Dependencies between maternal and fetal autonomic tone

Janine Zöllkau; Eva-Maria Dölker; Alexander Schmidt; Uwe Schneider; Dirk Hoyer

doi:10.1515/jpm-2018-0221

Article

Dependencies between maternal and fetal autonomic tone

Janine Zöllkau , Eva-Maria Dölker , Alexander Schmidt , Uwe Schneider and Dirk Hoyer

Published/Copyright: December 20, 2018

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From the journal Journal of Perinatal Medicine Volume 47 Issue 3

Abstract

Background

Disturbances in maternal physiology can cause changes in the fetal condition that may lead to impaired fetal development. Synchronous monitoring of cardiac autonomic tone via the assessment of the fetal and maternal heart rate (HR) and heart rate variability (HRV) may provide an appropriate diagnostic window.

Methods

Partial rank correlation coefficients between the maternal and fetal HR and HRV indices were calculated and verified by testing surrogate data in 315 magnetocardiographic (MCG) recordings from 141 healthy women pregnant with singleton fetuses [18+6 to 39+2 weeks gestational age (WGA)]. We assessed maternal self-perceived depression, anxiety and stress by means of the Depression, Anxiety, Stress Scales self-reporting instrument (DASS42G) questionnaire.

Results

The maternal HRV correlated positively with the fetal HRV, but negatively with the fetal HR. Correlation was |r|<0.2 in state-independent and gestational age (GA) <32 weeks, but |r|>0.2 in active sleep and GA ≥32 weeks. The DASS42G results correlated with the maternal HRV and HR, while the fetal HR and HRV were not influenced.

Conclusion

Correlations between maternal and fetal autonomic activation were statistically confirmed. They depend on the GA and active fetal state. As far as healthy subjects are concerned, maternal self-perceived stress, anxiety or depression is mirrored in maternal but not in fetal autonomic tone.

Keywords: fetal autonomic tone; fetal magnetocardiography; fetal maturation; heart rate variability; maternal autonomic tone; maternofetal correlation analysis

Corresponding author: Janine Zöllkau, MD, Department of Obstetrics and Gynecology, Jena University Hospital, Jena 07747, Germany; and Biomagnetic Center, Hans Berger Department of Neurology, Jena University Hospital, Jena, Germany, Tel.: +49 157 32961599

aUwe Schneider and Dirk Hoyer: These authors contributed equally to this work.

Acknowledgments

The recordings, preprocessing and technical service were performed by Franziska Jaenicke, Esther Heinicke, Anja Rudolph, Ulrike Wallwitz, Isabelle Kynass, Franziska Bode, Kathrin Kumm, Sophia Leibl, Adelina Pytlik, Stefan Claus, Tina Radtke and Ralph Huonker. We thank Nasim Kroegel for carefully editing the manuscript.

Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: AS, DH and US are supported by the German Research Foundation: Development of a clinically suitable marker of fetal autonomic maturation (Funder Id: DFG: Ho 1634/15-12, Schn 775/7-1). DH and US are supported by: Biomagnetic investigations of fetal autonomic and central nervous maturation and its disturbances due to intrauterine growth restriction and glucocorticoid administration (DFG: Ho 1634/12-2, Schn 775/2-3).
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

References

1. Barker DJ. The fetal and infant origins of adult disease. Br Med J 1990;301:1111.10.1136/bmj.301.6761.1111Search in Google Scholar

2. Seckl JR. Glucocorticoids, feto-placental 11 beta-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids 1997;62:89–94.10.1016/S0039-128X(96)00165-1Search in Google Scholar

3. Gitau R, Cameron A, Fisk NM, Glover V. Fetal exposure to maternal cortisol. Lancet 1998;352:707–8.10.1016/S0140-6736(05)60824-0Search in Google Scholar

4. Sandman CA, Wadhwa PD, Chicz-DeMet A, Dunkel-Schetter C, Porto M. Maternal stress, HPA activity, and fetal/infant outcome. Ann N Y Acad Sci 1997;814:266–75.10.1111/j.1749-6632.1997.tb46162.xSearch in Google Scholar

5. DiPietro JA, Hilton SC, Hawkins M, Costigan KA, Pressman EK. Maternal stress and affect influence fetal neurobehavioral development. Dev Psychol 2002;38:659–68.10.1037/0012-1649.38.5.659Search in Google Scholar

6. Dierckx B, Tulen JHM, van den Berg MP, Tharner A, Jaddoe VW, Moll HA, et al. Maternal psychopathology influences infant heart rate variability: Generation R Study. Psychosom Med 2009;71:313–21.10.1097/PSY.0b013e318198a82cSearch in Google Scholar

7. Teixeira JM, Fisk NM, Glover V. Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study. Br Med J 1999;318:153–7.10.1097/00006254-199909000-00003Search in Google Scholar

8. DiPietro JA, Costigan KA, Nelson P, Gurewitsch ED, Laudenslager ML. Fetal responses to induced maternal relaxation during pregnancy. Biol Psychol 2008;77:11–9.10.1016/j.biopsycho.2007.08.008Search in Google Scholar

9. Mulder EJ, Robles de Medina PG, Huizink AC, van den Bergh BR, Buitelaar JK, Visser GH. Prenatal maternal stress: effects on pregnancy and the (unborn) child. Early Hum Dev 2002;70:3–14.10.1016/S0378-3782(02)00075-0Search in Google Scholar

10. van Leeuwen P, Lange S, Bettermann H, Gronemeyer D, Hatzmann W. Fetal heart rate variability and complexity in the course of pregnancy. Early Hum Dev 1999;54:259–69.10.1016/S0378-3782(98)00102-9Search in Google Scholar

11. Moertl MG, Ulrich D, Pickel KI, Klaritsch P, Schaffer M, Flotzinger D, et al. Changes in haemodynamic and autonomous nervous system parameters measured non-invasively throughout normal pregnancy. Eur J Obstet Gynecol Reprod Biol 2009;144:S179–83.10.1016/j.ejogrb.2009.02.037Search in Google Scholar

12. Lange S, van Leeuwen P, Schneider U, Frank B, Hoyer D, Geue D, et al. Heart rate features in fetal behavioural states. Early Hum Dev 2009;85:131–5.10.1016/j.earlhumdev.2008.07.004Search in Google Scholar

13. Klinkenberg AV, Nater UM, Nierop A, Bratsikas A, Zimmermann R, Ehlert U. Heart rate variability changes in pregnant and non-pregnant women during standardized psychosocial stress. Acta Obstet Gynecol Scand 2009;88:77–82.10.1080/00016340802566762Search in Google Scholar

14. Bergh B. The influence of maternal emotion during pregnancy on fetal and neonatal behavior. J Prenat Perinat Psychol Health 1990;5:119–30.Search in Google Scholar

15. Schmidt A, Schneider U, Witte OW, Schleussner E, Hoyer D. Developing fetal motor-cardiovascular coordination analyzed from multi-channel magnetocardiography. Physiol Meas 2014;35:1943–59.10.1088/0967-3334/35/10/1943Search in Google Scholar

16. Hoyer D, Tetschke F, Jaekel S, Nowack S, Witte OW, Schleussner E, et al. Fetal functional brain age assessed from universal developmental indices obtained from neuro-vegetative activity patterns. PLoS One 2013;8:e74431.10.1371/journal.pone.0074431Search in Google Scholar

17. Nijhuis JG, Prechtl HF, Martin CB, Bots RS. Are there behavioural states in the human fetus? Early Hum Dev 1982;6:177–95.10.1016/0378-3782(82)90106-2Search in Google Scholar

18. Schneider U, Frank B, Fiedler A, Kaehler C, Hoyer D, Liehr M, et al. Human fetal heart rate variability-characteristics of autonomic regulation in the third trimester of gestation. J Perinat Med 2008;36:433–41.10.1515/JPM.2008.059Search in Google Scholar

19. Pillai M, James D. The development of fetal heart rate patterns during normal pregnancy. Obstet Gynecol 1990;76:812–6.10.1097/00006250-199011000-00017Search in Google Scholar

20. Zhuravlev YE, Rassi D, Mishin AA, Emery SJ. Dynamic analysis of beat-to-beat fetal heart rate variability recorded by SQUID magnetometer: quantification of sympatho-vagal balance. Early Hum Dev 2002;66:1–10.10.1016/S0378-3782(01)00225-0Search in Google Scholar

21. David M, Hirsch M, Karin J, Toledo E, Akselrod S. An estimate of fetal autonomic state by time-frequency analysis of fetal heart rate variability. J Appl Physiol 2007;102:1057–64.10.1152/japplphysiol.00114.2006Search in Google Scholar PubMed

22. TaskForce. 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. Eur Heart J 1996;17:354–81.10.1093/oxfordjournals.eurheartj.a014868Search in Google Scholar

23. Dalton KJ, Dawes GS, Patrick JE. The autonomic nervous system and fetal heart rate variability. Am J Obstet Gynecol 1983;146:456–62.10.1016/0002-9378(83)90828-1Search in Google Scholar

24. Yoshizato T, Koyanagi T, Takashima T, Satoh S, Akazawa K, Nakano H. The relationship between age-related heart rate changes and developing brain function: a model of anencephalic human fetuses in utero. Early Hum Dev 1994;36:101–12.10.1016/0378-3782(94)90037-XSearch in Google Scholar

25. Sachis PN, Armstrong DL, Becker LE, Bryan AC. Myelination of the human vagus nerve from 24 weeks postconceptional age to adolescence. J Neuropathol Exp Neurol 1982;41:466–72.10.1097/00005072-198207000-00009Search in Google Scholar PubMed

26. Longin E, Gerstner T, Schaible T, Lenz T, Konig S. Maturation of the autonomic nervous system: differences in heart rate variability in premature vs. term infants. J Perinat Med 2006;34:303–8.10.1515/JPM.2006.058Search in Google Scholar

27. Grant-Beuttler M, Glynn LM, Salisbury AL, Davis EP, Holliday C, Sandman CA. Development of fetal movement between 26 and 36-weeks’ gestation in response to vibro-acoustic stimulation. Front Psychol 2011;2:350.10.3389/fpsyg.2011.00350Search in Google Scholar PubMed PubMed Central

28. Hertogs K, Roberts AB, Cooper D, Griffin DR, Campbell S. Maternal perception of fetal motor activity. Br Med J 1979;2:1183–5.10.1136/bmj.2.6199.1183Search in Google Scholar PubMed PubMed Central

29. Raynes-Greenow CH, Gordon A, Li Q, Hyett JA. A cross-sectional study of maternal perception of fetal movements and antenatal advice in a general pregnant population, using a qualitative framework. BMC Pregnancy Childbirth 2013;13:32.10.1186/1471-2393-13-32Search in Google Scholar PubMed PubMed Central

30. Lange S, van Leeuwen P, Geue D, Hatzmann W, Gronemeyer D. Influence of gestational age, heart rate, gender and time of day on fetal heart rate variability. Med Biol Eng Comput 2005;43:481–6.10.1007/BF02344729Search in Google Scholar PubMed

Article note:

Partially presented as a poster at the 61^th Conference of the Deutsche Gesellschaft für Gynäkologie und Geburtshilfe e.V. (DGGG), Stuttgart, Germany, October 19–22, 2016.

Received: 2018-07-03

Accepted: 2018-10-30

Published Online: 2018-12-20

Published in Print: 2019-04-24

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https://doi.org/10.1515/jpm-2018-0221

Keywords for this article

fetal autonomic tone; fetal magnetocardiography; fetal maturation; heart rate variability; maternal autonomic tone; maternofetal correlation analysis