 Not significant 4.12 <0.0001 – 1–2, 1–3, 1–4, 2–3, (2–4)* 3-1, 3-2, 3-4

36.96 <0.0001 <0.0001 10.93 <0.0001 0.0015 0.30 Not significant 3.64 <0.0001 – 1–2, 1–3, 1–4, 2–3 3-1, 3-2, 3-4

The F ratio is computed based on Type III sum of squares of SPSS. **p shows p-values based on the assumption of sphericity, ***p based on adjusted degrees of freedom (maximum non-sphericity). Significant differences are shown on the grey background. Multiple comparisons for mean differences, significant differences at the 0.05 level, *(.) significant differences at the 0.1 level. All the tests are based on log-transformed data. Ages: 1: newborn, 2: 6 weeks, 3: 12 weeks, 4: 24 weeks. Situations: 1: before feeding, 2: pacifier sucking, 3: nutritive sucking, 4: after feeding.

in the vagal input. Vagal tone decreased during nutritive sucking. HR and HRV both returned to pre-feeding levels after feeding and the difference between before and after feeding was not significant. These results are consistent with previous research (Porges & Lipsitt, 1993; Portales et al., 1997; Suess et al., 2000) and lend support to the gustatory-vagal hypothesis (Porges & Lipsitt, 1993). Regardless of the age, HR and HRV behaved in the same way in the recordings, suggesting that this regulatory pattern is maintained throughout the suckling period. We also examined long-term variability in HR (SD2), which reflects sympathetic tone. SD2 decreased during feeding, demonstrating a reduction in sympathetic regulation. However, more research and longer recording periods are needed to explore the sympathetic nervous system influence on HRV during feeding and in infants. The recordings were made with same babies as repeated measurements at different ages, and the study provided information on the effect of age on HR and HRV during the first 6 months of life. However, the results are not directly comparable with previous studies because of differences in psychophysiological states during the recording sessions. In many studies the babies were asleep during recording, which allows larger data samples to be collected and fairly reliable estimates of long-term variability to be made. However, they completely lack the analysis of the maturation processes of reciprocal interaction. The results of Veerappan et al. (2000) were contrary to ours and to the gustatory-vagal hypothesis. They found the HF power to be higher in healthy preterm infants an hour after a meal than an hour before feeding. Their opposite finding might be explained by the recording time, which in their study was 1 hour after feeding. Immediate after-feeding recording probably catches different regulatory mechanisms from those an hour later. In our research, the long-term effects of feeding were not investigated. In general, HRV and HR responses during and after a meal change throughout life, but according to our results they remain stable during the first 6 months of life. There are many differences between the HRV responses of infants and adults. It is notable that the high frequency components decline in infants during feeding while in adults the power of

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low and very low components decreases. Thus, there seems to be a decrease in vagal output in infants, and a decrease in sympathetic activation in adults. Feeding combined with sucking in infants could particularly decrease the vagal output and in turn explain why their cardiac responses differ from adults. The difference in HRV also reflects the fact that sucking represents hard work for the babies. In our study, the HR variation decreased during feeding, while HR increased. This has also been widely reported in adults, particularly during exercise (Malik & Camm, 1990). It is well known that when HR increases, for example during physical activity, HRV decreases (Malik & Camm, 1990). In infants and children there is also a strong positive linear correlation between the RR interval and most HRV parameters (Massin & von Bernuth, 1997; Massin, Withofs, Mayens, Ravet, & G´erard, 2001; Schechtman & Harper, 1993). Unlike in adults, for an infant, especially a newborn baby, sucking milk is a demanding physical task, which consistently results in a reduction in the vagal input to the sinus node via the autonomic nervous system during the task in order to maintain better physical performance. From this perspective it is logical that pacifier sucking, being a less physically demanding task, did not cause such a vagal reduction. However, sucking a the breast is not as demanding a task for a 6-month-old baby as it is for a newborn, so the regulating phenomenon cannot be fully explained by physical exertion. The reduction in vagal tone may partly be explained by the synergy of sucking and gustatory stimulation, as Porges and Lipsitt (1993) demonstrated in their study, where the vagal tone decreased and HR increased along with increasing gustatory stimulation. On the other hand, in adults there is no change in HRV at high frequencies during eating, which suggests that sucking is an important determinant of this vagal regulation pattern. In the present study, pacifier sucking had no significant effect on HR or HRV at any age, which is in agreement with Di Pietro et al. (1994). In some previous studies pacifier sucking has decreased (Campos, 1994) and in others increased HR (Cohen et al., 2001, 1998). We agree with the conclusions of Cohen et al. (2001) on the contradictory findings of pacifier studies; the state before giving a pacifier is an important determinant of HR reactions. For instance, use of a pacifier following a painful procedure decreases HR (Campos, 1994). In the present study, the state of babies could not be stabilised during baseline recordings. The state varied from bawling to sleep, and that of an individual baby could even fluctuate during one recording session from crying to calm. In our study, HR was lowest in newborns, highest at the age of 6 weeks and then started to decrease. This phenomenon has been reported earlier, but the reason for it has not been elaborated. It is most likely related to the relative immaturity of the sympathetic nervous system at birth. (Garson, 2002) This finding may also suggest that sucking also functions as a stimulus for the maturation of the cardiovascular regulation. The development of HRV during aging has been studied from newborns to the elderly. Overall, aging is known to produce a decline in HRV (O’Brien, O’Hare, & Corrall, 1986; Umetani, Singer, McCraty, & Atkinson, 1998). Age seems to be an important determinant of HRV already during infancy and childhood. Finley and Nugent (1995) found that from 0 to 6 years LF and HF and total power components of variability as a well as the total power increased, followed by a decrease until 24 years of age. Villa et al. (2000) also found higher HF percentages and total power of HRV in children (mean age around 7 years) than in infants (mean age around 9 months). High frequency variability has been shown to increase significantly in 2–7 month olds (Kirjavainen et al., 2001). In the present study, most HRV variables (STD of RR, STD of HR, RMSSD, SD1, absolute power of HF band, absolute power of VHF band, SD2) were highest as newborn and lowest at the age of 6 weeks. Newborns differed from all other ages. Furthermore, there was a statistically significant increase in these parameters (except in SD2) from the age of 6–12 weeks. At the age of 24 weeks the trend was again decreasing, but the difference was not significant. Massin et al. (2001) found an increase in HRV frequency domain indices from 1 to 3 months followed by steady decreases up to 6 months. These findings are in line with our results. Here again, the study design differences restrict the comparison, since the previous studies were conducted during different sleeping states (e.g. REM sleep) (Massin et al., 2001). 5. Conclusions The present study demonstrated that the HR and HRV responses to nutritive and non-nutritive sucking remain stable during the first 6 months of life. The decrement of short-term HR variation during sucking lends support to the gustatory-vagal hypothesis. Tentative evidence of sympathetic downregulation was also found, but further studies with larger ECG samples are required for verification. The results revealed that cardiac responses to nutritive and non-nutritive sucking are different. Moreover, it seems that the difference between adult and infant HRV reactions

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during eating are not only due to sucking. However, according to our studies, the decrement in vagal activity during feeding that is characteristic of the suckling period pertained to both physical strain and adaptation mechanisms related to sucking. The study provides valuable follow-up information on the maturation of HR and HRV regulation during the first 6 months of life. The strength of our study is in the design: the recordings have been made with the same babies as repeated measurements through different ages.

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