Factors associated with timing of umbilical cord clamping in tertiary hospital of Nepal
Nelin et al. BMC Res Notes
Factors associated with timing of umbilical cord clamping in tertiary hospital of Nepal
Viktoria Nelin 0 2
Ashish KC 0 1 2
Ola Andersson 0 2
Nisha Rana 0 2
Mats Målqvist 0 2
0 International Maternal and Child Health, Department of Women's and Children's Health, Uppsala University, University Hospital , 751 85 Uppsala , Sweden
1 United Nation's Children's Fund (UNICEF) , Nepal Country Office, UN House, Pulchowk, Kathmandu , Nepal
2 International Maternal and Child Health, Department of Women's and Children's Health, Uppsala University, University Hospital , 751 85 Uppsala , Sweden
Objective: Delayed umbilical cord clamping (DCC) (≥ 60 s) is recognized to improve iron status and neurodevelopment compared to early umbilical cord clamping. The aim of this study is to identify current umbilical cord clamping practice and factors determining the timing of clamping in a low-resource setting where prevalence of anemia in infants is high. Results: A cross-sectional study design including 128 observations of clinical practice in a tertiary-level maternity hospital in Kathmandu, Nepal. Overall 48% of infants received DCC. The mean and median cord clamping times were 61 ± 33 and 57 (38-79) s, respectively. Univariate analysis showed that infants born during the night shift were five times more likely to receive DCC (OR 5.6, 95% CI 1.4-38.0). Additionally, infants born after an obstetric complication were 2.5 times more likely to receive DCC (OR 2.5, 95% CI 1.2-5.3), and babies requiring ventilation had a 65% lower likelihood of receiving DCC (OR 0.35, 95% CI 0.13-0.88). Despite the existence of standard protocols for cord clamping and its proven benefit, the lack of uniformity in the timing of cord clamping reveals poor translation of clinical guidelines into clinical practice. Clinical trial registration ISRCTN97846009
Clinical practice; Umbilical cord; Cord clamping; Nepal
Iron deficiency is associated with impaired
neurodevelopment, which can affect an individual’s cognitive,
motor, and behavioral abilities [
]. Globally, 43% of
the children below the age of 5 are anemic and 1.5% of
them are severely anemic; meaning that 273 million
children were anemic in the year 2011 [
]. In Nepal, 56%
of children under 5 are anemic, while 75% of children
between the ages of 6–11 months are anemic [
umbilical cord clamping (DCC), clamping the umbilical
cord ≥ 60 s after delivery, has been shown to reduce
anemia in infants in this setting [
], and identified as a highly
cost-effective intervention [
Delayed cord clamping has the potential to contribute
approximately 75 mg of iron, corresponding to more than
an infant’s 3-month requirement [
DCC has been shown to improve fine motor and social
skill development at 4 years of age . DCC also seems
to be protective against motor disability in very low birth
weight male infants, possibly as a result of increased
blood, red cell and stem cell volumes [
The 2012 World Health Organization (WHO)
guidelines on maternal, newborn, child, and adolescent health
recommends a delay in umbilical cord clamping of
1–3 min after delivery [
]. Improving the quality of
intrapartum care as well as health worker adherence to DCC
protocols will be critical to reduce the burden of
childhood anemia and its consequences. This is especially
relevant in low-income countries like Nepal where there is
an increased trend of institutional delivery; in 2014, 55%
of women delivered in a health facility [
]. We therefore
conducted this study to assess the health worker
adherence to DCC recommendations, and to identify the
factors associated with the timing of cord clamping. This
study was carried out as a baseline study for further
studies comparing early and late cord clamping at the same
This study was conducted at a tertiary, government-run
hospital in Kathmandu, Nepal, which is a central referral
hospital. In 2011, 23,155 total deliveries occurred at the
Deliveries occurred in three units, but observations for
this study were performed at the two sites where vaginal
deliveries occurred-Labor Room (LR) and the Maternal
and Newborn Service Center (MNSC).
Ethical approval for this observational study was
received from Nepal Health Research Council as a part of
a larger study evaluating the impact of a simplified
neonatal resuscitation protocol on perinatal outcomes [
Written consent was obtained from the hospital
administrator and matron, as well as nursing in-charge in each of
the delivery wards.
Observations for this cross-sectional study were
completed from July 10th to September 28th, 2013 by two
observers. Selection of cases for observation occurred
as women were admitted to either ward for expectant
vaginal delivery. Cases were chosen based on
observational shifts, i.e. the presence and ability of an observer
to watch each case through delivery of the infant.
Observations began during the first or second stage of labor
and continued until at least 1 h after delivery or until
the mother was transferred from the delivery ward,
whichever occurred first. To complete observations, the
researchers used printed checklists to record data and a
mobile phone stopwatch. The observer was present in
the background and did not interfere with healthcare
A structured checklist was developed using the
International Federation of Gynecology and Obstetrics
(FIGO) guidelines for active management of third stage
of labor (AMTSL) [
], the WHO guidelines on neonatal
], and other related literature [
capture the variables of interest. The checklist included
18 items relevant to the current study; see Additional
file 1: Annex S1 for a list of variables and data collection
No sample size calculations were completed, although
the aim was to observe at least fifty cases in both wards,
with the goal that after these observations, routine
practices could be determined. At least 12 deliveries during
each of the hospital duty shifts were observed to ensure
that potential changes in staffing routines throughout the
day were captured.
Data are shown as mean ± standard deviation (SD) or
as median and interquartile range (IQR). Statistical
analysis was done using R Commander, part of the R statistical
package (Version 3.0.3/3.1.1, R Foundation for
Statistical Computing, Vienna, Austria). For analysis purposes,
categorical variables were created from raw or
continuous variables. Variables categorized whether early cord
clamping (ECC) or DCC was used (DCC was defined
as ≥ 60 s); AMTSL was done or not done; the hospital
shift at the time of delivery was morning (07:00–13:00),
evening (13:00–19:00), or night (19:00–07:00); third stage
of labor was longer than 7 min or less; maternal blood
loss was more than 100 mL or not; the infant was born
preterm (< 37 weeks) or not; and whether the Apgar
score at 1 min was less than 7 or more. AMTSL was
considered complete if an uterotonic drug was given after the
infant’s delivery, controlled cord traction was completed,
and uterine massage was done at least once after
placental delivery. Seven minutes was chosen as a cutoff for a
“longer” third stage of labor as this was the third quartile
for length; likewise, 100 mL was chosen as the cutoff for
“greater” maternal blood loss as this was the third
Subgroups were compared using independent
samples t-tests or one-way analysis of variance (ANOVA) for
continuous variables; normal distribution was assumed.
However, a test for normal distribution was also done and
a comparison of the medians using a Kruskal–Wallis test
was also completed for any variable not normally
distributed. Chi Square analysis was used to compare
categorical data between ECC and DCC groups and/or MNSC
and LR groups. Finally, univariate logistic regression was
used to determine the association for receiving DCC.
Differences are considered significant when p < 0.05.
Of the 151 eligible cases, only 138 included
observations of the third stage of labor, either because
caesarean section was ordered or the delivery occurred
after the observational shift ended. Of these 138 cases,
only 128 included a measurement of timing of
umbilical cord clamping, as 10 infants had tight nuchal cords
(i.e. wrapped tightly around their necks), and in these
cases clamping and cutting was done before the entire
infant’s body was delivered (Fig. 1). Therefore, these
cases were excluded from analysis. Sixty-nine cases were
observed in the MNSC and 59 in the LR. All of the 128
singleton vaginal deliveries were spontaneous, with
episiotomy or without. The mean gestational age at birth
was 39.5 ± 1.9 weeks and twelve infants were preterm.
The mean birth weight of the sample population was
5 cases to OT
73 cases where
identified in LR
65 cases where
observed in LR
138 cases where third stage of labor
observation completed and used for
128 cases where timing of cord clamping
1 case to OT
10 cases with
cord and thus
prior to delivery
2967 ± 463 grams. There were a greater number of
female (77) than male (51) infants delivered (p = 0.02).
Overall, 48% of infants received DCC (≥ 60 s), 40%
had cord clamping between 30–59 s, and 12% prior to
30 s. In the MNSC, the low-risk ward, 52% of infants had
DCC, 41% had their cords clamped between 30–59 s,
and 7% before 30 s. In the LR, the higher-risk ward, DCC
was completed in 42% of cases, cord clamping occurred
between 30–59 s in 39% of infants, and prior to 30 s in
19% of infants. Cord clamping was completed at 3 min
or after in two cases. All infants were placed directly on
the mother’s abdomen after delivery, and were therefore
positioned above the perineum when clamping occurred.
Cord milking was never used.
Mean and median cord clamping times among
population subgroups are presented in Table 1. There was no
difference in the mean cord clamping times among any
of the subgroups. Timing of cord clamping was not
normally distributed, so the medians of each subgroup were
also compared. The median cord clamping time was
significantly higher in cases where no interventions were
given to the infant after delivery, as compared to those
cases where infants received any intervention. In all other
subgroups, median cord clamping times were similar.
Subgroup analyses comparing the use of DCC and ECC
are presented in Table 2. The use of DCC was
comparable in most population subgroups. However, there were
more deliveries on the night shift in the DCC group as
compared to the ECC group, and infants born during
the night shift were 5.6 times more likely to receive DCC
than ECC (OR 5.62, 95% CI 1.38–37.96). Women with
any obstetric complication during delivery had 2.5 times
more likelihood of receiving DCC (> 60 s) than those
who did not have any complication (OR 2.50, CI 95%
1.19–5.34). Babies requiring ventilation had a 65% lower
chance of receiving DCC (OR 0.35, 95% CI 0.13–0.88)
than did babies in whom ventilation was not required.
We found that the median time for cord clamping was
1 min and the timing of cord clamping was not
associated with place of delivery, use of AMTSL, increased
length of third stage of labor, increased maternal blood
loss, preterm birth, or Apgar score < 7 at 1 min. DCC
Labor/delivery complications included breech presentation, fetal distress, premature rupture of membranes, meconium staining, and various degrees of tears and
Interventions given to the infant included oxygen administration, penguin/bulb suction, electric suction, bag and mask ventilation, vigorous stimulation, and transfer
to the Postnatal Baby Unit
MNSC Maternal and Newborn Service Center, AMTSL Uterotonic administration + CCT + Uterine massage
a p value determined by Kruskal–Wallis test
b This variable includes one missing value where maternal blood loss not recorded
c This variable includes two missing values where gestational age was not available
was more likely in cases where there was any obstetric
complication and DCC was less likely in cases where
the infant was given any intervention post-delivery as
compared to those cases where the infants were given
Timing of umbilical cord clamping was not associated
with the use of AMTSL thus demonstrating that DCC
is not invited or enhanced by the use of AMTSL in this
setting. DCC was less likely in cases where the infant
received any intervention, possibly because in most cases
where the infant is perceived to require assistance for
stabilization the cord is clamped quickly to facilitate
providing care to the infant [
]. It is interesting to
emphasize that DCC was less likely in infants who received any
interventions since in past randomized controlled
trials examining DCC versus ECC, those infants who were
asphyxiated or in need of immediate resuscitation
measures were excluded due to concern for their clinical
condition and health outcomes. However, the umbilical cord
is not only a conduit for the transfer of blood, but also for
the delivery of oxygen to the foetus/infant through the
gas exchange function of the placenta.
OR (95% CI)a
Delayed cord clamping was used in about half of the
cases at this hospital, although the wide variation in
cord clamping times reveals the need for defined clinical
guidelines to direct practice in this setting. Additionally,
it is important to recognize potential barriers to the use
of DCC and to identify factors that would help facilitate a
change in clinical practice, as this is currently an
evidencebased recommendation. The future studies planned at this
hospital will aim to address some of the research gaps,
including the use of DCC in asphyxiated infants.
This study was conducted at a large delivery hospital in
Kathmandu in Nepal. Thus, the practices used here may
differ compared to other health centers across Nepal.
Due to its observational nature, there are some
potential biases in this study, including intra-/inter-observer
variation, as well as bias due to overt observation. This
study was part of a larger one examining the
implementation of the Helping Babies Breathe (HBB) protocol [
and the observers were also involved in the HBB
protocol training of some of the staff working in the delivery
wards during the observational period, thus elevating the
potential for desirability bias among health staff. Finally,
the primary aim of this study was to describe practices,
although we used logistic regression to compare groups,
and our small sample size limits the statistical power of
Additional file 1. Definitions of variables. Definitions of variables
(relevant to this study) contained in the structured checklist, and their
method of data collection.
AMTSL: active management of third stage of labor; DCC: delayed cord
clamping; ECC: early cord clamping; FIGO: International Federation of Gynecology
and Obstetrics; HBB: Helping Babies Breathe; IQR: interquartile range; LR: Labor
Room; MNSC: Maternal and Newborn Service Center; OR: odds ratio; SD:
standard deviation; WHO: World Health Organization.
VN, MM and AK conceptualized and designed the study. AK was the principal
applicant for funding. VN was responsible for the data collection and data
management. AK and VN were responsible for the data analysis and drafting
of the manuscript. OA and NR contributed to the development of the
manuscript. All authors read and approved the final manuscript.
The group is very grateful to the mothers who participated in the study.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets used and analysed during the current study are available from
the principal investigator with a reasonable request.
Consent for publication
Ethics approval and consent to participate
As indicated in the section “Study design”, the ethical review board of Nepal
Health Research Council approved this study with reference Reg. No. 37/2012
on 16 July 2012. All participants were provided with written informed consent
as indicated in the “Participants” section.
Funding for the study was provided through grants from the Swedish Society
of Medicine, Laerdal Foundation for Acute Medicine and Swedish International
Development Cooperation Agency.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
1. Lozoff B , Beard J , Connor J , Barbara F , Georgieff M , Schallert T. Long-lasting neural and behavioral effects of iron deficiency in infancy . Nutr Rev . 2006 ; 64 ( 5 Pt 2 ): S34 -43 (discussion S72-91).
2. Radlowski EC , Johnson RW . Perinatal iron deficiency and neurocognitive development . Front Hum Neurosci . 2013 ; 7 : 585 .
3. Haas JD , Brownlie Tt . Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship . J Nutr . 2001 ; 131 ( 2S -2): 676S -88S (discussion 688S-690S).
4. Stevens GA , Finucane MM , De-Regil LM , Paciorek CJ , Flaxman SR , Branca F , Pena-Rosas JP , Bhutta ZA , Ezzati M , Nutrition Impact Model Study G. Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995-2011: a systematic analysis of population-representative data . Lancet Global Health . 2013 ; 1 ( 1 ): e16 - 25 .
5. Ministry of Health and Population, New Era, ICF Macro, USAID. Nepal demographic and health survey . Kathmandu: New Era; 2011 .
6. Kc A , Rana N , Malqvist M , Jarawka Ranneberg L , Subedi K , Andersson O. Effects of delayed umbilical cord clamping vs early clamping on anemia in infants at 8 and 12 months: a randomized clinical trial . JAMA Pediatr . 2017 ; 171 ( 3 ): 264 - 70 .
7. Bhutta ZA , Ahmed T , Black RE , Cousens S , Dewey K , Giugliani E , Haider BA , Kirkwood B , Morris SS , Sachdev HP , et al. What works? Interventions for maternal and child undernutrition and survival . Lancet . 2008 ; 371 ( 9610 ): 417 - 40 .
8. Mercer JS , Erickson-Owens DA . Rethinking placental transfusion and cord clamping issues . J Perinat Neonat Nurs . 2012 ; 26 ( 3 ): 202 - 17 (quiz 218- 209 ).
9. World Health Organization. Guidelines on maternal, newborn, child and adolescent health approved by the WHO guidelines review committee . Geneva: WHO; 2013 .
10. UNICEF GoN. Multiple indicator cluster survey (MICS) . Kathmandu: UNICEF; 2015 .
11. Government of Nepal MoHP, Paropakar Maternity & Women's Hospital . Smarika, Annual Report . Kathmandu, Nepal; 2012 - 13 .
12. KC A , Målqvist M , Wrammert J , Verma S , Aryal DR , Clark R , KC NP , Vitrakoti R , Baral K , Ewald U. Implementing a simplified neonatal resuscitation protocol-helping babies breathe at birth (HBB)-at a tertiary level hospital in Nepal for an increased perinatal survival . BMC Pediatr . 2012 ; 12 : 159 .
13. Lalonde A , International Federation of G, Obstetrics. Prevention and treatment of postpartum hemorrhage in low-resource settings . Int J Gynaecol Obstet . 2012 ; 117 ( 2 ): 108 - 18 .
14. World Health Organization. Guidelines on basic newborn resuscitation . Geneva: WHO; 2012 .
15. Vivio D , Fullerton JT , Forman R , Mbewe RK , Musumali M , Chewe PM . Integration of the practice of active management of the third stage of labor within training and service implementation programming in Zambia . J Midwifery Womens Health . 2010 ; 55 ( 5 ): 447 - 54 .
16. Hutton EK , Stoll K , Taha N. An observational study of umbilical cord clamping practices of maternity care providers in a tertiary care center . Birth . 2013 ; 40 ( 1 ): 39 - 45 .
17. Bimbashi A , Ndoni E , Dokle A , Duley L . Care during the third stage of labour: obstetricians views and practice in an Albanian maternity hospital . BMC Pregnancy Childbirth . 2010 ; 10 : 4 .
18. Hutchon DJ . Immediate or early cord clamping vs delayed clamping . J Obstet Gynaecol J Inst Obstet Gynaecol . 2012 ; 32 ( 8 ): 724 - 9 .
19. KC A , Wrammert J , Clark RB , Ewald U , Vitrakoti R , Chaudhary P , Pun A , Raaijmakers H , Målqvist M. Reducing perinatal mortality in nepal using helping babies breathe . Pediatrics . 2016 ; 137 ( 6 ): e20150117 .