http://informahealthcare.com/jmf ISSN: 1476-7058 (print), 1476-4954 (electronic) J Matern Fetal Neonatal Med, 2014; 27(14): 1457–1461 ! 2014 Informa UK Ltd. DOI: 10.3109/14767058.2013.864275
ORIGINAL ARTICLE
Obstetricians’ attitudes and beliefs regarding umbilical cord clamping Angie C. Jelin1, Miriam Kuppermann1, Kristine Erickson2,3, Ronald Clyman4, and Jay Schulkin2
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1
Department of Obstetrics, Gynecology and Reproductive Sciences, University of California, San Francisco, CA, USA, 2American College of Obstetrics and Gynecologists, Washington, DC, USA, 3Department of Psychology, American University, Washington, DC, USA, and 4Department of Pediatrics, University of California, San Francisco, CA, USA Abstract
Keywords
Objective: Although delayed umbilical cord clamping has been demonstrated to reduce the incidence of intraventricular hemorrhage and neonatal sepsis, and decrease the need for neonatal transfusions (without affecting cord pH, Apgar scores or the need for phototherapy), the extent to which this practice is being employed is unknown. We conducted a survey of US obstetricians to assess their attitudes and beliefs about cord clamping. Study design: Questionnaires were randomly mailed to members of the American College of Obstetricians and Gynecologists (ACOG), and the Collaborative Ambulatory Research Network (CARN). The data were analyzed using Chi-square and Student t tests. Results: The response rates for the CARN and other ACOG members were 47% and 21%, respectively. Most (88%) responders reported their hospital had no umbilical cord clamping policy. The most frequent response for optimal timing of umbilical cord clamping, regardless of gestational age, was ‘‘don’t know’’. Potential for neonatal red blood cell transfusion was the only concern cited as a reason for being somewhat or very inclined to delay umbilical cord clamping (51%). Delayed neonatal resuscitation (76%) was listed as a reason to clamp the cord immediately, despite the paucity of literature to support immediate cord clamping in this cohort. Conclusion: Despite substantial evidence supporting the practice of delayed cord clamping, few institutions have policies regarding this practice. Moreover, obstetricians’ beliefs about the appropriate timing for umbilical cord clamping are not consistent with the evidence that demonstrates its beneficial impact on neonatal outcomes.
Delayed clamping, opinion, preterm, survey, term
Introduction Umbilical cord clamping is a procedure performed at every delivery. Redistribution of the blood in the infant-placental circuit occurs after birth, and the volemic state of the neonate is partially dependent upon when the umbilical cord is clamped [1]. Although immediate cord clamping is the norm for obstetricians in this country [2], physiological studies [3–6] and multiple RCTs suggest there are benefits to delaying umbilical cord clamping in both preterm [7–9] and term infants [10]. The amount of time considered to constitute a ‘‘delay’’ in umbilical cord clamping differs in preterm and term neonates. In preterm neonates, several studies have demonstrated decreases in intraventricular hemorrhage and need for neonatal transfusion when comparing a delay of 30–120 s, or milking of the umbilical cord, to immediate cord clamping
Address for correspondence: Angie C. Jelin, MD, Department of Obstetrics and Gynecology, University of California, San Francisco, 505 Parnassus Avenue, Box 0132, San Francisco, CA 94143, USA. Tel: 415-624-5206; 415-443-5638. Fax: 415-476-9305. E-mail: [email protected]
History Received 11 June 2013 Revised 28 October 2013 Accepted 6 November 2013 Published online 11 December 2013
[7–9,11–15]. Among full term infants, a delay of 3–5 min, or until cessation of pulsation of the cord, is associated with higher ferritin concentrations and less iron deficiency at 4 months of age [10,16]. Despite these known benefits of delayed clamping, there is still controversy in regard to the optimal timing of umbilical cord clamping in term and preterm infants. We sought to determine the extent to which obstetricians believe delayed cord clamping should be practiced and whether their attitudes toward this practice are reflective of the extensive body of literature.
Methods We developed a survey to assess obstetrician attitudes and beliefs about the optimal timing of umbilical cord clamping (see Appendix). To assess the respondents’ general views on the timing of cord clamping, we asked ‘‘How important do you think the time of umbilical cord clamping is on neonatal outcomes at the following gestational ages?’’ Gestational ages included 528 weeks, 28–31 weeks, 32–36 weeks and 436 weeks; response options included: (1) very important, (2) moderately important, (3) somewhat important, (4) not important at all, and (5) ‘‘I don’t know’’.
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We also asked what the responded thought the timing of cord clamping should be for each of the gestational ages listed above; in this case the response options included: (1) immediately, no milking; (2) immediately after milking, (3) 10–30 s; (4) 31–60 s; (5) 460 s; and (6) ‘‘I don’t know’’. Next the participants were asked to indicate the extent to which they agreed or disagreed with four statements (‘‘Cord clamping should not be delayed’’: (1) ‘‘if immediate resuscitation is indicated’’; (2) ‘‘in cases with placental abruption’’; (3) ‘‘in infants with placenta previa’’ and (4) ‘‘Umbilical cord milking can be used in place of delayed cord clamping’’). The response options for these items ranged from 1 to 5 with 1 ¼ strongly/mostly disagree to 5 ¼ strongly/ mostly agree. Finally, the respondents were asked to indicate the extent to which each of several different morbidities (maternal hemorrhage; neonatal hyperbilirubinemia, hypothermia, volume overload, delay in resuscitation, polycythemia, intraventricular hemorrhage, need for red blood cell transfusion and late onset sepsis) affected their cord clamping practices or recommendations. For these, the response options ranged from 1 ¼ ‘‘makes me very inclined to delay’’ to 5 ¼ ‘‘makes me very inclined to clamp immediately’’. After obtaining approval from the Institutional Review Board at the University of California, San Francisco (UCSF), we sent the survey to a random sample of 600 members of the American College of Obstetricians and Gynecologists (ACOG), including a random sample of 200 members of the College’s Collaborative Ambulatory Research (CARN). The CARN network is the only existing national collective of 1600 board-certified obstetricians–gynecologists who practice in a variety of ambulatory care settings throughout the United States and have been recruited to participate in survey studies. An initial mailing included the survey, a cover letter and a postage paid return envelope. Four subsequent mailings were sent to non-respondents. After compiling the initial responses, a follow-up post card was sent to non-respondents that included two of the original survey questions and demographic information to allow for comparison of ‘‘nonrespondents’’ to ‘‘respondents’’. All data were collected prior to the publication of the 2012 ACOG Committee Opinion on delayed cord clamping [17]. We used SPSS to analyze the data. Chi-square was used for inferential analysis and parametric data were compared using t tests. A Friedman test was used to evaluate the importance of timing. Post-hoc Dunn’ multiple comparisons test was then utilized to compare the responses about the importance of timing of umbilical cord clamping in term and preterm infants. Alpha level was set at p50.05.
J Matern Fetal Neonatal Med, 2014; 27(14): 1457–1461
All of the respondents were actively practicing obstetrics, and 2.8% reported being maternal fetal medicine specialists. Fifty-three percent of the respondents were male, 47% were female. The majority (79.5%) were White non-Hispanic, while 10.2% were Asian, 4.5% were White Hispanic, and the rest were African-American (1.7%) or Native American/Alaskan native (2.8%). Over half (61.4%) practiced in a group setting. Only 3.5% reported that their hospital had a delayed clamping policy. Is timing of umbilical cord clamping important? Physicians differed in their ratings of the importance of timing of umbilical cord clamping at different gestational ages. In general, respondents were more likely to rate the timing of umbilical cord clamping as ‘‘very important’’ for infants528 weeks, with a tendency towards rating the time of clamping as less important with increasing gestational age (Table 1). The most common response to a question about the importance of timing for infants 436 weeks’ gestation was ‘‘somewhat important’’. What is the optimal cord clamping time? Significant differences between responses to the item asking about the optimal timing for clamping for preterm versus term infants also emerged. For example, although the most frequent physician response was ‘‘don’t know’’ regardless of gestational age (42–55%), for infants 528 weeks’ gestation the second highest response was ‘‘immediately after milking’’ (19.9%) and for infants436 weeks’ gestation the second most common response was 460 s (20.9%; Table 2). How do potential morbidities affect your recommended cord clamping time? The survey respondents were asked to rate, on a five-point scale ranging from ‘‘makes me very inclined to delay’’ to ‘‘makes me very inclined to clamp immediately’’, the extent to which potential morbidities affected their umbilical cord clamping practices in preterm infants. Only three potential Table 1. How important is timing of cord clamping at birth?
Very important Moderately important Somewhat important Not important Don’t know
528 GA n%
28–31 GA n%
32–36 GA n%
436 GA n%
52 41 21 18 44
45 48 26 15 42
25 52 42 17 40
12 32 53 45 34
(29.5) (23.3) (11.9) (10.2) (25.0)
(25.6) (27.3) (14.8) (8.5) (23.9)
(14.2) (29.5) (23.9) (9.7) (27.7)
(6.8) (18.2) (30.1) (25.6) (19.3)
Bold values signify the highest percentage. Table 2. When should cord clamping be performed?
Results Ninety-three CARN members and 83 other ACOG members returned the completed survey, for response rates of 46.5% and 20.8%, respectively. There were no significant differences in the sociodemographic characteristics or responses provided by CARN versus non-CARN respondents. In addition, no significant differences emerged between respondents and non-respondents in gender, age or responses to the two survey questions included in the follow-up letter to non-respondents.
528 GA 28–31 GA 32–36 GA 436 GA n% n% n% n% Don’t know Immediately, no milking Immediately after milking 10–30 s 31–60 s 460 s
55 16 34 17 23 26
(32.2) (9.4) (19.9) (9.9) (13.5) (15.2)
50 14 32 23 22 30
(29.2) (8.2) (18.7) (13.5) (12.9) (17.5)
Bold values signify the highest percentage.
53 17 20 31 25 26
(30.8) (9.9) (11.6) (18.0) (14.5) (15.1)
42 28 16 23 27 36
(24.4) (16.3) (9.3) (13.4) (15.7) (20.9)
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Table 3. Do comorbidities affect timing of cord clamping in preterm infants?
Maternal hemorrhage Hyper-bilirubinemia Hypothermia Volume overload Delay in resuscitation Polycythemia IVH Need for red blood cell transfusion Late onset sepsis
Very inclined to delay n(%)
Somewhat inclined to delay n(%)
Has no effect on my practice n(%)
Somewhat inclined to clamp immediately n(%)
6 (3.6) 6 (3.6) 5 (3.0) 4 (2.4) 2 (1.2) 5 (3.1) 6 (3.8) 44 (27.5)
12 (7.1) 8 (4.8) 7 (4.3) 9 (5.5) 10 (6.2) 6 (3.7) 14 (8.8) 38 (23.8)
30 93 74 84 26 67 92 49
(17.9) (56.4) (45.1) (51.2) (16.1) (41.4) (57.9) (30.6)
35 (20.8) 31 (18.8) 43 (26.2) 36 (21.9) 49 (30.4) 43 (26.5) 21 (13.2) 12 (7.5)
11 (6.9)
18 (11.3)
93 (58.5)
15 (9.4)
Very inclined to clamp immediately n(%) (50.6) (16.4) (21.3) (18.9) (46.0) (25.3) (16.4) (10.6)
2 ¼ 115.6; p50.001 2 ¼ 151.3; p50.001 2 ¼ 98.9; p50.001 2 ¼ 122.9; p50.001 2 ¼ 107.85; p50.001 2 ¼ 87.4; p50.001 2 ¼ 149.6; p50.001 2 ¼ 34.2; p50.001
22 (13.8)
2 ¼ 149.3; p50.001
85 27 35 31 74 41 26 17
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Bold values signify the highest percentage.
comorbidities were reported to have an effect on these physicians’ inclinations. Specifically, half of the respondents (50.6%) were very inclined and 20.8% were somewhat inclined to clamp immediately in the context of potential maternal hemorrhage ( 2 ¼ 115.6; p50.001); 30.4% were somewhat and 46.0% were very inclined to do so for neonatal resuscitation ( 2 ¼ 107.85; p50.001); and 27.5% were very and 23.8% somewhat inclined to delay umbilical cord clamping for potential neonatal red blood cell transfusion ( 2 ¼ 34.2; p50.001) (Table 3). Do comorbidities affect practice if the obstetrician also believes timing is important? We evaluated the effect of comorbidities on the practice of the respondents who indicated that timing was ‘‘very or moderately important’’ versus ‘‘not important’’. The comorbidities that affected their cord clamping practices were dependent on the gestational age they believed the timing of cord clamping was important. Comorbidities which affected practice included a delay in neonatal resuscitation, hypothermia or neonatal transfusion. Obstetricians who indicated clamping was important for infants 532 weeks’ gestation also indicated that a delay in resuscitation was a potential morbidity that would cause them to recommend immediate cord clamping ( 2 ¼ 7.38; p ¼ 0.025). Respondents who reported timing was important at 436 weeks were more likely to practice immediate clamping in preterm infants for potential hypothermia ( 2 ¼ 6.89; p ¼ 0.03) and delay clamping if neonatal transfusion ( 2 ¼ 7.35; p ¼ 0.025) was of potential concern. Do comorbidities affect the opinion of timing if the obstetrician believed clamping should be delayed? We also evaluated the influence of comorbidities on physicians who reported believing in immediate or delayed clamping at 532 and at 436 weeks’ gestation. Respondents who believed cord clamping should be delayed for infants 532 weeks were significantly more inclined to practice immediate cord clamping in preterm infants if there was potential morbidity due to a delay in resuscitation ( 2 ¼ 6.0; p ¼ 0.043), and they also were more likely to practice delayed cord clamping for concern of neonatal transfusion ( 2 ¼ 8.52; p ¼ 0.014). Those who believed immediate cord clamping was important for infants 436 weeks’ gestation also practiced
clamping immediately for a potential delay in resuscitation in preterm infants ( 2 ¼ 11.87; p ¼ 0.003). Do situations affect the recommended time to clamp the cord? In response to a question asking the extent to which they believed cord clamping should not be delayed in certain situations, respondents reported that they strongly or mostly agreed that cord clamping should not be delayed in the following situations: if immediate resuscitation was indicated (69.6%), in cases with placental abruption (52.6%), or in cases of placenta previa (30.6%). When asked whether they agreed that umbilical cord milking should be used instead of delayed cord clamping, 40.4% of respondents reported that they ‘‘somewhat’’ or ‘‘strongly/mostly’’ agreed, 38.6% neither agreed nor disagreed and 21% ‘‘somewhat’’ or ‘‘strongly/ mostly’’ disagreed.
Discussion In this study of obstetricians practicing in the United States, we have shown that the practice of delayed cord clamping in both term and preterm infants has not been widely adopted. Despite the published evidence of the benefits associated with delayed umbilical cord clamping [7–9], only a small minority (3.5%) of the survey respondents reported that their institution had an umbilical cord clamping policy. This is in direct contrast to many European institutions, where delayed cord clamping is standard of care [13], and contrary to a recent ACOG committee opinion recommending delay in umbilical cord clamping (30–60 s) in preterm infants [17]. We also found that obstetricians’ opinions about the appropriate timing of delayed cord clamping and cord milking differed by gestational age. After excluding those who responded ‘‘don’t know’’, the respondents were more likely to believe umbilical cord clamping is important at earlier gestational ages. The majority of obstetricians reported that umbilical cord clamping should be delayed or milked for infants less than 28 weeks’ gestation. We also found that the obstetricians’ opinions about the risks and benefits of delayed cord clamping differed from what we hypothesized. The majority of respondents indicated that they would practice immediate cord clamping for maternal hemorrhage or a delay in neonatal resuscitation, while they would opt for delayed clamping for potential red
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blood cell transfusions in the neonate. Other potential neonatal comorbidities, including hyperbilirubinemia, hypothermia, volume overload, polycythemia, intraventricular hemorrhage or late onset sepsis, were not significantly associated with opinions of the appropriate timing of umbilical cord clamping. Results of our survey suggest that obstetricians who believe delayed cord clamping is important have opinions about the risks and benefits that are inconsistent with the current literature. The only comorbidity demonstrated in randomized controlled trials, which the respondents’ opinions were consistent with, was the practice of delayed cord clamping for potential neonatal transfusion [6,7,13]. While respondents were more likely to practice immediate clamping in the contexts of maternal hemorrhage or delay in neonatal resuscitation, these concerns are not consistent with the results of published randomized studies. The most unexpected finding is that even though there is published evidence of an association between lower risk of neonatal intraventricular hemorrhage and delayed cord clamping, this was not a significant concern of our respondents. We had hypothesized that obstetricians who thought delayed cord clamping was important or that it should be delayed in preterm infants would consider a decrease in intraventricular hemorrhage as an indication to delay; however, this was not found to be true. Despite the evidence regarding the benefits of delayed clamping that has accumulated from multiple randomized controlled trials, obstetricians still differ considerably on their opinions about the appropriate timing of umbilical cord clamping. Some of the concerns obstetricians have are not substantiated by the current evidence. Although additional evidence, such as a multi-centered randomized controlled trial, may be needed to fully address the concerns of some obstetricians, evidence-based educational interventions may be necessary to encourage delayed cord clamping practices.
Declaration of interest The authors report no conflicts of interest. This study was supported in part by the Centers for Disease Control and Prevention and Grant #R60 MC 05674 from the Maternal and Child Health Bureau, Health Resources and
J Matern Fetal Neonatal Med, 2014; 27(14): 1457–1461
Services Administration, Department of Health and Human Services.
References 1. Yao AC, Lind J. Blood flow in the umbilical vessels during the third stage of labor. Biol Neonate 1974;25:186–93. 2. Ononeze ABO, Hutchon DJR. Attitude of obstetricians toward delayed cord clamping: a questionnaire-based study. J Obstet Gynaecol 2009;29:223–4. 3. Polin RA, Fox W. Fetal and neonatal physiology. Philadelphia: W B Saunders; 1998. 4. Pietra, GG, D’Amodio MD, Leventhal MM, et al. Electron microscopy of cutaneous capillaries of newborn infants: effects of placental transfusion. Pediatrics 1968;42:678–83. 5. Windle W. Brain damage by asphyxia at birth. Scientific American 1969;221:76–84. 6. Yao A, Moinian M, Lind J. Distribution of blood between infant and placenta after birth. Lancet 1969;2:871–3. 7. Ibrahim H, Krouskop R, Lewis D, Dhanireddy R. Placental transfusion: umbilical cord clamping and preterm infants. J Perinat 2000;20:351–4. 8. Kinmond S, Aitchison TC, Holland BM, et al. Umbilical cord clamping and preterm infants: a randomised trial. BMJ 1993;306: 172–5. 9. Hofmeyr G, Bolton K, Bowen D, et al. Periventricular/intraventricular haemorrhage and umbilical cord clamping. Findings and hypothesis. S Afr Med J 1988;73:104–6. 10. Andersson O, Hellstrom-Westas L, Andersson D, Domellof M. Effect of delayed versus early umbilical cord clamping on neonatal outcomes and iron status at 4 months: a randomised controlled trial. BMJ 2011;343:d7157. 11. Rabe H, Reynolds G, Diaz-Rossello J. A systemic review and metaanalysis of a brief delay in clamping the umbilical cord of preterm infants. Neonatology 2008;93:138–44. 12. Hofmeyr G, Gobetz L, Bex PJ, et al. Periventricular/intraventricular hemorrhage following early and delayed umbilical cord clamping. A randomized controlled trial. Online J Curr Clin Trials 1993;Doc No.110. 13. Rabe H, Wacker A, Hulskamp G, et al. A randomized controlled trial of delayed cord clamping in very low birth weight preterm infants. Eur J Pediatr 2000;159:775–7. 14. Oh W, Fanaroff AA, Carlo WA, et al.; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Effects of delayed cord clamping in very-low-birth-weight infants. J Perinatol 2011;31:S68–71. 15. Mercer JS, Vohr BR, McGrath MM, et al. Delayed cord clamping in very preterm infants reduces the incidence of intraventricular hemorrhage and late-onset sepsis: a randomized controlled trial. Pediatrics 2006;117:1235–42. 16. Hutton EK, Hassan ES. Late vs early clamping of the umbilical cord in full-term neonates: systematic review and meta-analysis of controlled trials. JAMA 2007;297:1241–52. 17. Committee opinion no. 543: timing of umbilical cord clamping after birth. Obstet Gynecol 2012;120:1522–6.
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Appendix 1. How important do you think the time of umbilical cord clamping is on neonatal outcomes at the following gestational ages?
528 weeks 28–31 weeks 32–36 weeks 436 weeks
Very important
Moderately important
Somewhat important
Not important at all
I don’t know
1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ
9œ 9œ 9œ 9œ
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2. Is there an official policy at your institution/hospital that recommends the appropriate timing for clamping the umbilical cord for infants delivered before 32 weeks gestation? 1œ yes, there is a delayed cord clamping policy 2œ yes, there is an immediate cord clamping policy 3œ no, there is no policy 4œ I don’t know 3. Please indicate what you think the timing of umbilical cord clamping at each of the following gestational ages should be.
528 weeks 28–31 weeks 32–36 weeks 436 weeks
Immediately, no milking
Immediately after milking
10–30 seconds
31–60 seconds
460 seconds
I don’t know
1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ
5œ 5œ 5œ 5œ
9œ 9œ 9œ 9œ
4. Please indicate how much you agree or disagree with the following statements regarding the timing of umbilical cord clamping in preterm infants.
Strongly/mostly disagree
Somewhat disagree
Neither agree nor disagree
Somewhat agree
Strongly/ mostly agree
1œ
2œ
3œ
4œ
5œ
1œ
2œ
3œ
4œ
5œ
1œ 1œ
2œ 2œ
3œ 3œ
4œ 4œ
5œ 5œ
Cord clamping should not be delayed if immediate resuscitation is indicated. Cord clamping should not be delayed in cases with placental abruption. Cord clamping should not be delayed in infants with placenta previa. Umbilical cord milking can be used in place of delayed cord clamping.
5. Please indicate the extent to which each of the following potential morbidities affects your umbilical cord clamping recommendations or practice in preterm infants.
Potential of: Maternal hemorrhage Neonatal: Hyperbilirubinemia Hypothermia Volume overload A delay in resuscitation Polycythemia Intraventricular hemorrhage Need for red blood cell transfusion Late onset sepsis
Makes me very inclined to delay
Makes me somewhat inclined to delay
Has no effect on my practice
Makes me somewhat inclined to clamp immediately
Makes me very inclined to clamp immediately
1œ
2œ
3œ
4œ
5œ
1œ 1œ 1œ 1œ 1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ 2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ 3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ 4œ 4œ 4œ 4œ
5œ 5œ 5œ 5œ 5œ 5œ 5œ 5œ
ORIGINAL ARTICLE
Obstetricians’ attitudes and beliefs regarding umbilical cord clamping Angie C. Jelin1, Miriam Kuppermann1, Kristine Erickson2,3, Ronald Clyman4, and Jay Schulkin2
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by Nyu Medical Center on 05/11/15 For personal use only.
1
Department of Obstetrics, Gynecology and Reproductive Sciences, University of California, San Francisco, CA, USA, 2American College of Obstetrics and Gynecologists, Washington, DC, USA, 3Department of Psychology, American University, Washington, DC, USA, and 4Department of Pediatrics, University of California, San Francisco, CA, USA Abstract
Keywords
Objective: Although delayed umbilical cord clamping has been demonstrated to reduce the incidence of intraventricular hemorrhage and neonatal sepsis, and decrease the need for neonatal transfusions (without affecting cord pH, Apgar scores or the need for phototherapy), the extent to which this practice is being employed is unknown. We conducted a survey of US obstetricians to assess their attitudes and beliefs about cord clamping. Study design: Questionnaires were randomly mailed to members of the American College of Obstetricians and Gynecologists (ACOG), and the Collaborative Ambulatory Research Network (CARN). The data were analyzed using Chi-square and Student t tests. Results: The response rates for the CARN and other ACOG members were 47% and 21%, respectively. Most (88%) responders reported their hospital had no umbilical cord clamping policy. The most frequent response for optimal timing of umbilical cord clamping, regardless of gestational age, was ‘‘don’t know’’. Potential for neonatal red blood cell transfusion was the only concern cited as a reason for being somewhat or very inclined to delay umbilical cord clamping (51%). Delayed neonatal resuscitation (76%) was listed as a reason to clamp the cord immediately, despite the paucity of literature to support immediate cord clamping in this cohort. Conclusion: Despite substantial evidence supporting the practice of delayed cord clamping, few institutions have policies regarding this practice. Moreover, obstetricians’ beliefs about the appropriate timing for umbilical cord clamping are not consistent with the evidence that demonstrates its beneficial impact on neonatal outcomes.
Delayed clamping, opinion, preterm, survey, term
Introduction Umbilical cord clamping is a procedure performed at every delivery. Redistribution of the blood in the infant-placental circuit occurs after birth, and the volemic state of the neonate is partially dependent upon when the umbilical cord is clamped [1]. Although immediate cord clamping is the norm for obstetricians in this country [2], physiological studies [3–6] and multiple RCTs suggest there are benefits to delaying umbilical cord clamping in both preterm [7–9] and term infants [10]. The amount of time considered to constitute a ‘‘delay’’ in umbilical cord clamping differs in preterm and term neonates. In preterm neonates, several studies have demonstrated decreases in intraventricular hemorrhage and need for neonatal transfusion when comparing a delay of 30–120 s, or milking of the umbilical cord, to immediate cord clamping
Address for correspondence: Angie C. Jelin, MD, Department of Obstetrics and Gynecology, University of California, San Francisco, 505 Parnassus Avenue, Box 0132, San Francisco, CA 94143, USA. Tel: 415-624-5206; 415-443-5638. Fax: 415-476-9305. E-mail: [email protected]
History Received 11 June 2013 Revised 28 October 2013 Accepted 6 November 2013 Published online 11 December 2013
[7–9,11–15]. Among full term infants, a delay of 3–5 min, or until cessation of pulsation of the cord, is associated with higher ferritin concentrations and less iron deficiency at 4 months of age [10,16]. Despite these known benefits of delayed clamping, there is still controversy in regard to the optimal timing of umbilical cord clamping in term and preterm infants. We sought to determine the extent to which obstetricians believe delayed cord clamping should be practiced and whether their attitudes toward this practice are reflective of the extensive body of literature.
Methods We developed a survey to assess obstetrician attitudes and beliefs about the optimal timing of umbilical cord clamping (see Appendix). To assess the respondents’ general views on the timing of cord clamping, we asked ‘‘How important do you think the time of umbilical cord clamping is on neonatal outcomes at the following gestational ages?’’ Gestational ages included 528 weeks, 28–31 weeks, 32–36 weeks and 436 weeks; response options included: (1) very important, (2) moderately important, (3) somewhat important, (4) not important at all, and (5) ‘‘I don’t know’’.
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We also asked what the responded thought the timing of cord clamping should be for each of the gestational ages listed above; in this case the response options included: (1) immediately, no milking; (2) immediately after milking, (3) 10–30 s; (4) 31–60 s; (5) 460 s; and (6) ‘‘I don’t know’’. Next the participants were asked to indicate the extent to which they agreed or disagreed with four statements (‘‘Cord clamping should not be delayed’’: (1) ‘‘if immediate resuscitation is indicated’’; (2) ‘‘in cases with placental abruption’’; (3) ‘‘in infants with placenta previa’’ and (4) ‘‘Umbilical cord milking can be used in place of delayed cord clamping’’). The response options for these items ranged from 1 to 5 with 1 ¼ strongly/mostly disagree to 5 ¼ strongly/ mostly agree. Finally, the respondents were asked to indicate the extent to which each of several different morbidities (maternal hemorrhage; neonatal hyperbilirubinemia, hypothermia, volume overload, delay in resuscitation, polycythemia, intraventricular hemorrhage, need for red blood cell transfusion and late onset sepsis) affected their cord clamping practices or recommendations. For these, the response options ranged from 1 ¼ ‘‘makes me very inclined to delay’’ to 5 ¼ ‘‘makes me very inclined to clamp immediately’’. After obtaining approval from the Institutional Review Board at the University of California, San Francisco (UCSF), we sent the survey to a random sample of 600 members of the American College of Obstetricians and Gynecologists (ACOG), including a random sample of 200 members of the College’s Collaborative Ambulatory Research (CARN). The CARN network is the only existing national collective of 1600 board-certified obstetricians–gynecologists who practice in a variety of ambulatory care settings throughout the United States and have been recruited to participate in survey studies. An initial mailing included the survey, a cover letter and a postage paid return envelope. Four subsequent mailings were sent to non-respondents. After compiling the initial responses, a follow-up post card was sent to non-respondents that included two of the original survey questions and demographic information to allow for comparison of ‘‘nonrespondents’’ to ‘‘respondents’’. All data were collected prior to the publication of the 2012 ACOG Committee Opinion on delayed cord clamping [17]. We used SPSS to analyze the data. Chi-square was used for inferential analysis and parametric data were compared using t tests. A Friedman test was used to evaluate the importance of timing. Post-hoc Dunn’ multiple comparisons test was then utilized to compare the responses about the importance of timing of umbilical cord clamping in term and preterm infants. Alpha level was set at p50.05.
J Matern Fetal Neonatal Med, 2014; 27(14): 1457–1461
All of the respondents were actively practicing obstetrics, and 2.8% reported being maternal fetal medicine specialists. Fifty-three percent of the respondents were male, 47% were female. The majority (79.5%) were White non-Hispanic, while 10.2% were Asian, 4.5% were White Hispanic, and the rest were African-American (1.7%) or Native American/Alaskan native (2.8%). Over half (61.4%) practiced in a group setting. Only 3.5% reported that their hospital had a delayed clamping policy. Is timing of umbilical cord clamping important? Physicians differed in their ratings of the importance of timing of umbilical cord clamping at different gestational ages. In general, respondents were more likely to rate the timing of umbilical cord clamping as ‘‘very important’’ for infants528 weeks, with a tendency towards rating the time of clamping as less important with increasing gestational age (Table 1). The most common response to a question about the importance of timing for infants 436 weeks’ gestation was ‘‘somewhat important’’. What is the optimal cord clamping time? Significant differences between responses to the item asking about the optimal timing for clamping for preterm versus term infants also emerged. For example, although the most frequent physician response was ‘‘don’t know’’ regardless of gestational age (42–55%), for infants 528 weeks’ gestation the second highest response was ‘‘immediately after milking’’ (19.9%) and for infants436 weeks’ gestation the second most common response was 460 s (20.9%; Table 2). How do potential morbidities affect your recommended cord clamping time? The survey respondents were asked to rate, on a five-point scale ranging from ‘‘makes me very inclined to delay’’ to ‘‘makes me very inclined to clamp immediately’’, the extent to which potential morbidities affected their umbilical cord clamping practices in preterm infants. Only three potential Table 1. How important is timing of cord clamping at birth?
Very important Moderately important Somewhat important Not important Don’t know
528 GA n%
28–31 GA n%
32–36 GA n%
436 GA n%
52 41 21 18 44
45 48 26 15 42
25 52 42 17 40
12 32 53 45 34
(29.5) (23.3) (11.9) (10.2) (25.0)
(25.6) (27.3) (14.8) (8.5) (23.9)
(14.2) (29.5) (23.9) (9.7) (27.7)
(6.8) (18.2) (30.1) (25.6) (19.3)
Bold values signify the highest percentage. Table 2. When should cord clamping be performed?
Results Ninety-three CARN members and 83 other ACOG members returned the completed survey, for response rates of 46.5% and 20.8%, respectively. There were no significant differences in the sociodemographic characteristics or responses provided by CARN versus non-CARN respondents. In addition, no significant differences emerged between respondents and non-respondents in gender, age or responses to the two survey questions included in the follow-up letter to non-respondents.
528 GA 28–31 GA 32–36 GA 436 GA n% n% n% n% Don’t know Immediately, no milking Immediately after milking 10–30 s 31–60 s 460 s
55 16 34 17 23 26
(32.2) (9.4) (19.9) (9.9) (13.5) (15.2)
50 14 32 23 22 30
(29.2) (8.2) (18.7) (13.5) (12.9) (17.5)
Bold values signify the highest percentage.
53 17 20 31 25 26
(30.8) (9.9) (11.6) (18.0) (14.5) (15.1)
42 28 16 23 27 36
(24.4) (16.3) (9.3) (13.4) (15.7) (20.9)
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Table 3. Do comorbidities affect timing of cord clamping in preterm infants?
Maternal hemorrhage Hyper-bilirubinemia Hypothermia Volume overload Delay in resuscitation Polycythemia IVH Need for red blood cell transfusion Late onset sepsis
Very inclined to delay n(%)
Somewhat inclined to delay n(%)
Has no effect on my practice n(%)
Somewhat inclined to clamp immediately n(%)
6 (3.6) 6 (3.6) 5 (3.0) 4 (2.4) 2 (1.2) 5 (3.1) 6 (3.8) 44 (27.5)
12 (7.1) 8 (4.8) 7 (4.3) 9 (5.5) 10 (6.2) 6 (3.7) 14 (8.8) 38 (23.8)
30 93 74 84 26 67 92 49
(17.9) (56.4) (45.1) (51.2) (16.1) (41.4) (57.9) (30.6)
35 (20.8) 31 (18.8) 43 (26.2) 36 (21.9) 49 (30.4) 43 (26.5) 21 (13.2) 12 (7.5)
11 (6.9)
18 (11.3)
93 (58.5)
15 (9.4)
Very inclined to clamp immediately n(%) (50.6) (16.4) (21.3) (18.9) (46.0) (25.3) (16.4) (10.6)
2 ¼ 115.6; p50.001 2 ¼ 151.3; p50.001 2 ¼ 98.9; p50.001 2 ¼ 122.9; p50.001 2 ¼ 107.85; p50.001 2 ¼ 87.4; p50.001 2 ¼ 149.6; p50.001 2 ¼ 34.2; p50.001
22 (13.8)
2 ¼ 149.3; p50.001
85 27 35 31 74 41 26 17
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Bold values signify the highest percentage.
comorbidities were reported to have an effect on these physicians’ inclinations. Specifically, half of the respondents (50.6%) were very inclined and 20.8% were somewhat inclined to clamp immediately in the context of potential maternal hemorrhage ( 2 ¼ 115.6; p50.001); 30.4% were somewhat and 46.0% were very inclined to do so for neonatal resuscitation ( 2 ¼ 107.85; p50.001); and 27.5% were very and 23.8% somewhat inclined to delay umbilical cord clamping for potential neonatal red blood cell transfusion ( 2 ¼ 34.2; p50.001) (Table 3). Do comorbidities affect practice if the obstetrician also believes timing is important? We evaluated the effect of comorbidities on the practice of the respondents who indicated that timing was ‘‘very or moderately important’’ versus ‘‘not important’’. The comorbidities that affected their cord clamping practices were dependent on the gestational age they believed the timing of cord clamping was important. Comorbidities which affected practice included a delay in neonatal resuscitation, hypothermia or neonatal transfusion. Obstetricians who indicated clamping was important for infants 532 weeks’ gestation also indicated that a delay in resuscitation was a potential morbidity that would cause them to recommend immediate cord clamping ( 2 ¼ 7.38; p ¼ 0.025). Respondents who reported timing was important at 436 weeks were more likely to practice immediate clamping in preterm infants for potential hypothermia ( 2 ¼ 6.89; p ¼ 0.03) and delay clamping if neonatal transfusion ( 2 ¼ 7.35; p ¼ 0.025) was of potential concern. Do comorbidities affect the opinion of timing if the obstetrician believed clamping should be delayed? We also evaluated the influence of comorbidities on physicians who reported believing in immediate or delayed clamping at 532 and at 436 weeks’ gestation. Respondents who believed cord clamping should be delayed for infants 532 weeks were significantly more inclined to practice immediate cord clamping in preterm infants if there was potential morbidity due to a delay in resuscitation ( 2 ¼ 6.0; p ¼ 0.043), and they also were more likely to practice delayed cord clamping for concern of neonatal transfusion ( 2 ¼ 8.52; p ¼ 0.014). Those who believed immediate cord clamping was important for infants 436 weeks’ gestation also practiced
clamping immediately for a potential delay in resuscitation in preterm infants ( 2 ¼ 11.87; p ¼ 0.003). Do situations affect the recommended time to clamp the cord? In response to a question asking the extent to which they believed cord clamping should not be delayed in certain situations, respondents reported that they strongly or mostly agreed that cord clamping should not be delayed in the following situations: if immediate resuscitation was indicated (69.6%), in cases with placental abruption (52.6%), or in cases of placenta previa (30.6%). When asked whether they agreed that umbilical cord milking should be used instead of delayed cord clamping, 40.4% of respondents reported that they ‘‘somewhat’’ or ‘‘strongly/mostly’’ agreed, 38.6% neither agreed nor disagreed and 21% ‘‘somewhat’’ or ‘‘strongly/ mostly’’ disagreed.
Discussion In this study of obstetricians practicing in the United States, we have shown that the practice of delayed cord clamping in both term and preterm infants has not been widely adopted. Despite the published evidence of the benefits associated with delayed umbilical cord clamping [7–9], only a small minority (3.5%) of the survey respondents reported that their institution had an umbilical cord clamping policy. This is in direct contrast to many European institutions, where delayed cord clamping is standard of care [13], and contrary to a recent ACOG committee opinion recommending delay in umbilical cord clamping (30–60 s) in preterm infants [17]. We also found that obstetricians’ opinions about the appropriate timing of delayed cord clamping and cord milking differed by gestational age. After excluding those who responded ‘‘don’t know’’, the respondents were more likely to believe umbilical cord clamping is important at earlier gestational ages. The majority of obstetricians reported that umbilical cord clamping should be delayed or milked for infants less than 28 weeks’ gestation. We also found that the obstetricians’ opinions about the risks and benefits of delayed cord clamping differed from what we hypothesized. The majority of respondents indicated that they would practice immediate cord clamping for maternal hemorrhage or a delay in neonatal resuscitation, while they would opt for delayed clamping for potential red
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blood cell transfusions in the neonate. Other potential neonatal comorbidities, including hyperbilirubinemia, hypothermia, volume overload, polycythemia, intraventricular hemorrhage or late onset sepsis, were not significantly associated with opinions of the appropriate timing of umbilical cord clamping. Results of our survey suggest that obstetricians who believe delayed cord clamping is important have opinions about the risks and benefits that are inconsistent with the current literature. The only comorbidity demonstrated in randomized controlled trials, which the respondents’ opinions were consistent with, was the practice of delayed cord clamping for potential neonatal transfusion [6,7,13]. While respondents were more likely to practice immediate clamping in the contexts of maternal hemorrhage or delay in neonatal resuscitation, these concerns are not consistent with the results of published randomized studies. The most unexpected finding is that even though there is published evidence of an association between lower risk of neonatal intraventricular hemorrhage and delayed cord clamping, this was not a significant concern of our respondents. We had hypothesized that obstetricians who thought delayed cord clamping was important or that it should be delayed in preterm infants would consider a decrease in intraventricular hemorrhage as an indication to delay; however, this was not found to be true. Despite the evidence regarding the benefits of delayed clamping that has accumulated from multiple randomized controlled trials, obstetricians still differ considerably on their opinions about the appropriate timing of umbilical cord clamping. Some of the concerns obstetricians have are not substantiated by the current evidence. Although additional evidence, such as a multi-centered randomized controlled trial, may be needed to fully address the concerns of some obstetricians, evidence-based educational interventions may be necessary to encourage delayed cord clamping practices.
Declaration of interest The authors report no conflicts of interest. This study was supported in part by the Centers for Disease Control and Prevention and Grant #R60 MC 05674 from the Maternal and Child Health Bureau, Health Resources and
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Services Administration, Department of Health and Human Services.
References 1. Yao AC, Lind J. Blood flow in the umbilical vessels during the third stage of labor. Biol Neonate 1974;25:186–93. 2. Ononeze ABO, Hutchon DJR. Attitude of obstetricians toward delayed cord clamping: a questionnaire-based study. J Obstet Gynaecol 2009;29:223–4. 3. Polin RA, Fox W. Fetal and neonatal physiology. Philadelphia: W B Saunders; 1998. 4. Pietra, GG, D’Amodio MD, Leventhal MM, et al. Electron microscopy of cutaneous capillaries of newborn infants: effects of placental transfusion. Pediatrics 1968;42:678–83. 5. Windle W. Brain damage by asphyxia at birth. Scientific American 1969;221:76–84. 6. Yao A, Moinian M, Lind J. Distribution of blood between infant and placenta after birth. Lancet 1969;2:871–3. 7. Ibrahim H, Krouskop R, Lewis D, Dhanireddy R. Placental transfusion: umbilical cord clamping and preterm infants. J Perinat 2000;20:351–4. 8. Kinmond S, Aitchison TC, Holland BM, et al. Umbilical cord clamping and preterm infants: a randomised trial. BMJ 1993;306: 172–5. 9. Hofmeyr G, Bolton K, Bowen D, et al. Periventricular/intraventricular haemorrhage and umbilical cord clamping. Findings and hypothesis. S Afr Med J 1988;73:104–6. 10. Andersson O, Hellstrom-Westas L, Andersson D, Domellof M. Effect of delayed versus early umbilical cord clamping on neonatal outcomes and iron status at 4 months: a randomised controlled trial. BMJ 2011;343:d7157. 11. Rabe H, Reynolds G, Diaz-Rossello J. A systemic review and metaanalysis of a brief delay in clamping the umbilical cord of preterm infants. Neonatology 2008;93:138–44. 12. Hofmeyr G, Gobetz L, Bex PJ, et al. Periventricular/intraventricular hemorrhage following early and delayed umbilical cord clamping. A randomized controlled trial. Online J Curr Clin Trials 1993;Doc No.110. 13. Rabe H, Wacker A, Hulskamp G, et al. A randomized controlled trial of delayed cord clamping in very low birth weight preterm infants. Eur J Pediatr 2000;159:775–7. 14. Oh W, Fanaroff AA, Carlo WA, et al.; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Effects of delayed cord clamping in very-low-birth-weight infants. J Perinatol 2011;31:S68–71. 15. Mercer JS, Vohr BR, McGrath MM, et al. Delayed cord clamping in very preterm infants reduces the incidence of intraventricular hemorrhage and late-onset sepsis: a randomized controlled trial. Pediatrics 2006;117:1235–42. 16. Hutton EK, Hassan ES. Late vs early clamping of the umbilical cord in full-term neonates: systematic review and meta-analysis of controlled trials. JAMA 2007;297:1241–52. 17. Committee opinion no. 543: timing of umbilical cord clamping after birth. Obstet Gynecol 2012;120:1522–6.
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Appendix 1. How important do you think the time of umbilical cord clamping is on neonatal outcomes at the following gestational ages?
528 weeks 28–31 weeks 32–36 weeks 436 weeks
Very important
Moderately important
Somewhat important
Not important at all
I don’t know
1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ
9œ 9œ 9œ 9œ
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2. Is there an official policy at your institution/hospital that recommends the appropriate timing for clamping the umbilical cord for infants delivered before 32 weeks gestation? 1œ yes, there is a delayed cord clamping policy 2œ yes, there is an immediate cord clamping policy 3œ no, there is no policy 4œ I don’t know 3. Please indicate what you think the timing of umbilical cord clamping at each of the following gestational ages should be.
528 weeks 28–31 weeks 32–36 weeks 436 weeks
Immediately, no milking
Immediately after milking
10–30 seconds
31–60 seconds
460 seconds
I don’t know
1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ
5œ 5œ 5œ 5œ
9œ 9œ 9œ 9œ
4. Please indicate how much you agree or disagree with the following statements regarding the timing of umbilical cord clamping in preterm infants.
Strongly/mostly disagree
Somewhat disagree
Neither agree nor disagree
Somewhat agree
Strongly/ mostly agree
1œ
2œ
3œ
4œ
5œ
1œ
2œ
3œ
4œ
5œ
1œ 1œ
2œ 2œ
3œ 3œ
4œ 4œ
5œ 5œ
Cord clamping should not be delayed if immediate resuscitation is indicated. Cord clamping should not be delayed in cases with placental abruption. Cord clamping should not be delayed in infants with placenta previa. Umbilical cord milking can be used in place of delayed cord clamping.
5. Please indicate the extent to which each of the following potential morbidities affects your umbilical cord clamping recommendations or practice in preterm infants.
Potential of: Maternal hemorrhage Neonatal: Hyperbilirubinemia Hypothermia Volume overload A delay in resuscitation Polycythemia Intraventricular hemorrhage Need for red blood cell transfusion Late onset sepsis
Makes me very inclined to delay
Makes me somewhat inclined to delay
Has no effect on my practice
Makes me somewhat inclined to clamp immediately
Makes me very inclined to clamp immediately
1œ
2œ
3œ
4œ
5œ
1œ 1œ 1œ 1œ 1œ 1œ 1œ 1œ
2œ 2œ 2œ 2œ 2œ 2œ 2œ 2œ
3œ 3œ 3œ 3œ 3œ 3œ 3œ 3œ
4œ 4œ 4œ 4œ 4œ 4œ 4œ 4œ
5œ 5œ 5œ 5œ 5œ 5œ 5œ 5œ
