Guidelines on Deferred Cord Clampingand Cord Milking: A Systematic ReviewSugee Korale Liyanage, MSc,a,p Kiran Ninan, BHSc,a,p Sarah D. McDonald, MD, MSca,b,c,d

abstractCONTEXT: Deferred cord clamping (DCC) saves lives. It reduces extremely preterm infants’mortality by 30%, yet a minority of eligible infants receive it. This may in part be due to lack ofawareness or confidence in evidence, or conflicting or vague guidelines.

OBJECTIVE: To systematically review clinical practice guidelines and other statements on DCCand cord milking.

DATA SOURCES: Ten academic and guideline databases were searched.

STUDY SELECTION: Clinical practice guidelines and other statements (position statements andconsensus statements) providing at least 1 recommendation on DCC or umbilical cord milkingamong preterm or term infants were included.

DATA EXTRACTION: Data from included statements were extracted by 2 independent reviewers, anddiscrepancies were resolved through consensus. Guideline quality was appraised withmodified Appraisal of Guidelines for Research and Evaluation II and Appraisal of Guidelinesfor Research and Evaluation Recommendation Excellence tools.

RESULTS: Forty-four statements from 35 organizations were included. All endorsed DCC foruncompromised preterm infants, and 11 cautiously stated that cord milking may beconsidered when DCC is infeasible. Only half (49%) of the recommendations on the optimalduration of DCC were supported by high-quality evidence. Only 8% of statements citeda mortality benefit of DCC for preterm infants.

LIMITATIONS: Because systematic reviews of guidelines are relatively novel, there are few tools toinform study execution; however, we used the Appraisal of Guidelines for Research andEvaluation II and the Appraisal of Guidelines for Research and Evaluation RecommendationExcellence to assess quality and were methodologically informed by previous systematicreviews of guidelines.

CONCLUSIONS: Statements worldwide clearly encouraged DCC. Their implementability wouldbenefit from noting the preterm mortality benefit of DCC and more granularity.

bDivision of Maternal-Fetal Medicine and aDepartments of Obstetrics and Gynecology, cHealth Research Methods, Evidence, and Impact, and dRadiology, McMaster University, Hamilton,Ontario, Canada

pContributed equally as co-first authors

Ms Liyanage and Mr Ninan designed the data collection instruments, collected data, conducted the analyses, drafted the manuscript, and reviewed and revised themanuscript; Dr McDonald coordinated and supervised data collection and critically reviewed and revised the manuscript for important intellectual content; and allauthors conceptualized and designed the study and approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

This trial has been registered with PROSPERO (https://www.crd.york.ac.uk/prospero/) (identifier CRD42019143332).

To cite: Liyanage SK, Ninan K, McDonald SD. Guidelines on Deferred Cord Clamping and Cord Milking: A Systematic Review. Pediatrics. 2020;146(5):e20201429

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Cutting the umbilical cord isinevitable; but should it be rushed?Deferred cord clamping (DCC)facilitates the newborn infant’stransition to extrauterine life byallowing fetoplacental circulationto continue as the lungs expandafter birth.1 Umbilical cord milking(UCM) is when blood in the cut oruncut cord is squeezed toward theinfant.2

DCC reduces neonatal morbidityand mortality, especially amongpreterm infants. In a systematicreview of 18 randomized controlledtrials (RCTs), DCC (defined as $30seconds) reduced the risk ofmortality by 32% in preterminfants.3 RCTs revealed that DCCreduced the risks of intraventricularhemorrhage (IVH), necrotizingenterocolitis, and sepsis amongpreterm infants; reduced the needfor blood transfusions andrespiratory support; improved ironstores at 3 to 6 months; andimproved neurodevelopmentaloutcomes at 2 years.3–6

In a systematic review of 7 RCTs,UCM reduced the risks of IVH andoxygen requirement and improvedhemoglobin levels among preterminfants.7 However, a recent large RCTraised concerns about the risks of IVHwith UCM.8

DCC is a simple and inexpensivepractice,9,10 yet many healthproviders are reluctant to deferclamping.11,12 In California, at least42% of preterm infants (gestationalage ,32 weeks or birth weight,1500 g) admitted to neonatalintensive care in 2016 did not receiveDCC.13 In Canada, 40% of preterminfants and 53% of extremelypreterm infants admitted to a NICU in2018 did not receive DCC.14 This maybe, in part, because of the persistenceof custom, lack of awareness orconfidence in evidence, andconflicting or vague guidelines.15 Toaddress the latter three issues, wesystematically described the clinical

guidance on placental transfusionto identify gaps in guidance,concordance with evidence availableat the time (including benefits forpreterm mortality),3 andrecommendation quality.

METHODS

We conducted this systematic review(PROSPERO identifierCRD42019143332) according toavailable methodological guidance onconducting a systematic review ofguidelines.16,17

Data Sources

We searched the following 10academic and guideline databasesfrom January 1, 2010, to July 17, 2019(Supplemental Table 2): OvidMedline, Ovid Embase, CumulativeIndex to Nursing and Allied HealthLiterature, Cochrane Central Registerof Controlled Trials, Web of Science,Clinical Practice Guideline (CPG)Infobase, Guidelines InternationalNetwork, National Institute for Healthand Care Excellence (NICE) Evidence,Royal College of Obstetricians andGynaecologists Guidance, and TripMedical Database. We hand searchedthe Web sites of members of theInternational Federation ofGynaecology and Obstetrics that hadWeb sites with recommendationstatements (Supplemental Table 3).

Inclusion Criteria

With no language restrictions, weincluded the most recent versions ofCPGs and other recommendationstatements published after 2010 thatprovide at least 1 recommendation onDCC or UCM among preterm orterm infants. On the basis of thedefinition provided by the Instituteof Medicine, we defined CPGs asstatements developed by a dedicatedmultidisciplinary panel, after a thoroughreview of the evidence, to optimizepatient and practitioner decisions.18 Wealso reported on other statements thatcould not be described as CPGs (positionstatements and consensus statements) in

order to comprehensively summarize allrecommendations that inform healthproviders’ cord management practices.

Data Extraction

Two reviewers (S.K.L. and K.N.)independently screened the titles andabstracts and full texts. Data fromincluded full texts regarding guidelineauthorship, guideline developmentmethodology, DCC and UCMrecommendations, and sourcesof evidence supporting therecommendations were abstractedby using a piloted data extractionform. Discrepancies were discussedbetween reviewers to reachconsensus, and a third reviewer(S.D.M) was consulted, as necessary.

Quality Assessment

Two reviewers independentlyappraised the quality of includedstatements using the modifiedAppraisal of Guidelines for Researchand Evaluation II (AGREE II)instrument (Supplemental Table 4).19

AGREE II was modified to onlyinclude 3 of the 6 domains (scope andpurpose, clarity of presentation, andeditorial independence). Theremaining 3 domains (stakeholderinvolvement, rigor of development,and applicability) were removed for 3key reasons. First, only 3 domainswere scored so that the AGREE IIappraisal highlights the quality ofcord management recommendationsspecifically (rather than the quality ofrecommendations on other topics aswell), thus more accurately reflectingour research topic. Second, wewanted to prevent bias towardassessing the few guidelinesdedicated to cord management ashigher quality than the majority ofguidelines, which had a broader ordifferent focus (eg, preterm labor)and, thus, less comprehensiverecommendations on cordmanagement. Finally, because thereviewers were not experienced in alltopics addressed by the guidelines(eg, neonatal resuscitation), wewanted to avoid arbitrary scoring

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of areas in which we lackedknowledge.

The clinical credibility andimplementability of the relevantrecommendations on cordmanagement were appraised by usingAppraisal of Guidelines for Researchand Evaluation RecommendationExcellence (AGREE-REX)(Supplemental Table 4), whichcomprises 3 domains (clinicalapplicability, values and preferences,and implementability).20 We alsoapplied AGREE II and AGREE-REX toposition papers and consensusstatements. Although it is important tonote that these statements willinherently receive lower-qualityassessments because they do notfollow the rigorous CPG developmentmethodology that Appraisal ofGuidelines for Research and Evaluation(AGREE) is designed to assess, wewanted to appraise all statements usinga consistent framework.

AGREE advises users to determinetheir own thresholds to interpretscores according to the context oftheir study. Hence, in line witha number of other systematic reviewsof CPGs,21,22 we considered domainscores $50% to be consistent withhigher quality and domain scores,50% to be consistent with lowerquality. Because different domainswere not equally relevant in ourstudy, we did not pool togetherdomain scores, and instead wereported individual domain scores.

Data Analysis

We calculated the proportion ofstatements that recommended DCCand UCM for preterm or term infants.We reported on the details of therecommendations and theirconcordance with the highest level ofevidence available at the time ofpublication regarding the mortalitybenefit of DCC among preterm infantsbecause we hypothesized thatphysicians would be more likely toemploy DCC if it is supported by thistype of evidence.

RESULTS

The searches retrieved 4765 records(Fig 1). After excluding 1540duplicates, we screened 3225 titlesand abstracts and selected 311records for full-text screening. Beforeresolving discrepancies, the reviewershad 97% agreement for inclusion andexclusion of full texts. We included 44statements,23–66 of which 24 met thecriteria for a CPG because they weredeveloped by a dedicated national orinternational panel after a systematicsearch and synthesis of the evidenceto inform practitioner and patientdecisions.18 Twenty statements were

described as position papers orconsensus statements or could not beconfirmed to be a CPG because ofa lack of detail on guidelinedevelopment methodology or lack ofa comprehensive evidence search(Supplemental Table 5). The includedstatements represented the views of35 national and internationalprofessional societies, commonly inthe fields of obstetrics, midwifery,neonatology, pediatrics, andresuscitation. Statements addresseda global audience but predominantlyhigh-income countries: 33 of 44addressed 17 different high-income

FIGURE 1Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram ofa systematic review of CPGs and other recommendation statements on DCC and UCM. The flow ofstudies is summarized through the following stages in the systematic review: database searching,title and abstract screening, and full-text screening.

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countries, 4 specifically addressedEurope, 5 addressed 5 differentmiddle-income countries, and 3 hada global focus (Fig 2). The availableclinical guidelines on DCC and UCMare summarized in Figure 3 anddescribed in detail below.

Quality of Statements

Detailed and summarized AGREE IIand AGREE-REX scores are listed inSupplemental Table 4 and Figure 2,respectively. On the modifiedAGREE II instrument to assessmethodologic rigor, 18 of the 44

(41%) statements had high qualityin all 3 domains (scope andpurpose, clarity of presentation, andeditorial independence). On theAGREE-REX instrument to assess thequality of recommendations, 11statements (25%) were high qualityin all 3 domains (clinical applicability,values and preferences, andimplementability). Eight statements(18%) had high quality in alldomains of AGREE II and AGREE-REX,with statements by NICE32 and theWorld Health Organization

(WHO)41 having the highest scoresoverall.

On AGREE-REX, clinical applicabilityis used to assess the quality of theevidence review and applicability toclinicians and patients: 31 statementsscored high quality in this domain.Values and preferences was theweakest domain overall (only 11statements scoring high quality); it isused to assess efforts taken to makerecommendations and outcomesimportant to clinicians, patients, andpolicy- and decision-makers.

FIGURE 2Characteristics of Included CPG and Other Recommendation Statements on DCC and Cord Milking. The hourglass represents DCC. The scissors representUCM. AMTSL, active management of the third stage of labor; BW, birth weight; CD, cesarean delivery; CENTRAL, Central Register of Controlled Trials; CINAHL,Cumulative Index to Nursing and Allied Health Literature; ERC, European Resuscitation Council; GA, gestational age; ILCOR, International Liaison Committeeon Resuscitation; RDS, respiratory distress syndrome; SOGC, Society of Obstetricians and Gynaecologists of Canada; VD, vaginal delivery; VLBW, very lowbirth weight; red x, not recommended; green checkmark, recommended. aEach guideline also supplemented the literature searches with expert opinion,which includes clinicians within the guideline development group or external experts. bThe modified AGREE II domains (D) are as follows: D1, scope andpurpose; D4, clarity of presentation; and D6, editorial independence. The AGREE-REX domains are as follows: D1, clinical applicability; D2, values andpreferences; and D3, implementability. Green circles indicate high quality (domain score $50%), and red circles indicate low quality (domain score,50%). cMembers of the ILCOR include the American Heart Association, the European Resuscitation Council, the Heart and Stroke Foundation of Canada,the Australian and New Zealand Committee on Resuscitation, the Australian Resuscitation Council, the New Zealand Resuscitation Council, the Re-suscitation Councils of Southern Africa, the InterAmerican Heart Foundation, and the Resuscitation Council of Asia.

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Recommendations on DCC

Summary of DCC Recommendations

Forty-four statements containeda total of 70 recommendations onDCC for subpopulations(Supplemental Fig 5); 24recommendations were specific topreterm infants, with 3 for extremelypreterm infants (#28 weeks),29,33,62

and 3 addressing extremely pretermand moderately preterminfants.23,30,55 Thirty-one applied toboth preterm and term infants, and15 applied only to term infants (.37weeks). Two recommendations werespecific for multiple gestations.23,24

Three statements identifiedmonochorionic twins or multiples asa contraindication to DCC.23,31,34

Recommendations on DCC providedby CPGs are summarized in Figure 4,whereas those provided by non-CPGsare summarized in Supplemental Fig 6.

Three recommendations did notexplicitly endorse DCC in certaininstances. First, a committee opinion bythe American College of Obstetriciansand Gynecologists (ACOG) Committeeon Obstetric Practice stated that thereis insufficient evidence to recommendfor or against DCC in multiplegestations.24 Second, a CPG by theSociety of Obstetricians andGynaecologists of Canada stated that interm infants, the benefits of DCC mustbe balanced with the risks of neonataljaundice requiring phototherapy.43

Finally, a CPG by the Italian Task Force

for the Management of Umbilical CordClamping recommended immediateclamping in directed cord bloodcollection for at-risk families.23

Regarding mode of delivery, 3recommendations on preterminfants,23,57 3 on term infants,23,25,57

and 1 on both preterm or terminfants provided recommendationsspecific to DCC after cesareandelivery (CD).57

Optimal Timing To Defer Clamping

Fifty-one of 67 (76%)recommendations endorsing DCCmade a recommendation regardingthe optimal duration to deferclamping (Fig 4, Supplemental Fig 5).The shortest evidence-based

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durations included 30 to 60 secondsin preterm infants, 30 to 60 secondsin term infants, and #30 seconds inpreterm and term infants. The longestevidence-based durations included 30to 180 seconds in preterm infants,until cord pulsation ceases in terminfants, and $60 seconds in pretermand term infants. The most commonlyrecommended lower limit of optimalduration was at least a minute (20recommendations), whereas 10recommendations suggested anupper limit of at most a minute.

Among the 51 recommendations thatincluded an optimal timing, wereviewed the sources of evidence thatthe authors cited to support thesuggested time (Supplemental Fig 5).For 11 timings (22%), a source ofevidence was not cited. In 25 (50%),primary studies or systematicreviews were cited. In 6 (12%), theauthors cited other guidelines ratherthan primary research. For theremaining 9 (18%) recommendedtimings, the authors did cite evidence

to support the recommendation;however, there was a mismatchbetween either the upper or lowerlimit of the durations recommendedin the evidence sources and thedurations recommended in thestatements. Hence, we could notconfidently determine if and howthese recommendations wereinformed by the cited evidence,expert opinion, and authors’consensus decisions (SupplementalTable 6).

Contraindications to DCC

Common maternal and infantcontraindications to DCC includedsignificant maternal bleeding andunstable maternal conditions (6statements), the need for immediateneonatal resuscitation (29statements), an infant heart rate ,60beats per minute (2 statements),and suspected fetal asphyxia (1statement). Common uteroplacentalcontraindications included concernsabout the integrity of the cord

and placental circulation andplacental abruption or previa (7statements).

Recommendations on UCM

The 23 recommendations on UCM in20 statements were more cautiousand less detailed than those on DCC(Supplemental Table 7). Fifteenrecommendations suggested thatUCM may be considered when DCC isinfeasible and when there issignificant maternal bleeding, whenthere is a need for immediateneonatal support, or in emergencysituations. Only 4 recommendationsprovided suggestions on the numbersof times to milk the cord, rangingfrom 2 to 5 times. Thirteenstatements discouraged the routineuse of UCM because of insufficientevidence of its benefits and harms.

Concordance With Evidence on theMortality Benefit of Umbilical CordManagement

Given our hypothesis that clinicianswould be more likely to change

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practice on the basis of evidencerevealing benefit in compellingoutcomes, such as reductions in infantdeath, we examined the number ofstatements that used mortality data tojustify DCC. Among the 39 statementsthat provided recommendationsrelevant to preterm infants(recommendations for preterm orboth preterm and term infants), only 3(8% of statements) reporteda mortality benefit of DCC for preterminfants. Guidelines by the Italian TaskForce for the Management of UmbilicalCord Clamping23 and the EuropeanSociety for Paediatric Research56 bothreported the findings of the systematicreview by Fogarty et al,3 which foundthat DCC (mainly $60 seconds)significantly reduced hospitalmortality in preterm infants comparedwith immediate cord clamping.Additionally, the 2016 guideline by theConfalonieri Ragonese Foundation31

cited the results of a systematic reviewby Backes et al,67 which found thatDCC and UCM reduced mortalityamong preterm infants ,32 weeks’gestation (relative risk 0.42; 95%confidence interval 0.19–0.95).

In concordance with meta-analyticevidence, a mortality benefit forpreterm infants was reported in noneof the statements that providedrecommendations on UCM.7,68,69

DISCUSSION

In this systematic review, we included24 CPGs and 20 other statements,which together contained 70recommendations on DCC and 23recommendations on UCM for pretermand term infants. There was significantvariation between statements on thespecific details of performing DCC andUCM, despite all endorsing placentaltransfusion. Statements frequentlyfailed to cite the most compellingevidence of reductions in mortality inpreterm infants.

Strengths and Limitations

Motivated by the clinical goal ofimproving DCC rates by improvingguideline quality,15 wecomprehensively searched in multipleacademic and gray literature sourceswithout language or countryrestrictions. We included CPGs,consensus statements, and positionpapers; hence, we synthesized allretrieved recommendations that mayshape health providers’ practices. Inaddition, we reviewed theconcordance of recommendationswith cited evidence regarding theduration of DCC and the availability ofhigh-quality evidence on themortality benefits of placentaltransfusion for preterm infants.Finally, we used a modified AGREE II

and the AGREE-REX to appraise themethodologic quality andapplicability of all recommendations.

Our study also has limitations. First,given that using guidelines as thestudy type is relatively new in theworld of systematic reviews (althoughincreasing22,70), there is a lack of toolsto inform study design and execution.To mediate this limitation, we closelyfollowed methodologic guidance forsystematic reviews of CPGs byJohnston et al17 and referred topublished systematic reviews of CPGs.Second, we could not ascertain thelevel of authority possessed by eachauthoring organization, which wouldallow us to comment on the degree towhich particular recommendationsinfluence practitioners. Third, forfeasibility, we used Google Translate tointerpret guidelines not written inEnglish, when local translation wasnot available, for the followinglanguages: Estonian, French, German,Italian, Japanese, Romanian, andSpanish. Finally, because our searchstrategy was designed to captureguidelines that mention termsdescribing placental transfusion, weare unable to calculate the proportionof all perinatal guidelines thatcomment on cord management.

Interpretation of Findings

CPGs and other recommendationstatements published within the pastdecade agree that DCC should beoffered to stable preterm and terminfants. Furthermore, severalguidelines on preventing postpartumhemorrhage included DCC asa component of the activemanagement of the third stage oflabor, in line with evidence that DCCdoes not increase the risk of severepostpartum hemorrhage at term.71

There is significant heterogeneityamong recommendations about themethods of performing DCC,especially regarding the timing ofcord clamping. Indeed, even recentsystematic reviews and meta-analyses among preterm infants

FIGURE 3Summary of recommendations on DCC and cord milking in included statements. The proportions ofrecommendations on DCC (including the recommended optimal durations to defer clamping) andUCM are summarized.

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suggest deferring $30 seconds72 or$60 seconds3 but do not suggest anupper limit at which time to clampthe cord. One reason for this may bethat because most preterm infantsrequire early support, an optimaltime to clamp the cord has not yetbeen established. We identified a fewstatements recommending clampingthe cord at times that are not yetverified by robust evidence (eg,5 minutes, after delivery of theplacenta). To maximize the benefitsof DCC and prevent adverse effects,recommended durations shouldreflect high-quality evidence.

Nearly two-thirds of the statementsexclude nonvigorous infants whorequire immediate neonatal

resuscitation from receiving DCC inorder to move the infant away from themother to perform resuscitation.Unfortunately, this means that thesickest infants, who might benefit fromDCC the most, are excluded from thisintervention. Innovative technologicalsolutions that may address this issue arebeing studied: prototypes of mobiletrolleys that allow neonatal resuscitationto be performed with an intact cordhave revealed safety, feasibility, andacceptability among health providers(eg, Bedside Assessment, Stabilizationand Initial Cardiorespiratory Support,LifeStart).73,74 If proven to be beneficial,bringing resuscitation to the mother’sbedside will require changes to hospitalpolicy and ergonomics and collaborationbetween care providers, including

pediatricians, obstetricians, andmidwives.75

Beyond DCC, UCM is a potentialsimple alternative that can allowplacental transfusion to be quicklyperformed in infants who needimmediate resuscitation.69,75

Statements recommended UCM lessfrequently compared with DCC.Because milking disrupts the normalfetoplacental circulation to increaseblood flow to the infant more rapidlythan DCC, there are concerns thatUCM may have adverse effects.76

Guidelines echoed the need for moreresearch on UCM, some of which hasrecently emerged. A trial by Katheriaet al8 was prematurely terminatedbecause of concerns about severe IVH

FIGURE 4Recommendations on DCC by Included CPGs. AMTSL, active management of the third stage of labor; BW, birth weight; CD, cesarean delivery; CHD,congenital heart disease; GA, gestational age; I, infant contraindications; ILCOR, International Liaison Committee on Resuscitation; M, maternal contra-indications; PMTSL, physiologic management of the third stage of labor; PPH, postpartum hemorrhage; SOGC, Society of Obstetricians and Gynaecologistsof Canada; UP, uteroplacental contraindications; clock symbol, the recommended optimal timing for DCC. aThe statement by the Royal College ofMidwives58 includes a technical manual, which could not be found online. We inferred that it is a CPG using the summary of guideline methodologyprovided in the main guideline document. bThis statement is a compilation of 2 other WHO statements.41,46

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in infants born at 23 to 276 weeks’gestation who received UCM. In theirsystematic review, Balasubramanianet al69 also found significantlyincreased risk of severe IVH (grades 3or higher) among preterm infants,34 weeks who received UCMcompared with DCC in 4 RCTs.Importantly, the RCT by Katheriaet al,8 which was the only includedtrial that found significantly increasedrisk, contributed nearly half thesample size of the UCM versus DCCcomparison in this systematicreview.69 Ongoing trials amonginfants of older gestational ages andfollow-up studies on long-termneurodevelopmental outcomes willbe important to support futurerecommendations on UCM.77,78

Additionally, high-quality evidence onvarious cord milking techniques (eg,the number of milkings, speed ofmilking, and position of the infant)and studies on the outcomes of cordmilking among infants needingresuscitation are needed.

Increased granularity ofrecommendations may improvehealth providers’ ability andconfidence in performing DCC. Only 4statements were dedicated to DCC; allothers embedded recommendationsabout DCC within broader topics.Guidelines focused on cordmanagement would allow for specificrecommendations for subpopulations(eg, various preterm gestational ages,modes of delivery). Further guidanceis required on the position to hold the

infant, the sequence of administrationof uterotonic medications,temperature control, and otherdetails. Additionally, DCC’s life-savingbenefits to extremely preterm andpreterm infants3 should be noted asthe basis of recommendations.

The language we use to discuss DCCmay also encourage its practice andassist patients in understanding it asbeing a positive rather thana negative intervention. Among the33 English-language statements, only1 used the term “deferred cordclamping”51; all others referred to“delayed” or “late” cord clamping,which connote negativity and thatimmediate cord clamping is thenorm.12 Hence, we recommend that

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future guidelines and studies use themore neutral term, “deferred.”

Although many professional societiesadvocate DCC for preterm and terminfants, improved clarity and granularitycan improve the quality of guidance onthis issue. In this systematic review, wefound that guidelines representingdifferent professions within the samecountry provided differentrecommendations. For example,although the ACOG recommendeddeferring clamping for at least 30 to 60seconds for term infants,24 theAmerican College of Nurse-Midwivesrecommended deferring for up to5 minutes for vaginally delivered terminfants positioned skin to skin.25 Beforeits closure in 2018, the NationalGuideline Clearinghouse, an initiative ofthe US Department of Health andHuman Services, allowed healthproviders to succinctly synthesize andcompare guidelines on topics of interestto identify recommendations that aremost suitable to their clinical setting andpopulation. Our study provides thisknowledge synthesis with themethodologic rigor of a systematic

review and with quality appraisalof guidelines and recommendations. Theabundance and heterogeneityof guidelines on placental transfusionemphasize the need for an updatedresource for health providersthat compiles and compares the contentand quality of relevant statements.

To improve rates of DCC for infantsborn worldwide, strong guidelinesshould be amenable to adoption ineveryday clinical settings. Among ourincluded CPGs and otherrecommendation documents, 42%satisfactorily (domain score $50%)met the criteria within the AGREE-REXdomain of implementability, which isused to assess the suitability of therecommendations for local adoption.20

In their systematic review of 18 studiesconducted in high- and middle-incomecountries, Anton et al79 describebarriers to implementing placentaltransfusion in hospital settings. Generalchallenges included staff unawarenessand resistance to change, andpediatrician-specific concerns includeduncertainty about the role of placentaltransfusion when neonatal

resuscitation is needed and concernsabout potential adverse outcomes, suchas jaundice.79 Strategies to overcomebarriers to implementation includededucation, creating protocols, auditing,providing constructive feedback, andimproving multidisciplinarycollaboration.79 For example, the CPGby NICE provides a modifiable clinicalauditing tool for the third stage oflabor.51 Additionally, joint guidelines byobstetrical and pediatric care providersand establishing of opportunities formultidisciplinary communication, suchas a predelivery surgical pause andteam debriefing, may facilitateimproved rates of DCC. Beyondrevealing the evidence-informed natureof DCC, efforts to address resistance tochange and make DCC acceptable topolicy-makers, health workers, andfamilies will improve the rates of itsadoption to practice.26 Although wefound no country-specificrecommendation statements producedin low-income countries, the WHOpromotes the integration of DCC tonational childbirth and postnatal careprogramming worldwide by employingstrategies such as culturally

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appropriate education on DCC, linkingof implementation with otherinterventions (eg, improving women’shealth literacy), and robust monitoringand evaluation.26

Birth brings together manydisciplines; it is thus important thatorganizations guiding variousdisciplines are unified in theirmessages and use the current bestevidence to provide detailed,comprehensive, and locally applicablerecommendations so that change atthe level of the birth can beimplemented in a collaborative andsustainable way.10

CONCLUSIONS

In our systematic review of 44 CPGsand other recommendationstatements, we found that professionalmaternal and infant health societiesendorsed DCC to prevent neonatal

morbidity and mortality among stablepreterm and term infants. Only halfthe recommendations on the optionalduration of DCC were supported byprimary research or systematic reviewevidence, and in only 8% ofstatements was a mortality benefitof DCC for preterm infants reported.The current implementation of DCCmay be increased with the provision ofmore unified, detailed, and evidence-based guidance on cord management.

ACKNOWLEDGMENTS

We thank Ms Kaitlin Fuller, liaison andeducation librarian at Gerstein ScienceInformation Centre, University ofToronto, for her assistance indeveloping the search strategies. Wevalue the contributions of Ms RifaaFatima Ali and Ms Angel Gao in theadministrative aspects of the study.

ABBREVIATIONS

ACOG: American College of Obste-tricians and Gynecologists

AGREE: Appraisal of Guidelines forResearch and Evaluation

AGREE II: Appraisal of Guidelinesfor Research andEvaluation II

AGREE-REX: Appraisal of Guide-lines for Researchand EvaluationRecommendationExcellence

CD: cesarean deliveryCPG: clinical practice guidelineDCC: deferred cord clampingIVH: intraventricular hemorrhageNICE: National Institute for Health

and Care ExcellenceRCT: randomized controlled trialUCM: umbilical cord milkingWHO: World Health Organization

DOI: https://doi.org/10.1542/peds.2020-1429

Accepted for publication Jul 17, 2020

Address correspondence to Sarah D. McDonald, MD, MSc, Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology and Departments of

Radiology and Health Research Methods, Evidence, and Impact, McMaster University, 1280 Main St West, Room 3N52G, Hamilton, ON, Canada L8S 4L8.

E-mail: mcdonals@mcmaster.ca

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2020 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: Dr McDonald is supported by a Canadian Institutes of Health Research Tier II Canada Research Chair sponsor award (950-229920). The

Canadian Institutes of Health Research had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data;

preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication; and Ms Liyanage and Mr Ninan have indicated they have

no financial relationships relevant to this article to disclose.

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have no conflicts of interest relevant to this article to disclose.

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DOI: 10.1542/peds.2020-1429 originally published online October 21, 2020; 2020;146;Pediatrics

Sugee Korale Liyanage, Kiran Ninan and Sarah D. McDonaldGuidelines on Deferred Cord Clamping and Cord Milking: A Systematic Review

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DOI: 10.1542/peds.2020-1429 originally published online October 21, 2020; 2020;146;Pediatrics

Sugee Korale Liyanage, Kiran Ninan and Sarah D. McDonaldGuidelines on Deferred Cord Clamping and Cord Milking: A Systematic Review

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