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.

  • Article
  • Published:

The effect of umbilical cord milking on cerebral blood flow in very preterm infants: a randomized controlled study

Abstract

Objective

To compare the effect of umbilical cord milking (UCM) vs. early cord clamping (ECC) on cerebral blood flow (CBF).

Method

Preterm infants <31 weeks’ gestation were randomized to receive UCM or ECC at birth. Blood flow velocities and resistive & pulsatility indices of middle and anterior cerebral arteries were measured at 4–6 and 10–12 h after birth as an estimate of CBF.

Results

Randomization allocated 37 infants to UCM and 36 to ECC. Maternal and antenatal variables were similar. There were no significant differences between groups in middle or anterior CBF velocities and resistive indices at either study time point. CBF variables were not correlated with mean blood pressure, systemic blood flow, or intraventricular hemorrhage.

Conclusions

In very preterm infants, UCM compared with ECC was not shown to change CBF indices during the first 12 h of age or correlate with other hemodynamic measures or with intraventricular hemorrhage.

Trial registration

ClinicalTrials.gov: NCT01487187.

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

Access options

Buy this article

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

Similar content being viewed by others

References

  1. Katheria AC, Lakshminrusimha S, Rabe H, McAdams R, Mercer JS. Placental transfusion: a review. J Perinatol. 2017;37:105–11.

    Article  CAS  Google Scholar 

  2. Katheria AC, Truong G, Cousins L, Oshiro B, Finer NN. Umbilical cord milking versus delayed cord clamping in preterm infants. Pediatrics. 2015;136:61–69.

    Article  Google Scholar 

  3. Al-Wassia H, Shah PS. Efficacy and safety of umbilical cord milking at birth: a systematic review and meta-analysis. JAMA Pediatr. 2015;169:18–25.

    Article  Google Scholar 

  4. Sweet DG, Carnielli V, Greisen G, Hallman M, Ozek E, Plavka R, et al. European Consensus Guidelines on the Management of Respiratory Distress Syndrome—2016 Update. Neonatology. 2017;111:107–25.

    Article  CAS  Google Scholar 

  5. Hosono S, Mugishima H, Fujita H, Hosono A, Minato M, Okada T, et al. Umbilical cord milking reduces the need for red cell transfusions and improves neonatal adaptation in infants born less than 29 weeks’ gestation: a randomized controlled trial. Arch Dis Child Neonatal Fetal ed. 2008;93:F14–9.

    Article  CAS  Google Scholar 

  6. Hosono S, Mugishima H, Fujita H, Hosono A, Okada T, Takahashi S, et al. Blood pressure and urine output during the first 120 h of life in infants born at less than 29 weeks’ gestation related to umbilical cord milking. Arch Dis Child Fetal Neonatal Ed. 2009;94:F328–31.

    Article  CAS  Google Scholar 

  7. Katheria AC, Leone TA, Woelkers D, Garey DM, Rich W, Finer NN. The effects of umbilical cord milking on hemodynamics and neonatal outcomes in premature neonates. J Pediatr. 2014;164:1045–50.

    Article  Google Scholar 

  8. Backes CH, Rivera BK, Haque U, Bridge JA, Smith CV, Hutchon DJ, et al. Placental transfusion strategies in very preterm neonates: a systematic review and meta-analysis. Obstet Gynecol 2014;124:47–56.

  9. Katheria A, Blank D, Rich W, Finer N. Umbilical cord milking improves transition in premature infants at birth. PloS ONE. 2014; 9:e94085.

  10. Blank DA, Polglase GR, Kluckow M, Gill AW, Crossley KJ, Moxham A, et al. Haemodynamic effects of umbilical cord milking in premature sheep during the neonatal transition. Arch Dis Child Fetal Neonatal Ed. 2018;103:F539–F546.

    Article  Google Scholar 

  11. Takami T, Suganami Y, Sunohara D, Kondo A, Mizukaki N, Fujioka T, et al. Umbilical cord milking stabilizes cerebral oxygenation and perfusion in infants born before 29 weeks of gestation. J Pediatr. 2012;161:742–7.

    Article  Google Scholar 

  12. El-Naggar W, Simpson D, Hussain A, Armson A, Dodds L, Warren A, et al. Cord milking versus immediate clamping in preterm infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2019;104:F145–F150.

    Article  Google Scholar 

  13. Popat H, Robledo KP, Sebastian L, Evans N, Gill A, Kluckow M, et al. Effect of delayed cord clamping on systemic blood flow: a randomized controlled trial. J Pediatr. 2016;178:81–86.

    Article  Google Scholar 

  14. Nagano N, Saito M, Sugiura T, Miyahara F, Namba F, Ota E. Benefits of umbilical cord milking versus delayed cord clamping on neonatal outcomes in preterm infants: a systematic review and meta-analysis. PLoS ONE. 2018;13:e0201528.

    Article  Google Scholar 

  15. Katheria AC, Reister F, Essers J, Mendler M, Hummler H, Subramaniam A, et al. Association of umbilical cord milking vs delayed umbilical cord clamping with death or severe intraventricular hemorrhage among preterm infants. JAMA. 2019;322:1877–86.

    Article  Google Scholar 

  16. Banerjee J, Leung TS, Aladangady N. Cerebral blood flow and oximetry response to blood transfusion in relation to chronological age in preterm infants. Early Hum Dev. 2016;97:1–8.

    Article  CAS  Google Scholar 

  17. Noori S, Anderson M, Soleymani S, Seri I. Effect of carbon dioxide on cerebral blood flow velocity in preterm infants during postnatal transition. Acta Paediatr. 2014;103:e334–9.

    Article  CAS  Google Scholar 

  18. Bhatt S, Alison BJ, Wallace EM, Crossley KJ, Gill AW, Kluckow M, et al. Delaying cord clamping until ventilation onset improves cardiovascular function at birth in preterm lambs. J Physiol. 2013;591:2113–26.

    Article  CAS  Google Scholar 

  19. Hooper SB, Te Pas AB, Lang J, van Vonderen JJ, Roehr CC, Kluckow M, et al. Cardiovascular transition at birth: a physiological sequence. Pediatr Res. 2015;77:608–14.

    Article  Google Scholar 

  20. Niermeyer S, Velaphi S. Promoting physiologic transition at birth: re-examining resuscitation and the timing of cord clamping. Semin Fetal Neonatal Med. 2013;18:385–92.

    Article  Google Scholar 

  21. Bhatt S, Polglase GR, Wallace EM, Te Pas AB, Hooper SB. Ventilation before umbilical cord clamping improves the physiological transition at birth. Front Pediatr. 2014;2:113.

    Article  Google Scholar 

  22. Hansen NB, Stonestreet BS, Rosenkrantz TS, Oh W. Validity of Doppler measurements of anterior cerebral artery blood flow velocity: correlation with brain blood flow in piglets. Pediatrics. 1983;72:526–31.

    CAS  PubMed  Google Scholar 

  23. Greisen G, Johansen K, Ellison PH, Fredriksen PS, Mali J, Friis-Hansen B. Cerebral blood flow in the newborn infant: comparison of Doppler ultrasound and 133xenon clearance. J Pediatr. 1984;104:411–8.

    Article  CAS  Google Scholar 

  24. Benders MJ, Hendrikse J, de Vries L, Groenendaal F, van Bel F. Doppler- assessed cerebral blood flow velocity in the neonate as estimator of global cerebral blood volume flow measured using phase-contrast magnetic resonance angiography. Neonatology. 2013;103:21–6.

    Article  Google Scholar 

  25. Pezzati M, Dani C, Biadaioli R, Filippi L, Biagiotti R, Giani T, et al. Early postnatal Doppler assessment of cerebral blood flow velocity in healthy preterm and term infants. Dev Med Child Neurol. 2002;44:745–52.

    Article  Google Scholar 

  26. Gill AW. Postnatal cardiovascular adaptation. Arch Dis Child Fetal Neonatal Ed. 2019;104:F220–F224.

    Article  Google Scholar 

  27. Baenziger O, Stolkin F, Keel M, von Siebenthal K, Fauchere JC, Das Kundu S, et al. The influence of the timing of cord clamping on postnatal cerebral oxygenation in preterm neonates: a randomized, controlled trial. Pediatrics. 2007;119:455–9.

    Article  Google Scholar 

  28. Jaiswal P, Upadhyay A, Gothwal S, Chaudhary H, Tandon A. Comparison of umbilical cord milking and delayed cord clamping on cerebral blood flow in term neonates. Indian J Pediatr. 2015;82:890–5.

    Article  Google Scholar 

  29. Shortland DB, Levene M, Archer N, Shaw D, Evans D. Cerebral blood flow velocity recordings and the prediction of intracranial haemorrhage and ischaemia. J Perinat Med. 1990;18:411–7.

    Article  CAS  Google Scholar 

  30. Evans N, Kluckow M, Simmons M, Osborn D. Which to measure, systemic or organ blood flow? Middle cerebral artery and superior vena cava flow in very preterm infants. Arch Dis Child Fetal Neonatal Ed. 2002;87:F181–4.

    Article  CAS  Google Scholar 

  31. Vesoulis ZA, Mathur AM. Cerebral autoregulation, brain injury, and the transitioning premature infant. Front Pediatr. 2017;5:64.

    Article  Google Scholar 

  32. Rhee CJ, da Costa CS, Austin T, Brady KM, Czosnyka M, Lee JK. Neonatal cerebrovascular autoregulation. Pediatr Res. 2018;84:602–10.

    Article  Google Scholar 

  33. Vutskits L. Cerebral blood flow in the neonate. Paediatr Anaesth. 2014;24:22–9.

    Article  Google Scholar 

Download references

Funding

This project was supported by grants from both Nova Scotia Health Research Foundation (PSO-EST-2013-9023 EGMS 1813) and IWK Research Foundation (1008052). No honorarium or other form of payment was given to anyone to produce this manuscript.

Author contributions

WE-N was involved in study design, Research Ethics Board (REB) approval, performing echocardiography studies, data review and manuscript preparation. DS was involved in conducting echocardiography studies, data review and manuscript reviewing. AH was involved in reading and interpreting echocardiography studies, data review and manuscript reviewing. AA was involved in study design, REB approval and manuscript reviewing. AW was involved in study design, REB approval and manuscript reviewing. RW was involved in study design, REB approval and manuscript reviewing. DM was involved in study design, REB approval, and manuscript reviewing. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Walid El-Naggar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Naggar, W., McMillan, D., Hussain, A. et al. The effect of umbilical cord milking on cerebral blood flow in very preterm infants: a randomized controlled study. J Perinatol 41, 263–268 (2021). https://doi.org/10.1038/s41372-020-00780-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41372-020-00780-2

Search

Quick links