|
Relevance
Active management of the third stage of labor
(comprising administration of a uterotonic agent, cord clamping and
cutting, and controlled cord traction) has supplanted the ‘physiological’
(non-interventionist) approach [1]; as a consequence the umbilical cord is
usually clamped soon after delivery of the baby. The observation that the
cord can contain up to 20 mL of blood [2] raised the possibility of
delaying clamping to allow placental transfusion to the baby. One of the
major advantages could be to increase the circulating volume and
hemoglobin level. The benefits of the former include less respiratory
distress and reduced need for later transfusions [3,4]. Increasing the
hemoglobin level and iron stores is attractive because anemia in early
infancy is a frequent problem, especially in developing countries. However
these potential benefits need to be balanced against possible harmful
effects, for the mother (postpartum hemorrhage and its consequences)
[1,5,6] and infant (delayed resuscitation, hypothermia, polycythemia,
hyperbilirubinemia and risk of intraventricular hemorrhage). The issue is
complicated by the fact that term babies, preterm babies and very
premature babies could behave as different cohorts, making it difficult to
develop an empiric guideline for timing of cord clamping across all
gestations.
This systematic review explores the question: Does
delayed cord clamping (intervention) at delivery, improve maternal
and infant (population), short-term and long-term outcomes (outcome),
compared to early cord clamping (comparator)?
Current Best Evidence
An exhaustive literature search was undertaken in
September 2010, for randomized controlled trials (RCT) comparing delayed
cord clamping (DCC) defined as >30 seconds following delivery, versus
early cord clamping (ECC) defined as within 30 seconds of delivery;
reporting maternal and/or infant outcomes. The final updated search on 16
December 2010 in the Cochrane Library (search term "cord clamp" and
filter "Record title") yielded 3 Cochrane systematic reviews (CSR),
5 other systematic reviews, and 71 trials. Medline search on the same date
(search term: cord clamping; limits: randomized controlled
trial, meta-analysis) yielded 137 citations. The available systematic
reviews [7-12] were either outdated and/or had methodological limitations.
A total of 57 publications were short-listed as
potentially relevant. Thirty were excluded for the following reasons: not
RCT comparing DCC vs ECC (n=6), RCT but intervention in
either arm not according to definition of DCC or ECC (n=4), RCT but
intervention in control arm not described (n=1), outcome not of
interest (n=2), publications as editorials, correspondence or
commentaries (n=6), outdated systematic reviews (n=6), only
abstract available without data (n=5). Overall, 29 trial reports -
15 in term and 14 in preterm deliveries comprise current best evidence (Table
I); this includes two additional trials identified through searching
of bibliography of short-listed publications [23] and recent conference
proceedings [27].
Table I
Summary of Included RCTs
|
Setting [Ref] |
Participants |
DCC |
ECC |
Outcomes |
| |
|
n, timing of clamping |
n, timing of clamping |
|
|
Term Deliveries |
|
Argentina [13] |
>37 wk |
92, >150 sec; |
93, <20 sec
91, 45-75 sec |
Hct (6h,24-48h), PC, PC requiring ET, HB, Bil>16mg/ dl, Maternal blood
loss, Maternal Hct, multiple neonatal morbidities |
|
Argentina [14] |
>37 wk |
83, >150 sec; 83, 45-75 sec |
86, <20 sec |
Ferritin at 6mo, Mean Hb, Hb<10.5g/dl |
|
Mexico [15] |
>37 wk |
237, 2 min |
239, <20 sec |
Hct, clinical HB, Hb, PC, Hct (6mo, Ferritin (6mo), Total iron (6mo),
maternal blood loss |
|
Libya [16] |
37-42 wk |
58, ACCP |
46, <10 sec |
Hct, Hb, PC, HB, hyperviscosity, maternal Hct, maternal Hb |
|
India [17] |
>37 wk |
59, APD + IP lower |
48, ICC |
Hb (3mo), ferritin (3mo), maternal Hb, maternal ferritin |
|
Guatemala [18] |
>37 wk, weight >2 kg |
22, ACCP + IP lower; 22, ACCP + IP level |
21, ICC |
Hct, PC, Hct (2mo), Hb (2mo), ferritin (2mo), Maternal Hb, maternal
ferritin, maternal iron indices(at delivery and follow-up) |
|
India [19] |
>37 wk born to
anemic mothers |
49, APD + IP lower |
53, ICC |
Hb (birth), ferritin (birth), Hb (3mo), ferritin (3mo), anemia (3 mo),
breastfeeding, maternal Hb |
|
Iran [20] |
38-42 wk |
34, 3 min +IP at level |
34, <30 sec |
Hct (2h, 18h), PC, clinical signs of PC (2h, 18, 5d) |
|
Pakistan [21] |
Term |
100, ACCP + IP level |
100, ICC |
Hb, Bil |
|
Sweden [22] |
39-40 wk |
15, 3 min + IP level |
15, <10 sec |
Hct (birth, 24 h, 5d), blood viscosity, rheological parameters |
|
United Kingdom [23] |
Term |
483/480 |
DCC=ACCP or 5 min; ECC=ICC |
Apgar (5min), NICU adm, PT need, breastfeeding, maternal PPH, maternal
mean blood loss, maternal need for BT, MRP, length of third stage |
|
United Kingdom [24] |
37-42 wk |
296, 3 min |
256, ICC |
Respiratory problems, clinical HB, PT need, birth weight, feeding,
maternal PPH, MRP |
|
Canada [25] |
38-42 wk |
15, 1 min + IP lower |
15, <15 sec |
Hct, RBC volume, plasma volume, Bil |
|
Zambia [26] |
Term |
55, ACCP + IP lower |
50, <20 sec |
Hb, ET (1d), HB, birth weight, PT need, anemia (4mo), maternal blood
loss |
|
|
|
|
|
|
|
Sweden [27] |
Term |
200, >180 sec |
200, <10 sec |
Hb (2d), Hct (2d), Bil, respiratory symptoms, PC, PT need, Hb (4mo),
ferritin (4mo), Transferrin saturation (4mo), reticulocyte Hb (4mo),
anemia (4mo) |
|
Preterm Deliveries |
|
United Kingdom [28] |
24-32 wk |
23, 30-90 sec + IP lower |
23, ICC |
Hct, mean blood volume, CRIB score, transfusion requirement |
|
Switzerland [29] |
24-32 wk |
15, 60-90 sec + IP lower |
24, <20 sec |
Mortality, Hct (4h, 24h, 72h), cerebral bood flow (4h, 24h), tissue
oxygenation |
|
South Africa [30] |
<35 wk |
24, 60 sec + IP NS + ergometrine |
14, ICC |
Mortality, cerebral USG (6-72h), Apgar score, birth weight, SBP (5
min), cord blood gas |
|
Israel [31] |
24-35 wk |
30, 30-45 sec + IP lower |
35, 5-10 sec |
Mortality, Hct, MBP, IVH, BT need, no. of BT, PT need, peak Bil, PDA,
NEC |
|
Israel [32] |
24-35 wk |
30, 30-45 sec + IP lower |
35, 5-10 sec |
Levels of IgG, IgM, C3, C4(at birth), sepsis, days of AB, infections
in 1st mo. |
|
Australia [33] |
26-33 wk |
23, 30 sec |
23, ICC |
Mortality, Hct (1h, 4h), Apgar score, temperature, MV need, BT volume,
peak Bil, cerebral USG |
|
USA [34] |
24-32 wk |
16, 30-45 sec + IP lower |
16, 5-10 sec |
MBP, glucose, no. of volume expanders, volume transfused, peak bil,
IVH, suspected NEC |
|
USA [35] |
24-32 wk |
36, 30-45 sec + IP lower |
36, 5-10 sec |
Mortality, no. transfused, volume transfused, IVH, BPD, suspected NEC,
sepsis, LOS |
|
USA [36] |
24-32 wk |
29, 30-45 sec + IP lower |
29, 5-10 sec |
Neurodevelopmental outcome among survivors at 7mo |
|
United Kingdom [37] |
24-28 wk |
16, 30-45 sec + IP NS |
17, ICC |
Hct (4h), BT, resuscitation, Apgar score, BP (12 h), IVH, NEC, RoP,
LOS, PDA |
|
Germany [38] |
<33wk |
19, 45 sec + IP lower |
20, <20 sec + IP at lower |
No. of transfusions, volume transfused, Apgar score, BP, (1h,4h,24h),
RD (1d), IVH, PDA, PT need, PT duration |
|
USA [39] |
30-36 wk |
39/61 |
DCC=1 min + IP at lower; ECC=ICC |
Hct, BT, Apgar score, SNAP score, MV need, Bil, PT need |
|
USA [40] |
30-36 wk |
39, 1 min + IP lower |
61, ICC |
Mortality, IVH |
|
Holland [41] |
36-36 wk |
21, 3 min |
20, <30 sec |
Hct (1h, 10 wk), Hb (1h, 10 wk), glucose, Bil, PC, PT need, ferritin
(10wk) |
AB=antibiotics; ACCP=at cessation of cord pulsations; APD=after placental descent; Bil=Bilirubin;
BP=blood pressure; BPD=broncho-pulmonary dysplasia; BT=blood transfusion; DCC= delayed cord clamping;
ECC = early cord clamping; ET=exchange transfusion; Hb=haemoglobin; HB=hyperbilirubinemia; Hct=hematocrit;
ICC=immediate cord clamping; IP=infant position; IVH=intraventricular hemmorhage; LOS=late onset sepsis,
MBP=mean blood pressure; MRP=manual removal of placenta; MV=mechanical ventilation;
NEC=necrotizing enterocolitis; NICU=neonatal intensive care unit; NS=not specified; PC=polycythemia;
PDA=patent ductus arteriosus; PP=post-partum hemmorhage; PT=phototherapy; RBC=red blood cell;
RD=respiratory distress; RoP=retinopathy of prematurity; SBP=systolic blood pressure, USG=ultrasonography
|
Results of meta-analyses for 17 outcomes in term
deliveries and 16 outcomes in preterm deliveries are detailed in
Table II. The findings suggest limited clinically significant
benefits of delayed cord clamping for term infants; however it resulted in
significantly reduced incidence of intraventricular hemorrhage in preterm
neonates. Delayed clamping neither increases complications nor provides
benefits for mothers delivering at term; risks and benefits for mothers
delivering prematurely have not been explored in the trials.
Table II
Summary of Meta-Analysis of data pertaining to term deliveries
|
Outcome |
Trials (N) |
Participants (n) |
Effect size (95% CI) |
|
Term Deliveries |
|
Initial hematocrit (%) at birth |
6 |
1163 |
MD 2.38 (1.10, 3.67) |
|
Initial hemoglobin (g/dL) |
4 |
1059 |
MD 1.95 (0.81, 3.10) |
|
Hematocrit (%) at longest follow-up |
2 |
403 |
MD 1.72 (-2.00, 5.44) |
|
Hemoglobin (g/dl) at longest follow-up |
7 |
1318 |
MD 0.17 (-0.15, 0.49) |
|
Anemia at follow-up |
3 |
402 |
RR 0.85 (0.54, 1.35) |
|
Ferritin level (mcg/L) at longest follow-up |
4 |
857 |
MD 17.00 (12.15, 21.85) |
|
Admission to NICU |
2 |
1239 |
RR 0.96 (0.40, 2.33) |
|
Respiratory distress |
2 |
1008 |
RR 0.99 (0.35, 2.81) |
|
Hyperbilirubinemia or jaundice |
5 |
2210 |
RR 1.16 (0.92, 1.45) |
|
Requirement of phototherapy |
5 |
1974 |
RR 1.28 (0.48, 3.42) |
|
Polycythemia |
6 |
936 |
RR 1.22 (0.79, 1.87) |
|
Maternal PPH >500 mL |
4 |
1878 |
RR 0.82 (0.65, 1.04) |
|
Severe Maternal PPH (>1000mL) |
4 |
1684 |
RR 1.19 (0.67, 2.11) |
|
Maternal blood loss (mL) |
1 |
963 |
MD -6.36 (-47.66, 34.94) |
|
Maternal hemoglobin (g/dL) |
4 |
1175 |
MD 0.12 (-0.06, 0.30) |
|
Maternal ferritin level (mcg/L) |
2 |
154 |
MD -5.01 (-16.30, 6.28) |
|
Need for manual removal of placenta |
2 |
1315 |
RR 0.45 (0.22, 0.94) |
|
Preterm Deliveries |
|
Mortality |
9 |
503 |
RR 0.55 (0.21, 1.46) |
|
Hematocrit at birth |
9 |
457 |
MD 3.04 (2.58, 3.51) |
|
Requirement for transfusions |
6 |
358 |
RR 0.72 (0.54, 0.96) |
|
Number of transfusions administered |
4 |
144 |
MD -0.92 (-1.78, -0.05) |
|
Peak serum bilirubin (mg/dL) |
5 |
215 |
MD 0.91 (0.21, 1.60) |
|
Requirement of phototherapy |
3 |
180 |
RR 1.23 (0.94, 1.60) |
|
Patent ductus arteriosus |
4 |
183 |
RR 1.28 (0.62, 2.64) |
|
Intraventricular hemmorhage |
7 |
408 |
RR 0.49 (0.32, 0.74) |
|
Respiratory distress syndrome |
1 |
39 |
RR 1.84 (0.64, 5.30) |
|
Requirement of ventilatory support |
2 |
85 |
RR 1.09 (0.66, 1.81) |
|
Mean blood pressure |
2 |
97 |
MD 3.66 (0.74, 6.58) |
|
Necrotizing enterocolitis |
3 |
137 |
RR 0.47 (0.13, 1.69) |
|
Hemoglobin at longest follow-up |
1 |
34 |
MD 1.10 (0.35, 1.85) |
|
Ferritin at follow-up |
1 |
34 |
MD 19.00 (-60.93, 98.93) |
|
Hematocrit at follow-up |
1 |
34 |
MD 4.00 (0.53, 7.47) |
|
Bronchopulmonary dysplasia |
1 |
72 |
RR 1.33 (0.51, 3.46) |
CI=confidence interval, MD=mean difference, RR=relative risk
|
Critical Appraisal
Risk of bias: The 29 trials included in the two
components of this systematic review comprise current best evidence from
published literature. However, only 4 trials in term deliveries
[13,14,20,24] and 7 in preterm deliveries [31,32,34-36,39,40] could be
classified as having low risk of bias based on criteria in the Cochrane
Risk of Bias tool; the remainder had moderate or high [16,18,21,22,25,27]
risk of bias. Web Table I
summarizes the assessment of risk
of bias in the included trials. Data in term deliveries was too limited
for sensitivity analysis to assess impact of low(er) quality trials. Among
preterm deliveries, risk of mortality and intraventricular hemorrhage were
comparable among trials with low risk of bias (RR 0.25, 95% CI=0.04-1.45,
4 trials, n=308) and (RR 0.52; 95% CI=0.28-0.98, 4 trials, n=308)
respectively, suggesting robust results.
Participant characteristics: All the trials
included fairly stable pregnant women and used several exclusion criteria
prior to randomization. Similarly, babies likely to be at risk of adverse
outcomes were generally excluded. Therefore, the results pertain to a
fairly well-filtered cohort of mothers and babies; raising the problem of
distinguishing between efficacy and effectiveness of interventions. The
trials among preterms did not describe the indication/cause of preterm
delivery. This is important because antepartum hemorrhage, fetal distress,
etc could be contributory; in such situations DCC cannot be considered.
Procedural differences in trials: Although the
definition of ECC was fairly uniform across trials, DCC was defined in
multiple ways (time ranging from 30 seconds to 5 minutes). This implies
that trials with different DCC definitions could be heterogeneous enough
to warrant caution in interpreting results.
Further, besides the timing of cord clamping, the
position of the infant following delivery could independently affect
placental transfusion to the baby. Since there is no clear recommendation
on the ideal infant position following delivery [42], trials in term
babies positioned babies either lower than the introitus [17,19,25,26], or
at the same level [20-22] in the DCC arm. Position was not specified in
the ECC arm. One trial [18] had two DCC arms with position lower and at
level. Among preterms, the majority of trials used lower position with DCC
[28,29,31,32,34-36,39,40]. Only one trial [38] used the lower position for
both arms. The impact of position could not be ascertained in this
systematic review.
It is customary to administer an uterotonic drug during
the active management of the third stage; some trials included this
component in either or both arms. The relative impact of this also cannot
be established through this systematic review. Most trials included
vaginal deliveries; some included Caesarean section deliveries as well.
The relative differences (if any) between the two modes of delivery could
not be explored in this review.
Conflict of maternal and neonatal interest: The
current standard of care is to manage the third stage of labor actively
(rather than expectantly) [43]; hence DCC is not the preferred method from
the Obstetricians’ perspective. However, many Units are shifting to a
policy of DCC in term deliveries, expecting benefit for infants. Waiting
for DCC in a stable baby (not requiring resuscitation) does not pose a
problem from the pediatricians’ viewpoint. However, since DCC has limited
clinical benefits in term babies, this could create an apparent ‘conflict’
between maternal and neonatal interest, which can be resolved through
joint appraisal and application of current best evidence. Unfortunately,
none of the trials examined preferences of (maternal and neonatal)
personnel in the delivery team.
Extendibility
Most of the trials among term deliveries were conducted
in developing country populations, including two from India. However, all
were conducted in settings with facilities for management of potential
adverse maternal and neonatal consequences at the point-of-care; these
facilities are consistent with services at level II (and above) neonatal
care facilities. Limitations of manpower and/or material resources across
various delivery settings could preclude application of the evidence in
this systematic review.
Conflict of interest: None stated; Funding:
None.
|
EURECA Conclusions in the Indian Context
• For infants delivered at term, delayed cord
clamping results in very limited clinically significant, short and
long-term benefits; it neither increases maternal complications nor
provides maternal benefit.
• Among preterm deliveries, delayed cord clamping
results in significantly reduced risk of intraventricular hemorrhage
and marginal hemodynamic benefits in neonates. The risks and
benefits for mothers are not known.
|
References
1. Prendiville WJ, Harding JE, Elbourne DR, Stirrat GM.
The Bristol third stage trial: active versus physiological management of
third stage of labour. BMJ. 1988;297:1295-1300.
2. Brune T, Garritsen H, Witteler R, Schlake A,
Wüllenweber J, Louwen F, et al. Autologous placental blood transfusion for
the therapy of anemic neonates. Biol Neonat. 2002;81:236-43.
3. Hudson IRB, Holland BM, Jones JG, Turner TL, Wardrop
CAJ. First day total circulating red cell volume (RCV) predicts outcome in
preterm infants. Pediatr Res. 1990;27:209A.
4. Linderkamp O, Versmold HT, Fendel H, Reigel KP,
Betke K. Association of neonatal respiratory distress with birth asphyxia
and deficiency of red cell mass in premature infants. Eur J Pediatr.
1978;129:167-73
5. Inch S. Management of the third stage of labour:
another cascade of intervention? Midwifery. 1985;1:114-22.
6. WHO. Department of Making Pregnancy Safer. WHO
recommendations for the prevention of postpartum haemorrhage. Geneva: WHO,
2007.
7. McDonald SJ, Middleton P. Effect of timing of
umbilical cord clamping of term infants on maternal and neonatal outcomes.
Cochrane Database Syst Rev. 2008;2:CD004074.
8. Rabe H, Reynolds GJ, Diaz-Rosello JL. Early versus
delayed umbilical cord clamping in preterm infants. Cochrane Database Syst
Rev. 2004;4:CD003248.
9. van Rheenen P, 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 Pediatr. 2004;24:3-16.
10. Hutton E K, Hassan E S. Late vs early clamping of
the umbilical cord in full-term neonates: systematic review and
meta-analysis of controlled trials. JAMA. 2007;297:1241-52
11. Lainez VB, Bergel AE, Cafferata TML, Belizan CJ M.
Early or late umbilical cord clamping: a systematic review of the
literature. Anales de Pediatria. 2005;63:14-21.
12. Rabe H, Reynolds G, Diaz-Rossello J. A systematic
review and meta-analysis of a brief delay in clamping the umbilical cord
of preterm infants. Neonatology. 2008;93:138-44.
13. Ceriani Cernadas JM, Carroli G, Pellegrini L, Otaño
L, Ferreira M, Ricci C, 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:e779-86.
14. Ceriani Cernadas JM, Carroli G, Pellegrini L,
Ferreira M, Ricci C, Casas O, et al. The effect of early and
delayed umbilical cord clamping on ferritin levels in term infants at six
months of life: a randomized, controlled trial. Arch Argent Pediatr.
2010;108:201-8.
15. Chaparro CM, Neufeld LM, Tena Alavez G, Eguia-Líz
Cedillo R, Dewey KG. Effect of timing of umbilical cord clamping on iron
status in Mexican infants: a randomised controlled trial. Lancet.
2006;367:1997-2004.
16. Emhamed MO, van Rheenen P, Brabin BJ. The early
effects of delayed cord clamping in term infants born to Libyan mothers.
Trop Doct. 2004;34:218-22.
17. Geethanath RM, Ramji S, Thirupuram S, Rao YN.
Effect of timing of cord clamping on the iron status of infants at 3
months. Indian Pediatr. 1997;34 103-6.
18. Grajeda R, Pérez-Escamilla R, Dewey KG. Delayed
clamping of the umbilical cord improves hematologic status of Guatemalan
infants at 2 mo of age. Am J Clin Nutr. 1997;65:425-31.
19. Gupta R, Ramji S. Effect of delayed cord clamping
on iron stores in infants born to anemic mothers: a randomized controlled
trial. Indian Pediatr. 2002;39:130-5.
20. Jahazi A, Kordi M, Mirbehbahani NB, Mazloom SR. The
effect of early and late umbilical cord clamping on neonatal hematocrit. J
Perinatol. 2008;28: 23-5.
21. Jaleel R, Deeba F, Khan A. Timing of umbilical cord
clamping and neonatal haematological status. J Pakistan Med Assoc.
2009;59:468-70.
22. Linderkamp O, Nelle M, Kraus M, Zilow EP. The
effect of early and late cord-clamping on blood viscosity and other
hemorheological parameters in full-term neonates. Acta Paediatrica.
1992;81:745-50.
23. McDonald S. Timing of interventions in the third
stage of labour. International Confederation of Midwives 24th Triennial
Congress; 1996 May 26-31; Oslo, Norway. 1996:143.
24. No authors listed. A study of the relationship
between the delivery to cord clamping interval and the time of cord
separation. Oxford Midwives Research Group. Midwifery. 1991;7:167-76.
25. Saigal S, O’Neill A, Surainder Y, Chua LB, Usher R.
Placental transfusion and hyperbilirubinemia in the premature. Pediatrics.
1972;49:406-19.
26. van Rheenen P, de Moor L, Eschbach S, de Grooth H,
Brabin B. Delayed cord clamping and haemoglobin levels in infancy: a
randomised controlled trial in term babies. Trop Med Int Health.
2007;12:603-16.
27. Andersson O, Hellstrom-Westas L, Andersson D,
Domellof M. Early Versus Late Cord Clamping: Neonatal Outcomes and Iron
Status at 4 Months in Swedish Infants. Pediatric Academic Society 2010
abstracts. Accessed from URL: http://www.abstracts2view.com/pas/ on 29
december 2010.
28. Aladangady N, McHugh S, Aitchison TC, Wardrop CA,
Holland BM. Infants’ blood volume in a controlled trial of placental
transfusion at preterm delivery. Pediatrics. 2006;117:93-8.
29. 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.
30. Hofmeyr GJ, Bolton KD, Bowen DC, Govan JJ.
Periventricular/intraventricular haemorrhage and umbilical cord clamping.
Findings and hypothesis. S Afr Med J. 1988;73:104-6.
31. Kugelman A, Borenstein-Levin L, Riskin A,
Chistyakov I, Ohel G, Gonen R, et al. Immediate versus delayed umbilical
cord clamping in premature neonates born < 35 weeks: a prospective,
randomized, controlled study. Am J Perinatol. 2007;24:307-15.
32. Kugelman A, Borenstein-Levin L, Kessel A, Riskin A,
Toubi E, Bader D. Immunologic and infectious consequences of immediate
versus delayed umbilical cord clamping in premature infants: a
prospective, randomized, controlled study. J Perinat Med. 2009;37:281-7.
33. McDonnell M, Henderson-Smart DJ. Delayed umbilical
cord clamping in preterm infants: a feasibility study. J Paediatr Child
Health. 1997;33:308-10.
34. Mercer JS, McGrath MM, Hensman A, Silver H, Oh W.
Immediate and delayed cord clamping in infants born between 24 and 32
weeks: a pilot randomized controlled trial. J Perinatol. 2003;23:466-72.
35. Mercer JS, Vohr BR, McGrath MM, Padbury JF, Wallach
M, 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;117:1235-42.
36. Mercer JS, Vohr BR, Erickson-Owens DA, Padbury JF,
Oh W. Seven-month developmental outcomes of very low birth weight infants
enrolled in a randomized controlled trial of delayed versus immediate cord
clamping. J Perinatol. 2010;30:11-6.
37. Oh W, Carlo WA, Fanaroff AA, McDonald S, Donovan EF,
Poole K, et al. Delayed cord clamping in extremely low birthweight infants
- a pilot randomized controlled trial. Pediatr Res. 2002;5Suppl4:365-6.
38. Rabe H, Wacker A, Hülskamp G, Hörnig-Franz I,
Schulze-Everding A, Harms E, et al. A randomised controlled trial
of delayed cord clamping in very low birth weight preterm infants. Eur J
Pediatr. 2000;159:775-7.
39. Strauss RG, Mock DM, Johnson KJ, Cress GA,
Burmeister LF, Zimmerman MB, et al. A randomized clinical trial comparing
immediate versus delayed clamping of the umbilical cord in preterm
infants: short-term clinical and laboratory endpoints. Transfusion.
2008;48:658-65.
40. Strauss RG, Mock DM. A randomized clinical trial
comparing immediate vs delayed clamping of the umbilical cord In
preterm infants. Transfusion. 2007;47:21A.
41. Ultee CA, van der Deure J, Swart J, Lasham C, 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: F20-3.
42. Airey RJ, Farrar D, Duley L. Alternative positions
for the baby at birth before clamping the umbilical cord. Cochrane
Database Syst Rev. 2010;10:CD007555.
43. Prendiville WJ, Elbourne D, McDonald S. Active
versus expectant management in the third stage of labour. Cochrane
Database Syst Rev. 2009;3:CD000007.
|
