Introduction: Placental transfusion strategies in preterm newborns have not been evaluated in low- and middle-income countries (LMICs). The objective of this systematic review was to compare placental transfusion strategies in preterm newborns in LMICs, including delayed cord clamping (DCC) for various time intervals, DCC until cord pulsations stop, umbilical cord milking, and immediate cord clamping (ICC). Methods: Medline, Embase, CINAHL, and CENTRAL were searched from inception. Observational studies and randomized controlled trials (RCTs) were included. Two authors independently extracted data for Bayesian random-effects network meta-analysis (NMA) if more than 3 interventions reported an outcome or a pairwise meta-analysis was utilized. Results: Among newborns <34 weeks of gestation, NMA of 9 RCTs could not rule out benefit or harm for survival from DCC 30–60 s compared to ICC: relative risk (RR) (95% credible interval) 0.96 (0.78–1.12), moderate certainty, or any included strategy compared to each other (low to very low certainty). Among late preterm newborns, DCC 120 s might be associated with improved survival: RR (95% confidence interval) 1.11 (1.01–1.22), very low certainty. We could not detect differences in the risk of intraventricular hemorrhage grade > II and bronchopulmonary dysplasia for any included intervention (low to very low certainty). DCC 60 s and 120 s might improve the hematocrit level among all preterm newborns (very low certainty), and DCC 45 s may decrease the risk of receipt of inotropes among newborns <34 weeks of gestation (low certainty). Conclusions: In LMICs, DCC for 60 s and 120 s might improve hematocrit level in preterm newborns, and DCC for 45 s may decrease the risk of receipt of inotropes in newborns <34 weeks, with no conclusive effect on survival.

1.
Wyckoff
MH
,
Wyllie
J
,
Aziz
K
,
de Almeida
MF
,
Fabres
JW
,
Fawke
J
,
.
Neonatal life support 2020 international consensus on cardiopulmonary resuscitation and emergency cardiovascular care science with treatment recommendations
.
Resuscitation
.
2020
;
156
:
A156
87
.
2.
WHO
.
Guideline: delayed umbilical cord clamping for improved maternal and infant health and nutrition outcomes
.
Geneva
:
World Health Organization
;
2014
. Accessed 1st August 2022.
3.
Aziz
K
,
Lee
HC
,
Escobedo
MB
,
Hoover
AV
,
Kamath-Rayne
BD
,
Kapadia
VS
,
.
Part 5: neonatal resuscitation: 2020 American heart association guidelines for cardiopulmonary resuscitation and emergency cardiovascular care
.
Circulation
.
2020
;
142
(
16_Suppl l_2
):
S524
50
.
4.
Madar
J
,
Roehr
CC
,
Ainsworth
S
,
Ersdal
H
,
Morley
C
,
Rüdiger
M
,
.
European resuscitation council guidelines 2021: newborn resuscitation and support of transition of infants at birth
.
Resuscitation
.
2021
;
161
:
291
326
.
5.
Rabe
H
,
Gyte
GM
,
Díaz-Rossello
JL
,
Duley
L
.
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
.
2019
;
9
(
9
):
CD003248
.
6.
Seidler
AL
,
Gyte
GML
,
Rabe
H
,
Díaz-Rossello
JL
,
Duley
L
,
Aziz
K
,
.
Umbilical cord management for newborns <34 Weeks’ gestation: a meta-analysis
.
Pediatrics
.
2021
;
147
(
3
):
e20200576
.
7.
Gomersall
J
,
Berber
S
,
Middleton
P
,
McDonald
SJ
,
Niermeyer
S
,
El-Naggar
W
,
.
Umbilical cord management at term and late preterm birth: a meta-analysis
.
Pediatrics
.
2021
;
147
(
3
):
e2020015404
.
8.
Jasani
B
,
Torgalkar
R
,
Ye
XY
,
Syed
S
,
Shah
PS
.
Association of umbilical cord management strategies with outcomes of preterm infants: a systematic review and network meta-analysis
.
JAMA Pediatr
.
2021
;
175
(
4
):
e210102
.
9.
WHO
,
March of Dimes, PMNCH, Save the Children. 15 million preterm births: Priorities for action based on national, regional and global estimates
. In:
Howson
CP
,
Kinney
MV
,
Lawn
J
, editors.
Born too soon: the global action report on preterm birth
.
2012
. Accessed 1st July 2022.
10.
Thayyil
S
,
Pant
S
,
Montaldo
P
,
Shukla
D
,
Oliveira
V
,
Ivain
P
,
.
Hypothermia for moderate or severe neonatal encephalopathy in low-income and middle-income countries (HELIX): a randomised controlled trial in India, Sri Lanka, and Bangladesh
.
Lancet Glob Health
.
2021
;
9
(
9
):
e1273
85
. Erratum in: Lancet Glob Health. 2021;9(10):e1371.
11.
Tapas Bandyopadhyay, Viraraghavan Ramaswamy, Thangaraj Abiramalatha, Vandana Hegde, Gary M. Weiner, Daniele Trevisanuto. Placental transfusion strategies in low- and middle- income countries: A systematic review and meta-analysis. PROSPERO 2021 CRD42021268615 Available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42021268615. Accessed 10th July 2022.
12.
Hutton
B
,
Salanti
G
,
Caldwell
DM
,
Chaimani
A
,
Schmid
CH
,
Cameron
C
,
.
The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations
.
Ann Intern Med
.
2015
;
162
(
11
):
777
84
.
13.
Ouzzani
M
,
Hammady
H
,
Fedorowicz
Z
,
Elmagarmid
A
.
Rayyan: a web and mobile app for systematic reviews
.
Syst Rev
.
2016
;
5
(
1
):
210
.
14.
15.
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 X
.
1978
;
92
(
4
):
529
34
.
16.
Strand
ML
,
Simon
WM
,
Wyllie
J
,
Wyckoff
MH
,
Weiner
G
.
Consensus outcome rating for international neonatal resuscitation guidelines
.
Arch Dis Child Fetal Neonatal Ed
.
2020
;
105
(
3
):
328
30
.
17.
Bell
MJ
,
Ternberg
JL
,
Feigin
RD
,
Keating
JP
,
Marshall
R
,
Barton
L
,
.
Neonatal necrotizing enterocolitis: therapeutic decisions based upon clinical staging
.
Ann Surg
.
1978
;
187
(
1
):
1
7
.
18.
Sterne
JAC
,
Savović
J
,
Page
MJ
,
Elbers
RG
,
Blencowe
NS
,
Boutron
I
,
.
RoB 2: a revised tool for assessing risk of bias in randomised trials
.
BMJ
.
2019
;
366
:
l4898
.
19.
Sterne
JA
,
Hernán
MA
,
Reeves
BC
,
Savović
J
,
Berkman
ND
,
Viswanathan
M
,
.
ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions
.
BMJ
.
2016
;
355
:
i4919
.
20.
Guyatt
GH
,
Oxman
AD
,
Schünemann
HJ
,
Tugwell
P
,
Knottnerus
A
.
GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology
.
J Clin Epidemiol
.
2011
;
64
(
4
):
380
2
.
21.
Puhan
MA
,
Schünemann
HJ
,
Murad
MH
,
Li
T
,
Brignardello-Petersen
R
,
Singh
JA
,
, .
A GRADE Working Group approach for rating the quality of treatment effect estimates from network meta-analysis
.
BMJ
.
2014
;
349
(
sep24 5
):
g5630
.
22.
R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed August 7, 2020.
23.
Salanti
G
,
Ades
AE
,
Ioannidis
JP
.
Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial
.
J Clin Epidemiol
.
2011
;
64
(
2
):
163
71
.
24.
Bahar
N
,
Satar
M
,
Yılmaz
M
,
Büyükkurt
S
,
Özlü
F
,
Yapicioglu Yildizdas
H
.
The effects of umblical cord clamping time on lymphocyte subgroups in term and late preterm infants
.
Turk Pediatri Ars
.
2019
;
53
(
4
):
214
21
.
25.
Das
B
,
Sundaram
V
,
Kumar
P
,
Mordi
WT
,
Dhaliwal
LK
,
Das
R
.
Effect of placental transfusion on iron stores in moderately preterm neonates of 30-33 weeks gestation
.
Indian J Pediatr
.
2018
;
85
(
3
):
172
8
.
26.
Digal
KC
,
Singh
P
,
Srivastava
Y
,
Chaturvedi
J
,
Tyagi
AK
,
Basu
S
.
Effects of delayed cord clamping in intrauterine growth-restricted neonates: a randomized controlled trial
.
Eur J Pediatr
.
2021
;
180
(
6
):
1701
10
.
27.
Dipak
NK
,
Nanavati
RN
,
Kabra
NK
,
Srinivasan
A
,
Ananthan
A
.
Effect of delayed cord clamping on hematocrit, and thermal and hemodynamic stability in preterm neonates: a randomized controlled trial
.
Indian Pediatr
.
2017
;
54
(
2
):
112
5
.
28.
Dong
XY
,
Sun
XF
,
Li
MM
,
Yu
ZB
,
Han
SP
.
[Influence of delayed cord clamping on preterm infants with a gestational age of <32 weeks]
.
Zhongguo Dang Dai Er Ke Za Zhi
.
2016
;
18
(
7
):
635
8
.
29.
Fang
G
,
Jinqiu
Z
,
Weizhen
L
.
Contribution of different umbilical cord ligation methods to neonatal complications in preterm babies
.
J Shanghai Jiaotong University
.
2014
;
38
(
10
):
1197
202
.
30.
Gokmen
Z
,
Ozkiraz
S
,
Tarcan
A
,
Kozanoglu
I
,
Ozcimen
EE
,
Ozbek
N
.
Effects of delayed umbilical cord clamping on peripheral blood hematopoietic stem cells in premature neonates
.
J Perinat Med
.
2011
;
39
(
3
):
323
9
.
31.
Hemmati
F
,
Sharma
D
,
Namavar Jahromi
B
,
Salarian
L
,
Farahbakhsh
N
.
Delayed cord clamping for prevention of intraventricular hemorrhage in preterm neonates: a randomized control trial
.
J Matern Fetal Neonatal Med
.
2020
;
22
:
1
7
.
32.
Hofmeyr
GJ
,
Bolton
KD
,
Bowen
DC
,
Govan
JJ
.
Periventricular/intraventricular haemorrhage and umbilical cord clamping. Findings and hypothesis
.
S Afr Med J
.
1988
;
73
(
2
):
104
6
.
33.
Hofmeyr
GJ
,
Gobetz
L
,
Bex
PJ
,
Van der Griendt
M
,
Nikodem
C
,
Skapinker
R
,
.
Periventricular/intraventricular hemorrhage following early and delayed umbilical cord clamping: a randomized controlled trial
.
Online J Curr Clin Trials
.
1993
;
Doc No 110
:
[2002 words; 26 paragraphs]
.
34.
Malik
AU
,
Shahnawaz
K
,
Riaz
A
.
Comparison between the efficacy of early and delayed umbilical cord clamping in preterm infants
.
PJMHS
.
2013
;
7
(
4
):
992
5
.
35.
Niu
F
,
Wang
Y
,
Ren
X
.
Effect of umbilical cord milking and delayed cord clamping on mean blood pressure, cerebral blood flow and neurological assessment score in preterm infants
.
Jilin Medicine
.
2016
;
37
(
12
):
2900
2
.
36.
Rana
A
,
Agarwal
K
,
Ramji
S
,
Gandhi
G
,
Sahu
L
.
Safety of delayed umbilical cord clamping in preterm neonates of less than 34 weeks of gestation: a randomized controlled trial
.
Obstet Gynecol Sci
.
2018
;
61
(
6
):
655
61
.
37.
Ranjit
T
,
Nesargi
S
,
Rao
PNS
,
Sahoo
JP
,
Ashok
C
,
Chandrakala
BS
.
Effect of early versus delayed cord clamping on hematological status of preterm infants at 6 wk of age
.
Indian J Pediatr
.
2015
;
82
(
1
):
29
34
.
38.
Ruangkit
C
,
Bumrungphuet
S
,
Panburana
P
,
Khositseth
A
,
Nuntnarumit
P
.
A randomized controlled trial of immediate versus delayed umbilical cord clamping in multiple-birth infants born preterm
.
Neonatology
.
2019
;
115
(
2
):
156
63
.
39.
Sahoo
T
,
Thukral
A
,
Sankar
MJ
,
Gupta
SK
,
Agarwal
R
,
Deorari
AK
,
.
Delayed cord clamping in Rh-alloimmunised infants: a randomised controlled trial
.
Eur J Pediatr
.
2020
;
179
(
6
):
881
9
.
40.
Salae
R
,
Tanprasertkul
C
,
Somprasit
C
,
Bhamarapravatana
K
,
Suwannarurk
K
.
Efficacy of delayed versus immediate cord clamping in late preterm newborns following normal labor: a randomized control trial
.
J Med Assoc Thai
.
2016
;
99
(
Suppl 4
):
S159
65
.
41.
Shi
W
,
Peng
J
,
Chen
N
.
Effect of delayed cord clamping on outcome of delivery
.
Henan J Preventive Med
.
2017
;
28
:
85
7
.
42.
Sura
M
,
Osoti
A
,
Gachuno
O
,
Musoke
R
,
Kagema
F
,
Gwako
G
,
.
Effect of umbilical cord milking versus delayed cord clamping on preterm neonates in Kenya: a randomized controlled trial
.
PLoS One
.
2021
;
16
(
1
):
e0246109
.
43.
Varij Kazemi
M
,
Akbarianrad
Z
,
Zahedpasha
Y
,
Mehraein
R
,
Haghshenas Mojaveri
M
.
Effects of delayed cord clamping on intraventricular hemorrhage in preterm infants
.
Iran J Pediatr
.
2017
;
27
(
5
):
e6570
.
44.
Wong
L
,
Feng
L
,
Mirror
LM
.
Effect of delayed umbilical cord ligation on premature infants
.
Chinese Med Innovation
.
2018
;
15
(
25
):
120
2
.
45.
Yunis
M
,
Nour
I
,
Gibreel
A
,
Darwish
M
,
Sarhan
M
,
Shouman
B
,
.
Effect of delayed cord clamping on stem cell transfusion and hematological parameters in preterm infants with placental insufficiency: a pilot randomized trial
.
Eur J Pediatr
.
2021
;
180
(
1
):
157
66
.
46.
Zhang
L
,
Zhang
Y
,
ZhangW
.
Influence of delayed cord clamping on the outcome of moderate and late preterm infants
.
Chinese J Child Health Care
.
2018
;
26
(
8
):
843
53
.
47.
Zheng
Z
,
Zhang
J
,
Zhang
R
.
Effect of delayed umbilical cord ligation on the clinical outcome of premature infants born by eutocia
.
Clinical Medicine
.
2019
;
39
(
2
):
1
5
.
48.
Zhou
C
,
Fan
X
,
Li
L
.
Effect of different cord clamping methods on circulatory system in preterm infants with a gestational age less than 32 weeks
.
J Nursing Sci
.
2018
;
33
(
2
):
5
8
.
49.
Zhu
C
,
Gu
C
,
Wang
X
.
Effects of different umbilical cord clamping times for preterm infants on maternal and infant outcomes
.
J Nursing Sci
.
2020
;
35
(
7
):
34
6
.
50.
Zhulian
N
,
Chuande
L
,
Li
L
.
Influence of delayed umbilical cord clamping on hemoglobin level of preterm infants after birth
.
Chinese j practical med
.
2020
;
47
(
3
):
19
21
.
51.
Panda
S
,
Mishra
NR
,
Shukla
P
,
Nayak
BK
.
Early versus delayed cord clamping among preterms: a cohort study
.
Perinatology
.
2020
;
21
(
2
):
50
6
.
52.
Vadakkencherry Ramaswamy
V
,
Abiramalatha
T
,
Weiner
GM
,
Trevisanuto
D
.
A comparative evaluation and appraisal of 2020 American Heart Association and 2021 European Resuscitation Council neonatal resuscitation guidelines
.
Resuscitation
.
2021
;
167
:
151
9
.
53.
Sun
J
,
Wu
H
,
Zhao
M
,
Magnussen
CG
,
Xi
B
.
Prevalence and changes of anemia among young children and women in 47 low- and middle-income countries, 2000–2018
.
EClinicalMedicine
.
2021
;
1741
:
101136
.
54.
Lozoff
B
,
Georgieff
MK
.
Iron deficiency and brain development
.
Semin Pediatr Neurol
.
2006
;
13
(
3
):
158
65
.
55.
Ramaswamy
VV
,
Abiramalatha
T
,
Bandyopadhyay
T
,
Shaik
NB
,
Bandiya
P
,
Nanda
D
,
.
ELBW and ELGAN outcomes in developing nations-systematic review and meta-analysis
.
PLoS One
.
2021
;
16
(
8
):
e0255352
.
You do not currently have access to this content.