CONTEXT:

The International Liaison Committee on Resuscitation prioritized scientific review of umbilical cord management at term and late preterm birth.

OBJECTIVE:

To assess effects of umbilical cord management strategies (clamping timing and cord milking) in infants ≥34 weeks’ gestational age.

DATA SOURCES:

Cochrane Central Register of Controlled Trials, Medline, PubMed, Embase, Cumulative Index to Nursing and Allied Health Literature, and trial registries searched July 2019.

STUDY SELECTION:

Two authors independently assessed eligibility of randomized controlled trials.

DATA EXTRACTION:

Two authors independently extracted data and assessed evidence certainty (Grading of Recommendations Assessment, Development and Evaluations).

RESULTS:

We identified 46 studies (9159 women and their infants) investigating 7 comparisons. Compared with early cord clamping (ECC) <30 seconds, delayed cord clamping (DCC) ≥30 seconds (33 studies), intact-cord milking (1 study), and cut-cord milking (2 studies) probably improve hematologic measures but may not affect survival without neurodisability, anemia in early infancy, or maternal postpartum hemorrhage. No differences in major neonatal morbidities are seen in studies comparing methods of optimizing placental transfusion (DCC versus cut-cord milking [3 studies], longer delays in clamping [7 studies], or physiologic parameters [3 studies]). Strategies that promote increased placental transfusion may be associated with greater phototherapy use. Evidence for all outcomes was low or very low certainty.

LIMITATIONS:

Incompleteness and low certainty of findings limit applicability.

CONCLUSIONS:

Compared with ECC, DCC or cord milking increases hemoglobin and hematocrit immediately after birth in infants ≥34 weeks’ gestational age. The uncertain effects of DCC and cord milking compared with ECC on major morbidities limit usefulness of available evidence for policy and practice.

Umbilical cord management affects each of the 130 million infants born in the world every year. Cord management impacts not only the volume of placental transfusion but also the critical cardiovascular transition around the onset of breathing and/or ventilation.1,2 

In hopes of optimizing placental transfusion, a variety of techniques of cord management have been assessed, including immediate cord clamping, timed deferral or delay of cord clamping, clamping based on physiologic transition (such as cessation of cord pulsation or onset of respiration), and cord milking or stripping.

Cord management practices that facilitate optimal placental transfusion and support initial cardiorespiratory transition may have a significant impact on reducing deaths and mitigating other adverse outcomes related to birth asphyxia and hypoxic ischemic encephalopathy.

However, most late preterm and term infants, representing >90% of live births, will not require resuscitation. In this population, the major role of cord management may be to maximize the volume of placental transfusion to the infant and prevent the development of iron deficiency anemia, which is associated with impaired motor development, behavioral problems, and cognitive delays.35  In low- and middle-income countries, this may be of great importance where the prevalence of iron deficiency anemia has been reported to be as high as 33%.6 

Cord management strategies at birth may impact postpartum hemorrhage (PPH), which occurs in ∼2% of women giving birth.7  Antepartum hemorrhage is the leading cause of maternal mortality in most low-resource countries (approximately one-quarter of all maternal deaths globally) and is a significant cause of maternal morbidity and long-term disability.7  Guidance on proper management of the cord is important to ensure that women giving birth are not exposed to additional risk for PPH.

The 2015 International Liaison Committee on Resuscitation (ILCOR) statement identified many knowledge gaps in cord management at birth in a variety of neonatal populations.8  Since the latest ILCOR recommendations in 2015, a number of studies in which authors address delayed cord clamping (DCC) in term and late preterm infants have been published. Recommendations need to be reviewed and updated where appropriate.

In this review, we followed methodology outlined in the Cochrane Handbook for Systematic Reviews of Interventions and adhere to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) reporting guidelines.9,10  The protocol was registered prospectively with the International Prospective Register of Systematic Reviews (CRD42020155498). Methods are detailed in the Supplemental Information and summarized below.

We considered all randomized controlled trials (RCTs) comparing different policies and procedures regarding umbilical cord management in late preterm infants (34+0–36+6 weeks’ gestational age) and term infants (≥37+0 weeks’ gestational age). Multiple gestations were included.

Studies in which authors compare the following broad interventions were included (Supplemental Table 3):

  1. early cord clamping (ECC), defined as clamping the umbilical cord <30 seconds after birth, without cord milking;

  2. later or delayed cord clamping (DCC), defined as clamping the umbilical cord ≥30 seconds after birth or based on physiologic parameters (such as when cord pulsation has ceased or breathing has been initiated), without cord milking;

  3. intact-cord milking (ICM) (also referred to as “intact-cord stripping”), defined as repeated compression of the cord from the placental side toward the infant with the connection to the placenta intact at any time point within the first few minutes after birth; and

  4. cut-cord milking (CCM) (also referred to as “cut-cord stripping”), defined as drainage of the cord by compression from the cut end toward the infant after clamping and cutting a long segment.

The 8 specific comparisons of these various cord management techniques we attempted to assess are detailed in the Supplemental Information (Supplemental Table 3).

The review outcomes were selected in consultation with representatives from the World Health Organization (WHO) and ILCOR Neonatal Life Support Task Force. These outcomes were considered clinically relevant and therefore likely to influence clinical practice. Primary outcomes are survival without neurodisability, anemia in early infancy, and maternal PPH. Methods including outcome definitions, prespecified subgroup analyses, information sources, search strategy, study selection, data extraction, and evaluation of the risk of bias and certainty of evidence assessments are detailed in the Supplemental Information.

Overall, we identified 46 studies involving a total of 9159 women and their late preterm or term infants, of which 44 studies (including 8899 women and their late preterm or term infants) had data that could be included in the meta-analysis (Fig 1, Supplemental Information). In most studies, authors compared DCC ≥30 seconds with ECC (n = 33). In 7 studies, authors assessed different DCC times (≥60 vs <60 seconds); few or no studies were included in the remaining 6 prespecified comparisons (Fig 2).

FIGURE 1

PRISMA study flow diagram.

FIGURE 1

PRISMA study flow diagram.

Close modal
FIGURE 2

Comparison of umbilical cord management interventions. Comparisons of 8 umbilical interventions were proposed for this review, for which 7 comparisons included studies.

FIGURE 2

Comparison of umbilical cord management interventions. Comparisons of 8 umbilical interventions were proposed for this review, for which 7 comparisons included studies.

Close modal

Study and participant characteristics for included studies are outlined in Table 1 and Supplemental Table 4. The number of mother-infant pairs in the studies ranged from 30 (Backes et al11 ) to 755 (Kc et al12 ), with most (n = 32) performed in low- or middle-income countries.13  Thirty studies included only term infants and 2 studies included only late preterm infants (Salae et al14  and Ultee et al15 ). Most studies (n = 37) included singletons only.

TABLE 1

Participant Characteristics

StudyInterventionGestational Age, Mean (SD), wkBirth wt, Mean (SD), gCesarean Delivery, %Comparison
Al-Tawil et al33  2012 DCC 38.5 (1.1) 3348 (540.8) C1 
 ECC 38.2 (1.4) 3110 (390.8)  
Alzaree et al19  2018 DCC 38.9 (0.96) NR NR C4 
 Intact UCM 38.9 (0.90) NR NR  
Andersson et al31  2011 DCC 40.0 (11) 3629 (460) C1 
 ECC 40.1 (1.1) 3533 (486) 0.5  
Andersson et al23  2019 DCC later 39.6 (1.4) 3072 (401) C7 
 DCC earlier 39.6 (1.4) 3036 (372)  
Backes et al11  2015 DCC 39.2 (1.6) 3300 (700) NR C1 
 ECC 38.3 (1.4) 3400 (1200) NR  
Cavallin et al34  2019 DCC Median (IQR): 39 (39; 39) 3273 (372) 100 C1 
 ECC Median (IQR): 39 (39; 39) 3395 (571) 100  
Ceriani Cernadas et al35  2006 DCC (60 s) 39.1 (1.2) 3424 (382) 30 C1 
 DCC (180 s) 39.3 (1.1) 3420 (360) 28.3  
 ECC 39.3 (1.4) 3390 (395) 28.3  
Chaparro et al36  2006 DCC 38·8 (1.1) 3182 (369) C1 
 ECC 39·0 (1.1) 3196 (362)  
Chen et al24  2018a DCC (60 s) 40 (1) 3363 (398) C1 and C8 
 DCC (90 s) 40 (1) 3328 (314)  
 DCC (120 s) 40 (1) 3380 (456)  
 DCC (150 s) 40 (1) 3326 (324)  
 DCC (180 s) 40 (1) 3326 (320)  
 ECC (immediate) 40 (1) 3333 (90)  
 ECC (30 s) 40 (1) 3387 (399)  
 DCC physiologic 40 (1) 3340 (372)  
Chopra et al37  2018 DCC 37.4 (1.5) 2188 (334) 78.2 C1 
 ECC 37.7 (1.5) 2202 (389) 67.3  
Datta et al38  2017 DCC 35.6 (1) 2166 (429) 29.3 C1 
 ECC 35.4 (1) 2107 (463) 44.1  
De Paco et al39  2011 DCC 39.2 (0.9) 3220 (362.3) C1 
 ECC 39.6 (1.1) 3251 (406.5  
De Paco et al40  2016 DCC 39.5 (1.2) 3293 (422) NR C1 
 ECC 39.6 (1.1) 3181 (422) NR  
Emhamed et al41  2004 DCC NR 3390 (421) NR C1 
 ECC NR 3428 (424) NR  
Erickson-Owens et al17  2012 Intact UCM 39.2 (0.3) 3662(240) 100 C2 
 ECC 39.1 (0.1) 3524 (504) 100  
Fawzy et al42  2015 DCC Range: 38–41 Range: 3300–4000 NR C1 
 ECC Range: 37–40 Range: 3000–4500 NR  
Geethanath et al43  1997 DCC NR NR NR C1 
 ECC NR NR NR  
Grajeda et al44  1997 DCC (at placenta) 38.8 (0.9) 3200 (500) NR C1 
 DCC (below placenta) 38.4 (1.2) 3200 (500) NR  
 ECC 38.5 (1.2) 3000 (400) NR  
Gupta et al45  2002 DCC 39.1 (1.2) 2743 (407.8) NR C1 
 ECC 39.4 (1.1) 2707 (417) NR  
Ishaq et al46  2016b DCC (later) 37.5 (0.7) NR NR C7 
 DCC (earlier) 37.5 (0.7) NR NR  
Jahazi et al47  2008 DCC 39.6 (1.2) 3272 (329) NR C1 
 ECC 39.3 (0.9) 3008 (573) NR  
Jaiswal et al20  2015 DCC 38.7 (0.9) 2751 (390) 40 C5 
 DCC with UCM 38.6 (0.81) 2760 (300) 43  
Jaleel et al49  2009 DCC 38.7 (1.2) 3150 (550) 26 C1 
 ECC 38.4 (1.3) 3060 (390) 21  
Katheria et al48  2017 DCC (later) 39 (1) 3440 (523) C7 
 DCC (earlier) 39 (1) 3204 (302)  
Kc et al51  2017 DCC (later) 39.3 (1.1) 3029 (405) NR C7 
 DCC (earlier) 39.0 (1.2) 3015 (426) NR  
Kc et al12  2019 DCC (later) 39.4 (1.3) 3011 (382) NR C7 
 DCC (earlier) 39.4 (1.3) 3072 (399) NR  
Krishnan et al50  2015 DCC 38.5 (1.2) 2962 (372) C1 
 ECC 38.2 (2.1) 3008 (573)  
Mercer et al52  2017 DCC 39.5 (1) 3584 (497) 22 C1 
 ECC 39.4 (1) 3433 (454) 31  
Mohammad et al53  2019 DCC NR NR NR C1 
 ECC NR NR NR  
Nelson et al25  1980 DCC (time approach) 40.3 (1.3) 3489 (453) NR C8 
 Physiologic approach DCC 40.5 (1.3) 3437 (439) NR  
Nesheli et al54  2015b DCC NR NR C1 
 ECC NR NR  
Nouraie et al55  2019 DCC (later) 38.7 (0.9) 3204 (302) NR C7 
 DCC (earlier) 38.6 (0.8) 3259 (362) NR  
Oxford Midwives Research Group56  1991 DCC 39.9 (1.2) 3431 (445) NR C1 
 ECC 40.0 (1.1) 3406 (440) NR  
Philip57  1973 DCC NR 3590 (452) NR C1 
 ECC NR 3543 (534) NR  
Saigal et al58  1972 DCC (30 s) Mean (range): 40.2 (38–43) Mean (range): 3463 (2740–4120) C1 
 DCC (60 s) Mean (range): 40 (38–41) Mean (range): 3380 (2750–4350) — 
 ECC (immediate) Mean (range): 40.2 (38–43) Mean (range): 3521 (2685–4040)  
Salae et al14  2016 DCC 35.7 (1.0) 2528 (239) C1 
 ECC 36.0 (0.8) 2663 (260)  
Salari et al59  2014 DCC 38.5 (1.1) 3040 (258.3)c C1 
 ECC 38.1 (0.9) 3029 (306)c  
Spears et al60  1966 DCC (later) NR NR C7 
 DCC (earlier) NR NR  
Sun et al26  2017 DCC (time) 39.62 (0.88) 3139 (491) 100 C8 
 Physiologic DCC 39.63 (0.89) 3190 (441) 100  
Ultee et al15  2008 DCC 36.05 (0.65) 2753 (193) C1 
 ECC 36.08 (0.74) 2174 (432)  
Upadhyay et al18  2013 Cut-cord UCM 37.3 (1.72) 2750 (410) NR C3 
 ECC (no UCM) 37.3 (1.69) 2640 (320) NR  
Van Rheenen et al61  2007 DCC 40.0 (1.5) 3124 (326) C1 
 ECC 40.0 (1.7) 3119 (328)  
Vatansever et al21  2018a DCC 38.9 (1.0) 3307 (355) 50.9 C1, C3, and C5 
 Cut-cord UCM 38.8 (1.0) 3352 (338) 50.9  
 ECC 38.9 (0.96) 3306 (397) 59.7  
Vural et al62  2019 DCC 39.6 (1.1) 4354 (175) 48 C1 
 ECC 39.6 (1.3) 4337 (211) 65  
Withanathantrige et al63  2017 DCC (60–75 s) Mean (IQR): 38 (37.8–38.2) NR 100 C1 
 DCC (120–135 s) Mean (IQR): 37.9 (37.7–38.1) NR 100  
 ECC Mean (IQR): 37.9 (37.6–38.2) NR 100  
Yadav et al22  2015a DCC (90 s) no UCM 38.4 (0.9) 2790 (310) NR C1 and C5 
 DCC (90s s) + UCM 38.2 (0.9) 2740 (290) NR  
 ECC (30 s) + UCM 38.5 (0.9) 2860 (280) NR  
StudyInterventionGestational Age, Mean (SD), wkBirth wt, Mean (SD), gCesarean Delivery, %Comparison
Al-Tawil et al33  2012 DCC 38.5 (1.1) 3348 (540.8) C1 
 ECC 38.2 (1.4) 3110 (390.8)  
Alzaree et al19  2018 DCC 38.9 (0.96) NR NR C4 
 Intact UCM 38.9 (0.90) NR NR  
Andersson et al31  2011 DCC 40.0 (11) 3629 (460) C1 
 ECC 40.1 (1.1) 3533 (486) 0.5  
Andersson et al23  2019 DCC later 39.6 (1.4) 3072 (401) C7 
 DCC earlier 39.6 (1.4) 3036 (372)  
Backes et al11  2015 DCC 39.2 (1.6) 3300 (700) NR C1 
 ECC 38.3 (1.4) 3400 (1200) NR  
Cavallin et al34  2019 DCC Median (IQR): 39 (39; 39) 3273 (372) 100 C1 
 ECC Median (IQR): 39 (39; 39) 3395 (571) 100  
Ceriani Cernadas et al35  2006 DCC (60 s) 39.1 (1.2) 3424 (382) 30 C1 
 DCC (180 s) 39.3 (1.1) 3420 (360) 28.3  
 ECC 39.3 (1.4) 3390 (395) 28.3  
Chaparro et al36  2006 DCC 38·8 (1.1) 3182 (369) C1 
 ECC 39·0 (1.1) 3196 (362)  
Chen et al24  2018a DCC (60 s) 40 (1) 3363 (398) C1 and C8 
 DCC (90 s) 40 (1) 3328 (314)  
 DCC (120 s) 40 (1) 3380 (456)  
 DCC (150 s) 40 (1) 3326 (324)  
 DCC (180 s) 40 (1) 3326 (320)  
 ECC (immediate) 40 (1) 3333 (90)  
 ECC (30 s) 40 (1) 3387 (399)  
 DCC physiologic 40 (1) 3340 (372)  
Chopra et al37  2018 DCC 37.4 (1.5) 2188 (334) 78.2 C1 
 ECC 37.7 (1.5) 2202 (389) 67.3  
Datta et al38  2017 DCC 35.6 (1) 2166 (429) 29.3 C1 
 ECC 35.4 (1) 2107 (463) 44.1  
De Paco et al39  2011 DCC 39.2 (0.9) 3220 (362.3) C1 
 ECC 39.6 (1.1) 3251 (406.5  
De Paco et al40  2016 DCC 39.5 (1.2) 3293 (422) NR C1 
 ECC 39.6 (1.1) 3181 (422) NR  
Emhamed et al41  2004 DCC NR 3390 (421) NR C1 
 ECC NR 3428 (424) NR  
Erickson-Owens et al17  2012 Intact UCM 39.2 (0.3) 3662(240) 100 C2 
 ECC 39.1 (0.1) 3524 (504) 100  
Fawzy et al42  2015 DCC Range: 38–41 Range: 3300–4000 NR C1 
 ECC Range: 37–40 Range: 3000–4500 NR  
Geethanath et al43  1997 DCC NR NR NR C1 
 ECC NR NR NR  
Grajeda et al44  1997 DCC (at placenta) 38.8 (0.9) 3200 (500) NR C1 
 DCC (below placenta) 38.4 (1.2) 3200 (500) NR  
 ECC 38.5 (1.2) 3000 (400) NR  
Gupta et al45  2002 DCC 39.1 (1.2) 2743 (407.8) NR C1 
 ECC 39.4 (1.1) 2707 (417) NR  
Ishaq et al46  2016b DCC (later) 37.5 (0.7) NR NR C7 
 DCC (earlier) 37.5 (0.7) NR NR  
Jahazi et al47  2008 DCC 39.6 (1.2) 3272 (329) NR C1 
 ECC 39.3 (0.9) 3008 (573) NR  
Jaiswal et al20  2015 DCC 38.7 (0.9) 2751 (390) 40 C5 
 DCC with UCM 38.6 (0.81) 2760 (300) 43  
Jaleel et al49  2009 DCC 38.7 (1.2) 3150 (550) 26 C1 
 ECC 38.4 (1.3) 3060 (390) 21  
Katheria et al48  2017 DCC (later) 39 (1) 3440 (523) C7 
 DCC (earlier) 39 (1) 3204 (302)  
Kc et al51  2017 DCC (later) 39.3 (1.1) 3029 (405) NR C7 
 DCC (earlier) 39.0 (1.2) 3015 (426) NR  
Kc et al12  2019 DCC (later) 39.4 (1.3) 3011 (382) NR C7 
 DCC (earlier) 39.4 (1.3) 3072 (399) NR  
Krishnan et al50  2015 DCC 38.5 (1.2) 2962 (372) C1 
 ECC 38.2 (2.1) 3008 (573)  
Mercer et al52  2017 DCC 39.5 (1) 3584 (497) 22 C1 
 ECC 39.4 (1) 3433 (454) 31  
Mohammad et al53  2019 DCC NR NR NR C1 
 ECC NR NR NR  
Nelson et al25  1980 DCC (time approach) 40.3 (1.3) 3489 (453) NR C8 
 Physiologic approach DCC 40.5 (1.3) 3437 (439) NR  
Nesheli et al54  2015b DCC NR NR C1 
 ECC NR NR  
Nouraie et al55  2019 DCC (later) 38.7 (0.9) 3204 (302) NR C7 
 DCC (earlier) 38.6 (0.8) 3259 (362) NR  
Oxford Midwives Research Group56  1991 DCC 39.9 (1.2) 3431 (445) NR C1 
 ECC 40.0 (1.1) 3406 (440) NR  
Philip57  1973 DCC NR 3590 (452) NR C1 
 ECC NR 3543 (534) NR  
Saigal et al58  1972 DCC (30 s) Mean (range): 40.2 (38–43) Mean (range): 3463 (2740–4120) C1 
 DCC (60 s) Mean (range): 40 (38–41) Mean (range): 3380 (2750–4350) — 
 ECC (immediate) Mean (range): 40.2 (38–43) Mean (range): 3521 (2685–4040)  
Salae et al14  2016 DCC 35.7 (1.0) 2528 (239) C1 
 ECC 36.0 (0.8) 2663 (260)  
Salari et al59  2014 DCC 38.5 (1.1) 3040 (258.3)c C1 
 ECC 38.1 (0.9) 3029 (306)c  
Spears et al60  1966 DCC (later) NR NR C7 
 DCC (earlier) NR NR  
Sun et al26  2017 DCC (time) 39.62 (0.88) 3139 (491) 100 C8 
 Physiologic DCC 39.63 (0.89) 3190 (441) 100  
Ultee et al15  2008 DCC 36.05 (0.65) 2753 (193) C1 
 ECC 36.08 (0.74) 2174 (432)  
Upadhyay et al18  2013 Cut-cord UCM 37.3 (1.72) 2750 (410) NR C3 
 ECC (no UCM) 37.3 (1.69) 2640 (320) NR  
Van Rheenen et al61  2007 DCC 40.0 (1.5) 3124 (326) C1 
 ECC 40.0 (1.7) 3119 (328)  
Vatansever et al21  2018a DCC 38.9 (1.0) 3307 (355) 50.9 C1, C3, and C5 
 Cut-cord UCM 38.8 (1.0) 3352 (338) 50.9  
 ECC 38.9 (0.96) 3306 (397) 59.7  
Vural et al62  2019 DCC 39.6 (1.1) 4354 (175) 48 C1 
 ECC 39.6 (1.3) 4337 (211) 65  
Withanathantrige et al63  2017 DCC (60–75 s) Mean (IQR): 38 (37.8–38.2) NR 100 C1 
 DCC (120–135 s) Mean (IQR): 37.9 (37.7–38.1) NR 100  
 ECC Mean (IQR): 37.9 (37.6–38.2) NR 100  
Yadav et al22  2015a DCC (90 s) no UCM 38.4 (0.9) 2790 (310) NR C1 and C5 
 DCC (90s s) + UCM 38.2 (0.9) 2740 (290) NR  
 ECC (30 s) + UCM 38.5 (0.9) 2860 (280) NR  

This table reveals selected key characteristics for the comparator groups in each trial, including gestational age at birth, birth wt, and mode of birth (cesarean delivery), indicating that in most studies, these characteristics were similar across comparator groups. In no study did authors report antenatal steroid administration. C, review comparison; IQR, interquartile range; NR, not reported; UCM, umbilical cord milking; —, not applicable.

a

Included in >1 comparison.

b

No data included in review meta-analysis.

c

Unclear whether mean and SD (authors report as “median birth weight”).

The studies covered a variety of timings of cord clamping and positioning of the infant (Supplemental Table 4). Timing of DCC assessed in the included studies ranged between 30 and ≥120 seconds; most studies delayed by 30 to 45 seconds.

Overall, study-level risk of bias was mixed to high (Fig 3, Supplemental Table 5). Most studies had unclear allocation concealment, difficulties with adequate blinding of participants and personnel because of the nature of the intervention, and a high level of attrition. Most of the studies were also at high or unclear risk of selective reporting because of a lack of prospectively registered protocols and inadequate reporting. All outcomes selected for Grading of Recommendations Assessment, Development and Evaluations (GRADE) assessment were rated as very low or low-certainty evidence (Supplemental Tables 613). In addition to the design limitations outlined above, there was also considerable imprecision (usually because of low event rates for many outcomes and small numbers of studies per outcome). There was some inconsistency in findings between studies because of unclear or missing definitions of outcomes.

Comparison 1. Later DCC (≥30 Seconds After Birth) Compared to ECC (<30 Seconds)

We identified 33 studies comparing DCC at ≥30 seconds to ECC in 5263 mothers and their late preterm or term infants (Supplemental Information).

The main outcomes are addressed in Table 2, with priority (GRADE-assessed) outcomes reported in the text below. All outcomes were assessed as very low certainty, except for PPH, which was low certainty.

TABLE 2

Summary of Effects for Priority GRADE-Assessed Outcomes

OutcomeNo. StudiesNo. ParticipantsRR or MD, Fixed or Random EffectsEffect Estimate (95% CI)I2, %Certainty (GRADE)
Comparison 1: later DCC (≥30 s) compared to ECC (<30 s)       
 Neonatal mortality 537 RR, fixed 2.54 (0.50 to 12.74) Very low 
 Resuscitation 329 RR, fixed 5.08 (0.25 to 103.58) NA Very low 
 NICU admission 10 1968 RR, fixed 1.16 (0.69 to 1.95) Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 1352 MD, random 1.17 higher (0.48 to 1.86 higher) 89 Very low 
 Hematocrit at birth (within first 24 h), % 12 2183 MD, random 3.38 higher (2.08 to 4.67 higher) 81 Very low 
 Hyperbilirubinemia requiring phototherapy 15 2814 RR, fixed 1.28 (0.90 to 1.82) 19 Very low 
 Anemia at 4–6 mo (infant) 937 RR, fixed 1.01 (0.75 to 1.37) Very low 
 Ferritin concentrations at 3–6 mo (infant), µg/L 286 MD, random 87.02 higher (1.89 lower to 175.94 higher) 96 Very low 
 PPH 10 2675 RR, fixed 0.89 (0.70 to 1.13) 13 low 
 Severe PPH 1828 RR, fixed 0.75 (0.42 to 1.35) Very low 
 Manual removal of placenta 247 RR, fixed 0.58 (0.21 to 1.65) NA low 
 Neurodevelopment: ASQ-3 total score at 4 ya 245 MD, fixed 3.40 points higher (2.86 lower to 9.66 higher) NA Very low 
Comparison 2: ICM versus ECC       
 NICU admission 24 RR, fixed 0 events NA Very low 
Comparison 3: CCM versus ECC       
 Neonatal mortality 200 RR, fixed 0.20 (0.01 to 4.11) NA Very low 
 NICU admission 200 RR, fixed 0 events NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 200 MD, fixed 1.60 higher (0.96 to 2.24 higher) NA Very low 
 Hematocrit at birth, % 200 MD, fixed 4.30 higher (2.36 to 6.24 higher) NA Very low 
 Hyperbilirubinemia requiring phototherapy 200 RR, fixed 0 events NA Very low 
Comparison 5: later DCC versus CCM       
 Neonatal mortality 300 RR, fixed 1.00 (0.09 to 10.90) NA Very low 
 NICU admission 200 RR, fixed 1.83 (0.71 to 4.77) NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 500 MD, fixed 0.56 lower (0.21 to 0.92 lower) Very low 
 Hematocrit at birth, % 500 MD, random 1.60 lower (0.09 to 3.11 lower) 45 Very low 
 Hyperbilirubinemia requiring phototherapy 500 RR, fixed 1.36 (0.66 to 2.81) Very low 
Comparison 7: DCC ≥60 s versus <60 s       
 Neonatal mortality 231 RR, fixed 0.10 (0.01 to 1.98) NA Very low 
 Resuscitation 60 RR, fixed 0.40 (0.08 to 1.90) NA Very low 
 Moderate to severe HIE (Sarnat score ≥2)b 60 RR, fixed 0 events NA Very low 
 NICU admission 291 RR, fixed RR 0.73 (0.40 to 1.35) 26 Very low 
 Respiratory support 60 RR, fixed 0.53 (0.27 to 1.07) NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 60 MD, fixed 1.30 higher (0.14 lower to 2.46 higher) NA Very low 
 Hyperbilirubinemia requiring phototherapy 906 RR, random 1.93 (1.00 to 3.72) 60 Very low 
Comparison 8: DCC based on time since birth compared to physiologic approach to cord clamping       
 Neonatal mortality 338 RR, fixed 5.00 (0.24 to 103.37) NA Very low 
 Resuscitation 338 RR, fixed 1.67 (0.84 to 3.30) NA Very low 
 NICU admission 878 RR, random 2.58 (0.04 to 163.65) 80 Very low 
 Hematocrit at birth (within first 24 h), % 540 MD, fixed 1.40 lower (2.79 lower to 0.01 lower) NA Very low 
 Hyperbilirubinemia requiring phototherapy 932 RR, fixed 0.88 (0.53 to 1.44) Very low 
 PPH 594 RR, fixed 0.92 (0.40 to 2.07) Very low 
 Severe PPH 540 RR, fixed 1.82 (0.10 to 33.4) NA Very low 
 Postpartum infection 54 RR, fixed 0.15 (0.01 to 2.83) NA Very low 
OutcomeNo. StudiesNo. ParticipantsRR or MD, Fixed or Random EffectsEffect Estimate (95% CI)I2, %Certainty (GRADE)
Comparison 1: later DCC (≥30 s) compared to ECC (<30 s)       
 Neonatal mortality 537 RR, fixed 2.54 (0.50 to 12.74) Very low 
 Resuscitation 329 RR, fixed 5.08 (0.25 to 103.58) NA Very low 
 NICU admission 10 1968 RR, fixed 1.16 (0.69 to 1.95) Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 1352 MD, random 1.17 higher (0.48 to 1.86 higher) 89 Very low 
 Hematocrit at birth (within first 24 h), % 12 2183 MD, random 3.38 higher (2.08 to 4.67 higher) 81 Very low 
 Hyperbilirubinemia requiring phototherapy 15 2814 RR, fixed 1.28 (0.90 to 1.82) 19 Very low 
 Anemia at 4–6 mo (infant) 937 RR, fixed 1.01 (0.75 to 1.37) Very low 
 Ferritin concentrations at 3–6 mo (infant), µg/L 286 MD, random 87.02 higher (1.89 lower to 175.94 higher) 96 Very low 
 PPH 10 2675 RR, fixed 0.89 (0.70 to 1.13) 13 low 
 Severe PPH 1828 RR, fixed 0.75 (0.42 to 1.35) Very low 
 Manual removal of placenta 247 RR, fixed 0.58 (0.21 to 1.65) NA low 
 Neurodevelopment: ASQ-3 total score at 4 ya 245 MD, fixed 3.40 points higher (2.86 lower to 9.66 higher) NA Very low 
Comparison 2: ICM versus ECC       
 NICU admission 24 RR, fixed 0 events NA Very low 
Comparison 3: CCM versus ECC       
 Neonatal mortality 200 RR, fixed 0.20 (0.01 to 4.11) NA Very low 
 NICU admission 200 RR, fixed 0 events NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 200 MD, fixed 1.60 higher (0.96 to 2.24 higher) NA Very low 
 Hematocrit at birth, % 200 MD, fixed 4.30 higher (2.36 to 6.24 higher) NA Very low 
 Hyperbilirubinemia requiring phototherapy 200 RR, fixed 0 events NA Very low 
Comparison 5: later DCC versus CCM       
 Neonatal mortality 300 RR, fixed 1.00 (0.09 to 10.90) NA Very low 
 NICU admission 200 RR, fixed 1.83 (0.71 to 4.77) NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 500 MD, fixed 0.56 lower (0.21 to 0.92 lower) Very low 
 Hematocrit at birth, % 500 MD, random 1.60 lower (0.09 to 3.11 lower) 45 Very low 
 Hyperbilirubinemia requiring phototherapy 500 RR, fixed 1.36 (0.66 to 2.81) Very low 
Comparison 7: DCC ≥60 s versus <60 s       
 Neonatal mortality 231 RR, fixed 0.10 (0.01 to 1.98) NA Very low 
 Resuscitation 60 RR, fixed 0.40 (0.08 to 1.90) NA Very low 
 Moderate to severe HIE (Sarnat score ≥2)b 60 RR, fixed 0 events NA Very low 
 NICU admission 291 RR, fixed RR 0.73 (0.40 to 1.35) 26 Very low 
 Respiratory support 60 RR, fixed 0.53 (0.27 to 1.07) NA Very low 
 Hemoglobin concentrations at birth (within first 24 h), g/dL 60 MD, fixed 1.30 higher (0.14 lower to 2.46 higher) NA Very low 
 Hyperbilirubinemia requiring phototherapy 906 RR, random 1.93 (1.00 to 3.72) 60 Very low 
Comparison 8: DCC based on time since birth compared to physiologic approach to cord clamping       
 Neonatal mortality 338 RR, fixed 5.00 (0.24 to 103.37) NA Very low 
 Resuscitation 338 RR, fixed 1.67 (0.84 to 3.30) NA Very low 
 NICU admission 878 RR, random 2.58 (0.04 to 163.65) 80 Very low 
 Hematocrit at birth (within first 24 h), % 540 MD, fixed 1.40 lower (2.79 lower to 0.01 lower) NA Very low 
 Hyperbilirubinemia requiring phototherapy 932 RR, fixed 0.88 (0.53 to 1.44) Very low 
 PPH 594 RR, fixed 0.92 (0.40 to 2.07) Very low 
 Severe PPH 540 RR, fixed 1.82 (0.10 to 33.4) NA Very low 
 Postpartum infection 54 RR, fixed 0.15 (0.01 to 2.83) NA Very low 

The results of the meta-analysis for the a priori, selected priority (GRADE-assessed) outcomes are summarized. Comparison 4 included only 1 study in which the authors did not report on any of the priority outcomes, and comparison 6 included no studies; therefore, no results are reported for these 2 comparisons. HIE, hypoxic ischemic encephalopathy; I2, statistical heterogeneity; NA, not available.

a

Squires J, Twombly E, Bricker D, Potter L. ASQ-3 User’s Guide. 3rd ed. Baltimore, MD: Brookes Publishing Co; 2009.

b

Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol. 1976;10:696–705.

Neonatal Outcomes

Compared to ECC, it is uncertain whether DCC impacts on neonatal mortality (risk ratio [RR] 2.54 [95% confidence interval (CI) 0.50 to 12.74]; risk difference [RD] 0.01 [95% CI −0.01 to 0.03]; 4 studies, 537 infants), the need for resuscitation (RR 5.08 [95% CI 0.25 to 103.58]; RD 0.01 [95% CI −0.02 to 0.04]; 3 studies, 329 infants), or admission to the NICU (RR 1.16 [95% CI 0.69 to 1.95]; RD 0.00 [95% CI −0.01 to 0.02]; 10 studies, 1968 infants) (Fig 4). The use of phototherapy to treat hyperbilirubinemia was possibly higher for DCC ≥30 seconds compared to ECC (RR 1.28 [95% CI 0.90 to 1.82]; RD 0.01 [95% CI −0.00 to 0.03]; 15 studies, 2814 infants) perhaps more so in term infants (RR 1.54 [95% CI 1.01 to 2.34]; RD 0.01 [95% CI 0.00 to 0.03]; 13 studies, 2691 infants) (Fig 5). Hypoxic ischemic encephalopathy and respiratory support were not reported by any studies.

FIGURE 3

Risk of bias summary. The risk of bias graph is a review of authors’ judgments about each risk of bias item, presented as percentages across all included studies.

FIGURE 3

Risk of bias summary. The risk of bias graph is a review of authors’ judgments about each risk of bias item, presented as percentages across all included studies.

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FIGURE 4

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: admission to the NICU or special care nursery. a For the DCC group, we have combined 2 groups from this trial: the one with clamping at 1 minute and the other at 3 minutes. b The number of participants per group was estimated by using the percentage reported for outcomes. df, degree of freedom; I2, statistical heterogeneity; M-H, Mantel-Haenszel.

FIGURE 4

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: admission to the NICU or special care nursery. a For the DCC group, we have combined 2 groups from this trial: the one with clamping at 1 minute and the other at 3 minutes. b The number of participants per group was estimated by using the percentage reported for outcomes. df, degree of freedom; I2, statistical heterogeneity; M-H, Mantel-Haenszel.

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Hematologic Measures

Compared to ECC, DCC ≥30 seconds may improve hematologic measures, including hemoglobin within 24 hours after birth (mean difference [MD] 1.17 g/dL [95% CI 0.48 to 1.86]; random effects; 9 studies, 1352 infants) (Fig 6) and 7 days after birth (MD 1.11 g/dL [95% CI 0.40 to 1.82]; random effects; 3 studies, 695 infants) as well as hematocrit concentrations at 24 hours after birth (MD 3.38% [95% CI 2.08 to 4.67]; random effects; 12 studies, 2183 infants) (Fig 7). There was little to no difference in the number of infants with anemia 4 to 6 months after birth (RR 1.01 [95% CI 0.75 to 1.37]; RD 0.00 [95% CI −0.04 to 0.04]; 4 studies, 937 infants).

FIGURE 5

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; hyperbilirubinemia treated with phototherapy. a The study included 8 groups. We combined the 2 groups with clamping <30 seconds for the ECC group and the 5 groups with cord clamping >30 seconds for the DCC group. b The DCC group includes 2 of the groups assessed: clamping at 60 to 75 seconds and clamping at 120 to 135 seconds. c The ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; I2, statistical heterogeneity; M-H, Mantel-Haenszel.

FIGURE 5

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; hyperbilirubinemia treated with phototherapy. a The study included 8 groups. We combined the 2 groups with clamping <30 seconds for the ECC group and the 5 groups with cord clamping >30 seconds for the DCC group. b The DCC group includes 2 of the groups assessed: clamping at 60 to 75 seconds and clamping at 120 to 135 seconds. c The ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; I2, statistical heterogeneity; M-H, Mantel-Haenszel.

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FIGURE 6

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: hemoglobin within the first 24 hours after birth (by timing of cord clamping). a At 24 hours. b Within 24 hours. c Within 24 hours. d At 12 hours; number of participants estimated from n (%) reported for outcomes. e At 18 hours; hemoglobin assessed at 2 time points within 24 hours postbirth (2 and 18 hours). f At 1 hour postbirth. g ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; IV, inverse variance; I2, statistical heterogeneity.

FIGURE 6

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: hemoglobin within the first 24 hours after birth (by timing of cord clamping). a At 24 hours. b Within 24 hours. c Within 24 hours. d At 12 hours; number of participants estimated from n (%) reported for outcomes. e At 18 hours; hemoglobin assessed at 2 time points within 24 hours postbirth (2 and 18 hours). f At 1 hour postbirth. g ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; IV, inverse variance; I2, statistical heterogeneity.

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FIGURE 7

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: hematocrit within the first 24 hours after birth (by timing of cord clamping). a At 24 hours postbirth. b At 6 hours; data for delayed cord clamping were obtained by combining data from 2 study arms. c At birth. d At 24 hours; 2 groups with clamping <30 seconds were combined for the ECC group; 5 groups with clamping ≥30 seconds were combined for late clamping. e At 2 hours. f Within 24 hours. g Assessed at 2 time points (2 and 18 hours), with the highest value used, which was the assessment at 2 hours. h At 24 hours; SD was calculated from the reported SE value. i Assessed at 2 time points (2 and 18 hours), with the highest value used (18 hours). j At 1 hour. k At 2 hours. l ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; IV, inverse variance; I2, statistical heterogeneity.

FIGURE 7

Forest plot for comparison 1: later DCC (≥30 seconds after birth) compared to early cord (<30 seconds) clamping; outcome: hematocrit within the first 24 hours after birth (by timing of cord clamping). a At 24 hours postbirth. b At 6 hours; data for delayed cord clamping were obtained by combining data from 2 study arms. c At birth. d At 24 hours; 2 groups with clamping <30 seconds were combined for the ECC group; 5 groups with clamping ≥30 seconds were combined for late clamping. e At 2 hours. f Within 24 hours. g Assessed at 2 time points (2 and 18 hours), with the highest value used, which was the assessment at 2 hours. h At 24 hours; SD was calculated from the reported SE value. i Assessed at 2 time points (2 and 18 hours), with the highest value used (18 hours). j At 1 hour. k At 2 hours. l ECC group: cord clamped at ∼10 seconds and milked; DCC includes 2 combined groups: cord clamped at 90 seconds with no milking and cord clamped at 90 seconds and milked. df, degree of freedom; IV, inverse variance; I2, statistical heterogeneity.

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Infant and/or Early Childhood Outcomes

In the included studies, none of the authors assessed our primary infant outcome of survival without moderate to severe neurodevelopmental impairment in early childhood (up to and including 4 years). One study did not reveal evidence of differences in neurodevelopment between DCC ≥30 seconds and ECC at 4 years, including Ages and Stages Questionnaire, Third Edition (ASQ-3) total scores (MD 3.40 points [95% CI −2.86 to 9.66]; 245 children).16 

Maternal Outcomes

Compared to ECC, DCC ≥30 seconds may make little or no difference to maternal complications including PPH ≥500 mL (RR 0.89 [95% CI 0.70 to 1.13]; RD −0.01 [95% CI −0.03 to 0.01]; 10 studies, 2675 women). In no studies did authors report on maternal deaths (up to 1 year after delivery) or severe morbidity.

Other outcomes for this comparison are detailed in Supplemental Table 14.

Comparison 2: ICM Versus ECC

We identified 1 study of 24 infants evaluating ICM compared to ECC.17 

Neonatal Outcomes

Few clinical outcomes were reported. No effect of ICM was seen on admission to the NICU or special care nursery (RR not estimable; RD 0.00 [95% CI −0.15 to 0.15]), clinical jaundice (RR 1.19 [95% CI 0.89 to 1.59]; RD 0.17 [95% CI −0.07 to 0.41]), or exchange transfusion (RR not estimable; RD 0.00 [95% CI −0.15 to 0.15]).

Hematologic Measures

Compared to ECC, ICM may improve hematologic measures including hemoglobin concentrations (grams per deciliter) within the first 7 days after birth (MD 2.20 [95% CI 0.48 to 3.92]) and hematocrit (percentage) within the first 7 days after birth (MD 7.50 [95% CI 2.30 to 12.70]).

Maternal Outcomes

None of our priority maternal outcomes were reported for this comparison.

Other outcomes for this comparison are detailed in Supplemental Table 15.

Comparison 3: CCM Versus ECC

We identified 1 study of 200 infants evaluating CCM compared to ECC in which authors reported on priority (GRADE-assessed) outcomes18  (Supplemental Table 3 in Supplemental Information).

Neonatal Outcomes

No impact of CCM was seen on admission to the NICU or special care nursery (RR not estimable; RD 0.00 [95% CI −0.02 to 0.02]), neonatal mortality (RR 0.20 [95% CI 0.01 to 4.11]; RD −0.02 [95% CI −0.05 to 0.01]), or hyperbilirubinemia requiring phototherapy (RR not estimable; RD [0.00 95% CI −0.02 to 0.02]).

Hematologic Measures

Compared to ECC, CCM may improve hematologic measures at 24 and 72 hours of life including hemoglobin concentrations (grams per deciliter) within the first 24 hours after birth (MD 1.60 [95% CI 0.96 to 2.24]), hematocrit (percentage) within the first 24 hours after birth (MD 4.30 [95% CI 2.36 to 6.24]), hemoglobin concentrations (grams per deciliter) within first 7 days after birth (MD 1.10 [95% CI 0.74 to 1.46]), and hematocrit (percentage) within the first 7 days after birth (MD 4.00 [95% CI 2.29 to 5.71]).

Maternal Outcomes

None of our priority maternal outcomes were reported for this comparison.

Other outcomes for this comparison are detailed in Supplemental Table 16.

Comparison 4: Later DCC Versus ICM

We identified 1 study of 250 infants evaluating this comparison in which authors reported outcomes identified as critical or important.19 

Other outcomes for this comparison are detailed in Supplemental Table 17.

Comparison 5: Later DCC Versus CCM

We identified 3 studies of 740 infants evaluating DCC compared to CCM.2022 

Neonatal Outcomes

Compared to CCM, DCC does not reveal differences in neonatal mortality (RR 1.00 [95% CI 0.09 to 10.90]; RD 0.00 [95% CI −0.02 to 0.02]; 1 study, 300 infants), admission to the NICU or special care nursery (RR 1.83 [95% CI 0.71 to 4.77]; RD 0.05 [95% CI −0.03 to 0.13]; 1 study, 200 infants), or phototherapy for the treatment of hyperbilirubinemia (RR 1.36 [95% CI 0.66 to 2.81]; RD 0.02 [95% CI −0.02 to 0.06]; 2 studies, 500 infants).

Hematologic Measures

Lower hemoglobin and hematocrit values at 24 hours and 7 days of life were seen in infants receiving DCC compared to CCM, including hemoglobin concentrations (grams per deciliter) within the first 24 hours after birth (MD −0.56 [95% CI −0.92 to −0.21]; 2 studies, 500 infants), hematocrit (percentage) within the first 24 hours after birth (MD −1.60 [95% CI −3.11 to −0.09]; 2 studies, 500 infants), hemoglobin concentrations (grams per deciliter) within first 7 days after birth (MD −0.47 [95% CI −0.81 to −0.13]; 2 studies, 500 infants), and hematocrit (percentage) within first 7 days after birth (MD −1.11 [95% CI −2.12 to −0.09]; 2 studies, 500 infants).

Maternal Outcomes

None of our priority maternal outcomes were reported for this comparison.

Other outcomes for this comparison are detailed in Supplemental Table 18.

Comparison 6: ICM Versus CCM

We identified no studies in which authors compared ICM to CCM.

Comparison 7.DCC ≥60 Compared to <60 Seconds

We identified 7 studies including 2745 mothers and their infants for inclusion (Table 1). In 1 study, authors recruited only infants who required resuscitation.23  Few clinically important measures were available for analysis.

Neonatal Outcomes

Compared to DCC <60 seconds, DCC ≥ 60 seconds may make little or no difference to neonatal mortality (RR 0.10 [95% CI 0.01 to 1.98]; RD 0.01 [95% CI −0.01 to 0.03]; 1 trial, 231 infants), resuscitation (RR 0.40 [95% CI 0.08 to 1.90]; RD −0.10 [95% CI −0.26 to 0.06]; 1 trial, 60 infants), admission to the NICU (RR 0.73 [95% CI 0.40 to 1.35]; RD −0.04 [95% CI −0.12 to 0.04]; fixed effects; 2 studies, 291 infants), moderate to severe hypoxic ischemic encephalopathy (no events; 1 study, 60 infants), or respiratory support (RR 0.53 [95% CI 0.27 to 1.07]; RD −0.23 [95% CI −0.47 to 0.01]; 1 trial, 60 infants). The need for hyperbilirubinemia to be treated with phototherapy was possibly higher for DCC ≥60 seconds (RR 1.93 [95% CI 1.00 to 3.72]; RD 0.09 [95% CI −0.08 to 0.25]; random effects; 2 studies, 906 infants).

Hematologic Measures

Compared to DCC <60 seconds, hemoglobin concentrations at 24 hours after birth were higher with clamping delayed ≥60 seconds (MD 1.30 g/dL [95% CI 0.14 to 2.46]; 1 trial, 60 infants). Hematocrit in the first 24 hours was not reported.

Infant and/or Early Childhood Outcomes

In a single study of 540 children, moderate to severe neurodevelopmental impairment in early childhood was reduced with later clamping, with generally better scores in the delayed ≥60 seconds group than in the <60 seconds group. Anemia and ferritin concentrations in infancy were not reported.

Maternal Outcomes

None of our priority maternal outcomes were reported for this comparison.

Other outcomes for this comparison can be found in Supplemental Table 19. No indication of differences between the groups was seen for the few outcomes reported.

Comparison 8: DCC Based on Time Since Birth Versus Physiologic Parameters to Cord Clamping

We identified 3 studies involving 1113 mother-infant pairs in which authors evaluated this comparison.2426 

Neonatal Outcomes

No differences between DCC based on timing versus physiologic parameters were seen in clinical outcomes, including neonatal mortality (RR 5.00 [95% CI 0.24 to 103.37]; RD 0.01 [95% CI −0.01 to 0.03]; 1 study, 338 infants), admission to the NICU (RR 2.58 [95% CI 0.04 to 163.65]; RD 0.02 [95% CI −0.04 to 0.09]; 2 studies, 878 infants), or hyperbilirubinemia requiring phototherapy (RR 0.88 [95% CI 0.53 to 1.44]; RD −0.01 [95% CI −0.05 to 0.03]; 3 studies, 932 infants).

Hematologic Measures

DCC based on timing may be less effective than the physiologic approach on hematocrit (percentage) within the first 24 hours after birth (MD −1.40 [95% CI −2.79 to −0.01]; 1 study, 540 infants), hemoglobin concentrations (grams per deciliter) within the first 7 days after birth (MD −1.70 [95% CI −1.97 to −1.43]; 1 study, 338 infants), hematocrit (percentage) within the first 7 days after birth (MD −6.50 [95% CI −7.64 to −5.36]; 1 study, 338 infants).

Maternal Outcomes

None of our priority maternal outcomes were reported for this comparison.

Other outcomes for this comparison are detailed in Supplemental Table 20.

The subgroup analyses revealed no clear subgroup differences for any of the selected clinically important outcomes except for hematocrit (percentage) 24 hours after birth, which suggested a favorable effect for DCC ≥30 seconds compared to ECC that was greater in studies performed in high-income countries than in low- or middle-income countries (Supplemental Table 21).

We identified 46 studies comparing cord management interventions. In most (33), the authors compared DCC ≥30 seconds after birth to ECC (clamping <30 seconds after birth). In none of these studies did authors report our primary outcome of survival without moderate to severe neurodevelopmental impairment. Evidence was evaluated as either very low or low certainty.

No differences between DCC ≥30 seconds and ECC (33 studies) were seen in neonatal mortality, need for resuscitation or admission to NICU, although there was a possible increase in phototherapy treatment in the delayed group. Although hemoglobin and hematocrit concentrations were higher 24 hours and 7 days after birth in the delayed group, there was little or no difference seen in anemia at 4 to 6 months after birth. Although the 24-hour and 7-day results were statistically significant, these results are of uncertain clinical significance. Child neurodevelopment and maternal outcomes did not reveal clear differences between DCC ≥30 seconds and early clamping. For delayed clamping ≥60 vs <60 seconds (7 studies), no differences were apparent for neonatal mortality, need for resuscitation, or admission to neonatal intensive care, although (as above) there was a possible increase in the need for phototherapy to treat hyperbilirubinemia in the group delayed ≥60 seconds. Hemoglobin concentrations at birth were higher in the group delayed ≥60 seconds, and no studies reported later hematologic measures. In 1 study, authors reported better early childhood neurodevelopment scores in the group delayed ≥60 seconds compared to <60 seconds clamping.

The most recent Cochrane systematic review considering timing of umbilical cord clamping in term infants (McDonald et al27 ) included 15 studies (involving 3911 women and infant pairs). McDonald et al27  did not show differences in neonatal mortality or morbidity between later (generally at least 180 seconds) and early clamping (usually 15 seconds). They showed that hemoglobin concentration in infants at 24 hours after birth was higher in the later cord clamping group, and fewer infants in the ECC group received phototherapy to treat hyperbilirubinemia.27  These findings are broadly consistent with those of our updated review, which now includes data from more than twice as many studies and participants.

The 2013 review included only term infants.27  Our review includes “late preterm” as well as term infants. Although late preterm infants have a higher risk than term infants for admission to the NICU and poor developmental outcomes, they do not have the same degree of serious morbidities experienced by less mature preterm infants.28  In general, care and outcomes, in the absence of additional risk factors for illness such as infection, congenital anomalies, or birth injury, tend to be more similar to term rather than to very preterm infants, prompting our grouping these categories together. The effects of cord management at birth for preterm infants before 34 weeks’ gestation29  and all preterm infants30  are considered in 2 separate systematic reviews.

Whereas McDonald et al27  specified neonatal mortality as the primary infant outcome, in this review, we specified survival without evidence of moderate or severe neurodevelopmental impairment as the primary outcome, as per ILCOR consensus. The incorporation of data from new studies (through July 2019) and of studies including late preterm infants, however, has not provided additional evidence of the effect of cord management strategies on childhood neurodevelopmental outcomes. Perhaps reflecting logistic and financial challenges in long-term follow-up assessment of study cohorts, in only 1 study did authors report outcomes in early childhood for later clamping compared to early clamping (≥30 vs <30 seconds).31  In the study, the authors assessed neurodevelopment using parental responses to the ASQ-3. There were no between-group differences in the overall scores for the tested domains (communication, gross and fine motor, problem solving, personal-social) at 4 months, 12 months, and 4 years of age. The total number of tested children was small, with only 245 participants assessed up to 4 years (61% of randomly assigned children).

For the most commonly studied comparisons of delayed versus early clamping (≥30 vs <30 seconds) and later clamping at ≥60 vs <60 seconds, there is low-certainty evidence of improved hemoglobin and hematocrit status in the neonatal period and improved iron status in infancy without sufficient evidence of reducing iron deficiency anemia or improving survival and/or neurodevelopmental outcomes in early childhood. The increased rates of phototherapy-treated hyperbilirubinemia warrant attention when practicing DCC in term infants.

Currently, there is insufficient evidence for recommending cord milking and physiologic approaches to improve infant outcomes.

Maternal Outcomes

In this review, we identified low-certainty evidence that DCC ≥30 seconds versus ECC <30 seconds did not affect the risk of PPH (>500 mL) or the risk of severe PPH (>1000 mL), downgraded for risk of bias in the included studies and imprecision of the effect estimate. No studies reporting priority maternal outcomes were identified among those assessing clamping after ≥60 seconds versus <60 seconds or any of the other cord management strategies.

In no studies have authors evaluated the effects of different cord management strategies on maternal mortality or other severe morbidity.

Additional trials assessing cord management strategies in late preterm and term infants are warranted. These could be used to assess the various techniques used in practice, including cord milking, or delay >60 seconds, or a physiologic approach to cord clamping (typically defined as cessation of cord pulsation). Trials should be informed by prospectively registered protocols with core outcome sets to minimize protocol deviations. Longer-term follow-up, particularly for anemia during infancy and neurodevelopment, is required to inform policy and practice. Large-scale RCTs or population-based studies are needed because most outcomes occur infrequently. Effects of different cord clamping management strategies should be assessed and reported for important population subgroups including infants requiring resuscitation.

Strengths of this review include rigorous methods, such as using a prospectively registered protocol and comprehensive search strategy, 2 reviewers independently completing each step of the review process, and using GRADE to determine certainty of evidence.32  The author team is a multidisciplinary collaboration of experts in systematic reviews, neonatology, and obstetrics from the ILCOR Neonatal Life Support Task Force, Cochrane Neonatal, and Cochrane Pregnancy and Childbirth.

The overall incompleteness and uncertainty of findings from available RCTs limits the applicability of this review. For many reported comparisons and outcomes, certainty of evidence was low or very low mainly because of risk of bias and imprecision and in some cases because of inconsistency; alternatively, no studies were available. In this review, pairwise comparisons were undertaken. We did not conduct analyses comparing all available comparisons simultaneously (network meta-analysis). Our subgroup analyses were limited by most studies not reporting outcomes separately by subgroup, indicating a possible role for individual participant data meta-analyses to address these questions.

Additionally, definitions for early and delayed clamping and milking varied across studies. Delayed clamping ranged from 30 seconds to >3 minutes, and early clamping ranged from within 5 seconds to within 30 seconds. Thus, in some instances, early and delayed clamping groups overlapped and may have received similar interventions.

Compared to ECC, DCC (at ≥30 seconds) and cord milking led to increased hemoglobin and hematocrit immediately after birth in infants ≥34 weeks’ gestational age. Longer-term benefits on anemia at 4 to 6 months or on neurodevelopmental status were not seen. The effects of later clamping or use of cord milking in term and late preterm infants on survival without neurodisability, anemia in early infancy, or maternal PPH (and most other outcomes reported) are uncertain, inhibiting the usefulness of currently available evidence for informing and influencing policy and practice.

We thank Carol Friesen (Cochrane Neonatal) for developing and conducting literature searches. We thank the following members of the ILCOR Scientific Advisory Committee and Neonatal Life Support Task Force for their input and assistance in developing the protocol and offering feedback on the review: Myra H. Wyckoff, MD, chair; Jonathan Wyllie, MBChB, BSC, vice chair; Khalid Aziz, MBBS, BA, MA, Med(IT); Maria Fernanda de Almeida, MD; Jorge W. Fabres, MD; Joe Fawke, MD; Ruth Guinsburg, MD, PhD; Shigeharu Hosono, MD, PhD; Tetsuya Isayama, MD, MSc, PhD; Vishal S. Kapadia, MD, MSCS; Han-Suk Kim, MD, PhD; Helen G. Liley, MBChB; Chris JD McKinlay, MBChB, PhD; Lindsay Mildenhall, MBChB; Jeffrey M. Perlman, MBChB; Yacov Rabi, MD; Charles C. Roehr, MD, PhD; Edgardo Szyld, MD, MSc; Daniele Trevisanuto, MD; Sithembiso Velaphi, MBChB, FC Ped, PhD; and Gary Weiner, MD.

Dr Gomersall conceptualized the protocol, designed the data collection forms, selected studies for inclusion, extracted data, assessed the risk of bias and certainty of evidence, conducted the analyses, drafted the initial manuscript, and reviewed and revised the manuscript; Drs Berber and McDonald conceptualized the protocol, designed the data collection forms, selected studies for inclusion, extracted data, assessed the risk of bias and certainty of evidence, conducted the analyses, and reviewed the manuscript; Ms Ovelman assisted with protocol development and study selection and reviewed and prepared the manuscript; Drs Soll and Middleton conceptualized the protocol, supervised study selection, data extraction, the risk of bias and certainty of evidence assessments, and data analyses, and drafted, reviewed, and revised the manuscript; Drs Niermeyer, El-Naggar, Davis, and Schmölzer conceptualized the protocol and critically reviewed the manuscript for important intellectual content; and all authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

This trial has been registered with the International Prospective Register of Systematic Reviews (https://www.crd.york.ac.uk/prospero/) (identifier CRD42020155498).

FUNDING: Funded by the American Heart Association on behalf of the International Liaison Committee on Resuscitation for conduct of the systematic review and article submission. This review has also been funded in part by the Vermont Oxford Network through support of Cochrane Neonatal.

     
  • ASQ-3

    Ages and Stages Questionnaire, Third Edition

  •  
  • CCM

    cut-cord milking

  •  
  • CI

    confidence interval

  •  
  • DCC

    delayed cord clamping

  •  
  • ECC

    early cord clamping

  •  
  • GRADE

    Grading of Recommendations Assessment, Development and Evaluations

  •  
  • ICM

    intact-cord milking

  •  
  • ILCOR

    International Liaison Committee on Resuscitation

  •  
  • MD

    mean difference

  •  
  • PPH

    postpartum hemorrhage

  •  
  • PRISMA

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses

  •  
  • RCT

    randomized controlled trial

  •  
  • RD

    risk difference

  •  
  • RR

    risk ratio

  •  
  • WHO

    World Health Organization

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11

Competing Interests

POTENTIAL CONFLICT OF INTEREST: The following authors received payment from the American Heart Association on behalf of the International Liaison Committee on Resuscitation to complete this systematic review: Drs Gomersall and Middleton and Prof McDonald received honorariums as expert systematic reviewers for the Knowledge Synthesis Unit; Dr Berber received payment as research associate with the Knowledge Synthesis Unit; Ms Ovelman and Dr Soll are employees of the Vermont Oxford Network; Dr Soll and Ms Ovelman work in the editorial office for Cochrane Neonatal, which received a contract from the American Heart Association as a Knowledge Synthesis Unit to undertake this systematic review for the International Liaison Committee on Resuscitation; the other authors have indicated they have no potential conflicts of interest to disclose.

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

Supplementary data