Transfusion and Apheresis Science 48 (2013) 247–252

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Transfusion and Apheresis Science

journal homepage: www.elsevier.com/locate/transci

Factors predicting the hematopoietic stem cells content

of the umbilical cord blood
Suleimman A. Al-Sweedan a,⇑, Lama Musalam b, Basil Obeidat b
a
Department of Pediatrics, Jordan University of Science & Technology, P.O. Box 4614, Irbid 21110, Jordan
b
Jordan University of Science & Technology, Irbid, Jordan

a r t i c l e i n f o a b s t r a c t

Article history: Umbilical cord blood (UCB) has been demonstrated to be alternative source of hematopoi-
Received 8 January 2012 etic stem cells (HSCs). Unfortunately, the wide use of UCB Transplantation is limited due to
Received in revised form 23 October 2012 the low number of HSCs. The aim of this study was to determine factors that affect the
Accepted 10 January 2013
number of HSCs collected from UCB. 200 eligible donors were included for HSCs testing,
including total nucleated cells (TNCs) and CD34+ cell number, by using univariate and mul-
tivariate analysis. In univariate analysis, factors positively associated with higher number
Keywords:
of TNCs were maternal weight (P = 0.002), preeclampsia (P = 0.03), neonatal weight
Content
Hematopoietic
(P < 0.001), neonatal platelet count (P = 0.02), neonatal Rh (P = 0.03), gestational age
Stem cell (P = 0.04) and delivery type (P < 0.001). Factors positively associated with higher number
Umbilical cord of CD34+ cells were maternal weight (P < 0.007), preeclampsia (P = 0.02), maternal hyper-
tension (P = 0.02) neonatal weight (P < 0.001), neonatal Rh type (P = 0.02) and delivery type
(P = 0.04). In multivariate analysis, factors significantly influence TNCs were neonatal
weight (P < 0.001), preeclampsia (P = 0.008), neonatal Rh type (P = 0.02) and delivery type
(P < 0.001). While factors significantly influence number of CD34+ cells were maternal
weight (P = 0.025), neonatal weight (P = 0.005), neonatal Rh (P = 0.006), nuchal cord
(P = 0.026) and delivery type (P = 0.009). Conclusions factors significantly influence TNCs
content of UCB were neonatal weight, preeclampsia, neonatal Rh and delivery type. While
factors significantly influence number of CD34+ cells were maternal weight, neonatal
weight, neonatal Rh, nuchal cord and delivery type.
Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction high frequency of severe graft versus host disease (GVHD)

Hematopoietic stem cells (HSCs) are primitive cells that
maintain the structural and functional integrity of the
hematopoietic system [1,2]. Bone marrow (BM), peripheral
blood and umbilical cord blood (UCB) are sources that pro-
vide HSCs [3,4]. HSCs transplantation is an important key
for treating certain hematologic, genetic and malignant
disorders [5,6]. Access to BM transplantation is limited
by difficulties in finding suitable HLA-matched donors for
patients without matched siblings [7,8]. Even with fully
matched allogeneic BM grafts, its success is limited by a
⇑ Corresponding author. Tel.: +962 799051255.
E-mail address: sweedan@just.edu.jo (S.A. Al-Sweedan).
in the recipient [7]. Last decade has witnessed an increase
in the use of UCB as an alternative source of HSCs for allo-
genic transplantation due to several advantages of UCB
[9–15]. Practical advantages include ease of collection of
material that is discarded routinely, exists in almost limit-
less supply [16], without any discomfort or risk to the do-
nor, its prompt availability as a frozen graft and unlikely to
transmit infectious agents to the recipient [17,18]. More-
over, UCB Transplantation permits more liberal HLA-
matching [19]. So, it can be given to fully or partially
HLA-matched related or unrelated recipients [11,14]. UCB
shows decreased immune responses to alloantigen, with
a reported low incidence of severe acute and chronic GVHD
[20–22]. Efficacy of UCB Transplantation correlates mainly

1473-0502/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.transci.2013.01.003
248 S.A. Al-Sweedan et al. / Transfusion and Apheresis Science 48 (2013) 247–252
with HSCs dose and success being associated with the total
nucleated cells (TNCs) and CD34+ cells content infused
[23–26]. TNCs infused has been considered a reliable and
reproducible indicator of transplantation outcomes
[27,28]. Number of CD34+ cells is used as an additional
parameter to assess hematopoietic potential of UCB unit
[29,30]. Unfortunately, one restriction that limits the use
of UCB Transplantation, especially in large children and
adult patients, is the relatively low number of HSCs har-
vested from single UCB unit [15,31]. This results in slower
time to engraftment and higher transplant related mortal-
ity [16,32].
2. Materials and methods
2.1. Study design
A cross-sectional study design was used to examine the
association of certain study factors on the TNCs and CD34+
cells content of the UCB units.
2.2. Study population
2.2.1. Sampling population
Hospitals based study was carried out on 200 women
admitted to Princess Badea’a Hospital/Irbid/Jordan over
7 months period between Aug/2008 and Feb/2009. All
study subjects provided written informed consent in
accordance with the Helsinki declaration which was ap-
proved by the Institutional Review Board at Jordan Univer-
sity of Science and Technology.
2.2.2. Criteria for donor eligibility
Medical record of each mother participated in UCB
donation was reviewed. Mothers having any inherited,
infectious, including HIV I, HIV II, HBV and HCV, or any
other diseases or taking medications during pregnancy
were excluded. Other exclusion neonatal criteria were
the presence of congenital abnormality in the newborn,
twins, stillbirth or neonatal death. All infants 5-min Apgar
score was (9–10) and the results of the cardiotocogram
(CTG) were normal.
2.3. Data collection
2.3.1. UCB collection
UCB units were harvested ex-utero using open system
from both spontaneous vaginal and cesarean sections
deliveries with the help of the obstetricians and midwives.
Umbilical cord was clamped immediately after the
delivery process as close as possible to the infant within
30 s of birth. Then, a second clamp was applied around
5 cm from the first and the cord was cut between the
two clamps.
Two blood samples were drawn from the umbilical vein
at the most distal possible vein puncture site (closest to the
second clamp to minimize the loss of UCB) using needles
attached to EDTA anticoagulant blood tubes. After that,
the umbilical vein was un cannulated and blood was
drained by gravity from the transected end of the cord into
graduated sterile container until blood flow stopped. Total
volume of UCB was recorded, before these containers had
been discarded. Samples were kept in the refrigerator until
sent to the laboratory at KAUH/Irbid/Jordan within 24–
48 h of the collection for testing.
2.3.2. UCB testing
Two anticoagulant UCB specimens were drawn from
each subject for TNC and CD34+ cells measurement. Nucle-
ated cells content per micro liter of UCB (WBC counts)
were enumerated by an automated autoanalyzer (using
Pentra 80 autoanalyzer) at the Hematology Lab. This was
used to calculate the TNC content per UCB sample by mul-
tiplying WBC count with the UCB volume which is illus-
trated by the following equation: TNC count (per
unit) = WBC count  total UCB volume. The percentages
of CD34+ cells (the fraction of CD34+ cells within the leu-
kocyte population) were quantified by standard flow
cytometry using (FACScalibur cytometer with CellQuest
Pro software) which is based on using phycoerythrin (PE)
labeled monoclonal anti-CD34+ antibody after RBCs lysis
using lysing solution. Then, the absolute number of
CD34+ cells per UCB sample was measured by multiplying
the relative CD34+ cell count (percentage) with the of total
nucleated cells as detailed in the following equation: Abso-
lute number of CD34+ cells (per unit) = % CD34+ cells TNC
count.
2.3.3. Data collection of maternal, neonatal and obstetric
factors
Data collection sheets that included maternal, neonatal
and obstetric factors were filled from each participant
using medical record review or direct observation.
Maternal factors obtained include (Age, weight, smok-
ing status, ABO-Rh blood group, hypertension and pre-
eclampsia. While neonatal factors obtained include:
(gender, neonatal weight, birth order, ABO-Rh blood group,
hemoglobin concentration, platelet count and gestational
age). Finally, the examined obstetric factors were: delivery
type of either spontaneous vaginal or cesarean sections
and presence of nuchal cord (which is wrapping of umbil-
ical cord around the neck of the baby).
2.3.4. Statistical analysis
Statistical analysis was performed using the Statistical
Package for Social Sciences (SPSSs, version 15.0) software.
Descriptive statistics were provided to display the charac-
teristics of UCB HSC variables and maternal, neonatal and
obstetric factors. Data were analyzed for univariate analy-
sis using Spearman’s correlation coefficient for continuous
variables and Student’s t-test for categorical variables.
Multiple linear backward regression was also performed
to examine the effect of the various maternal, neonatal
and obstetric factors on the UCB HSC variables. Statistical
significance for all tests was considered at P value < 0.05.
3. Results
UCB was collected from 200 women; their mean age
was 28.29 years with a range of 18–44 years. 92% of the
 S.A. Al-Sweedan et al. / Transfusion and Apheresis Science 48 (2013) 247–252 249

babies were full term (37–42) weeks and 8% were prema- Table 2
ture babies delivered less than 37 weeks. Characteristics of Characteristics of the categorical variables of maternal,
neonatal and obstetric factors.
UCB variables, maternal factors, and neonatal factors are
shown in Tables 1 and 2. In univariate analysis, factors Variables Percentage (%)
positively associated with higher content of TNCs were Smoking status
maternal weight (P = 0.002), neonatal weight (P < 0.001), Yes 11.6
neonatal platelet count (P = 0.02), gestational age No 88.4

(P = 0.04) neonatal Rh type (negative vs. positive) Maternal ABO type

((1210.44 ± 480.58) 106) vs. ((999.68 ± 451.28) 106) (P = O 40.4
A 40.4
0.03), delivery type (vaginal vs. cesarean sections) B 14.3
((1077.13 ± 465.89) 106) vs. ((770.31 ± 321.84) 106) AB 4.9
(P < 0.001), and preeclampsia (yes vs. no) ((1218.94 ± Maternal Rh type
395.13) 106) vs. ((1008.12 ± 461.01) 106) (P = 0.03) as pre- Positive 86.3
sented in Table 3a (for continuous variables) and Table 3b Negative 13.7
(for categorical variables). On the other hand, factors posi- Preeclampsia
tively associated with higher number of CD34+ cells were Yes 8
maternal weight (P = 0.007), neonatal weight (P < 0.001), No 92
neonatal Rh type (negative vs. positive) ((25.20 ± 17.52) Hypertension
106) vs. ((17.20 ± 10.86) 106) (P = 0.02), delivery type Yes 9.5
No 90.5
(vaginal vs. cesarean sections) ((18.99 ± 12.55) 106) vs.
((14.11 ± 8.48) 106) (P = 0.04), preeclampsia (yes vs. no) Neonatal gender
Male 50.5
((23.69 ± 12.21) 106) vs. ((17.68 ± 11.98) 106) (P = 0.02)
Female 49.5
and hypertension (yes vs. no) ((23.38 ± 12.46) 106) vs.
Neonatal ABO type
((17.61 ± 11.94) 106) (P = 0.02) as outlined in Tables 3a
O 41
(for continuous variables) and Table 3b (for categorical A 38.5
variables). Multivariate analysis showed that main factors B 14
that significantly influencing TNCs were preeclampsia (wo- AB 6.5
man suffering from preeclampsia was helpful in obtaining Neonatal Rh type
0.16 more of TNCs value than those the non preeclampsia Positive 88
one) (P = 0.008), neonatal weight (0.43 increase of TNCs va- Negative 12

lue for each gram increase in the baby weight) (P < 0.001), Delivery type
neonatal Rh-type (negative Rh type of the newborn corre- Vaginal 83
Cesarean 17
lated with greater count of CD34+ cells of about 0.14)
(P = 0.02) and delivery type (normal vaginal deliveries Presence of nuchal cord
Yes 25
had 0.22 more amount of TNCs value than those from No 75
cesarean sections) (P < 0.009), as summarized in Table 4.
On the other hand, the results of multivariate model for
studying factors significantly influencing number of
CD34+ cells content are outlined in Table 5. These factors count was 0.21 higher for each gram increase in the neona-
were maternal weight (each kilogram increased in mater- tal weight) (P = 0.005), neonatal Rh-type (negative Rh type
nal weight was responsible for 0.17 increase in CD34+ cells of the newborn correlated with greater count of CD34+
value) (P < 0.025), neonatal weight (Likewise, CD34+ cell cells of about 0.20) (P = 0.002), delivery type (normal vag-
inal delivery was associated with 0.18 more yield of CD34+
cells compared to cesarean sections) (P = 0.009) and nuchal
Table 1
cord (in which absence of nuchal cord associated with 0.15
Characteristics of UCB variables, maternal factors, and neonatal factors. higher CD34+ cells content) (P = 0.026).

Variables Mean ± std. Range

deviation
4. Discussion
UCBa volume (ml) 75.69 ± 20.76 30–155
TNCb (106) 1024.97 ± 458.80 276–2562
CD34+ cells number (106) 18.16 ± 12.08 2.27–71.81 Many previous studies worldwide pointed out the im-
Maternal age (year) 28.29 ± 5.85 18–44 pact of several maternal, neonatal and obstetric factors
Maternal weight (kg) 74.62 ± 12.85 45–114 on the concentration of HSCs of the UCB units. Indeed, this
Neonatal weight (gm) 3200 ± 491.35 1400–4650
is the first study dealt with this topic in our country and
Neonatal [hemoglobin]c (gm/dl) 15.55 ± 1.90 10.9–24.8
Neonatal platelet count 334.32 ± 110.25 24–718 the Middle East. Ballen et al., indicated that maternal age
(103/mm3) had no effect on the laboratory parameters of UCB units.
Gestational age (week) 38.89 ± 1.89 28–42 Heavier babies had higher TNCs and CD34 cells. Babies
Birth order 3.18 ± 2.03 1–11
with longer gestational age had higher cell counts [33].
a
UCB = umbilical cord blood. The weight of infant is a consistent predictor in the prior
b
TNCs = total nucleated cells. analysis, where neonatal weight was the most significant
c
[hemoglobin] = hemoglobin concentration. of all factors assessed. This observation is not surprising
250 S.A. Al-Sweedan et al. / Transfusion and Apheresis Science 48 (2013) 247–252

Table 3a
Correlation coefficient of TNCs and CD34+ cells number with certain factors.

Continuous variables TNCs CD34+ cell number

Spearman coefficient P value Spearman coefficient P value
Maternal weight (per kg) 0.22 0.002 0.19 0.007
Neonatal weight (per gm) 0.43 <0.001 0.27 <0.001
Neonatal platelet count (per unit) 0.17 0.02 0.13 0.07
Gestational age (per week) 0.15 0.04 0.07 0.29

Table 3b
T-test Distribution of TNCs and CD34+ cells number with certain factors.

Categorical variables TNCs CD34+ cell number

(Mean ± SD)  106 P value (Mean ± SD)  106 P value
Neonatal Rh-type (negative vs. positive) 1210.44 ± 480.58 vs. 999.68 ± 451.28 0.03 25.20 ± 17.52 vs. 17.20 ± 10.86 0.02
Delivery type (vaginal vs. cesarean section) 1077.13 ± 465.89 vs. 770.31 ± 321.84 <0.001 18.99 ± 12.55 vs. 14.11 ± 8.48 0.04
Preeclampsia (yes vs. no) 1218.94 ± 395.13 vs. 1008.12 ± 461.01 0.03 23.69 ± 12.21 vs. 17.68 ± 11.98 0.02
Hypertension (yes vs. no) 1159.95 ± 482.09 vs. 1010.80 ± 455.36 0.13 23.38 ± 12.46 vs. 17.61 ± 11.94 0.02

of the blood through the cord and less volume and HSCs
Table 4
Factors significantly influence TNCs in multivariate analysis. content obtained. Moreover, this study found infant gender
and gestational age were not statistically significant fac-
Variables Beta coefficient P value
tors, as indicated by ours. On the other hand, Askari and
Preeclampsia coworkers showed opposite results to our study. They sug-
No 0.16 0.008
gested that female newborns and cesarean sections were
Yes
positively associated with greater product indicators by
Neonatal weight (per gm) 0.43 <0.001
using univariate analysis [34]. This result contradicted
Neonatal Rh-type with a large cohort study by Cairo et al. which approved
Positive 0.14 0.02
that male baby was associated significantly with an in-
Negative
crease in the CD34+ cells [20], and still disagreed with ours.
Delivery type
It is noteworthy that neonatal gender was considered as a
Cesarean 0.22 0.009
Vaginal huge argumentation point in the prior reports with antag-
onized results. In all situations, there was no obvious
explanation. George et al. concluded that neonatal birth
weight, but not gender or gestational age correlated
Table 5
Factors significantly influence number of CD34+ cells in multivariate
strongly with UCB cell counts [25], supported strongly
analysis. our study. Furthermore, our results disapproved with Yam-
ada and colleagues who found that cesarean sections may
Variables Beta coefficient P value
allow collection of significantly increased volume of UCB
Maternal weight (per kg) 0.17 0.025 and numbers of CD34+ cells compared to vaginal deliveries
Neonatal weight (per gm) 0.21 0.005 [35]. It is expected that during cesarean section delivery,
Neonatal Rh-type there is chance of missing more cord blood and forming
Positive 0.20 0.002 clots, leading to obtain less volume of UCB units compared
Negative with vaginal delivery. A study by Jan et al. investigated in
Delivery type its multivariate analysis that babies delivered via cesarean
Cesarean 0.18 0.009 sections had more CD34+ cells and volume, but lower
Vaginal
TNCs. Similar results were found for either baby of shorter
Nuchal cord gestational age or in male infant. Moreover, mothers with
Yes 0.15 0.026
No
fewer previous live births had UCB with more TNCs [36].
These conclusions antagonized ours. On the other hand,
this study added babies with larger birth weight had high-
in view of the well-known direct correlation between in- er CD34+ cell count and TNCs and maternal age had no ef-
fant and placental weight and fetoplacental blood volume. fect on those parameters, which one hundred percent
Moreover, having more volume expectedly associated with matched ours. Only one study in the literature evaluated
more nucleated cells and CD34+ cells content. Jones et al. the possible effect of infant ABO-Rh (D) blood group on
indicated that delivery type, nuchal cord, and birth weight the proliferative and self-renewal capacity of UCB CD34+
were factors significantly influence the volume of UCB [7]. cells. It has suggested that ex vivo proliferation of CD34+
These results were similar to those obtained by us except cells with O phenotype may be greater than that of cells
for the presence of nuchal cord. We suggested that pres- with the A or B phenotypes [37]. This result disagreed with
ence of nuchal cord may restrict mechanically the passage ours in the part of neonatal ABO blood group had no effect
 S.A. Al-Sweedan et al. / Transfusion and Apheresis Science 48 (2013) 247–252
on CD34+ cells yield. Surbek et al. indicated pregnancies af-
fected by compared with control subjects [38]. This result
went against ours. The relationship between preeclampsia
and high cell count of UCB units is unclear. This factor was
evaluated once in the literature. However, it is noteworthy
that the unequal distribution and wide difference between
the two categories of this factor might contribute to inac-
curate analysis. In which pregnancies suffering from pre-
eclampsia consisted only 8% of the total population
compared to the non preeclampsia group (92%). This wide
difference was also noted in our study between categories
of the following factors (mothers suffering from hyperten-
sion, neonatal Rh-type and delivery type). Our study was
the first in the literature that evaluated the impact of
maternal weight during pregnancy on the content of UCB
of the HSCs. This factor was found to be a significant and
strong predictor that positively increased number of
CD34+ cells of UCB units, and should be added to the stan-
dard cord blood donor criteria for donation. Furthermore,
other factors that firstly examined in our study were preg-
nancies suffering from hypertension, neonatal ABO blood
group, neonatal platelet count and neonatal hemoglobin
concentration which all had no effect on the outcome vari-
ables. And depending on our study, there should not be ta-
ken in consideration during donation. Neonatal Rh-type
was other factor studied for the first time and showed a
significant association with TNCs and CD34+ cells content
of the UCB units. Regarding smoking status, there were
contradictory results between the previous studies. So, fur-
ther analysis including more details about the -quantity of
smoking per day, since when it has been started and the
type of cigarettes- should be performed. Moreover, the ef-
fect of the wide range between percentages of smokers
(11.6%) and nonsmokers (88.4%) presented in our study
should be overcome.
In conclusion, our study suggested factors that signifi-
cantly influence TNCs content of UCB units were neonatal
weight, pregnancies affected with preeclampsia, neonatal
Rh type and delivery type. While factors significantly influ-
ence number of CD34+ cells were maternal weight, neona-
tal weight, neonatal Rh type, nuchal cord and delivery type.
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