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Impact of skin-to-skin contact on the autonomic nervous system in the preterm infant and his mother
Infant Behavior and Development 49 (2017) 83–86
Contents lists available at ScienceDirect
Infant Behavior and Development journal homepage: www.elsevier.com/locate/inbede
Short communication
Impact of skin-to-skin contact on the autonomic nervous system in the preterm infant and his mother L. Butruillea,b, L. Stormea,c
MARK
⁎,1
, A. Blouinc,1, J. De Jonckheerea,d, S. Murc, T. Margezb, T. Rakzaa,c,
a
EA4489, Environnement périnatal et santé, Faculté de médecine, Université de Lille, France Mdoloris Medical Systems, Loos, France c Pôle Femme Mère Nouveau-né, Hôpital Jeanne de Flandre, CHRU de Lille, France d INSERM CIC-IT 1403, Maison Régionale de la Recherche clinique, CHRU de Lille, France b
AR TI CLE I NF O
AB S T R A CT
Keywords: Kangaroo care Premature infant Autonomic nervous system
Before, during and after mother-newborn skin-to-skin contact (SSC), parasympathetic activity was evaluated by heart rate variability (HRV) analysis. SSC had a favorable impact on maternal and premature infant parasympathetic activities with a more pronounced response for neonates when the basal HRV values were lower, without modifications of EDIN scores, temperatures or oxygen saturation.
1. Introduction Preterm infant is at high risk to face learning and behavioral difficulties with attention deficit and emotional disturbance (Delobel-Ayoub et al., 2009). Furthermore, preterm birth and mother-infant separation due to prolonged hospitalization caused maternal stress, anxiety and depression, which contributes to alter bonding processes (Feldman and Eidelman, 2007). Skin-to-skin contact (SSC) is a widespread procedure, well-known to improve the cardio-respiratory stabilization (Bergman, Linley, & Fawcus, 2004), the temperature regulation, the stress or pain response, the behavioral states and to offer a better sleep organization during the neonatal period. It improves the long term cognitive and psychomotor development (Feldman, Rosenthal, & Eidelman, 2014) and it promotes bonding (Tessier et al., 1998). SSC also encourages mother-infant interactions and reassures the mothers on their maternal abilities (Bigelow, Power, MacLellan-Peters, Alex, & McDonald, 2012). Heart rate variability (HRV) analysis is a non-invasive method able to evaluate autonomic nervous system activity (Akselrod et al., 1981). Some studies have shown that high frequencies (over 0.15 Hz) correspond to parasympathetic activity (Saul et al., 1991), whereas low frequencies correspond to both parasympathetic and sympathetic activities (Anon, 1996). In adults, pain, fear or anxiety phenomena reduce high frequencies HRV, revealing a decreasing parasympathetic activity due to unpleasant stimuli (Miu, Heilman, & Miclea, 2009; Appelhans and Luecken, 2008). In infants, lower high frequencies HRV that reflects low parasympathetic nervous system activity, were observed during surgery (Sabourdin et al., 2013;Migeon et al., 2013) or during nociceptive stimuli (Oberlander, Grunau, Pitfield, Whitfield, & Saul, 1999; Avez-Couturier et al., 2016). Our HRV analysis is well correlated to neonatal behavioral pain scale score (EDIN, Echelle de Douleur et d’Inconfort du Nouveau-né, (Debillon et al., 2001) in the postoperative period (Faye et al., 2010) or after assisted deliveries (De Jonckheere et al., 2011). Herein, we hypothesize that SSC could potentiate maternal and neonatal parasympathetic activities. We have measured high
⁎
Corresponding author at: EA4489 Environnement Périnatal et Santé, Faculté de Médecine Pôle Recherche, 1, place de Verdun, Lille Cedex 59035, France. E-mail address: [email protected] (L. Butruille). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.infbeh.2017.07.003 Received 18 October 2016; Received in revised form 26 May 2017; Accepted 16 July 2017 0163-6383/ © 2017 Elsevier Inc. All rights reserved.
Infant Behavior and Development 49 (2017) 83–86
L. Butruille et al.
frequencies HRV using two specific indexes: ANI (Analgesia Nociception Index) for mothers and NIPE (Newborn Infant Parasympathetic Evaluation) for infants; before, during and after SSC. We also studied the impact of SSC according to newborns’ basal parasympathetic tone. 2. Methods This pilot study was prospective and observational. Inclusion criteria were: birth before 37 weeks of amenorrhea, patients hospitalized in neonatal intensive care unit older than 3 days-old; with a minor respiratory distress (FiO2 < 30%), without mechanical ventilation. Patients with congenital malformation, brain injuries, perinatal asphyxia, painkillers treatments and corticosteroid therapy were excluded from the study. Parents were orally informed and gave their consent. The study respected the Helsinki declaration. Newborns were installed on their mother’s chest in decubitus ventral position (inclination degree 30−40°). Maternal and neonatal HRV indexes were recorded: 1) 30 min before the installation in SSC, 2) during SSC and 3) 30 min after the end of the session (when the infant was back in his bed). Environmental parameters (noise, light, alarms) were controlled by a dedicated nurse and were the same for all the recordings. Recordings were performed in semi-darkness of artificial light, and sound levels were reduced and maintained as lower as possible through the use of centralized alarms and the reduction of the person number in the room. No intervention was performed from 30 min before the beginning to the end of the recording except the installation on the mother’s chest. All children were under continuous enteral and parenteral feeding. During the study, EDIN score (De Jonckheere et al., 2011), and oxygen requirements were reported by a nurse before and after SSC session. Temperature, oxygen saturation, and heart rate were recording continuously by specific sensors during the experiment and averaged according to the three study periods. Maternal heart rate was also recorded during all the session. The ANI technology is already detailed by Jeanne, Clément, De Jonckheere, Logier, & Tavernier, 2012. An algorithm allows a real time analysis in a 64 s moving window (moving period 1 s) of high frequencies HRV between 0.15 and 0.40 Hz for the ANI and over 0.15 Hz (Alexandre et al., 2013) for the NIPE (NIPE monitor® and ANI monitor ®, Mdoloris Medical Systems, Loos, France). Maternal ANI and neonatal NIPE are numerical values between 0 and 100. A high NIPE or ANI value correspond to a high parasympathetic activity, so it reflects patient’s wellbeing. ANI and NIPE values were recorded continuously during the three periods: before, during and after SSC and then averaged during each period. We have evaluated the difference (ΔNIPE) between the NIPE value at the beginning of the SSC (=basal NIPE) and the NIPE value at 60 min of SSC. We have determined a NIPE threshold from the regression line resulting to basal NIPE and ΔNIPE values (Fig. 1). Consequently, data were grouped relative to NIPE threshold. Data are presented as medians and 1st-3rd quartiles. Non parametric Friedman and Wilcoxon tests were used for time repeated values and Mann-Whitney tests were used for comparison between both groups. The significance threshold was fixed at P < 0.05. Statistical analysis were realized with SPSS 20.0 Software (IBM, New York, United States). 3. Results Twenty two infants (13 boys and 9 girls) and their mothers were included in the study. Mothers were 32 (30–34) years old with a parity at 2 (1–2). The infants’ median birth term were 27 + 2 (26 + 0–29 + 3) weeks of amenorrhea (WA), and the median birth weight was 900 [530–1210] g. At the moment of the study newborns were at a median age of 31 + 4 (29 + 2–31 + 5) WA and weighed 1100 (970–1490) g. Oxygen saturation (upper than 95% for both groups), oxygen requirements (21%), body temperature (36.0–36.4) and EDIN scores (lower or equal to 2) were not significantly different when we compared the periods before, during and after the SSC. The repartition of respiratory support was as followed: CPAP (Continuous Positive Airway Pressure, 64%), oxygen with nasal cannula (27%), Optiflow (4.5%) and Ambient Air (4.5%).
Fig. 1. Relation between the Newborn Infant Parasympathetic Evaluation variations (ΔNIPE) and the basal NIPE value, 60 min after the beginning of skin-to-skin contact.
84
Infant Behavior and Development 49 (2017) 83–86
L. Butruille et al.
Table 1 Maternal and neonatal heart rate and wellbeing indexes: ANI and NIPE. NIPE ≥ 57 group n=9
Friedman (P value)
n = 22
NIPE < 57 group n = 13
All patients
NIPE < 57
NIPE ≥ 57
Mann-Whitney (P value) < 57 vs ≥57
96 (87–102)
95 (83–99)
97 (93–103)
< 0.0001
< 0.0001
0.032
0.356
84 (81–89) ***
83 (79–85) **
86 (82 −89) *
91 (86–101)
94 (83–108)
All patients
Maternal parameters
HEART RATE Before HEART RATE During HEART RATE After ANI Before ANI During ANI After
++
90 (87–92)
0.117
+
0.867
+++
70 (59–79) 80 (72–83) * 75 (54–79)
75 (66–80) 80 (76–85) 76 (49–80)
+++
66 (55–69) 77 (70–81) 70 (54–77)
< 0.0001
0.005
0.044
0.095 0.349 0.841
0.956
0.794
0.459
0.089
+
+++
Neonatal parameters
HEART RATE Before HEART RATE During HEART RATE After NIPE Before NIPE During NIPE After
159 (147–167)
154 (149–160)
169 (163–172)
155 (150–164)
154 (148–156)
162 (152–164)
0.301
155 (151–165)
153 (150–158)
165 (157–166)
0.151
55 (50–60) 56 (51–61) 56 (51–61)
51 (48–52) 55 (50–58) * 51 (49–54) +
60 (60–62) 57 (52–61) 59 (56–61)
0.588
0.040
0.187
< 0.0001 0.640 0.023
Data are presented as medians (1st quartile–3rd quartile). Wilcoxon tests: * data during versus before; + data after versus during. One symbol when P ≤ 0.05, two symbols when P ≤ 0.01, three symbols P ≤ 0.001.
The Fig. 1 shows that there was a significant correlation between the basal NIPE value and the ΔNIPE at 60 min after the beginning to SSC (P = 0.001). Hence, we used the relation between basal NIPE value and ΔNIPE to determine graphically a threshold: 57. Positive ΔNIPE values were found when infants presented a basal NIPE value < 57, it represented an increase of neonatal parasympathetic activity in comparison to the parasympathetic activity that preceded the installation on the mother’s chest; whereas negative ΔNIPE values were found when the basal NIPE value was upper or equal to 57. Then we have realized a sub-analysis of ANI, NIPE and heart rate parameters as represented in Table 1. Maternal heart rate decreased during the SSC and recovered basal value at the end of the session. ANI values were lower at the end of SSC in both groups. Neonatal heart rate values were similar during all studied periods for both groups. To finish, the main results is that the NIPE rose during the SSC only in the group with basal NIPE value < 57 (P = 0.024) and return to the value before the SSC after the session. The group with basal NIPE ≥ 57 showed a slight but not significant NIPE drop during the SSC. 4. Discussion A strong reduction of parasympathetic nervous system activity and a failure of maturation was found in very preterm newborn infants (Patural et al., 2008). Thereby, we hypothesize that SSC could potentiate maternal and neonatal parasympathetic activities. Our data showed a significant increase of ANI during the SSC for the mothers. This data associated to the fall of heart rate during the session confirmed the parasympathetic nervous system activation. When the infants were less comfortable at the beginning of SSC (basal NIPE < 57), our data showed a rise of NIPE values, but we did not show any benefit of SSC on the parasympathetic activity when infants were more comfortable at the beginning of the session (basal NIPE ≥ 57). We are conscious that the subgroups did not reveal any significant difference in their EDIN scores before the SSC, and we assume that the behavioral pain scale is not enough sensitive in the low values, herein EDIN values were ≤ 2. The threshold found in this study (value: 57) corresponds exactly to the threshold found by Boselli et al. in a study on postoperative pain felt by adult patients. Authors found that an ANI value under 57 reflected a patient’s discomfort (Boselli et al., 2013). Other studies have observed an increase of high frequencies HRV during SSC (McCain, Ludington-Hoe, Swinth, & Hadeed, 2005; Feldman and Eidelman, 2003). More precisely, Feldman et al. found that 1 h/day of SSC during 24 consecutive days increased the vagal tone of 37 weeks-old infants compared to a control group. It suggests a better maturation of the parasympathetic nervous system (Feldman and Eidelman, 2003). If SSC was associated to maternal singing, benefits on parasympathetic nervous system stimulation are higher and there was less maternal anxiety (Arnon et al., 2014). High frequencies HRV was also increased by a hand containment associated to a reading (Alexandre et al., 2013), or by massages (Smith et al., 2013). Moreover, the reduction of high frequencies HRV after a heel prick is attenuated when the child is in SSC (Cong, Ludington-Hoe, McCain, & Fu, 2009; Choudhary et al., 2016). Maternal depression reduces mother-infant interactions and reduces the infant’s parasympathetic tone. A study of 56 preterm infants revealed that the parasympathetic activity evaluated by high frequencies HRV at 37 weeks of postconceptional age was correlated to the quality of early interactions at 3 months of age. The authors found that parasympathetic activity level is a predictor of mother-infant interactions (Feldman and Eidelman, 2007). Taken together, our data indicate that neonates comfort should be 85
Infant Behavior and Development 49 (2017) 83–86
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taken in consideration before SSC to optimize favorable impact on parasympathetic tone, especially for preterm infants. However, further investigations are needed to confirm our results with more data, and with a specific attention to maternal anxiety and/or depression. 5. Conclusion We have shown with our study that SSC increased parasympathetic activity only when the basal NIPE value was low at the beginning; and for the first time we observed a raise of mother’s parasympathetic activity during SSC. SSC contributes to improve the parasympathetic activity of preterm infant that is susceptible to enhance the mother-infant relationship. This hypothesis offers a new explanation to child psychiatrist on the understanding of bonding processes. Conflicts of interest L.B. was employed by Mdoloris Medical Systems. J.D.J. is shareholder of the Mdoloris Medical Systems company. Acknowledgements This study has been realized thanks to the Neodoloris project, financed by the Agence Nationale pour la Recherche (ANR 11 TecSan 011). A fuller report could be provided upon request. References Akselrod, S., Gordon, D., Ubel, F. A., Shannon, D. C., Berger, A. C., & Cohen, R. J. (1981). Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science, 213, 220–222. Alexandre, C., De Jonckheere, J., Rakza, T., Mur, S., Carette, D., Logier, R., et al. (2013). Impact of cocooning and maternal voice on the autonomic nervous system activity in the premature newborn infant]. Archives de Pediatrie, 20, 963–968. Anon (1996). Heart rate variability: standards of measurement physiological interpretation and clinical use. Task force of the european society of cardiology and the North American society of pacing and electrophysiology. Circulation, 93, 1043–1065. Appelhans, B. M., & Luecken, L. J. (2008). Heart rate variability and pain: Associations of two interrelated homeostatic processes. Biological Psychology, 77, 174–182. Arnon, S., Diamant, C., Bauer, S., Regev, R., Sirota, G., & Litmanovitz, I. (2014). Maternal singing during kangaroo care led to autonomic stability in preterm infants and reduced maternal anxiety. Acta Paediatrica, Oct(103), 1039–10344. Avez-Couturier, J., De Jonckheere, J., Jeanne, M., Vallée, L., Cuisset, J. M., & Logier, R. (2016). Assessment of procedural pain in children using analgesia nociception index: A pilot study. Clinical Journal of Pain [Epub ahead of print]. Bergman, N. J., Linley, L. L., & Fawcus, S. R. (2004). Randomized controlled trial of skin-to-skin contact from birth versus conventional incubator for physiological stabilization in 1200- to 2199-gram newborns. Acta Paediatri, 93, 779–785. Bigelow, A., Power, M., MacLellan-Peters, J., Alex, M., & McDonald, C. (2012). Effect of mother/infant skin-to-skin contact on postpartum depressive symptoms and maternal physiological stress. Journal of Obstetric, Gynecologic, and Neonatal Nursing, 41, 369–382. Boselli, E., Daniela-Ionescu, M., Bégou, G., Bouvet, L., Dabouz, R., Magnin, C., et al. (2013). Prospective observational study of the non-invasive assessment of immediate postoperative pain using the analgesia/nociception index (ANI). British Journal of Anaesthesia, 111, 453–459. Choudhary, M., Dogiyal, H., Sharma, D., Datt Gupta, B., Madabhavi, I., Choudhary, J. S., et al. (2016). To study the effect of Kangaroo Mother Care on pain response in preterm neonates and to determine the behavioral and physiological responses to painful stimuli in preterm neonates: a study from western Rajasthan. J Matern Fetal Neonatal Med, 29, 826–831. Cong, X., Ludington-Hoe, S. M., McCain, G., & Fu, P. (2009). Kangaroo Care modifies preterm infant heart rate variability in response to heel stick pain: pilot study. Early Human Development, 85, 561–567. De Jonckheere, J., Rakza, T., Logier, R., Jeanne, M., Jounwaz, R., & Storme, L. (2011). Heart rate variability analysis for newborn infants prolonged pain assessment. Conference Proceeding of the IEEE Engineering in Medicine and Biology Society, 2011, 7747–7750. Debillon, T., Zupan, V., Rayault, N., Magny, J., Dehan, M., & Abu-Saad, H. (2001). Development and initial validation of the EDIN scale, a new tool for assessing prolonged pain in preterm infants. Archives of Disease in Childhood. Fetal and Neonatal Edition, 85, 36–41. Delobel-Ayoub, M., Arnaud, C., White-Koning, M., Casper, C., Pierrat, V., Garel, M., et al. (2009). EPIPAGE Study Group: Behavioral problems and cognitive performance at 5 years of age after very preterm birth: The EPIPAGE Study. Pediatrics, 123, 1485–1492. Faye, P. M., De Jonckheere, J., Logier, R., Kuissi, E., Jeanne, M., Rakza, T., et al. (2010). Newborn infant pain assessment using heart rate variability analysis. Clinical Journal of Pain, 26, 777–782. Feldman, R., & Eidelman, A. I. (2003). Skin-to-skin contact (kangaroo care) accelerates autonomic and neurobehavioural maturation in preterm infants. Developmental Medicine & Child Neurology, 45(4), 274–281. Feldman, R., & Eidelman, A. I. (2007). Maternal postpartum behavior and the emergence of infant–mother and infant–father synchrony in preterm and full-term infants: The role of neonatal vagal tone. Developmental Psychobiology, 49, 290–302. Feldman, R., Rosenthal, Z., & Eidelman, A. I. (2014). Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biological Psychiatry, 75, 56–64. Jeanne, M., Clément, C., De Jonckheere, J., Logier, R., & Tavernier, B. (2012). Variations of the analgesia nociception index during general anaesthesia for laparoscopic abdominal surgery. Journal of Clinical Monitoring and Computing, 26, 289–294. McCain, G. C., Ludington-Hoe, S. M., Swinth, J. Y., & Hadeed, A. J. (2005). Heart rate variability responses of a preterm infant to kangaroo care. Journal of Obstetric, Gynecologic, and Neonatal Nursing, 34, 689–694. Migeon, A., Desgranges, F. P., Chassard, D., Blaise, B. J., De Queiroz, M., Stewart, A., et al. (2013). Pupillary reflex dilatation and analgesia nociception index monitoring to assess the effectiveness of regional anesthesia in children with sevoflurane. Paediatric Anaesthesia, 12, 1160–1165. Miu, A. C., Heilman, R. M., & Miclea, M. (2009). Reduced heart rate variability and vagal tone in anxiety: trait versus state, and the effects of autogenic training. Autonomic Neuroscience, 145, 99–103. Oberlander, T. F., Grunau, R. E., Pitfield, S., Whitfield, M. F., & Saul, J. P. (1999). The developmental character of cardiac autonomic responses to an acute noxious event in 4- and 8-month-old healthy infants. Pediatric Research, 45, 519–525. Patural, H., Pichot, V., Jaziri, F., Teyssier, G., Gaspoz, J. M., Roche, F., et al. (2008). Automatic cardiac control of very preterm newborns: A prolonged dysfunction. Early Human Development, 84, 681–6873. Sabourdin, N., Arnaout, M., Louvet, N., Guye, M. L., Piana, F., & Constant, I. (2013). Pain monitoring in anesthetized children: First assessment of skin conductance and analgesianociception index at different infusion rates of remifentanil. Paediatric Anaesthesia, 23, 149–155. Saul, J. P., Berger, R. D., Albrecht, P., Stein, S. P., Chen, M. H., & Cohen, R. J. (1991). Transfer function analysis of the circulation: Unique insights into cardiovascular regulation. American Journal of Physiology, 261, H1231–45. Smith, S. L., Lux, R., Haley, S., Slater, H., Beachy, J., & Moyer-Mileur, L. J. (2013). The effect of massage on heart rate variability in preterm infants. Journal of Perinatology, 33, 59–64. Tessier, R., Cristo, M., Velez, S., Giron, M., de Calume, Z. F., Ruiz-Palaez, J. G., et al. (1998). Kangaroo mother care and the bonding hypothesis. Pediatrics, 102 [e17-e17].
86
Contents lists available at ScienceDirect
Infant Behavior and Development journal homepage: www.elsevier.com/locate/inbede
Short communication
Impact of skin-to-skin contact on the autonomic nervous system in the preterm infant and his mother L. Butruillea,b, L. Stormea,c
MARK
⁎,1
, A. Blouinc,1, J. De Jonckheerea,d, S. Murc, T. Margezb, T. Rakzaa,c,
a
EA4489, Environnement périnatal et santé, Faculté de médecine, Université de Lille, France Mdoloris Medical Systems, Loos, France c Pôle Femme Mère Nouveau-né, Hôpital Jeanne de Flandre, CHRU de Lille, France d INSERM CIC-IT 1403, Maison Régionale de la Recherche clinique, CHRU de Lille, France b
AR TI CLE I NF O
AB S T R A CT
Keywords: Kangaroo care Premature infant Autonomic nervous system
Before, during and after mother-newborn skin-to-skin contact (SSC), parasympathetic activity was evaluated by heart rate variability (HRV) analysis. SSC had a favorable impact on maternal and premature infant parasympathetic activities with a more pronounced response for neonates when the basal HRV values were lower, without modifications of EDIN scores, temperatures or oxygen saturation.
1. Introduction Preterm infant is at high risk to face learning and behavioral difficulties with attention deficit and emotional disturbance (Delobel-Ayoub et al., 2009). Furthermore, preterm birth and mother-infant separation due to prolonged hospitalization caused maternal stress, anxiety and depression, which contributes to alter bonding processes (Feldman and Eidelman, 2007). Skin-to-skin contact (SSC) is a widespread procedure, well-known to improve the cardio-respiratory stabilization (Bergman, Linley, & Fawcus, 2004), the temperature regulation, the stress or pain response, the behavioral states and to offer a better sleep organization during the neonatal period. It improves the long term cognitive and psychomotor development (Feldman, Rosenthal, & Eidelman, 2014) and it promotes bonding (Tessier et al., 1998). SSC also encourages mother-infant interactions and reassures the mothers on their maternal abilities (Bigelow, Power, MacLellan-Peters, Alex, & McDonald, 2012). Heart rate variability (HRV) analysis is a non-invasive method able to evaluate autonomic nervous system activity (Akselrod et al., 1981). Some studies have shown that high frequencies (over 0.15 Hz) correspond to parasympathetic activity (Saul et al., 1991), whereas low frequencies correspond to both parasympathetic and sympathetic activities (Anon, 1996). In adults, pain, fear or anxiety phenomena reduce high frequencies HRV, revealing a decreasing parasympathetic activity due to unpleasant stimuli (Miu, Heilman, & Miclea, 2009; Appelhans and Luecken, 2008). In infants, lower high frequencies HRV that reflects low parasympathetic nervous system activity, were observed during surgery (Sabourdin et al., 2013;Migeon et al., 2013) or during nociceptive stimuli (Oberlander, Grunau, Pitfield, Whitfield, & Saul, 1999; Avez-Couturier et al., 2016). Our HRV analysis is well correlated to neonatal behavioral pain scale score (EDIN, Echelle de Douleur et d’Inconfort du Nouveau-né, (Debillon et al., 2001) in the postoperative period (Faye et al., 2010) or after assisted deliveries (De Jonckheere et al., 2011). Herein, we hypothesize that SSC could potentiate maternal and neonatal parasympathetic activities. We have measured high
⁎
Corresponding author at: EA4489 Environnement Périnatal et Santé, Faculté de Médecine Pôle Recherche, 1, place de Verdun, Lille Cedex 59035, France. E-mail address: [email protected] (L. Butruille). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.infbeh.2017.07.003 Received 18 October 2016; Received in revised form 26 May 2017; Accepted 16 July 2017 0163-6383/ © 2017 Elsevier Inc. All rights reserved.
Infant Behavior and Development 49 (2017) 83–86
L. Butruille et al.
frequencies HRV using two specific indexes: ANI (Analgesia Nociception Index) for mothers and NIPE (Newborn Infant Parasympathetic Evaluation) for infants; before, during and after SSC. We also studied the impact of SSC according to newborns’ basal parasympathetic tone. 2. Methods This pilot study was prospective and observational. Inclusion criteria were: birth before 37 weeks of amenorrhea, patients hospitalized in neonatal intensive care unit older than 3 days-old; with a minor respiratory distress (FiO2 < 30%), without mechanical ventilation. Patients with congenital malformation, brain injuries, perinatal asphyxia, painkillers treatments and corticosteroid therapy were excluded from the study. Parents were orally informed and gave their consent. The study respected the Helsinki declaration. Newborns were installed on their mother’s chest in decubitus ventral position (inclination degree 30−40°). Maternal and neonatal HRV indexes were recorded: 1) 30 min before the installation in SSC, 2) during SSC and 3) 30 min after the end of the session (when the infant was back in his bed). Environmental parameters (noise, light, alarms) were controlled by a dedicated nurse and were the same for all the recordings. Recordings were performed in semi-darkness of artificial light, and sound levels were reduced and maintained as lower as possible through the use of centralized alarms and the reduction of the person number in the room. No intervention was performed from 30 min before the beginning to the end of the recording except the installation on the mother’s chest. All children were under continuous enteral and parenteral feeding. During the study, EDIN score (De Jonckheere et al., 2011), and oxygen requirements were reported by a nurse before and after SSC session. Temperature, oxygen saturation, and heart rate were recording continuously by specific sensors during the experiment and averaged according to the three study periods. Maternal heart rate was also recorded during all the session. The ANI technology is already detailed by Jeanne, Clément, De Jonckheere, Logier, & Tavernier, 2012. An algorithm allows a real time analysis in a 64 s moving window (moving period 1 s) of high frequencies HRV between 0.15 and 0.40 Hz for the ANI and over 0.15 Hz (Alexandre et al., 2013) for the NIPE (NIPE monitor® and ANI monitor ®, Mdoloris Medical Systems, Loos, France). Maternal ANI and neonatal NIPE are numerical values between 0 and 100. A high NIPE or ANI value correspond to a high parasympathetic activity, so it reflects patient’s wellbeing. ANI and NIPE values were recorded continuously during the three periods: before, during and after SSC and then averaged during each period. We have evaluated the difference (ΔNIPE) between the NIPE value at the beginning of the SSC (=basal NIPE) and the NIPE value at 60 min of SSC. We have determined a NIPE threshold from the regression line resulting to basal NIPE and ΔNIPE values (Fig. 1). Consequently, data were grouped relative to NIPE threshold. Data are presented as medians and 1st-3rd quartiles. Non parametric Friedman and Wilcoxon tests were used for time repeated values and Mann-Whitney tests were used for comparison between both groups. The significance threshold was fixed at P < 0.05. Statistical analysis were realized with SPSS 20.0 Software (IBM, New York, United States). 3. Results Twenty two infants (13 boys and 9 girls) and their mothers were included in the study. Mothers were 32 (30–34) years old with a parity at 2 (1–2). The infants’ median birth term were 27 + 2 (26 + 0–29 + 3) weeks of amenorrhea (WA), and the median birth weight was 900 [530–1210] g. At the moment of the study newborns were at a median age of 31 + 4 (29 + 2–31 + 5) WA and weighed 1100 (970–1490) g. Oxygen saturation (upper than 95% for both groups), oxygen requirements (21%), body temperature (36.0–36.4) and EDIN scores (lower or equal to 2) were not significantly different when we compared the periods before, during and after the SSC. The repartition of respiratory support was as followed: CPAP (Continuous Positive Airway Pressure, 64%), oxygen with nasal cannula (27%), Optiflow (4.5%) and Ambient Air (4.5%).
Fig. 1. Relation between the Newborn Infant Parasympathetic Evaluation variations (ΔNIPE) and the basal NIPE value, 60 min after the beginning of skin-to-skin contact.
84
Infant Behavior and Development 49 (2017) 83–86
L. Butruille et al.
Table 1 Maternal and neonatal heart rate and wellbeing indexes: ANI and NIPE. NIPE ≥ 57 group n=9
Friedman (P value)
n = 22
NIPE < 57 group n = 13
All patients
NIPE < 57
NIPE ≥ 57
Mann-Whitney (P value) < 57 vs ≥57
96 (87–102)
95 (83–99)
97 (93–103)
< 0.0001
< 0.0001
0.032
0.356
84 (81–89) ***
83 (79–85) **
86 (82 −89) *
91 (86–101)
94 (83–108)
All patients
Maternal parameters
HEART RATE Before HEART RATE During HEART RATE After ANI Before ANI During ANI After
++
90 (87–92)
0.117
+
0.867
+++
70 (59–79) 80 (72–83) * 75 (54–79)
75 (66–80) 80 (76–85) 76 (49–80)
+++
66 (55–69) 77 (70–81) 70 (54–77)
< 0.0001
0.005
0.044
0.095 0.349 0.841
0.956
0.794
0.459
0.089
+
+++
Neonatal parameters
HEART RATE Before HEART RATE During HEART RATE After NIPE Before NIPE During NIPE After
159 (147–167)
154 (149–160)
169 (163–172)
155 (150–164)
154 (148–156)
162 (152–164)
0.301
155 (151–165)
153 (150–158)
165 (157–166)
0.151
55 (50–60) 56 (51–61) 56 (51–61)
51 (48–52) 55 (50–58) * 51 (49–54) +
60 (60–62) 57 (52–61) 59 (56–61)
0.588
0.040
0.187
< 0.0001 0.640 0.023
Data are presented as medians (1st quartile–3rd quartile). Wilcoxon tests: * data during versus before; + data after versus during. One symbol when P ≤ 0.05, two symbols when P ≤ 0.01, three symbols P ≤ 0.001.
The Fig. 1 shows that there was a significant correlation between the basal NIPE value and the ΔNIPE at 60 min after the beginning to SSC (P = 0.001). Hence, we used the relation between basal NIPE value and ΔNIPE to determine graphically a threshold: 57. Positive ΔNIPE values were found when infants presented a basal NIPE value < 57, it represented an increase of neonatal parasympathetic activity in comparison to the parasympathetic activity that preceded the installation on the mother’s chest; whereas negative ΔNIPE values were found when the basal NIPE value was upper or equal to 57. Then we have realized a sub-analysis of ANI, NIPE and heart rate parameters as represented in Table 1. Maternal heart rate decreased during the SSC and recovered basal value at the end of the session. ANI values were lower at the end of SSC in both groups. Neonatal heart rate values were similar during all studied periods for both groups. To finish, the main results is that the NIPE rose during the SSC only in the group with basal NIPE value < 57 (P = 0.024) and return to the value before the SSC after the session. The group with basal NIPE ≥ 57 showed a slight but not significant NIPE drop during the SSC. 4. Discussion A strong reduction of parasympathetic nervous system activity and a failure of maturation was found in very preterm newborn infants (Patural et al., 2008). Thereby, we hypothesize that SSC could potentiate maternal and neonatal parasympathetic activities. Our data showed a significant increase of ANI during the SSC for the mothers. This data associated to the fall of heart rate during the session confirmed the parasympathetic nervous system activation. When the infants were less comfortable at the beginning of SSC (basal NIPE < 57), our data showed a rise of NIPE values, but we did not show any benefit of SSC on the parasympathetic activity when infants were more comfortable at the beginning of the session (basal NIPE ≥ 57). We are conscious that the subgroups did not reveal any significant difference in their EDIN scores before the SSC, and we assume that the behavioral pain scale is not enough sensitive in the low values, herein EDIN values were ≤ 2. The threshold found in this study (value: 57) corresponds exactly to the threshold found by Boselli et al. in a study on postoperative pain felt by adult patients. Authors found that an ANI value under 57 reflected a patient’s discomfort (Boselli et al., 2013). Other studies have observed an increase of high frequencies HRV during SSC (McCain, Ludington-Hoe, Swinth, & Hadeed, 2005; Feldman and Eidelman, 2003). More precisely, Feldman et al. found that 1 h/day of SSC during 24 consecutive days increased the vagal tone of 37 weeks-old infants compared to a control group. It suggests a better maturation of the parasympathetic nervous system (Feldman and Eidelman, 2003). If SSC was associated to maternal singing, benefits on parasympathetic nervous system stimulation are higher and there was less maternal anxiety (Arnon et al., 2014). High frequencies HRV was also increased by a hand containment associated to a reading (Alexandre et al., 2013), or by massages (Smith et al., 2013). Moreover, the reduction of high frequencies HRV after a heel prick is attenuated when the child is in SSC (Cong, Ludington-Hoe, McCain, & Fu, 2009; Choudhary et al., 2016). Maternal depression reduces mother-infant interactions and reduces the infant’s parasympathetic tone. A study of 56 preterm infants revealed that the parasympathetic activity evaluated by high frequencies HRV at 37 weeks of postconceptional age was correlated to the quality of early interactions at 3 months of age. The authors found that parasympathetic activity level is a predictor of mother-infant interactions (Feldman and Eidelman, 2007). Taken together, our data indicate that neonates comfort should be 85
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taken in consideration before SSC to optimize favorable impact on parasympathetic tone, especially for preterm infants. However, further investigations are needed to confirm our results with more data, and with a specific attention to maternal anxiety and/or depression. 5. Conclusion We have shown with our study that SSC increased parasympathetic activity only when the basal NIPE value was low at the beginning; and for the first time we observed a raise of mother’s parasympathetic activity during SSC. SSC contributes to improve the parasympathetic activity of preterm infant that is susceptible to enhance the mother-infant relationship. This hypothesis offers a new explanation to child psychiatrist on the understanding of bonding processes. Conflicts of interest L.B. was employed by Mdoloris Medical Systems. J.D.J. is shareholder of the Mdoloris Medical Systems company. 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