Effects of Delayed Cord Clamping on Neonatal Hematological Status at Maternity Teaching Hospital in Sulaimani City/Iraq

Effects of Delayed Cord Clamping on Neonatal Hematological Status at Maternity Teaching Hospital in Sulaimani City/Iraq

Nazera Salam Mena¹, Dr. Atiya Kareem Mohammed^2*

¹Assist. Lecturer, Maternal Neonatal Nursing Department, College of Nursing,          University of Sulaimani, Iraq.                                                                                

² Assist. Professor Dr., Maternal Neonate Nursing Department, College of Nursing, University of Sulaimani, Iraq.  

*Corresponding author: Dr. Atiya Kareem Mohammed

Email:  atiya.mohammed@univsul.edu.iq

ABSTRACT

Background: Infants born at full term consistently had better hematologic and iron status in the short- and long-term when the umbilical cord clamping was delayed for at least 2 minutes after birth.  Aim: In this study, the bilirubin serum, hemoglobin, and hematocrit levels of term newborns who underwent early cord clamping versus delayed cord clamping following a typical vaginal delivery were compared. Material and Method: A true experimental study involving (160) pregnant women from the labor ward who were in the second stage of labor. Participants were randomly assigned between the 1st of July 2021 and the 1st of February 2022, samples were selected by using a simple random sampling technique through the Structured Interviewing Questionnaire and the neonatal outcome, hematological parameters (Hemoglobin and Hematocrit), and total serum bilirubin level at the 72 hours after birth, and the participants were randomly divided into two groups early cord clamping (< 1 minute), and delayed cord clamping (more than 1 minute). Descriptive and inferential statistics were applied to the data analysis. A structured interviewing questionnaire; includes two parts socio-demographic characteristics of the pregnant women with early and delayed cord clamping on neonatal outcomes (Hemoglobin, Hematocrit, and Total Serum Bilirubin). Result: Among the 160 participants who completed the study 80 were control group (early cord clamping) and 80 were study group (delayed cord clamping) group. Delayed cord clamping was associated with higher hemoglobin, and hematocrit among newborns after 72 hours. Neonatal hemoglobin ranged from 16.8 ± 1.99 g/dl and there was a statistical reduction in early when compared to the late cord clamping group (17.9± 1.33 respectively). Serum bilirubin ranged from 6.28± 2.89 and there was a significant reduction in early when compared to the late-cord clamping group (8.27± 3.52 respectively). Conclusion: The use of a delayed cord clamp is helpful because it is a quick, easy, and safe maneuver. Delaying cord clamping in term newborns resulted in higher hemoglobin and hematocrit levels without having an unfavorable impact on neonatal characteristics, and significantly higher newborn hematocrit and neonatal hemoglobin levels. In addition to a large rise in blood volume and red cell volume in newborns, it reduces anemia.

Keywords: Delayed Cord Clamping, Neonatal Outcomes. Hematocrit, Hemoglobin, Total Serum Bilirubin, and hematological parameters.  

Received: 03 September 202X, Accepted: 15 December 2021, Available online: 20 January 202X

INTRODUCTION

The uterus and fetus must be connected by the umbilical cord (Mebarki, M. et al., 2021). A flexible, tube-like structure joins a fetus to the placenta of the mother. An organ is connected to the uterine wall by the placenta, which in turn connects to the mother's blood supply (Khier, A., & Elghazaly, E. A., 2015). 

 A little connecting stalk that connects the embryo to its trophoblastic shell is the beginning of the development of the umbilical cord on the 19th or 20th day following fertilization (Gupta, T. et al., 2018) (Um, S. et al., 2020). The primitive umbilical cord grows out of this shell, and by the fifth week of pregnancy, the intestinal loop has been added to the primitive cord's contents. Around the 12th week of pregnancy, the primitive umbilical cord retracts to the fetus's abdomen, and the mature cord, which has two umbilical arteries and an umbilical vein bathed in Wharyon jelly and all wrapped in an amniotic membrane, continues to develop (Cardoso, R. M. et al., 2021).

The umbilical vein transports oxygenated blood with nourishment from the placenta to the fetus, and the umbilical arteries convey oxygen-depleted blood with waste material from the unborn baby to the placenta (Seidler, A. L. et al., 2021).  

The typical umbilical cord has up to 40 helical turns and measures 50 to 60 centimeters in length and 2 cm in diameter. Fetal morbidity and death can increase as a result of abnormalities in the umbilical cord. Because the newborn can now breathe on its own, the umbilical cord is therefore clamped, then cut, and the remaining umbilical cord is delivered with the placenta after birth (Gomersall, J. et al., 2021).

The newborn is separated from the mother by cutting or clamping the umbilical cord. Umbilical cord cutting is the process of tying that cord using nippers in order to stop the placenta's supply of blood to the fetus (Katheria, A. C. et al., 2017). There are two ways to get the umbilical cord clamped during spontaneous labor: the first is immediate umbilical cord clamping within 30 minutes after the birth. Umbilical cord clamping is delayed for at least 1 minute following birth in the second modality. Due to diminished cardiac output, cerebral blood flow is lowered once more after one minute (De Bernardo, G. et al., 2020).  

As part of the active management of the third stage of labor, the World Health Organization (WHO) no longer recommends early cord clamping because the research indicates that it does not affect preventing postpartum hemorrhage (WHO, 2012). The WHO advised delaying cord clamping for all deliveries in 2014 while beginning newborn care, with early clamping advised if the baby needs immediate and advanced resuscitation (WHO, 2014).

Delaying cord clamping by three minutes after birth in term newborns increased venous hematocrit levels measured six hours later, within physiological ranges, and lowered the prevalence of neonatal anemia without having any negative effects on the neonates or their mothers (Korkut, S. et al., 2021). Early cord clamping was demonstrated to cause substantial bradycardia, along with a brief increase in carotid artery pressure, marked hypotension, and a decline in cardiac output and cerebral circulation (Korkut, S. et al., 2021).

Infants' hemoglobin and hematocrit levels are influenced by a variety of circumstances; delayed cord clamping raises hemoglobin levels in newborns (Ashish, K. C. et al., 2016). Hemoglobin levels may fall after birth if the placenta is cut or divided if a fetal artery is torn or punctured if the baby is held much above the level of the placenta for a while before the umbilical cord is clamped. Compared to newborns with early umbilical cord clamping, individuals with delayed cord clamping have a 32% larger blood volume (Nouraie, S. et al., 2019). Additionally, children with delayed cord clamping at 6 months of age have greater serum ferritin levels. Even in the US, early umbilical cord clamping is still encouraged despite some evidence to the contrary. In premature newborns, delayed cord clamping improves blood circulation, lessens the need for blood transfusions, and lowers the risk of intraventricular hemorrhage (Nouraie, S. et al., 2019).

 In both term and preterm infants, delayed umbilical cord clamping has been associated with increased hemoglobin levels and iron status, improved baby and child neurodevelopment, less anemia, higher blood pressure, fewer transfusions, and decreased incidence of intraventricular hemorrhage, chronic lung disease, necrotizing enterocolitis, and late-onset sepsis, according to the growing body of research. Polycythemia, jaundice, a greater need for phototherapy, maternal postpartum hemorrhage, or the demand for maternal blood transfusions are among the potential drawbacks of delaying cord clamping (Fogarty, M. et al., 2018).

 After several hours, if the cord clamping is postponed and the placenta transfusion is complete, the plasma volume decreases, leaving a significant amount of Red Blood Cells (RBC) (Mneimneh, S. et al., 2019). When such RBCs are destroyed, bilirubin and a significant amount of iron are left behind. The amount of iron produced by delaying cord clamping is 20–30 mg/kg, which is sufficient for the fetus's needs for at least three months. However, the resultant bilirubin will increase the risk of jaundice necessitating phototherapy (Mneimneh, S. et al., 2019).

On the other hand, a delayed cord clamping technique where the cord is clamped 3 minutes after birth can raise the mean neonatal hemoglobin concentration and hematocrit. Additionally, it is linked to improved cardiac acclimatization, the prevention of infant anemia, and a shorter third stage of labor, which lowers the risk of neonatal distress. Late cord clamping may have an impact on the neonatal Apgar score because the newborn needs enough blood volume for oxygen transport and tissue perfusion. (Qian, Y. et al., 2019).

The purpose of this research was to assess the impact of delayed umbilical cord clamping on neonatal outcomes and to compare the effects of early and delayed umbilical cord clamping on neonatal outcomes. According to the World Health Organization, the study also examined the outcomes for neonates following delayed cord clamping.

METHOD

Design of the study: The true- experimental study was carried out at the sole and important governmental Maternity Teaching Hospital in Sulaimani City.                                                                                                                

Study Population: a simple random sampling technique of 160 pregnant women who are beyond their 37^th to 42^nd of gestation and fall into many age categories. The study was done between the 1^st of July 2021 and the 1^st of February 2022. The criteria of inclusion for choosing pregnant women were to be between weeks 37 and 42 or to be full-term mothers, prime mothers, or mothers who had many pregnancies. Mothers were older than 18 years old, and birth weights ranged from 2.500 to 4000 gm. If a woman has a negative Rhesus factor status, she was excluded from some labors. Mothers who don't cooperate, have problems with the newborn (such as intrauterine growth retardation, and congenital malformation).                                                         

A panel of 10 experts determined the content validity, and the reliability was determined by the correlation coefficient, which was r 0.87. (Statistically adequate).                                                                     

Data collection: Direct interviews with study participants were used to obtain data. The sociodemographic features, any prior obstetric history, reproductive history, and neonatal hematological parameters (including hemoglobin, hematocrit, and total serum bilirubin level at the 72-hour postpartum fetus) were all assessed as part of a questionnaire created for this purpose.                                                                           

Data Collection Procedure: The survey's entire sample was chosen using a straightforward random sampling procedure. The Maternity Teaching Hospital divided these into two groups of 80 each as the study groups (delayed cord clamping) and 80 each as the control groups (early cord clamping). The result for newborns is. Hematological indicators (hemoglobin and hematocrit), total serum bilirubin level at 72 hours after birth, and the need for admission to the neonatal intensive care unit are examples of late neonatal outcomes (NICU).                                                                                                                                       

Statistical analysis: The statistical package for social sciences (SPSS) version 22 was used to computerize and analyze the data, Statistics (both descriptive and inferential) were used to analyze the data. To describe the characteristics of the study participants, frequency, percentage, mean, and standard deviation were used. The nominal distribution of the data was assessed using the association using the Chi-square test. When the projected count of > 20% of the combined excel cells scored below 5, Fisher's exact test was applied. The mean differences between the groupings for early cord clamping and late cord clamping were compared using an independent (t) test. Significance is measured by the p-value. At a p-value of 0.05, a statistically significant difference was regarded, at a p-value of 0.001, a highly statistically significant difference was examined, and at a p-value > 0.05, non-significant results were shown.

    RESULT

 Table (1) shows that both groups had high percentages of Multipara participants, with 71.3 percent in the control groups and 70% in the study groups and that the majority of the samples (34.4%) in both groups were over 30. Also, both groups delivered their infants between 38 and 40 weeks of gestation. Additionally, the information in this table shows a relationship between both the control and the study groups in terms of age and parity. This table also shows that there was no statistically significant difference in gestational age between the two groups, even though the p-value was equal to the common alpha of (p. value = 0.000). Table (2) shows a comparison of neonatal studies conducted after 72 hours for the DCC and ECC groups. On the third day of life, there were extremely statistically significant variations (p 0.001) in newborn Hb and HCT. On the third day of life, total bilirubin considerably changes between the DCC and ECC groups. In contrast to 85.0% of the DCC group at 3 days old, the majority of the ECC group (93.7%) had normal bilirubin levels. Only 3.7% of people in the DCC group had high intermediate-risk bilirubin levels, as opposed to 2.5% in the ECC group. The total bilirubin had a mean of (6.28±2.89) mg/dl and a standard deviation of (8.27±3.52) mg/dl in the DCC group, where the mean was significantly higher than in the ECC group. Additionally, it was shown that there was a statistically significant difference in anemia between the two groups (p=0.023), but not in polycythemia (p=0.912).

Table (3) this table shows that more than half of both groups had infants weighing 3.5 kg or higher. All of the study group samples were crying and breathing before the chord was clamped, compared to 82.5 percent of the control group samples, who were crying and breathing before the cutting of the cord. For both groups, the majority of participants (75.6%) delivered placentas with normal weights, and the majority of women (90.6%) had umbilical cords with normal cord lengths. According to the placenta item, all factors in the relationship between the study and the control groups were found to be statistically significant (p-value 0.05). 

Table (7) these tables show how delayed cord clamping timing and newborn outcomes are related. It demonstrates that there was no statistically significant change in the length of the umbilical cord with the time of late cord clamping (P > 0.05), but there was a difference in the weight of the fetus and placenta with the delay in cord clamping (P < 0.05). Table (4) there was a significant association between both groups regarding early and late cord clamping (p 0.05), and the mean early cord clamping of the women in the control group (29.4 seconds) was significant (p 0.01); the majority (70.0%) of a woman within control group (immediate cord clamping less than thirty seconds just after the birth of the fetus), and (56.2%) of the women in the study group (delayed cord clamping 1-3 minutes after birth) (3.65 minutes).

Table (5) Age, parity, and time of delayed cord clamping were statistically different (less than 0.05), however, there was no significant statistical difference between gestational age, and time of late cord clamping (P > 0.05), based on this table.                                       

Table (6) these tables show how delayed cord clamping timing and newborn outcomes are related. It demonstrates that while there was no statistically significant difference between total bilirubin count and the time of delayed cord clamping (P > 0.05), there was a statistically significant difference between the mean and standard deviation of neonatal (hemoglobin and hematocrit) with the time of delayed cord clamping.

Table 1: Socio-demographic variables on the mothers in the two groups:

      **By Chi-square test.   *By Fisher’s exact test.             

       †By t-test for two independent samples

Table 2: Distribution of the study samples according to neonatal characteristics’ outcomes.

*By Fisher’s-exact test. **By Chi-square test. †By t-test for two independent samples

Table 3: Distribution of the study samples according to the placenta and umbilical cord.

  **By Chi-square test.                      *By Fisher’s exact test.                

Table 4: Distribution of the study samples according to the time of umbilical cord clamping.                                                                                                               

     *By Fisher’s exact test.                

DCC group was

divided into the 30–60 s DCC group (n= 256) and the

61–120 s DCC group (n= 163). Not all neonates had

hematological results. The heel blood sample size of 1–

3 days in the ECC group was 61, 25 and 33, and in the

DCC group was 53, 46 and 32, respectively (Fig. 1).

There were no significant differences in age, gravidity,

parity, gestational age, fetal birth weight, fetal sex and

Apgar score at 1 min and 5 min between the ECC group

and DCC group or DCC subgroups (p> 0.05) (Table 1).

DCC group was

divided into the 30–60 s DCC group (n= 256) and the

61–120 s DCC group (n= 163). Not all neonates had

hematological results. The heel blood sample size of 1–

3 days in the ECC group was 61, 25 and 33, and in the

DCC group was 53, 46 and 32, respectively (Fig. 1).

There were no significant differences in age, gravidity,

parity, gestational age, fetal birth weight, fetal sex and

Apgar score at 1 min and 5 min between the ECC group

and DCC group or DCC subgroups (p> 0.05) (Table 1).

Table 5: Association between the time of delayed cord clamping and socioemographic data.                                                                                                                                             

                       **By Chi-square test.                 *By Fisher’s exact test

Table 6: Association between the time of delayed cord clamping and neonatal outcomes

Table 7: Association between the time of delayed cord clamping and neonatal outcomes.

 **By Chi-square test           †by t-test for two independent samples

   DISCUSSION                                                                                                                   

     In total, 160 women were participating in the study. These women were either selected for the research group (n=80) who delayed cord clamping or in the control group (n=80) who had early cord clamping. Without a scientific evaluation of its potential effects on the health and development of a newborn, immediate cord clamping has developed a Standard procedure as part of the industrialized world's active management of the third stage of labor. Additionally, it is thought that early cord clamping as part of active treatment of the third stage of labor considerably lowers the risk of postpartum hemorrhage. Many active management guidelines require early cord clamping, which has encouraged some to suggest that postpartum hemorrhage risk could rise with delayed cord clamping. On the other hand, a recent World Health Organization protocol for managing the third stage of labor substituted delayed cord clamping for early cord clamping to produce significant maternal and newborn advantages.                                                                                               

 In this study, the mean age of the study group was (Mean± SD 28.5± 5.76), and 36.2% of the women in the study group were older than 30 years old. This distribution conflicts with the findings of Ahmed, S. S., (2017) in Egypt, who came to the conclusion that 53.3% of the women were in the 30- to 35-year-old age range. However, Elgzar, W. T., Ibrahim, H. A., & Elkhateeb, H. H. (2017) found that participants were typically between the ages of 20 and 30 years in their study.                                                                 

  The current study found a statistically significant difference between the early and delayed groups to respective age groups in terms of socio-demographic parameters. This finding contrasted with that of Elgzar, W. T., Ibrahim, H. A., & Elkhateeb, (2017), who found no significant association between socio-demographic data between both groups. Both groups were comparable with no significant difference regarding the obstetric history (multiparous), and gestational age (early cord clamping and delayed cord clamping).                                                                                           

 In a comparison of neonatal hematological parameters during the third day of life between the DCC and ECC groups, there was a highly significant increase in neonatal hemoglobin, and hematocrit, as well as a statistically significant increase in total serum bilirubin count. These results are consistent with those of the study by Elgzar, W. T., Ibrahim, H. A., and Elkhateeb, H. H., (2017), which discovered a highly significant correlation between the two groups' total serum bilirubin, hemoglobin, and hematocrit (early cord clamping and delayed cord clamping).                                                         

     According to the current study, only 66.2% of the study group's neonates were heavier than 3.5 kg, and there was no statistically significant correlation between birth weight with either group (early cord clamping and delayed cord clamping). The study by Ashish, K.C., et al. (2021), which came to the conclusion that there was a statistically significant difference in the weight of newborns and both groups, did not come to the same conclusion as ours.

   The results of this study showed that neither early nor late cord clamping groups showed a significant difference in placental weight or cord length (632.797.2&654.5118.5 and 65.011.7& 65.112.8, respectively).

         There was a significant association between both groups regarding early and late cord clamping (p 0.001) between the majority (70.0%) of the women in the control group (early cord clamping less than 30 seconds after the birth of the fetus) and (56.2%) of the women in the study group (delayed cord clamping 1-3 minutes after birth).                                                                                                                                

 According to the present study, there was no significant correlation between gestational age and two subgroups of delayed cord clamping (P > 0.05), however, there was a significant relationship between age, parity, and delayed cord clamping (P 0.05). Our findings did not agree with those of Qian, Y., et al. (2019), who found no statistically significant correlation between demographic factors and either of the two delayed cord clamping subgroups or the overall delayed cord clamping group (P > 0.05).                                                                                                                               

 Based on the present study, there was a statistically significant difference (P < 0.05) between the weight of the newborn and the two categories with delayed cord clamping. In contrast to the research conducted by Qian, Y., et al., (2019), our results indicated that there was no statistically significant difference in newborn weight between the groups receiving delayed cord clamping or among the two subgroups of delayed cord clamping (P > 0.05).                                                                                  

CONCLUSION: Delaying cord clamping increases hemoglobin and hematocrit without negatively affecting neonatal outcomes, shortens labor stages, and reduces the requirement for oxygen therapy for neonates. Additionally, the DCC group had a considerably higher mean total bilirubin level. In the first several months of life, delayed umbilical cord clamping increases iron storage. When the umbilical cord is clamped more slowly, there is a little increase in term newborns who need phototherapy for their jaundice. When doing delayed cord clamping on term infants, obstetrician-gynecologists and other obstetric care professionals should make sure that systems are in place to detect and treat neonatal jaundice. Finally, the results of the current study validated the research hypothesis and met the study's objective. Now that there is local data, a practice guideline can be developed to encourage delayed cord clamping at the Maternity Teaching Hospital in Sulaimani City.                                                                                      

ETHICAL CONSIDERATIONS

The scientific and ethics committees of the nursing and health sciences colleges at the University of Sulaimani authorized the study. Before collecting data, formal authorization was obtained from health and government authorities. Before collecting data, the study sample provided informed permission. The study received ethical approval from the Institutional Ethics Committee. 

RECOMMENDATION:

The Ministry of Health and hospital management should preserve delayed cord clamping as a standard procedure. According to the results of our study, obstetricians and midwives are paying more attention to delayed cord clamping as part of routine care and are emphasizing this practice as one of the overall quality standards to achieve the benefits for mothers and babies under the control of delayed cord clamping time. Create a program to educate expectant mothers about the advantages of delaying cord clamping, and apply the same research with a large sample size in various contexts.     

  LIMITATIONS OF THE STUDY

Some mothers refuse to allow blood to be drawn from their infants to test their hemoglobin, total serum bilirubin, and hematocrit levels. 72 hours later, the mother was expected to go to the Centers for Registration Bureau of Births and Deaths, but she never showed up, therefore the information is gone. It is challenging to collect blood from a baby due to its tiny veins. Low blood draws, which are insufficient for testing, present another challenge.

FUNDING
There are no funding sources. 

Conflict of Interest

The authors declare that they have no competing interests.

REFERENCES

Ahmed, S. S., Faheim, S. S., Hassan, H. E., & Meabed, M. A. (2017). Quasi-Experimental Study to Assess Consequences of Early Versus Delay Umbilical Cord Clamping on Maternal and Neonatal Outcomes in Beni-Suef city.

Ashish, K. C., Budhathoki, S. S., Thapa, J., Niermeyer, S., Gurung, R., Singhal, N., & Network, N. N. (2021). Impact of stimulation among non-crying neonates with intact cord versus clamped cord on birth outcomes: an observation study. BMJ paediatrics open, 5(1).

               https://doi.org/10.1136/bmjpo-2021-001207   

 Cardoso, R. M., Rodrigues, S. C., Gomes, C. F., Duarte, F. V., Romao, M., Leal, E. C., & Simões-Correia, J. (2021). Development of an optimized and scalable method for isolation of umbilical cord blood-derived small extracellular vesicles for future clinical use. Stem cells translational medicine, 10(6), 910-921. https://doi.org/10.1002/sctm.20-0376  

 De Bernardo, G., Giordano, M., De Santis, R., Castelli, P., Sordino, D., Trevisanuto, D., & Perrone, S. (2020). A randomized controlled study of immediate versus delayed umbilical cord clamping in infants born by elective caesarean section. Italian Journal of Pediatrics, 46(1), 1-6.

           https://doi.org/10.1186/s13052-020-00835-2  

 Elgzar, W. T. I., Ibrahim, H. A. F., & Elkhateeb, H. H. (2017). Effects of Deferred Versus Early Umbilical Cord Clamping on Maternal and Neonatal Outcomes. American Journal of Nursing, 5(4), 115-128.https://doi.org/10.12691/ajnr-5-4-3

 Fogarty, M., Osborn, D. A., Askie, L., Seidler, A. L., Hunter, K., Lui, K., ... & Tarnow-Mordi, W. (2018). Delayed vs early umbilical cord clamping for preterm infants: a systematic review and meta-analysis. American journal of obstetrics and gynecology, 218(1), 1-18.

https://doi.org/10.1016/j.ajog.2017.10.231

 Gomersall, J., Berber, S., Middleton, P., McDonald, S. J., Niermeyer, S., El-Naggar, W., ... & Soll, R. F. (2021). Umbilical cord management at term and late preterm birth: a meta-analysis. Pediatrics, 147(3).

https://doi.org/10.1542/peds.2020-015404

 Gupta, T., Singh, S., Gupta, S., & Gupta, N. (2018). Normal implantation, placentation, and fetal development. In Recurrent Pregnancy Loss (pp. 13-40). Springer, Singapore.

https://doi.org/10.1007/978-981-10-7338-0_2

 Katheria, A. C., Lakshminrusimha, S., Rabe, H., McAdams, R., & Mercer, J. S. (2017). Placental transfusion: a review. Journal of Perinatology, 37(2), 105-111.

https://doi.org/10.1038/jp.2016.151

 Khier, A., & Elghazaly, E. A. (2015). Correlation between the Umbilical Cord Morphology and Birth Weight in Full Term Sudanese Neonates (Doctoral dissertation, University of Gezira).

Korkut, S., Oğuz, Y., Bozkaya, D., Türkmen, G. G., Kara, Ö., Uygur, D., & Oğuz, Ş. S. (2021). Evaluation of the effects of delayed cord clamping in infants of diabetic mothers. American journal of perinatology, 38(03), 242-247.

https://doi.org/10.1055/s-0039-1695799

 Mebarki, M., Abadie, C., Larghero, J., & Cras, A. (2021). Human umbilical cord-derived mesenchymal stem/stromal cells: a promising candidate for the development of advanced therapy medicinal products. Stem Cell Research & Therapy, 12(1), 1-1

https://doi.org/10.1186/s13287-021-02222-y

Mneimneh, S., El Tal, R., Jomaa, M., Hamad, N., Yafawi, R., Ezzeddine, J., & Rajab, M. (2019). CPQ Women and Child Health (2019) 1: 5 Research Article.

 Nouraie, S., Akbari, S. A., Vameghi, R., & Baghban, A. A. (2019). The effect of the timing of umbilical cord clamping on hemoglobin levels, neonatal outcomes and developmental status in infants at 4 months old. Iranian Journal of Child Neurology, 13(1), 45.

 Qian, Y., Ying, X., Wang, P., Lu, Z., & Hua, Y. (2019). Early versus delayed umbilical cord clamping on maternal and neonatal outcomes. Archives of gynecology and obstetrics, 300(3), 531-543.

https://doi.org/10.1007/s00404-019-05215-8

 Seidler, A. L., Gyte, G. M., Rabe, H., Díaz-Rossello, J. L., Duley, L., Aziz, K., ... & Soll, R. (2021). Umbilical cord management for newborns< 34 weeks' gestation: a meta-analysis. Pediatrics, 147(3).

https://doi.org/10.1542/peds.2020-0576

 Um, S., Ha, J., Choi, S. J., Oh, W., & Jin, H. J. (2020). Prospects for the therapeutic development of umbilical cord blood-derived mesenchymal stem cells. World Journal of Stem Cells, 12(12), 1511.

https://doi.org/10.4252/wjsc.v12.i12.1511

 World Health Organization. (2012). WHO recommendations for the prevention and treatment of postpartum hemorrhage

 [cited 2018 November 19]. Available from: https://www.who.int/reproductivehealth/publications/maternal_perinatal_health/9789241548502/en/.

 World Health Organization. (2014). Guideline: delayed umbilical cord clamping for improved maternal and infant health and nutrition outcomes. World Health Organization.