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:

Umbilical cord milking reduces the risk of intraventricular hemorrhage in preterm infants born before 32 weeks of gestation

Journal of Perinatology volume 39, pages 547–553 (2019)Cite this article

Subjects

Abstract

Objective

Intraventricular hemorrhage (IVH) is a common complication in extremely preterm infants. We aimed to demonstrate that umbilical cord milking (UCM) would reduce the incidence of IVH in this at risk population.

Study design

We compared the incidence of IVH in a prospective cohort of consecutively born preterm infants <32 weeks’ gestation receiving UCM (n = 33) with a historical cohort that underwent immediate cord clamping (ICC) (n = 36).

Results

No significant differences regarding perinatal characteristics were present between both groups except for chorioamnionitis and preterm rupture of membranes which were more frequent in the UCM group. There was a significant reduction in the incidence of IVH in the UCM group as compared to the ICC group (UCM vs. ICC = 12 vs. 33%, p = 0.037; OR = 0.276 (95% CI 0.079–0.967; p = 0.033; NNT = 4.7) and a reduction in the number of transfusions (UCM vs. ICC = 56 vs. 30%, p = 0.035; OR = 0.348 (0.129–0.938; p = 0.033; NNT = 3.8). UCM was safe for mothers (similar decrease in maternal hemoglobin) and offspring.

Conclusion

UCM significantly reduced the incidence of IVH in preterm infants < 32 weeks’ gestation without associated complications for mother or offspring.

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

Similar content being viewed by others

References

  1. García-Muñoz Rodrigo F, Díez Recinos AL, García-Alix Pérez A, Figueras Aloy J, Vento Torres M. Changes in perinatal care and outcomes in newborns at the limit of viability in Spain: the EPI-SEN Study. Neonatology. 2015;107:120–9.

    Article  Google Scholar 

  2. Rabe H, Diaz-Rossello JL, Duley L, Dowswell T. Effect of timing of umbilical cord clamping and other strategies to influence placental transfusion at preterm birth on maternal and infant outcomes. Cochrane Database Syst Rev. 2012; 8. https://doi.org/10.1002/14651858.CD003248.pub3.

  3. Committee on Obstetric Practice, American College of Obstetricians and Gynecologists. Committee Opinion no.543: timing of umbilical cord clamping after birth. Obstet Gynecol. 2012;120:1522–6.

    Article  Google Scholar 

  4. Perlman JM, Wyllie J, Kattwinkel J, Wyckoff MH, Aziz K, Guinsburg R. et al. On behalf of the Neonatal Resuscitation Chapter CollaboratorsPart 7: neonatal resuscitation: 2015 International consensus on cardiopulmonary resuscitation and emergency cardiovascular care science with treatment recommendations. Circulation. 2015;132:S204–241.

    Article  Google Scholar 

  5. Sommers R, Stonestret BS, Oh W, Laptook A, Yanowitz TD, Raker C, et al. Hemodynamic effects of delayed cord clamping in premature infants. Pediatrics. 2012;129:667–72.

    Article  Google Scholar 

  6. 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 at less than 29 weeks’ gestation: a randomized controlled trial. Arch Dis Child Fetal Neonatal Ed. 2008;93:14–9.

    Article  Google Scholar 

  7. March MI, Hacker MR, Parson AW, Modest AM, de Veciana M. The effects of umbilical cord milking in extremely preterm infants: a randomized controlled trial. J Perinatol. 2013;33:763–7.

    Article  CAS  Google Scholar 

  8. 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 

  9. Katheria A, Blank D, Rich W, Finer N. Umbilical cord milking improves transition in premature infants at birth. PLoS One. 2014;7:e94085.

    Article  Google Scholar 

  10. Alan S, Arsan S, Okulu E, Akin IM, Kilic A, Taskin S, et al. Effects of umbilical cord milking on the need for packed red blood cell transfusions and early neonatal hemodynamic adaptation in preterm infants born ≤1500 g: a prospective, randomized, controlled trial. J Pediatr Hematol Oncol. 2014;36:e493–8.

    Article  Google Scholar 

  11. Song SY, Kim Y, Kang BH, Yoo HJ, Lee M. Safety of umbilical cord milking in very preterm neonates: a randomized controlled study. Obstet Gynecol Sci. 2017;60:527–34.

    Article  Google Scholar 

  12. 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 

  13. Dang D, Zhang C, Shi S, Mu X, Lv X, Wu H. Umbilical cord milking reduces need for red cell transfusions and improves neonatal adaptation in preterm infants: Meta-analysis. J Obstet Gynaecol Res. 2015;41:890–5.

    Article  Google Scholar 

  14. Rabe H, Jewison A, Alvarez RF, Crook D, Stilton D, Bradley R, et al. Milking compared with delayed cord clamping to increase placental transfusion in preterm neonates: a randomized controlled trial. Obstet Gynecol. 2011;117:205–11.

    Article  Google Scholar 

  15. Katheria AC, Truong G, Cousins L, Oshiro B, Finer NN. umbilical cord milking versus delayed cord clamping in preterm infants. Pediatrics. 2015;136:61–9.

    Article  Google Scholar 

  16. Katheria A, Garey D, Truong G, Akshoomoff N, Steen J, Maldonado M, et al. A randomized clinical trial of umbilical cord milking vs delayed cord clamping in preterm infants: neurodevelopmental outcomes at 22-26 months of corrected age. J Pediatr. 2018;194:76–80.

    Article  Google Scholar 

  17. Nagano N, Saito N, 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 https://doi.org/10.1371/journal.pone.0201528. 30

    Article  PubMed  PubMed Central  Google Scholar 

  18. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1500 gm. J Pediatr. 1978;92:529–34.

    Article  CAS  Google Scholar 

  19. Moro M, Vento M (eds). In: De guardia en Neonatologia. 3rd ed. Madrid: Panamericana; 2016. p. 650–9.

  20. International Committee for the Classification of Retinopathy of Prematurity. The international classification of retinopathy of prematurity revisited. Arch Ophthalmol 2005;123:991–9.

  21. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2001;163:1723.

    Article  CAS  Google Scholar 

  22. Bell MJ, Ternberg J, Fengin RR. Neonatal necrotizing enterocolitis: therapeutic decisions based on clinical staging. Ann Surg. 1978;187:1–7.

    Article  CAS  Google Scholar 

  23. Rezaie P, Dean A. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology. 2002;22:106–32.

    Article  Google Scholar 

  24. Gibbs RS, Blanco JD, St Clair PJ, Castaneda YS. Quantitative bacteriology of amniotic fluid from women with clinical intraamniotic infection at term. J Infect Dis. 1982;145:1–8.

    Article  CAS  Google Scholar 

  25. Anonymous. Practice Bulletin No.160: Premature rupture of membranes. Obstet Gynecol. 2016; 127:39-51.

  26. Bolisetty S, Dhawan A, Abdel-Latif M, Bajuk B, Stack J, Lui K. Intraventricular hemorrhage and neurodevelopmental outcomes in extreme preterm infants. Pediatrics. 2014;133:55–62.

    Article  Google Scholar 

  27. Osborn DA, Evans N, Kluckow M. Hemodynamic and antecedent risk factors of early and late periventricular/intraventricular haemorrhage in premature infants. Pediatrics. 2003;112:33–9.

    Article  Google Scholar 

  28. Kluckow M, Evans N. Low superior vena cava flow and intraventricular haemorrhage in preterm infants. Arch Dis Child Fetal Neonatal Ed. 2000;82:188–94.

    Article  Google Scholar 

  29. 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 gestation. J Pediatr. 2012;161:742–7.

    Article  Google Scholar 

  30. Rabe H, Sawyer A, Amess P, Ayers S. Neurodevelopmental outcomes at 2 and 3.5 years for very preterm babies enrolled in a randomized trial of milking the umbilical cord versus delayed cord clamping. Neonatology. 2016;109:113–9.

    Article  Google Scholar 

  31. El-Naggar W, Simpson D, Hussain A, Armson A, Doods L, Warren A, et al. Cord milking versus immediate clamping in preterm infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal 2018. https://doi.org/10.1136/archdischild-2018-314757.

  32. Blank DA, Polglase GR, Kluckow M, Gill AW, Crossley KJ, Moxham A, et al. Haemodinamic effects of umbilical cord milking in premature sheep during neonatal transition. Arch Dis Child Fetal Neonatal 2017 https://doi.org/10.1136/archdischild-2017-314005.

  33. Katheria A, Poeltler D, Durham J, Steen J, Rich W, Arnell K, et al. Neonatal resuscitation with an intact cord: a randomized clinical trial. J Pediatr. 2016;178:75–80.

    Article  Google Scholar 

  34. Meyer MP, Nevill E, Wong MM. Provision of respiratory support compared to no respiratory support before cord clamping for preterm infants. Cochrane Database Syst Rev. 2018;3:CD012491 https://doi.org/10.1002/14651858.CD012491.pub2.

    Article  PubMed  Google Scholar 

  35. Gano D, Ho ML, Partridge JC, Glass HC, Xu D, Barkovich AJ, et al. Antenatal exposure to magnesium sulfate is associated with reduced cerebellar hemorrhage in preterm newborns. J Pediatr. 2016;178:68–74.

    Article  CAS  Google Scholar 

  36. Patel S, Clark EAS, Rodriguez CE, Metz TD, Abbaszadeh M, Yoder BA. Effect of umbilical cord milking on morbidity and survival in extremely low gestational age neonates. Am J Obstet Gynecol. 2014;211:519.e1–7.

    Article  Google Scholar 

  37. Kilicdag H, Gulcan H, Hanta D, Torer B, Gokmen Z, Ozdemir SI, et al. Is umbilical cord milking always an advantage? J Matern Fetal Neonatal Med. 2016;29:615–8.

    Article  Google Scholar 

  38. Carroll J. Human cord blood for the hypoxic-ischemic neonate. Pediatr Res. 2012;71:459–63.

    Article  CAS  Google Scholar 

  39. Li J, McDonald CA, Fahey MC, Jenkin G, Miller SL. Could cord blood cell therapy reduce preterm brain injury? Front Neurol. 2014;5:200.

    PubMed  PubMed Central  Google Scholar 

  40. Vatansever B, Demirel G, Ciler Eren E, Erel O, Neselioglu S, Karavar NH, et al. Is early cord clamping or cord milking best? J Mater Fetal Neonatal Med. 2018;31:877–80.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to especially thank the families for their generosity in accepting participate in the study. We also would like to thank the obstetric team and the nursing staff in the delivery room for their essential contribution.

Funding

M Vento acknowledges a FIS PI17/0131 grant from the Instituto de Investigación Sanitaria Carlos III (Ministry of Science, Innovation and Universities; Kingdom of Spain)

Author information

Authors and Affiliations

  1. Division of Neonatology, General and University Hospital, Castellon, Spain

    J. d. Toledo, S. Rodilla, A. Pérez-Iranzo & A. Delgado

  2. Division of Obstetrics and Gynecology, General and University Hospital, Castellon, Spain

    Y. Maazouzi

  3. Division of Neonatology, University and Polytechnic Hospital La Fe, Valencia, Spain

    M. Vento

  4. Health Research Institute La Fe, Valencia, Spain

    M. Vento

Authors
  1. J. d. Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Rodilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Pérez-Iranzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Delgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Y. Maazouzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Vento
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JDT conceived the study and contributed to its design, enrolled patients, retrieved and analyze the data, and wrote the draft of the manuscript. SR enrolled patients, retrieved and analyze the data, and wrote the draft of the manuscript. AP-I enrolled patients, retrieved and analyze the data, and wrote the draft of the manuscript, AD enrolled patients, retrieved and analyze the data, and wrote the draft of the manuscript, YM, enrolled patients, retrieved and analyze the data, and wrote the draft of the manuscript, MV contributed to the study design, supervised data analysis, and wrote the final version of the manuscript.

Corresponding author

Correspondence to M. Vento.

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

Toledo, J.d., Rodilla, S., Pérez-Iranzo, A. et al. Umbilical cord milking reduces the risk of intraventricular hemorrhage in preterm infants born before 32 weeks of gestation. J Perinatol 39, 547–553 (2019). https://doi.org/10.1038/s41372-019-0329-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41372-019-0329-6

This article is cited by

Search

Advanced search

Quick links