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Prenatal smoking and drinking are associated with altered newborn autonomic functions

Pediatric Research volume 93, pages 242–252 (2023)Cite this article

Abstract

Background

Prenatal smoking and drinking are associated with sudden infant death syndrome and neurodevelopmental disorders. Infants with these outcomes also have altered autonomic nervous system (ANS) regulation. We examined the effects of prenatal smoking and drinking on newborn ANS function.

Methods

Pregnant women were enrolled in Northern Plains, USA (NP) and Cape Town (CT), South Africa. Daily drinking and weekly smoking data were collected prenatally. Physiological measures were obtained during sleep 12–96 h post-delivery.

Results

In all, 2913 infants from NP and 4072 from CT were included. In active sleep, newborns of mothers who smoked throughout pregnancy, compared to non-smokers, had higher breathing rates (2.2 breaths/min; 95% CI: 0.95, 3.49). Quit-early smoking was associated with reductions in beat-to-beat heart rate variability (HRV) in active (−0.08 s) and quiet sleep (−0.11 s) in CT. In girls, moderate-high continuous smoking was associated with increased systolic (3.0 mmHg, CI: 0.70, 5.24) and diastolic blood pressure (2.9 mmHg, CI: 0.72, 5.02). In quiet sleep, low-continuous drinking was associated with slower heart rate (−4.5 beat/min). In boys, low-continuous drinking was associated with a reduced ratio of low-to-high frequency HRV (−0.11, CI: −0.21, −0.02).

Conclusions

These findings highlight potential ANS pathways through which prenatal drinking and smoking may contribute to neurodevelopment outcomes.

Impact

  • In this prospective cohort study of 6985 mother–infant dyads prenatal drinking and smoking were associated with multiple ANS parameters.

  • Smoking was associated with increased neonatal breathing rates among all infants, and heart rate variability (HRV) and blood pressure (BP) among girls.

  • Drinking was associated with reductions in HR and BP among all newborns, and reductions in the ratio of low to-high frequency HRV among boys.

  • These findings suggest that prenatal smoking and drinking alter newborn ANS which may presage future neurodevelopmental disorders.

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Fig. 1
Fig. 2: Marginal means in each exposure categories, stratified by study site and infant sex.

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Acknowledgements

The authors gratefully acknowledge the cooperation of the study participants, PASS investigators, the PASS Steering Committee Chairman Gary D.V. Hankins, MD, and members of the National Institute of Child Health and Human Development advisory safety monitoring board: Elizabeth Thom, Ph.D. (Chair); Reverend Phillip Cato, Ph.D.; James W. Collins Jr, MD, MPH; Terry Dwyer, MD, MPH; George Macones, MD; Philip A. May, Ph.D.; Jeff Murray, MD; Richard M. Pauli, MD, Ph.D.; Raymond W. Redline, MD; and Michael Varner, MD. Furthermore, the following individuals made significant contributions to the research and warrant recognition: DCAC: Idania Ramirez, MPH; Jamie Collins, MA; Laura Spurchise, MPH; DBPC: Richard A. Belliveau, BA; Kristin McMillan, BA; Megan Minter, MS; PAC: Johnston T. Grier, BA; Emilia F. Vignola, BA; Joseph J. Violaris, BA. All contributors were compensated by one or more of the listed funding sources.

The following institutions and researchers comprise the PASS Network (additional network members other than authors listed): Data Coordinating and Analysis Center (DCAC): Director: Kimberly Dukes, Ph.D.; Codirector: Lisa M. Sullivan, PhD; Biostatistics: Tara Tripp, MA; Project Management and Regulatory Affairs: Julie M. Petersen, BA; Rebecca A. Young, MPH; Data Management and Information Technology: Travis Baker, BS; Derek Petersen, BS; Gregory Toland, MS. Developmental Biology and Pathology Center (DBPC): Director: Hannah C. Kinney, MD; Assistant Director: Robin L. Haynes, Ph.D.; Coinvestigators: David S. Paterson, Ph.D.; Kevin G. Broadbelt, PhD; Kyriacos Markianos, Ph.D.; Ingrid A. Holm, MD; Theonia Boyd, MD; Drucilla Roberts, MD; Richard G. Goldstein, MD; Hanno Stein, Ph.D.; Technicians: Claire Maggiotto, BS; Catherine Hassett, BS. Comprehensive Clinical Site Northern Plains: Coinvestigators: Donald Habbe, MD; H. Eugene Hoyme, MD; William Massello III, MD; Bradley Randall, MD; Mary Ann Sens, MD, Ph.D.; Catherine Stoos, MD, Peter Van Eerden, MD; Project Management: Whitney Adler, BA; Elizabeth Berg, RN; Jessica Gromer, RN; Bethany Norton, MA; Liz Swenson, RN; Deb Tobacco, MA. Comprehensive Clinical Site South Africa: Project Management: Erna Carstens, RN; Mandy Potter, RN; Lucy Brink, MSc; Sylvia Abrahams, RN; Allison Borchardt, RN; Noorjahan Bosman, RN; Ciska Botha, BSocSc; Lehana Breytenbach, RN; Lucille Burger, RN; Carina Carstens, BCur (Nursing); Erna Carstens, RN; Weslin Charles, Hons BA (Psychology); Milly de Jager, RN; Carlie du Plessis, RN; Sandra Felix, RN; Nicola James (Nel), MCur (Nursing); Ronnie Jurgens, RN; Belda Klukowski, RN; Mugeleigh Lakay, MCur (Nursing); Samacia Maloy, RN; Marilyn Mentor, RN; Petra Opperman, RN; Berenice Pillay, RN; Mandy Potter, RN; Earl Prinsloo, BA Hons (Sociology); Sonja Schell, RN; Marisa van der Spuy, BCur (Nursing); Mariëtta Warwick, RN. Physiology Assessment Center (PAC): Project Management: Daianna Rodriguez, BA; Albany Perez, BA; Data Processing: Margaret C. Shair, BA; Tracy Thai, BA. National Institutes of Health: Project Scientists: Marian Willinger, PhD (National Institute of Child Health and Human Development); Dale Herald, Ph.D. (National Institute on Alcohol Abuse and Alcoholism); Howard J. Hoffman, Ph.D. (National Institute on Deafness and Other Communication Disorders); Chuan-Ming Li, MD, Ph.D. (National Institute on Deafness and Other Communication Disorders); Program Officers: Bill Dunty, Ph.D. (National Institute on Alcohol Abuse and Alcoholism); Tonse Raju, MD, DCH (National Institute of Child Health and Human Development); Gordon B. Hughes, MD (National Institute on Deafness and Other Communication Disorders).

Funding

This research was supported by grants UH3OD023279, U01HD055154, U01HD045935, U01HD055155, and U01AA016501, issued by the Office of the Director, National Institutes of Health of the National Institutes of Health, National Institute on Alcohol Abuse and Alcoholism, Eunice Kennedy Shriver National Institute of Child Health and Human Development, and the National Institute on Deafness and Other Communication Disorders. Ayesha Sania is supported by UH3OD023279-05S1, re-entry supplement from Office of the Director, NIH, and Office of Research on Women Health (ORWH). The opinions expressed in this paper are those of the authors and do not necessarily represent the official views of the National Institutes of Health, the Eunice Kennedy Shriver National Institute of Child Health and Development, the National Institute on Alcohol Abuse and Alcoholism, or the National Institute on Deafness and Other Communication Disorders.

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Author notes

  1. These authors contributed equally: Ayesha Sania, Michael M. Myers.

Authors and Affiliations

  1. Department of Psychiatry, Columbia University Irving Medical Center, New York, NY, 10032, USA

    Ayesha Sania, Michael M. Myers, Nicolò Pini, Maristella Lucchini, J. David Nugent, Lauren C. Shuffrey, Jennifer Barbosa & William P. Fifer

  2. Division of Developmental Neuroscience, New York State Psychiatric Institute, New York, NY, 10032, USA

    Ayesha Sania, Michael M. Myers, Nicolò Pini, Maristella Lucchini, J. David Nugent, Lauren C. Shuffrey & William P. Fifer

  3. Department of Statistics, Columbia University, New York, NY, 10032, USA

    Shreya Rao

  4. Avera Research Institute, Sioux Falls, SD, 57108, USA

    Jyoti Angal & Amy J. Elliott

  5. Department of Pediatrics, University of South Dakota School of Medicine, Sioux Falls, SD, 57069, USA

    Jyoti Angal & Amy J. Elliott

  6. Department of Obstetrics and Gynaecology, Faculty of Medicine and Health Science, Stellenbosch University, Cape Town, Western Cape, 7530, South Africa

    Hein J. Odendaal

  7. Department of Pediatrics, Columbia University Irving Medical Center, New York, NY, 10032, USA

    William P. Fifer

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Contributions

A.S. conceptualized and conducted statistical analysis, drafted the initial manuscript, and reviewed and revised the manuscript. M.M.M. was a principal investigator of the study; he conceptualized and designed the study, supervised data collection and data processing, drafted the manuscript, reviewed, and revised it. A.J.E., W.P.F., and H.J.O. were principal investigators of the study, they acquired funding, contributed to data analyses and interpretation of the results, and writing of the manuscript. N.P. M.L., and L.C.S. contributed to the interpretation of results and drafting the manuscript. J.D.N., J.B., and J.A. participated in study supervision, data collection and processing, drafting and critical revision of the manuscript. S.R. participated in data analysis and drafting of the manuscript. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

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Correspondence to Ayesha Sania.

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Written informed consent was obtained from all participants. Ethical approval was obtained from Stellenbosch University, Avera Health, Sanford Health, the Indian Health Service and from participating Tribal Nations.

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Sania, A., Myers, M.M., Pini, N. et al. Prenatal smoking and drinking are associated with altered newborn autonomic functions. Pediatr Res 93, 242–252 (2023). https://doi.org/10.1038/s41390-022-02060-5

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