Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Clinical Research Article
  • Published:

Maturation of cardioventilatory physiological trajectories in extremely preterm infants

Pediatric Research volume 95, pages 1060–1069 (2024)Cite this article

Abstract

Background

In extremely preterm infants, persistence of cardioventilatory events is associated with long-term morbidity. Therefore, the objective was to characterize physiologic growth curves of apnea, periodic breathing, intermittent hypoxemia, and bradycardia in extremely preterm infants during the first few months of life.

Methods

The Prematurity-Related Ventilatory Control study included 717 preterm infants <29 weeks gestation. Waveforms were downloaded from bedside monitors with a novel sharing analytics strategy utilized to run software locally, with summary data sent to the Data Coordinating Center for compilation.

Results

Apnea, periodic breathing, and intermittent hypoxemia events rose from day 3 of life then fell to near-resolution by 8–12 weeks of age. Apnea/intermittent hypoxemia were inversely correlated with gestational age, peaking at 3–4 weeks of age. Periodic breathing was positively correlated with gestational age peaking at 31–33 weeks postmenstrual age. Females had more periodic breathing but less intermittent hypoxemia/bradycardia. White infants had more apnea/periodic breathing/intermittent hypoxemia. Infants never receiving mechanical ventilation followed similar postnatal trajectories but with less apnea and intermittent hypoxemia, and more periodic breathing.

Conclusions

Cardioventilatory events peak during the first month of life but the actual postnatal trajectory is dependent on the type of event, race, sex and use of mechanical ventilation.

Impact

  • Physiologic curves of cardiorespiratory events in extremely preterm-born infants offer (1) objective measures to assess individual patient courses and (2) guides for research into control of ventilation, biomarkers and outcomes.

  • Presented are updated maturational trajectories of apnea, periodic breathing, intermittent hypoxemia, and bradycardia in 717 infants born <29 weeks gestation from the multi-site NHLBI-funded Pre-Vent study.

  • Cardioventilatory events peak during the first month of life but the actual postnatal trajectory is dependent on the type of event, race, sex and use of mechanical ventilation.

  • Different time courses for apnea and periodic breathing suggest different maturational mechanisms.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The frequency (number of events/day) and exposure (number of min/day) of apnea events by chronological age, postmenstrual age, and gestational age.
Fig. 2: The frequency (number of events/day) and exposure (number of min/day) of periodic breathing events by chronological age, postmenstrual age, and gestational age.
Fig. 3: The frequency (number of events/day) and exposure (number of min/day) of intermittent hypoxemia (IH) < 80% events by chronological age, postmenstrual age, and gestational age.
Fig. 4: The frequency (number of events/day) and exposure (number of min/day) of IH < 90% events by chronological age, postmenstrual age, and gestational age.
Fig. 5: The frequency (number of events/day) and exposure (number of min/day) of bradycardia events by chronological age, postmenstrual age, and gestational age.
Fig. 6: Median frequency and exposure of apnea, periodic breathing, IH < 80%, IH < 90%, and bradycardia events by sex, race and chronological age.

Similar content being viewed by others

Data availability

The datasets generated and analyzed during the current study are not publicly available due to embargo until after publication of the primary outcome manuscripts, at which point they will become available in the NHLBI’s Biologic Specimen and Data Repository Information Coordinating Center (BioLINCC biolincc.nhlbi.nih.gov). The datasets are available from the corresponding author on reasonable request.

References

  1. Di Fiore, J. M. et al. A higher incidence of intermittent hypoxemic episodes is associated with severe retinopathy of prematurity. J. Pediatr. 157, 69–73 (2010).

    PubMed  PubMed Central  Google Scholar 

  2. Di Fiore, J. M. et al. Patterns of oxygenation, mortality, and growth status in the surfactant positive pressure and oxygen trial cohort. J. Pediatr. 186, 49.e41–56.e41 (2017).

    Google Scholar 

  3. Di Fiore, J. M. et al. Early inspired oxygen and intermittent hypoxemic events in extremely premature infants are associated with asthma medication use at 2 years of age. J. Perinatol. 39, 203–211 (2019).

    PubMed  Google Scholar 

  4. Poets, C. F. et al. Association between intermittent hypoxemia or bradycardia and late death or disability in extremely preterm infants. JAMA 314, 595–603 (2015).

    CAS  PubMed  Google Scholar 

  5. Fairchild, K. D., Nagraj, V. P., Sullivan, B. A., Moorman, J. R. & Lake, D. E. Oxygen desaturations in the early neonatal period predict development of bronchopulmonary dysplasia. Pediatr. Res. 85, 987–993 (2019).

    PubMed  Google Scholar 

  6. Sullivan, B. A. et al. Early heart rate characteristics predict death and morbidities in preterm infants. J. Pediatr. 174, 57–62 (2016).

    PubMed  PubMed Central  Google Scholar 

  7. Sullivan, B. A. et al. Early pulse oximetry data improves prediction of death and adverse outcomes in a two-center cohort of very low birth weight infants. Am. J. Perinatol. 35, 1331–1338 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Sullivan, B. A. et al. Clinical and vital sign changes associated with late-onset sepsis in very low birth weight infants at 3 NICUs. J. Neonatal Perinatal Med. 14, 553–561 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Raffay, T. M. et al. Neonatal intermittent hypoxemia events are associated with diagnosis of bronchopulmonary dysplasia at 36 weeks postmenstrual age. Pediatr. Res. 85, 318–323 (2019).

    PubMed  Google Scholar 

  10. Vesoulis, Z. A. et al. Early hypoxemia burden is strongly associated with severe intracranial hemorrhage in preterm infants. J. Perinatol. 39, 48–53 (2019).

    PubMed  Google Scholar 

  11. Fairchild, K. D. et al. Vital signs and their cross-correlation in sepsis and NEC: a study of 1,065 very-low-birth-weight infants in two NICUs. Pediatr. Res. 81, 315–321 (2017).

    PubMed  Google Scholar 

  12. Nagraj, V. P., Sinkin, R. A., Lake, D. E., Moorman, J. R. & Fairchild, K. D. Recovery from bradycardia and desaturation events at 32 weeks corrected age and NICU length of stay: an indicator of physiologic resilience? Pediatr. Res. 86, 622–627 (2019).

    PubMed  PubMed Central  Google Scholar 

  13. Fairchild, K. et al. Clinical associations of immature breathing in preterm infants: part 1-central apnea. Pediatr. Res. 80, 21–27 (2016).

    PubMed  PubMed Central  Google Scholar 

  14. Patel, M. et al. Clinical associations with immature breathing in preterm infants: part 2-periodic breathing. Pediatr. Res. 80, 28–34 (2016).

    PubMed  PubMed Central  Google Scholar 

  15. Cummings, J. J. & Polin, R. A. Oxygen targeting in extremely low birth weight infants. Pediatrics 138, e1–e9 (2016).

    Google Scholar 

  16. Di Fiore, J. M. et al. Low oxygen saturation target range is associated with increased incidence of intermittent hypoxemia. J. Pediatr. 161, 1047–1052 (2012).

    PubMed  PubMed Central  Google Scholar 

  17. Dennery, P. A. et al. Pre-Vent: the prematurity-related ventilatory control study. Pediatr. Res. 85, 769–776 (2019).

    PubMed  PubMed Central  Google Scholar 

  18. Laird, P. et al. The critical care data exchange format: a proposed flexible data standard for combining clinical and high-frequency physiologic data in critical care. Physiol. Meas. https://doi.org/10.1088/1361-6579/abfc9b (2021).

  19. Vergales, B. D. et al. Accurate automated apnea analysis in preterm infants. Am. J. Perinatol. 31, 157–162 (2014).

    PubMed  Google Scholar 

  20. Clark, M. T. et al. Stochastic modeling of central apnea events in preterm infants. Physiol. Meas. 37, 463–484 (2016).

    PubMed  PubMed Central  Google Scholar 

  21. Finer, N. N., Higgins, R., Kattwinkel, J. & Martin, R. J. Summary proceedings from the apnea-of-prematurity group. Pediatrics 117, S47–S51 (2006).

    PubMed  Google Scholar 

  22. Mohr, M. A. et al. Quantification of periodic breathing in premature infants. Physiol. Meas. 36, 1415–1427 (2015).

    PubMed  PubMed Central  Google Scholar 

  23. Di Fiore, J. M. et al. The relationship between patterns of intermittent hypoxia and retinopathy of prematurity in preterm infants. Pediatr. Res. 72, 606–612 (2012).

    PubMed  PubMed Central  Google Scholar 

  24. Barrington, K. J. & Finer, N. N. Periodic breathing and apnea in preterm infants. Pediatr. Res. 27, 118–121 (1990).

    CAS  PubMed  Google Scholar 

  25. Glotzbach, S. F., Baldwin, R. B., Lederer, N. E., Tansey, P. A. & Ariagno, R. L. Periodic breathing in preterm infants: incidence and characteristics. Pediatrics 84, 785–792 (1989).

    CAS  PubMed  Google Scholar 

  26. Di Fiore, J. M., Martin, R. J. & Gauda, E. B. Apnea of prematurity-perfect storm. Respir. Physiol. Neurobiol. 189, 213–222 (2013).

    PubMed  Google Scholar 

  27. Gauda, E. B., McLemore, G. L., Tolosa, J., Marston-Nelson, J. & Kwak, D. Maturation of peripheral arterial chemoreceptors in relation to neonatal apnoea. Semin. Neonatol. 9, 181–194 (2004).

    PubMed  Google Scholar 

  28. Erickson, G., Dobson, N. R. & Hunt, C. E. Immature control of breathing and apnea of prematurity: the known and unknown. J. Perinatol. 41, 2111–2123 (2021).

    PubMed  PubMed Central  Google Scholar 

  29. Poets, C. F. Apnea of prematurity: what can observational studies tell us about pathophysiology? Sleep Med. 11, 701–707 (2010).

    PubMed  Google Scholar 

  30. Martin, R. J. & Wilson, C. G. Apnea of prematurity. Compr. Physiol. 2, 2923–2931 (2012).

    PubMed  Google Scholar 

  31. Eichenwald, E. C., Aina, A. & Stark, A. R. Apnea frequently persists beyond term gestation in infants delivered at 24 to 28 weeks. Pediatrics 100, 354–359 (1997).

    CAS  PubMed  Google Scholar 

  32. Henderson-Smart, D. J. The effect of gestational age on the incidence and duration of recurrent apnoea in newborn babies. Aust. Paediatr. J. 17, 273–276 (1981).

    CAS  PubMed  Google Scholar 

  33. Weintraub, Z. et al. The morphology of periodic breathing in infants and adults. Respir. Physiol. 127, 173–184 (2001).

    CAS  PubMed  Google Scholar 

  34. Fenner, A., Schalk, U., Hoenicke, H., Wendenburg, A. & Roehling, T. Periodic breathing in premature and neonatal babies: incidence, breathing pattern, respiratory gas tensions, response to changes in the composition of ambient air. Pediatr. Res. 7, 174–183 (1973).

    CAS  PubMed  Google Scholar 

  35. Seppä-Moilanen, M., Andersson, S. & Kirjavainen, T. Supplemental oxygen treats periodic breathing without effects on sleep in late-preterm infants. Neonatology 119, 567–574 (2022).

    PubMed  Google Scholar 

  36. Edwards, B. A., Sands, S. A. & Berger, P. J. Postnatal maturation of breathing stability and loop gain: the role of carotid chemoreceptor development. Respir. Physiol. Neurobiol. 185, 144–155 (2013).

    PubMed  Google Scholar 

  37. McDonald, F. B., Williams, R., Sheehan, D. & O’Halloran, K. D. Early life exposure to chronic intermittent hypoxia causes upper airway dilator muscle weakness, which persists into young adulthood. Exp. Physiol. 100, 947–966 (2015).

    PubMed  Google Scholar 

  38. Dylag, A. M. et al. Long-term effects of recurrent intermittent hypoxia and hyperoxia on respiratory system mechanics in neonatal mice. Pediatr. Res. 81, 565–571 (2017).

    CAS  PubMed  Google Scholar 

  39. Di Fiore, J. M., MacFarlane, P. M. & Martin, R. J. Intermittent hypoxemia in preterm infants. Clin. Perinatol. 46, 553–565 (2019).

    PubMed  PubMed Central  Google Scholar 

  40. Vagedes, J., Poets, C. F. & Dietz, K. Averaging time, desaturation level, duration and extent. Arch. Dis. Child. Fetal Neonatal 98, F265–F266 (2013).

    Google Scholar 

  41. Askie, L. M. et al. Association between oxygen saturation targeting and death or disability in extremely preterm infants in the neonatal oxygenation prospective meta-analysis collaboration. JAMA 319, 2190–2201 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Di Fiore, J. M. et al. Prematurity and postnatal alterations in intermittent hypoxaemia. Arch. Dis. Child. Fetal Neonatal 106, 557–559 (2021).

    Google Scholar 

  43. Schumacher, R. E., Farrell, P. M. & Olson, E. B. Jr Circulating 5-hydroxytryptamine concentrations in preterm newborns. Pediatr. Pulmonol. 3, 117–122 (1987).

    CAS  PubMed  Google Scholar 

  44. Cummings, K. J. & Leiter, J. C. Take a deep breath and wake up: the protean role of serotonin preventing sudden death in infancy. Exp. Neurol. 326, 113165 (2020).

    CAS  PubMed  Google Scholar 

  45. Valeeva, G., Valiullina, F. & Khazipov, R. Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front. Cell. Neurosci. 7, 20 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Myers, M. M. et al. Developmental profiles of infant EEG: overlap with transient cortical circuits. Clin. Neurophysiol. 123, 1502–1511 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Vanhatalo, S. & Kaila, K. Development of neonatal EEG activity: from phenomenology to physiology. Semin. Fetal Neonatal Med. 11, 471–478 (2006).

    PubMed  Google Scholar 

  48. Carroll, J. L. Developmental plasticity in respiratory control. J. Appl. Physiol. 94, 375–389 (2003).

    CAS  PubMed  Google Scholar 

  49. Bavis, R. W. & MacFarlane, P. M. Developmental plasticity in the neural control of breathing. Exp. Neurol. 287, 176–191 (2017).

    PubMed  Google Scholar 

  50. Pawar, A., Peng, Y. J., Jacono, F. J. & Prabhakar, N. R. Comparative analysis of neonatal and adult rat carotid body responses to chronic intermittent hypoxia. J. Appl. Physiol. 104, 1287–1294 (2008).

    PubMed  Google Scholar 

  51. Bavis, R. W., Russell, K. E., Simons, J. C. & Otis, J. P. Hypoxic ventilatory responses in rats after hypercapnic hyperoxia and intermittent hyperoxia. Respir. Physiol. Neurobiol. 155, 193–202 (2007).

    CAS  PubMed  Google Scholar 

  52. Logan, S. et al. Chronic intermittent hyperoxia alters the development of the hypoxic ventilatory response in neonatal rats. Respir. Physiol. Neurobiol. 220, 69–80 (2016).

    ADS  PubMed  Google Scholar 

  53. Esquer, C., Claure, N., D’Ugard, C., Wada, Y. & Bancalari, E. Role of abdominal muscles activity on duration and severity of hypoxemia episodes in mechanically ventilated preterm infants. Neonatology 92, 182–186 (2007).

    PubMed  Google Scholar 

  54. Kato, I. et al. Developmental characteristics of apnea in infants who succumb to sudden infant death syndrome. Am. J. Respir. Crit. 164, 1464–1469 (2001).

    CAS  Google Scholar 

  55. Bairam, A. et al. Sex-based differences in apnoea of prematurity: a retrospective cohort study. Exp. Physiol. 103, 1403–1411 (2018).

    CAS  PubMed  Google Scholar 

  56. Nagraj, V. P., Lake, D. E., Kuhn, L., Moorman, J. R. & Fairchild, K. D. Central apnea of prematurity: does sex matter? Am. J. Perinatol. 38, 1428–1434 (2021).

    PubMed  Google Scholar 

  57. Dormishian, A., Schott, A., Aguilar, A. C., Bancalari, E. & Claure, N. Pulse oximetry reliability for detection of hypoxemia under motion in extremely premature infants. Pediatr. Res. 93, 118–124 (2023).

    CAS  PubMed  Google Scholar 

  58. Dimaguila, M. A., Di Fiore, J. M., Martin, R. J. & Miller, M. J. Characteristics of hypoxemic episodes in very low birth weight infants on ventilatory support. J. Pediatr. 130, 577–583 (1997).

    CAS  PubMed  Google Scholar 

  59. Chavez, L. & Bancalari, E. Caffeine: some of the evidence behind its use and abuse in the preterm infant. Neonatology 119, 428–432 (2022).

    PubMed  Google Scholar 

Download references

Acknowledgements

The National Institutes of Health (NIH) and the National Heart, Lung, and Blood Institute (NHLBI) provided grant support through cooperative agreements. While NHLBI staff had input into study design, conduct, analysis, and manuscript drafting, the content and views expressed in this article are solely the responsibility of the authors and do not necessarily represent the official views of NIH or the U.S. Department of Health and Human Services. Participating sites collected and stored the data while the University of Virginia (UVa), the lead data and coordinating center (LDCC), analyzed the data. The co-PIs at each site had full access to her/his individual site data and take responsibility for the integrity of the raw waveforms while Dr. Randall Moorman (LDCC co-PI) and Dr. Douglas Lake (LDCC co-PI) take responsibility for the integrity of the data and accuracy of the data analysis. We are indebted to our medical and nursing colleagues and the infants and their parents who agreed to take part in this study. The following individuals, in addition to those listed as authors, participated in this study: NIH/NHLBI: Neil Aggarwal: NHLBI, Division of Lung Diseases, Bethesda, MD; Lawrence Baizer: NHLBI, Division of Lung Diseases, Bethesda, MD; Peyvand Ghofrani: NHLBI, Division of Lung Diseases, Bethesda, MD; Aaron Laposky: NHLBI, Division of Lung Diseases, Bethesda, MD; Aruna Natarajan: NHLBI, Division of Lung Diseases, Bethesda, MD; Barry Schmetter: NHLBI, Division of Lung Diseases, Bethesda, MD; OSMB: Estelle Gauda (Chair): University of Toronto Hospital for Sick Children, Division of Neonatology, Toronto, Ontario; Jonathan Davis: Tufts Clinical and Translational Science Institute, Division of Newborn Medicine, Boston, MA; Roberta Keller: University of California, San Francisco School of Medicine, Department of Pediatrics, San Francisco CA; Robinder Khemani: Children’s Hospital Los Angeles, Department of Anesthesiology and Critical Care Medicine, Los Angeles, CA; Renee Moore: Drexel University Department of Epidemiology and Biostatistics, Philadelphia, PA; Elliott Weiss: Department of Pediatrics, University of Washington School of Medicine, Seattle, WA; University of Virginia: Amy Camblos: UVa School of Medicine, Clinical Trials Office, UVa School of Medicine, Charlottesville, VA; Gina Duda: UVa School of Medicine, Clinical Trials Office, UVa School of Medicine, Charlottesville, VA; Abigail Flower: UVa, Data Science Institute, Charlottesville, VA; Steven Fowler: UVa School of Medicine, Clinical Trials Office, UVa School of Medicine, Charlottesville, VA; Patcharin Pramoonjago: UVa School of Medicine, Biorepository and Tissue Research Facility, Charlottesville, VA; Craig Rumpel: UVa School of Medicine, Biorepository and Tissue Research Facility, Charlottesville, VA; Northwestern University: Michael Carroll: Ann & Robert H. Lurie Children’s Hospital of Chicago and Stanley Manne Children’s Research Institute, Data Analytics and Reporting, Chicago, IL; Bradley Hopkins: Ann & Robert H. Lurie Children’s Hospital of Chicago, Pediatric Autonomic Medicine, Chicago, IL; University of Alabama at Birmingham: David Paydarfar: University of Texas Austin, Department of Neurology at Dell Medical School, Austin, TX; Elisabeth Salisbury: University of Massachusetts Medical School, Department of Pediatrics and Neurology, Worcester, MA; Bradley Troxler: University of Alabama at Birmingham School of Medicine, Division of Pulmonary and Sleep Medicine, Department of Pediatrics, Birmingham, AL; Washington University: Ryan Colvin: Washington University School of Medicine in St. Louis, Division of General Medicine, St. Louis, MO; Joey Egan: St. Louis Children’s Hospital, Respiratory Care, St. Louis, MO; Elise Eiden: Washington University School of Medicine in St. Louis, Institute for Informatics, St. Louis, MO; Jeffery Hoover: Washington University School of Medicine in St. Louis, Division of Newborn Medicine, St. Louis, MO; Laura Linneman: Washington University School of Medicine in St. Louis, St. Louis, MO; Daniel Mammel: Washington University School of Medicine in St. Louis, Division of Newborn Medicine, St. Louis, MO; Michael McLeland: St. Louis Children’s Hospital, Sleep Laboratory, St. Louis, MO; Harley Pyles: St. Louis Children’s Hospital, Respiratory Care, St. Louis, MO; Barbara Warner: Washington University School of Medicine in St. Louis, Division of Newborn Medicine, St. Louis, MO.

Funding

This work was supported by NIH grants as follows: University of Virginia (NCT03174301): U01 HL133708, HL133708-05S1; Case Western Reserve University: U01 HL133643, The Gerber Foundation; Northwestern University: U01 HL133704; University of Alabama at Birmingham: U01 HL133536; University of Miami: U01 HL133689; Washington University: U01 HL133700.

Author information

Author notes

  1. These authors contributed equally: Debra E. Weese-Mayer, Juliann M. Di Fiore.

Authors and Affiliations

  1. Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Debra E. Weese-Mayer & Aaron Hamvas

  2. Division of Autonomic Medicine, Department of Pediatrics, Ann & Robert H Lurie Children’s Hospital of Chicago and Stanley Manne Children’s Research Institute, Chicago, IL, USA

    Debra E. Weese-Mayer & Narayanan Krishnamurthi

  3. Department of Pediatrics, Case Western Reserve University, School of Medicine, Cleveland, OH, USA

    Juliann M. Di Fiore, Anna Maria Hibbs & Richard J. Martin

  4. Department of Pediatrics, Division of Neonatology, UH Rainbow Babies & Children’s Hospital, Cleveland, OH, USA

    Juliann M. Di Fiore, Anna Maria Hibbs & Richard J. Martin

  5. Division of Cardiovascular Medicine, Center for Advanced Medical Analytics and Department of Internal Medicine, University of Virginia School of Medicine, Charlottesville, VA, USA

    Douglas E. Lake, Jiaxing Qiu, Amanda M. Zimmet, Katy N. Krahn & J. Randall Moorman

  6. Division of Neonatology, Department of Pediatrics, Holtz Children’s Hospital - Jackson Memorial Medical Center, University of Miami Miller School of Medicine, Miami, FL, USA

    Nelson Claure, Eduardo Bancalari & Alaleh Dormishian

  7. Division of Neonatology, Department of Pediatrics, University of Alabama at Birmingham School of Medicine, Birmingham, AL, USA

    Namasivayam Ambalavanan, Waldemar A. Carlo, Deborah Laney & Colm P. Travers

  8. Department of Pediatrics, Washington University School of Medicine in St. Louis, St. Louis, MO, USA

    James S. Kemp

  9. Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, USA

    John L. Carroll

  10. Division of Neonatology, Department of Pediatrics, Ann & Robert H Lurie Children’s Hospital of Chicago and Stanley Manne Children’s Research Institute, Chicago, IL, USA

    Aaron Hamvas

  11. Public Health Sciences, University of Virginia School of Medicine, Charlottesville, VA, USA

    Sarah J. Ratcliffe & J. Randall Moorman

  12. Department of Electrical Engineering, University of Texas Tyler, Tyler, TX, USA

    Premananda Indic

  13. Hasbro Children’s Hospital, Brown University, Warren Alpert School of Medicine, Providence, RI, USA

    Phyllis A. Dennery

  14. University of Virginia Center for Advanced Medical Analytics, Charlottesville, VA, USA

    Karen D. Fairchild

  15. Pediatric Autonomic Medicine, Ann & Robert H. Lurie Children’s Hospital of Chicago and Stanley Manne Children’s Research Institute, Chicago, IL, USA

    Allaa Fadl-Alla, Erin K. Lonergan & Casey M. Rand

  16. Department of Pediatrics, University Hospitals Cleveland Medical Center, Rainbow Babies & Children’s Hospital, Cleveland, OH, USA

    Arlene Zadell

  17. Department of Electrical and Computer Engineering, University of Alabama at Birmingham, Birmingham, AL, USA

    Arie Nakhmani

  18. Division of Neonatology, Department of Pediatrics, University of Miami Miller School of Medicine, Holtz Children’s Hospital – University of Miami/Jackson Memorial Medical Center, Miami, FL, USA

    Alini Schott & Ana Cecilia Aguilar

  19. Washington University School of Medicine in St. Louis, St. Louis, MO, USA

    Julie Hoffmann

Authors
  1. Debra E. Weese-Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juliann M. Di Fiore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Douglas E. Lake
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anna Maria Hibbs
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nelson Claure
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiaxing Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Namasivayam Ambalavanan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eduardo Bancalari
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. James S. Kemp
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Amanda M. Zimmet
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. John L. Carroll
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Richard J. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Katy N. Krahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Aaron Hamvas
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Sarah J. Ratcliffe
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Narayanan Krishnamurthi
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Premananda Indic
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Alaleh Dormishian
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Phyllis A. Dennery
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. J. Randall Moorman
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

the Prematurity-Related Ventilatory Control (Pre-Vent) Investigators

  • Karen D. Fairchild
  • , Allaa Fadl-Alla
  • , Erin K. Lonergan
  • , Casey M. Rand
  • , Arlene Zadell
  • , Arie Nakhmani
  • , Waldemar A. Carlo
  • , Deborah Laney
  • , Colm P. Travers
  • , Alini Schott
  • , Ana Cecilia Aguilar
  •  & Julie Hoffmann

Contributions

D.E.W.-M.: substantial contributions to design of study, overseeing enrollment, data collection, safety, analysis and interpretation of data, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. Equal first author. J.D.F.: substantial contributions to design of work and subject recruitment, data collection, safety, analysis and interpretation of data, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. Equal first author. D.L., J.Q., A.M.Z.: substantial contributions to design of work, data analytics, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. A.M.H., N.C., N.A., E.B., J.S.K., J.L.C., R.M., K.K., A.H., P.I., A.D.: substantial contributions to design of study, overseeing enrollment, data collection, and safety, analysis and interpretation of data, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. S.J.R.: substantial contributions to design of study, analysis and interpretation of data, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. N.K.: substantial contributions to design of work, data analytics, interpretation of data, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. P.A.D.: substantial contributions to analysis and interpretation of data, final approval, agreement to be accountable for all aspects of work including accuracy and integrity. J.R.M.: substantial contributions to design of study and work, data analytics, drafting of work, final approval, agreement to be accountable for all aspects of work including accuracy and integrity.

Corresponding authors

Correspondence to Debra E. Weese-Mayer or Juliann M. Di Fiore.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

Institutional Review Board (IRB) approval was obtained at all sites. Waiver of consent was approved by the LDCC IRB and 3 of 5 CRC IRBs, while 2 CRC sites obtained consent.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weese-Mayer, D.E., Di Fiore, J.M., Lake, D.E. et al. Maturation of cardioventilatory physiological trajectories in extremely preterm infants. Pediatr Res 95, 1060–1069 (2024). https://doi.org/10.1038/s41390-023-02839-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41390-023-02839-0

Search

Advanced search

Quick links