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American Academy of Pediatrics
Article

Benefits of Delayed Cord Clamping in Red Blood Cell Alloimmunization

Charles Garabedian, Thameur Rakza, Elodie Drumez, Marion Poleszczuk, Louise Ghesquiere, Bénédicte Wibaut, Marie-Hélène Depoortere, Pascal Vaast, Laurent Storme and Véronique Houfflin-Debarge
Pediatrics March 2016, 137 (3) e20153236; DOI: https://doi.org/10.1542/peds.2015-3236
Charles Garabedian
aDepartment of Obstetrics,
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Thameur Rakza
bNeonatology Unit, and
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Elodie Drumez
cDepartment of Biostatistics, University of Lille North of France, CHRU Lille, France; and
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Marion Poleszczuk
aDepartment of Obstetrics,
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Louise Ghesquiere
aDepartment of Obstetrics,
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Bénédicte Wibaut
dInstitute of Hematology and Transfusion, Jeanne de Flandre Hospital, CHRU of Lille, France;
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Marie-Hélène Depoortere
aDepartment of Obstetrics,
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Pascal Vaast
aDepartment of Obstetrics,
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Laurent Storme
bNeonatology Unit, and
eFaculty of Medicine, University of Lille North of France, CHRU Lille, France
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Véronique Houfflin-Debarge
aDepartment of Obstetrics,
eFaculty of Medicine, University of Lille North of France, CHRU Lille, France
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Abstract

BACKGROUND AND OBJECTIVE: Several studies have shown the benefits of delayed cord clamping (DCC) in preterm and in healthy newborns at short and long term. Our objective was to evaluate the potentials benefits and risks of DCC in red cell alloimmunization.

METHODS: This was a comparative before/after study of all living born neonates followed after fetal anemia requiring in utero transfusion. DCC was defined as cord clamping 30 seconds after birth.

RESULTS: We included a continuous series of 72 neonates: 36 without DDC (group 1) and 36 with DDC (group 2). Hemoglobin at birth was lower in group 1 (10.2 vs 13.4 g/dL, P = .0003); 7 (25%) neonates in group 1 vs 24 (70.6%) in group 2 had no anemia at birth (P = .004). The rate of transfusion was similar between the 2 groups. Postnatal exchange transfusions were more likely performed in the group without DCC than in the group with DCC (47.2% vs 19.4%, P = .0124). Delay between birth and first transfusion was higher in group 2 (0 [0–13] vs 1 [0–21], P = .0274). The maximum level of bilirubin, the rate of intensive phototherapy, and the total duration of phototherapy were similar in the 2 groups.

CONCLUSIONS: This study highlights a significant benefit of DCC in anemia secondary to red blood cell alloimmunization with a resulting decreased postnatal exchange transfusion needs, an improvement in the hemoglobin level at birth and longer delay between birth and first transfusion with no severe hyperbilirubinemia.

  • Abbreviations:
    DCC —
    delayed cord clamping
    ET —
    postnatal exchange transfusion
    Hb —
    hemoglobin
    ICC —
    immediate cord clamping
    IUT —
    in utero transfusion
    MCA PSV —
    middle cerebral artery peak systolic velocity
    PT —
    phototherapy
  • What’s Known on This Subject:

    Delayed cord clamping in preterm birth and in healthy newborns allows a significant increase in hematocrit and hemoglobin at birth, and in ferritin level leading to a significant decrease in the risk of anemia in the first months of life.

    What This Study Adds:

    This is the first study evaluating delayed cord clamping in red cell alloimmunization. It allows an increase of hemoglobin at birth, longer delay before first neonatal transfusion and a diminution of exchange transfusion without more neonatal complication due to hyperbilirubinemia.

    Immune hemolytic disease of the newborn is responsible for neonatal anemia and jaundice. Therapeutic support of this pathology requires, according to the degree of severity, phototherapy (PT), and/or exchange transfusion (ET), and/or blood transfusions, and/or immunoglobulin infusion.1–3

    Approximately 25% to 60% of the total blood volume of fetal placental circulation (54–160 mL) and 60% of fetal red blood cells is found in the placental circulation.4,5 This blood is rich in hematopoietic stem cells.6 At birth, delayed cord clamping (DCC) allows placental blood transfusion, which can represent up to one-quarter to one-third of the total blood volume of the newborn at term.5 Several trials and meta-analyses have studied the benefits of DCC versus early cord clamping.7–17 In preterm infants, Rabe et al16 showed, in a meta-analysis of 10 studies describing a total of 454 preterm infants, that major benefits of the DCC were higher circulating blood volume during the first 24 hours of life, less need for blood transfusions (P = .004), and less incidence of intraventricular hemorrhage (P = .002). Recently, Chiruvolu et al18 confirmed those results with a reduction of early red blood cell transfusion in the DCC group compared with an historical cohort (13.3% vs 33%) (odds ratio 0.11, 0.03–0.41). In healthy newborns, after delayed clamping, it was observed at birth a significant increase in hematocrit and hemoglobin (Hb) in the physiologic range, and an increase in ferritin level leading to a significant decrease in the risk of anemia in the first months of life.9,12 At 4 years of age, DCC compared with early cord clamping improved scores in the fine-motor and social domains, especially in boys.19 However, DCC has never been studied in case of alloimmunization. Our hypothesis is that DCC allows a higher rate of Hb at birth allowing less need for transfusions (blood transfusions or ET), which can decrease neonatal morbidity linked to those procedures. However, reserves concerning DCC in red blood cell alloimmunization are the risks of overloading the newborn with additional incompatible red blood cells, leading to increased levels of bilirubin.

    In 2009, we began DCC in cases of red cell alloimmunization with a history of utero transfusions. Our objective was to evaluate the potentials benefits and risks of DCC in a comparative before/after study.

    Methods

    This is a comparative before/after study, from January 2001 to December 2014, of all living neonates followed after fetal anemia requiring in utero transfusion (IUT). We included a continuous series of neonates with DCC and compared it with a similar continuous series of historic cohort with immediate cord clamping (ICC). Ethical approval was granted by the French Ethics Committee of research in Obstetrics and Gynecology (CEROG OBS 2012-02-04).

    In the first few years of the study, IUT was indicated whenever the optical index at 450 nm (DOD450) fell in zone III of the Liley diagram.20 This technique was progressively replaced by the middle cerebral artery peak systolic velocity (MCA PSV). Fetal anemia was defined as MCA PSV greater than 1.5 to 1.55 MoM.21 Technical realization of IUT was the same as previously described.22 IUT was performed until the 34th week of gestation. Beyond this age, fetal extraction was discussed with the perinatal specialists.

    In our center, we have a systematic policy of DCC in premature infants born before 34 weeks of gestation, in agreement with the recommendations of the European Resuscitation Council.23 Since 2009, we have extended our DCC protocol to include cases of red cell alloimmunization with a history of utero transfusions. We have defined DCC as cord clamping 30 seconds after birth.

    Hb level was evaluated during the first hour of life. Our neonatal management was similar as previously described.24 Phototherapy (PT) was administered with 2 devices (Tunnel MIDEPREMA, Tours, France, and NATUS NeoBlue, Natus Medical Inc, San Carlos, CA). During the study period, the neonatal protocol changed and PT was systematically done in case of alloimmunization since. ET was performed with double-volume transfusion (160 mL/kg) using irradiated and leukocyte-depleted erythrocytes and our criteria for ET were bilirubin level at birth >3.5 mg/dL or bilirubin levels above threshold in combination with failure of PT. Indication for red blood cell transfusion was Hb level at birth <10 g/dL or if clinical symptoms of anemia were present.

    Data concerning obstetric history, antenatal management, and neonatal outcome until the discharge from the NICU were collected.

    Statistics

    We compared 2 groups: 1 without DCC (ICC group) during the first period of the study (January 2001–June 2009) and 1 with DCC (June 2009–December 2014). The primary outcome was the need of blood transfusion or ET after birth. Secondary outcomes were Hb level at birth, free serum bilirubin postnatal maximum levels, duration of PT, transfer rate to the neonatal unit, and duration of initial hospitalization.

    Qualitative variables are expressed as frequency (percentage) and quantitative variables as mean ± SD or median (range) in case of non-Gaussian distribution (normality of distribution was checked graphically and by using the Shapiro–Wilk test). Comparisons between the 2 groups were made using the χ2 test (or Fisher exact test when expected cell frequency was <5) for qualitative variables and the Student t test (or Mann-Whitney U test for non-Gaussian distribution) for quantitative variables.

    Statistical testing was done at the 2-tailed α level of 0.05. Data were analyzed by using the SAS software package, release 9.4 (SAS Institute, Inc, Cary, NC).

    Results

    We included a continuous series of 72 neonates: 36 with ICC and 36 with DCC. Cord clamping was done in all neonates of group DCC. Characteristics of the population are summarized in Table 1. The main antibody was Rhesus D (80.6% in group 1 and 72.2% in group 2). There were no differences between the 2 groups regarding the age, the gestity, and the rate of hydrops fetalis.

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    TABLE 1

    Population

    Gestational age and Hb at first IUT were comparable (Table 2). Antenatal management was similar during the periods with comparable delay between last IUT and birth, and same rate of MCA PSV ≥1.5 MoM before delivery. We observed 5 emergency cesarean deliveries (4 in ICC group and 1 in DCC group) secondary to bradychardia during the IUT. Cord clamping was done before resuscitation by the pediatrician.

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    TABLE 2

    Ante Natal Management

    Gestational age at birth and birth weight were lower in the ICC group (Table 3). Hemoglobin at birth was higher in the DCC group (5.6 ± 2.4 vs 6.7 ± 2.5 g/dL, P = .0003); 7 (25%) neonates in the ICC group versus 24 (70.6%) in the DCC group had no anemia at birth (Hb >12 g/dL) (P = .004).

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    TABLE 3

    Neonatal Data

    The rate of neonatal transfusion was similar between the 2 groups. Postnatal ETs were more likely performed in the ICC group than in the DCC group (47.2% vs 19.4%, P = .0124). The delay between birth and first transfusion was higher in DCC group (0 [0–13] vs 1 [0–21] day, P = .0274). The maximum level of bilirubin was comparable between the 2 groups; 83.3% of neonates required PT (intensive or not) in ICC group versus 97.1% in DCC group. The rate of intensive PT and the total duration of PT were similar in the 2 groups (P = .49 and P = .66).

    No neonatal death was observed during the study period.

    Discussion

    To our knowledge, this is the first description of DCC in moderate or severe immune anemia since red blood cell alloimmunization was excluded from all previous studies. Our study demonstrated a significant benefit of DCC in immune anemia managed by IUT. We observed a significant increase in Hb levels at birth, a longer delay between birth and first transfusion, and a decrease in the postnatal ET with no maternal or neonatal adverse impact of DCC.

    The rationale for the benefits of DCC in infants with red blood cell alloimmunization is to allow a higher rate of Hb at birth, decreasing the numbers of postnatal exchange and top-up transfusions. Previous studies in preterm and term neonates shown an increase of Hb and of hematocrit in case of DCC.7,9,13,14,25 In our population, we observed an increase of Hb at birth in the DDC group. We can relate this higher Hb rate to the implementation of DDC and not to a change in our practice: delay between last IUT and birth was similar between the groups and we showed in a previous study that the use of PSV MCA did not modify our antenatal management.20

    Our series found a significant decrease of ET in children with immune hemolytic disease after DCC. This procedure is attempted in severe anemia and/or severe hyperbilirubinemia, particularly if the PT fails. Postnatal ET rate usually varies from 16% to 71% in case of alloimmunization.1–3 This result is particularly interesting because of neonatal morbidity linked to this procedure. The mortality rate is estimated to be between 0.5% and 2.0% and the morbidity rate varies from 5.0% to 74.0%.26,27 The main complications are mostly linked to the umbilical vein catheterization and to the transfusion risks.28 On the contrary, the rate of transfusions and the median number of transfusions were similar between the 2 groups. One major benefit of DCC is the delay between birth and first transfusion. We observed in our population a gain of 4 days of life before first transfusion in the DCC group. This avoids transfusion in emergencies and allows a better organization of neonatal care.

    Reserves concerning DCC in red blood cell alloimmunization were the risks of overloading the newborn with additional incompatible red blood cells, leading to increased levels of bilirubin and, in very severe cases, severe jaundice and kernicterus.29 In our study we did not find a difference in maximal bilirubin levels in the 2 groups. In red blood cell alloimmunization, all newborns are subjected to PT in the first hours of life as well as enhanced surveillance to prevent the progression into a severe jaundice.28 We observed a high rate and of PT in the DCC group but a lower rate of intensive PT. There was no severe complication, such as kernicterus. This high rate of PT can be also explained by a change in our neonatal practice with systematic PT during the first hours of life in case of red blood cell alloimmunization. Data on late-onset jaundice and DCC are variable in the literature. Van Rheenen et al17 found an increased risk of hyperbilirubinemia of 12%, with no increase in the PT or ET needs. On the contrary, Arca et al30 and McDonald et al12 found a significant increase in neonates requiring PT after delayed clamping.

    Although many randomized controlled trials have evaluated the benefits of DCC versus ICC in term and preterm infants, the ideal timing for cord clamping has yet to be established.31 The definition of delayed umbilical cord clamping varied between studies from 30 and 180 seconds. McDonnel et al32 had a mean DCC of 31 seconds. Kugelman et al33 and Mercer et al13 proposed a DCC of 30 to 45 seconds, whereas Aladangady et al34 had 60 to 90 seconds. The longest was 180 seconds.35 Our protocol was a preliminary study and we chose the minimal duration recommended (30 seconds).

    This study is the first to evaluate the impact of DCC in neonatal management in red cell alloimmunization. Due to the study design (before/after study), potentially covariates may be unevenly distributed between groups. One potential bias is the change in neonatal practices for PT during the study period. In the ICC group, neonates were smaller, born earlier, and more likely by cesarean. These factors may influence the study findings. However, it seems difficult to conduce a randomized trial due to the low prevalence of alloimmunization and to the known benefits of DCC.

    Conclusions

    DCC has already demonstrated its benefits in preterm birth, with a decrease in the transfusion needs. This study highlights a significant benefit of DCC in moderate to severe anemia secondary to red blood cell alloimmunization with resulting decreased postnatal ET needs, and an improvement in the Hb level at birth, with no severe hyperbilirubinemia. We recommend DCC with duration of 30 seconds in infants at risk for red blood cell alloimmunization neonatal anemia only if the monitoring and management of jaundice can be optimal. It will be interesting to evaluate the long-term effects of DCC in this population.

    Footnotes

      • Accepted November 24, 2015.
    • Address correspondence to Charles Garabedian, MD, Pôle d’Obstétrique, Hôpital Jeanne de Flandre, CHRU Lille, Avenue Eugène Avinée, 59037 Lille Cedex, France. E-mail: charles.garabedian{at}chru-lille.fr
    • FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

    • FUNDING SOURCE: No external funding.

    • POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

    References

    1. ↵
      1. De Boer IP,
      2. Zeestraten ECM,
      3. Lopriore E,
      4. van Kamp IL,
      5. Kanhai HHH,
      6. Walther FJ
      . Pediatric outcome in Rhesus hemolytic disease treated with and without intrauterine transfusion. Am J Obstet Gynecol. 2008;198(1):54.e1–54.e4pmid:18166305
      OpenUrlCrossRefPubMed
      1. McGlone L,
      2. Simpson JH,
      3. Scott-Lang C,
      4. Cameron AD,
      5. Brennand J
      . Short-term outcomes following intrauterine transfusion in Scotland. Arch Dis Child Fetal Neonatal Ed. 2011;96(1):F69–F70pmid:19395394
      OpenUrlCrossRefPubMed
    2. ↵
      1. Weisz B,
      2. Rosenbaum O,
      3. Chayen B,
      4. Peltz R,
      5. Feldman B,
      6. Lipitz S
      . Outcome of severely anaemic fetuses treated by intrauterine transfusions. Arch Dis Child Fetal Neonatal Ed. 2009;94(3):F201–F204pmid:19000998
      OpenUrlAbstract/FREE Full Text
    3. ↵
      1. Yao AC,
      2. Moinian M,
      3. Lind J
      . Distribution of blood between infant and placenta after birth. Lancet. 1969;2(7626):871–873pmid:4186454
      OpenUrlPubMed
    4. ↵
      1. Farrar D,
      2. Airey R,
      3. Law GR,
      4. Tuffnell D,
      5. Cattle B,
      6. Duley L
      . Measuring placental transfusion for term births: weighing babies with cord intact. BJOG. 2011;118(1):70–75pmid:21083868
      OpenUrlCrossRefPubMed
    5. ↵
      1. Wardrop CA,
      2. Holland BM
      . The roles and vital importance of placental blood to the newborn infant. J Perinat Med. 1995;23(1-2):139–143pmid:7658315
      OpenUrlCrossRefPubMed
    6. ↵
      1. Ceriani Cernadas JM,
      2. Carroli G,
      3. Pellegrini L, et al
      . The effect of timing of cord clamping on neonatal venous hematocrit values and clinical outcome at term: a randomized, controlled trial. Pediatrics. 2006;117(4). Available at: www.pediatrics.org/cgi/content/full/117/4/e779pmid:16567393
      1. Ghavam S,
      2. Batra D,
      3. Mercer J, et al
      . Effects of placental transfusion in extremely low birthweight infants: meta-analysis of long- and short-term outcomes. Transfusion. 2014;54(4):1192–1198pmid:24843886
      OpenUrlCrossRefPubMed
    7. ↵
      1. Hutton EK,
      2. Hassan ES
      . Late vs early clamping of the umbilical cord in full-term neonates: systematic review and meta-analysis of controlled trials. JAMA. 2007;297(11):1241–1252pmid:17374818
      OpenUrlCrossRefPubMed
      1. Kinmond S,
      2. Aitchison TC,
      3. Holland BM,
      4. Jones JG,
      5. Turner TL,
      6. Wardrop CA
      . Umbilical cord clamping and preterm infants: a randomised trial. BMJ. 1993;306(6871):172–175pmid:8443480
      OpenUrlAbstract/FREE Full Text
      1. March MI,
      2. Hacker MR,
      3. Parson AW,
      4. Modest AM,
      5. de Veciana M
      . The effects of umbilical cord milking in extremely preterm infants: a randomized controlled trial. J Perinatol. 2013;33(10):763–767pmid:23867960
      OpenUrlCrossRefPubMed
    8. ↵
      1. McDonald SJ,
      2. Middleton P,
      3. Dowswell T,
      4. Morris PS
      . Effect of timing of umbilical cord clamping of term infants on maternal and neonatal outcomes. Cochrane Database Syst Rev. 2013;7:CD004074pmid:23843134
      OpenUrlPubMed
    9. ↵
      1. Mercer JS,
      2. Vohr BR,
      3. McGrath MM,
      4. Padbury JF,
      5. Wallach M,
      6. Oh W
      . Delayed cord clamping in very preterm infants reduces the incidence of intraventricular hemorrhage and late-onset sepsis: a randomized, controlled trial. Pediatrics. 2006;117(4):1235–1242pmid:16585320
      OpenUrlAbstract/FREE Full Text
    10. ↵
      1. Rabe H,
      2. Wacker A,
      3. Hülskamp G, et al
      . A randomised controlled trial of delayed cord clamping in very low birth weight preterm infants. Eur J Pediatr. 2000;159(10):775–777pmid:11039135
      OpenUrlCrossRefPubMed
      1. Rabe H,
      2. Diaz-Rossello JL,
      3. Duley L,
      4. 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:CD003248pmid:22895933
      OpenUrlPubMed
    11. ↵
      1. Rabe H,
      2. Reynolds G,
      3. Diaz-Rossello J
      . A systematic review and meta-analysis of a brief delay in clamping the umbilical cord of preterm infants. Neonatology. 2008;93(2):138–144pmid:17890882
      OpenUrlCrossRefPubMed
    12. ↵
      1. van Rheenen P,
      2. Brabin BJ
      . Late umbilical cord-clamping as an intervention for reducing iron deficiency anaemia in term infants in developing and industrialised countries: a systematic review. Ann Trop Paediatr. 2004;24(1):3–16pmid:15005961
      OpenUrlCrossRefPubMed
    13. ↵
      1. Chiruvolu A,
      2. Tolia VN,
      3. Qin H, et al
      . Effect of delayed cord clamping on very preterm infants. Am J Obstet Gynecol. 2015;213(5):676.e1–676.e7pmid:26196456
      OpenUrlCrossRefPubMed
    14. ↵
      1. Andersson O,
      2. Lindquist B,
      3. Lindgren M,
      4. Stjernqvist K,
      5. Domellöf M,
      6. Hellström-Westas L
      . Effect of delayed cord clamping on neurodevelopment at 4 years of age: a randomized clinical trial. JAMA Pediatr. 2015;169(7):631–638pmid:26010418
      OpenUrlCrossRefPubMed
    15. ↵
      1. Garabedian C,
      2. Vaast P,
      3. Behal H, et al
      . Management of severe fetal anemia by Doppler measurement of middle cerebral artery: are there other benefits than reducing invasive procedures? Eur J Obstet Gynecol Reprod Biol. 2015;192:27–30pmid:26142913
      OpenUrlCrossRefPubMed
    16. ↵
      1. Mari G,
      2. Deter RL,
      3. Carpenter RL, et al; Collaborative Group for Doppler Assessment of the Blood Velocity in Anemic Fetuses
      . Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal red-cell alloimmunization. N Engl J Med. 2000;342(1):9–14pmid:10620643
      OpenUrlCrossRefPubMed
    17. ↵
      1. Garabedian C,
      2. Philippe M,
      3. Vaast P, et al
      . Is intrauterine exchange transfusion a safe procedure for management of fetal anaemia? Eur J Obstet Gynecol Reprod Biol. 2014;179:83–87pmid:24965985
      OpenUrlCrossRefPubMed
    18. ↵
      1. Perlman JM,
      2. Wyllie J,
      3. Kattwinkel J, et al; Neonatal Resuscitation Chapter Collaborators
      . Neonatal resuscitation: 2010 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science with Treatment Recommendations. Pediatrics. 2010;126(5). Available at: www.pediatrics.org/cgi/content/full/126/5/e1319pmid:20956431
    19. ↵
      1. Garabedian C,
      2. Rakza T,
      3. Thomas D, et al
      . Neonatal outcome after fetal anemia managed by intrauterine transfusion. Eur J Pediatr. 2015;174(11):1535–1539pmid:26032762
      OpenUrlCrossRefPubMed
    20. ↵
      1. Duley L,
      2. Batey N
      . Optimal timing of umbilical cord clamping for term and preterm babies. Early Hum Dev. 2013;89(11):905–908pmid:24075205
      OpenUrlCrossRefPubMed
    21. ↵
      1. Keenan WJ,
      2. Novak KK,
      3. Sutherland JM,
      4. Bryla DA,
      5. Fetterly KL
      . Morbidity and mortality associated with exchange transfusion. Pediatrics. 1985;75(2 pt 2):417–421pmid:3969351
      OpenUrlAbstract/FREE Full Text
    22. ↵
      1. Jackson JC
      . Adverse events associated with exchange transfusion in healthy and ill newborns. Pediatrics. 1997;99(5). Available at: www.pediatrics.org/cgi/content/full/99/5/E7pmid:9113964
    23. ↵
      1. Smits-Wintjens VEHJ,
      2. Walther FJ,
      3. Lopriore E
      . Rhesus haemolytic disease of the newborn: postnatal management, associated morbidity and long-term outcome. Semin Fetal Neonatal Med. 2008;13(4):265–271pmid:18387863
      OpenUrlCrossRefPubMed
    24. ↵
      1. American Academy of Pediatrics Subcommittee on Hyperbilirubinemia
      . Management of hyperbilirubinemia in the newborn infant 35 or more weeks of gestation. Pediatrics. 2004;114(1):297–316pmid:15231951
      OpenUrlAbstract/FREE Full Text
    25. ↵
      1. Arca G,
      2. Botet F,
      3. Palacio M,
      4. Carbonell-Estrany X
      . Timing of umbilical cord clamping: new thoughts on an old discussion. J Matern Fetal Neonatal Med. 2010;23(11):1274–1285pmid:20059441
      OpenUrlCrossRefPubMed
    26. ↵
      1. Raju TNK,
      2. Singhal N
      . Optimal timing for clamping the umbilical cord after birth. Clin Perinatol. 2012;39(4):889–900pmid:23164185
      OpenUrlCrossRefPubMed
    27. ↵
      1. McDonnell M,
      2. Henderson-Smart DJ
      . Delayed umbilical cord clamping in preterm infants: a feasibility study. J Paediatr Child Health. 1997;33(4):308–310pmid:9323618
      OpenUrlCrossRefPubMed
    28. ↵
      1. Kugelman A,
      2. Borenstein-Levin L,
      3. Riskin A, et al
      . Immediate versus delayed umbilical cord clamping in premature neonates born < 35 weeks: a prospective, randomized, controlled study. Am J Perinatol. 2007;24(5):307–315pmid:17516307
      OpenUrlCrossRefPubMed
    29. ↵
      1. Aladangady N,
      2. McHugh S,
      3. Aitchison TC,
      4. Wardrop CAJ,
      5. Holland BM
      . Infants’ blood volume in a controlled trial of placental transfusion at preterm delivery. Pediatrics. 2006;117(1):93–98pmid:16396865
      OpenUrlAbstract/FREE Full Text
    30. ↵
      1. Ultee CA,
      2. van der Deure J,
      3. Swart J,
      4. Lasham C,
      5. van Baar AL
      . Delayed cord clamping in preterm infants delivered at 34 36 weeks’ gestation: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2008;93(1):F20–F23pmid:17307809
      OpenUrlAbstract/FREE Full Text
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    1 Mar 2016
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    Benefits of Delayed Cord Clamping in Red Blood Cell Alloimmunization
    Charles Garabedian, Thameur Rakza, Elodie Drumez, Marion Poleszczuk, Louise Ghesquiere, Bénédicte Wibaut, Marie-Hélène Depoortere, Pascal Vaast, Laurent Storme, Véronique Houfflin-Debarge
    Pediatrics Mar 2016, 137 (3) e20153236; DOI: 10.1542/peds.2015-3236

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    Benefits of Delayed Cord Clamping in Red Blood Cell Alloimmunization
    Charles Garabedian, Thameur Rakza, Elodie Drumez, Marion Poleszczuk, Louise Ghesquiere, Bénédicte Wibaut, Marie-Hélène Depoortere, Pascal Vaast, Laurent Storme, Véronique Houfflin-Debarge
    Pediatrics Mar 2016, 137 (3) e20153236; DOI: 10.1542/peds.2015-3236
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