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Stress
The International Journal on the Biology of Stress
Volume 27, 2024 - Issue 1
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Research Article

Exposure to prenatal stressors and infant autonomic nervous system regulation of stress

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Article: 2327328 | Received 11 Sep 2023, Accepted 02 Mar 2024, Published online: 18 Mar 2024

References

  • Ali, N., & Nater, U. (2020). Salivary alpha-amylase as a biomarker of stress in behavioral medicine. International Journal of Behavioral Medicine, 27(3), 1–10. https://doi.org/10.1007/s12529-019-09843-x
  • Andrianome, S., Gobert, J., Hugueville, L., Stéphan-Blanchard, E., Telliez, F., & Selmaoui, B. (2017). An assessment of the autonomic nervous system in the electrohypersensitive population: A heart rate variability and skin conductance study. Journal of Applied Physiology (Bethesda, Md.: 1985), 123(5), 1055–1062. https://doi.org/10.1152/japplphysiol.00229.2017
  • Antolic, A., Wood, C. E., & Keller-Wood, M. (2018). Chronic maternal hypercortisolemia in late gestation alters fetal cardiac at birth. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 314(3), R342–R352. https://doi.org/10.1152/ajpregu.00296.2017
  • Aye, C., Lewandowski, A., Oster, J., Upton, R., Davis, E., Kenworthy, Y., Boardman, H., Yu, G., Siepmann, T., Adwani, S., McCormick, K., Sverrisdottir, Y., & Leeson, P. (2018). Neonatal autonomic function after pregnancy complications and early cardiovascular development. Pediatric Research, 84(1), 85–91. https://doi.org/10.1038/s41390-018-0021-0
  • Bar-Haim, Y., Marshall, P. J., & Fox, N. A. (2000). Developmental changes in heart period and high-frequency heart period variability from 4 months to 4 years of age. Developmental Psychobiology, 37(1), 44–56. https://doi.org/10.1002/1098-2302(200007)37:1<44::AID-DEV6>3.0.CO;2-7
  • Berry, C. A., Quinn, K. A., Portillo, N., & Shalowitz, M. U. (2006). Reliability and validity of the Spanish version of the crisis in family systems–revised. Psychological Reports, 98(1), 123–132. https://doi.org/10.2466/pr0.98.1.123-132
  • Berry, C. A., Quinn, K., Shalowitz, M., & Wolf, R. (2001). Validation of the crisis in family systems–revised: A contemporary measure of life stressors. Psychological Reports, 88(3 Pt 1), 713–724. https://doi.org/10.2466/pr0.2001.88.3.713
  • Bleker, L., van Dammen, L., Leeflang, M., Limpens, J., Roseboom, T., & de Rooij, S. (2020). Hypothalamic-pituitary-adrenal axis and autonomic nervous system reactivity in children prenatally exposed to maternal depression: A systematic review of prospective studies. Neuroscience and Biobehavioral Reviews, 117, 243–252. https://doi.org/10.1016/j.neubiorev.2018.05.033
  • Bosquet Enlow, M., King, L., Schreier, H., Howard, J., Rosenfield, D., Ritz, T., & Wright, R. (2014). Maternal sensitivity and infant autonomic and endocrine stress responses. Early Human Development, 90(7), 377–385. https://doi.org/10.1016/j.earlhumdev.2014.04.007
  • Bush, N., Jones-Mason, K., Coccia, M., Caron, Z., Alkon, A., Thomas, M., Coleman-Phox, K., Wadhwa, P., Laraia, B., Adler, N., & Epel, E. (2017). Effects of pre- and postnatal maternal stress on infant temperament and autonomic nervous system reactivity and regulation in a diverse, low-income population. Development and Psychopathology, 29(5), 1553–1571. https://doi.org/10.1017/S0954579417001237
  • Cacioppo, J. T., Tassinary, L. G., & Berntson, G. G. (2017). Handbook of psychophysiology (4th ed., pp. 197–198). Cambridge University Press.
  • Cerritelli, F., Frasch, M., Antonelli, M., Viglione, C., Vecchi, S., Chiera, M., & Manzotti, A. (2021). A review on the vagus nerve and autonomic nervous system during fetal development: Searching for critical windows. Frontiers in Neuroscience, 15, 721605. https://doi.org/10.3389/fnins.2021.721605
  • Chiera, M., Cerritelli, F., Casini, A., Barsotti, N., Boschiero, D., Cavigioli, F., Corti, C., & Manzotti, A. (2020). Heart rate variability in the perinatal period: A critical and conceptual review. Frontiers in Neuroscience, 2514, 561186. PMID: 33071738; PMCID: PMC7544983. https://doi.org/10.3389/fnins.2020.561186
  • Christopoulos, G., Uy, M., & Yap, W. (2019). The body and the brain: Measuring skin conductance responses to understand the emotional experience. Organizational Research Methods, 22(1), 394–420. https://doi.org/10.1177/1094428116681073
  • Conradt, E., & Ablow, J. (2010). Infant physiological response to the still-face paradigm: Contributions of maternal sensitivity and infants’ early regulatory behavior. Infant Behavior & Development, 33(3), 251–265. https://doi.org/10.1016/j.infbeh.2010.01.001
  • Cubillo, A., Tkalcec, A., Oldenhof, H., Unternaehrer, E., Raschle, N., Kohls, G., Nauta-Jansen, L., Hervas, A., Fernandez-Rivas, A., Konrad, K., Popma, A., Freitag, C., de Brito, S., Fairchild, G., & Stadler, C. (2023). Linking heart rate variability to psychological health and brain structure in adolescents with and without conduct disorder. Frontiers in Psychiatry, 2714, 1101064. https://doi.org/10.3389/fpsyt.2023.1101064
  • Fu, M., Song, W., Yu, G., Yu, Y., & Yang, Q. (2023). Risk factors for length of NICU stay of newborns: A systematic review. Frontiers in Pediatrics, 11, 1121406. https://doi.org/10.3389/fped.2023.1121406
  • Fyfe, K., Yiallourou, S., Wong, F., Odoi, A., Walker, A., & Horne, R. (2015). The effect of gestational age at birth on post-term maturation of heart rate variability. Sleep, 38(10), 1635–1644. https://doi.org/10.5665/sleep.5064
  • Glover, V., O’Donnell, K., O’Connor, T., & Fisher, J. (2018). Prenatal maternal stress, fetal programming, and mechanisms underlying later psychopathology—A global perspective. Development and Psychopathology, 30(3), 843–854. https://doi.org/10.1017/S095457941800038X
  • Goldstein, D., Bentho, O., Park, M., & Sharabi, Y. (2011). Low-frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac autonomic outflows by baroreflexes. Experimental Physiology, 96(12), 1255–1261. https://doi.org/10.1113/expphysiol.2010.056259
  • Goldstein, D., & Cheshire, W. (2018). Roles of catechol neurochemistry in autonomic function testing. Clinical Autonomic Research: Official Journal of the Clinical Autonomic Research Society, 28(3), 273–288. https://doi.org/10.1007/s10286-018-0528-9
  • Grossman, P., & Taylor, E. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74(2), 263–285. https://doi.org/10.1016/j.biopsycho.2005.11.014
  • Hashiguchi, K., Kuriyama, N., Koyama, T., Matsui, D., Ozaki, E., Hasegawa, T., Tokuda, S., Niwa, F., Iwasa, K., Watanabe, I., Teramukai, S., Kitawaki, J., Watanabe, Y., Uehara, R., & Hosoi, H. (2020). Validity of stress assessment using heart-rate variability in newborns. Pediatrics International: Official Journal of the Japan Pediatric Society, 62(6), 694–700. https://doi.org/10.1111/ped.14149
  • Horackova, H., Karahoda, R., Vachalova, V., Turkova, H., Abad, C., & Staud, F. (2022). Functional characterization of dopamine and norepinephrine transport across the apical and basal plasma membranes of the human placental syncytiotrophoblast. Scientific Reports, 12(1), 11603. https://doi.org/10.1038/s41598-022-15790-7
  • Hunter, S., Freedman, R., Law, A., Christians, U., Holzman, J., Johnson, Z., & Hoffman, M. (2021). Maternal corticosteroids and depression during gestation and decreased fetal heart rate variability. Neuroreport, 32(14), 1170–1174. https://doi.org/10.1097/WNR.0000000000001711
  • Jacob, S., Byrne, M., & Keenan, K. (2009). Neonatal physiological regulation is associated with perinatal factors: A study of neonates born to healthy African American women living in poverty. Infant Mental Health Journal, 30(1), 82–94. https://doi.org/10.1002/imhj.20204
  • Javorka, K., Haskova, K., Czippelova, B., Zibolen, M. & Javorka, M. (2021). Blood pressure variability and baroreflex sensitivity in premature newborns - An effect of postconceptional and gestational age. Frontiers in Pediatrics, 9, 653573. https://doi.org/10.3389/fped.2021.653573.
  • Jung, W., Jang, K., & Lee, S. (2019). Heart and brain interaction of psychiatric illness: A review focused on heart rate variability, cognitive function, and quantitative electroencephalography. Clinical Psychopharmacology and Neuroscience: The Official Scientific Journal of the Korean College of Neuropsychopharmacology, 17(4), 459–474. https://doi.org/10.9758/cpn.2019.17.4.459
  • Kemp, A., & Quintana, D. (2013). The relationship between mental and physical health: Insights from the study of heart rate variability. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 89(3), 288–296. https://doi.org/10.1016/j.ijpsycho.2013.06.018
  • Kim, H., Cheon, E., Bai, D., Lee, Y., & Koo, B. (2018). Stress and heart rate variability: A meta-analysis and review of the literature. Psychiatry Investigation, 15(3), 235–245. https://doi.org/10.30773/pi.2017.08.17
  • Köhler-Dauner, F., Roder, E., Gulde, M., Mayer, I., Fegert, J. M., Ziegenhain, U., & Waller, C. (2022). Maternal sensitivity modulates child’s parasympathetic mode and buffers sympathetic activity in a free play situation. Frontiers in Psychology, 1913, 868848. PMID: 35529563; PMCID: PMC9068013. https://doi.org/10.3389/fpsyg.2022.868848
  • Kroenke, K., Spitzer, R. L., & Williams, J. B. (2001). The PHQ-9: Validity of a brief depression severity measure. Journal of General Internal Medicine, 16(9), 606–613. https://doi.org/10.1046/j.1525-1497.2001.016009606.x
  • Laborde, S., Mosley, E., & Thayer, J. (2017). Heart rate variability and cardiac vagal tone in psychophysiological research: Recommendations for experiment planning, data analysis, and data reporting. Frontiers in Psychology, 8, 213. https://doi.org/10.3389/fpsyg.2017.00213
  • Lautarescu, A., Craig, M., & Glover, V. (2020). Prenatal stress: Effects on fetal and child brain development. International Review of Neurobiology, 150, 17–40. https://doi.org/10.1016/bs.irn.2019.11.002
  • Lester, B., Conradt, E., Lagasse, L., Tronick, E., Padbury, J., & Marsit, C. (2018). Epigenetic programming by maternal behavior in the human infant. Pediatrics, 142(4), e20171890. https://doi.org/10.1542/peds.2017-1890
  • Lin, Y., & Diedrich, A. (2022). Methods on the assessment of human baroreflex function. Frontiers in Neuroscience, 2816, 965406. PMID: 35837120; PMCID: PMC9274245. https://doi.org/10.3389/fnins.2022.965406
  • Lobel, M., Cannella, D. L., Graham, J. E., DeVincent, C., Schneider, J., & Meyer, B. A. (2008). Pregnancy-specific stress, prenatal health behaviors, and birth outcomes. Health Psychology: official Journal of the Division of Health Psychology, American Psychological Association, 27(5), 604–615. https://doi.org/10.1037/a0013242
  • Longin, E., Gerstner, T., Schaible, T., Lenz, T., & König, S. (2006). Maturation of the autonomic nervous system: Differences in heart rate variability in premature vs. term infants. Journal of Perinatal Medicine, 34(4), 303–308. https://doi.org/10.1515/JPM.2006.058
  • McCraty, R., & Shaffer, F. (2015). Heart rate variability: New perspectives on physiological mechanisms, assessment of self-regulatory capacity, and health risk. Global Advances in Health and Medicine, 4(1), 46–61. https://doi.org/10.7453/gahmj.2014.073
  • Mesman, J., van Ijzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2009). The many faces of the still-face paradigm: A review and meta-analysis. Developmental Review, 29(2), 120–162. https://doi.org/10.1016/j.dr.2009.02.001
  • Mulkey, S., & Du Plessis, A. (2019). Autonomic nervous system development and its impact on neuropsychiatric outcome. Pediatric Research, 85(2), 120–126. https://doi.org/10.1038/s41390-018-0155-0
  • Noben, L., Verdurmen, K., Warmerdam, G., Vullings, R., Oei, S., & van Laar, J. (2019). The fetal electrocardiogram to detect the effects of betamethasone on fetal heart rate variability. Early Human Development, 130, 57–64. https://doi.org/10.1016/j.earlhumdev.2019.01.011
  • Oliveira, V., von Rosenberg, W., Montaldo, P., Adjei, T., Mendoza, J., Shivamurthappa, V., Mandic, D., & Thayyil, S. (2019). Early postnatal heart rate variability in healthy newborn infants. Frontiers in Physiology, 10, 922. https://doi.org/10.3389/fphys.2019.00922
  • Patural, H., Pichot, V., Flori, S., Giraud, A., Franco, P., Pladys, P., Beuchée, A., Roche, F., & Barthelemy, J. (2019). Autonomic maturation from birth to 2 years: Normative values. Heliyon, 75(3), e01300. https://doi.org/10.1016/j.heliyon.2019.e01300
  • Phillips, D. (2007). Programming of the stress response: A fundamental mechanism underlying the long-term effects of the fetal environment? Journal of Internal Medicine, 261(5), 453–460. https://doi.org/10.1111/j.1365-2796.2007.01801.x
  • Pinto, T., Nogueira-Silva, C., & Figueiredo, B. (2023). Fetal heart rate variability and infant self-regulation: The impact of mother’s prenatal depressive symptoms. Journal of Reproductive and Infant Psychology. Advance online publication. https://doi.org/10.1080/02646838.2023.2257730
  • Piquer, B., Fonseca, J. L., & Lara, H. E. (2017). Gestational stress, placental norepinephrine transporter and offspring fertility. Reproduction (Cambridge, England), 153(2), 147–155. https://doi.org/10.1530/REP-16-0312
  • Polanska, K., Krol, A., Merecz-Kot, D., Jurewicz, J., Makowiec-Dabrowska, T., Chiarotti, F., Calamandrei, G., & Hanke, W. (2017). Maternal stress during pregnancy and neurodevelopmental outcomes of children during the first 2 years of life. Journal of Paediatrics and Child Health, 53(3), 263–270. https://doi.org/10.1111/jpc.13422
  • Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74(2), 116–143. https://doi.org/10.1016/j.biopsycho.2006.06.009
  • Rash, J., Campbell, T., Letourneau, N., & Giesbrecht, G. (2015). Maternal cortisol during pregnancy is related to infant cardiac vagal control. Psychoneuroendocrinology, 54, 78–89. https://doi.org/10.1016/j.psyneuen.2015.01.024
  • Ritz, T., Schulz, S. M., Rosenfield, D., Wright, R. J., & Bosquet Enlow, M. (2020). Cardiac sympathetic activation and parasympathetic withdrawal during psychosocial stress exposure in 6-month-old infants. Psychophysiology, 57(12), e13673. https://doi.org/10.1111/psyp.13673
  • Rosenfeld, C. (2021). The placenta-brain-axis. Journal of Neuroscience Research, 99(1), 271–283. https://doi.org/10.1002/jnr.24603
  • Rotenberg, S., & McGrath, J. (2016). Inter-relation between autonomic and HPA axis activity in children and adolescents. Biological Psychology, 117, 16–25. https://doi.org/10.1016/j.biopsycho.2016.01.015
  • Shaffer, F., & Ginsberg, J. P. (2017). An overview of heart rate variability metrics and norms [Review]. Frontiers in Public Health, 5, 258. https://doi.org/10.3389/fpubh.2017.00258
  • Sharifi-Heris, Z., Rahmani, A., Axelin, A., Rasouli, M., & Bender, M. (2023). Heart rate variability and pregnancy complications: Systematic review. Interactive Journal of Medical Research, 12, e44430. PMID: 37276013 PMCID: 10280337 https://doi.org/10.2196/44430
  • Suurland, J., van der Heijden, K. B., Smaling, H., Huijbregts, S., van Goozen, S., & Swaab, H. (2017). Infant autonomic nervous system response and recovery: Associations with maternal risk status and infant emotion regulation. Development and Psychopathology, 29(3), 759–773. https://doi.org/10.1017/S0954579416000456
  • Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation, 93(5), 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
  • Thayer, J., Ahs, F., Fredrikson, M., Sollers, J., & Wager, T. (2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience and Biobehavioral Reviews, 36(2), 747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009
  • The, A., Reijmerink, I., van der Laan, M., & Cnossen, F. (2020). Heart rate variability as a measure of mental stress in surgery: A systematic review. International Archives of Occupational and Environmental Health, 93(7), 805–821. https://doi.org/10.1007/s00420-020-01525-6
  • Thomas, B., Claassen, N., Becker, P., & Viljoen, M. (2019). Validity of commonly used heart rate variability markers of autonomic nervous system function. Neuropsychobiology, 78(1), 14–26. https://doi.org/10.1159/000495519
  • Tronick, E. Z. (2003). Things still to be done on the still-face effect. Infancy, 4(4), 475–482. https://doi.org/10.1207/S15327078IN0404_02
  • Turan, A., & Kaya, C. (2023). Effect of maternal cortisol levels on fetal heart rate patterns in primiparous pregnant women in the third trimester. Revista da Associacao Medica Brasileira (1992), May 1969(5), e20221610. https://doi.org/10.1590/1806-9282.20221610
  • Verdurmen, K., Renckens, J., van Laar, J., & Oei, S. (2013). The influence of corticosteroids on fetal heart rate variability: A systematic review of the literature. Obstetrical & Gynecological Survey, 68(12), 811–824. https://doi.org/10.1097/OGX.0000000000000007
  • Verma, A., Weir, A., Drummond, J., & Mitchell, B. F. (2005). Performance profile of an outcome measure: Morbidity Assessment Index for Newborns. Journal of Epidemiology and Community Health, 59(5), 420–426. https://doi.org/10.1136/jech.2003.019109
  • Weiss, S., Keeton, V., Richoux, S., Cooper, B., & Niemann, S. (2023). Exposure to antenatal corticosteroids and infant cortisol regulation. Psychoneuroendocrinology, 2023 147, 105960., PMC9968454, https://doi.org/10.1016/j.psyneuen.2022.105960
  • Weiss, S. J., & Niemann, S. (2015). Effects of antenatal corticosteroids on cortisol and heart rate reactivity of preterm infants. Biological Research for Nursing, 17(5), 487–494. https://doi.org/10.1177/1099800414564860
  • Wu, W., Adams, C., Stevens, K., Chow, K., Freedman, R., & Patterson, P. (2015). The interaction between maternal immune activation and alpha 7 nicotinic acetylcholine receptor in regulating behaviors in the offspring. Brain, Behavior, and Immunity, 46, 192–202. https://doi.org/10.1016/j.bbi.2015.02.005
  • Ziemssen, T., & Siepmann, T. (2019). The investigation of the cardiovascular and sudomotor autonomic nervous system: A review. Frontiers in Neurology, 1210, 53. PMID: 30809183; PMCID: PMC6380109. https://doi.org/10.3389/fneur.2019.00053
  • Zietlow, A.-L., Nonnenmacher, N., Reck, C., Ditzen, B., & Müller, M. (2019). Emotional stress during pregnancy–Associations with maternal anxiety disorders, infant cortisol reactivity, and mother–child interaction at pre-school age. Frontiers in Psychology, 10, 2179. https://doi.org/10.3389/fpsyg.2019.02179