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Original Article

Evaluation of Neonatal Jaundice Based on the Severity of

Hyperbilirubinemia
Hassan Boskabadi, Majid Sezavar1, Maryam Zakerihamidi2

Department of Pediatrics, Introduction: Recognition of the characteristics of neonatal jaundice with

Abstract
Neonatal Research Centre,
Faculty of Medicine,
different levels of severity can help the physician with appropriate treatment and
Mashhad University prediction of complications. This study aimed to determine the characteristics of
of Medical Sciences, neonatal jaundice in different levels of severity. Materials and Methods: This
1
Department of Pediatrics, cross‑sectional study was performed on 3005 neonates referring to the   Neonatal
Faculty of Medicine, Intensive Care Unit, Clinic, and Emergency ward in Ghaem Hospital of Mashhad,
Mashhad University of Iran, from 2009 to 2018. Sampling was carried out through the convenience
Medical Sciences, Mashhad,
2
Department of Midwifery,
sampling method. The data collection tool was a researcher‑made questionnaire,
School of Medical Sciences, including laboratory evaluation, as well as assessment of maternal and neonatal
Islamic Azad University, characteristics. The newborns were divided into six groups based on the serum
Tonekabon Branch, bilirubin level and then compared in terms of characteristics, causes, and prognosis
Tonekabon, Iran according to the severity of jaundice. The data were analyzed using the Student’s
t‑test and Chi‑square test. Results: In most cases, the present of jaundice was
reported between 2 and 3  days of birth, and the age of neonates’ reference was
between 6 and 8  days of birth. Causes of neonatal jaundice included unknown
reasons  (61.25%), increased production of bilirubin  (22%), severe weight
loss (7%), infections (5.3%), endocrine disorders (2.5%), and other causes (1.7%).
In jaundice level lower than 25  mg/dl, about 15% of neonates were reported with
complications; however, at the bilirubin level higher than 35 mg/dl, approximately
40% of newborns had complications. Conclusion: The known causes of the
jaundice were mostly observed in the increased bilirubin production level higher
Received: 25th July, 2019
Revision: 08th September, 2019 than 25 mg/dl.
Accepted: 19th November, 2019
Publication: 29th January, 2020 Keywords: Dehydration, hyperbilirubinemia, infection, neonates

Introduction neonatal jaundice are prematurity, race, drugs, high

N eonatal hyperbilirubinemia is observed as
the serum total bilirubin level is higher than
5 mg/dl (i.e., 86 µmol/L).[1] Neonatal jaundice is a
common problem that is benign in most cases; however,
high levels of bilirubin are neurotoxic and can lead to
serious damage to the brain.[2] Therefore, the American
Academy of Pediatrics recommends that the neonates
who are discharged within the first 48 h should have
two follow‑up visits. The first and the second follow‑up
visits should be during the 1st–3rd  and 3rd–5th  days,
respectively. If no follow‑up is possible, the neonatal
discharge is delayed from the 3rd to 4th days until the
risk period is passed.[3] Some of the risk factors for
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altitude, polycythemia, male gender, trisomy 21,
cephalohematoma, breastfeeding, weight loss, delayed
meconium pass, history of jaundice in family,[4] ABO
or RH incompatibility, mode of delivery, and maternal
diabetes.[5]
Kernicterus or bilirubin encephalopathy, as a preventable
neurological syndrome with undesirable side effects,
is caused by unconjugated bilirubin deposition in the
Address for correspondence: Dr. Maryam Zakerihamidi,
Department of Midwifery, School of Medical Sciences,
Islamic Azad University, Tonekabon Branch, Tonekabon, Iran.
E‑mail: maryamzakerihamidi@yahoo.co.nz
This is an open access article distributed under the terms of the Creative Commons
Attribution‑NonCommercial‑ShareAlike 4.0 License, which allows others to remix,
tweak, and build upon the work non‑commercially, as long as the author is credited
and the new creations are licensed under the identical terms.
For reprints contact: reprints@medknow.com

DOI: How to cite this article: Boskabadi H, Sezavar M, Zakerihamidi M. Evaluation

10.4103/jcn.JCN_81_19 of neonatal jaundice based on the severity of hyperbilirubinemia. J Clin
Neonatol 2020;9:46-51.

46 © 2020 Journal of Clinical Neonatology | Published by Wolters Kluwer ‑ Medknow

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Boskabadi, et al.: Neonatal jaundice based on the severity
cortical nuclei and brain stem.[6] Kernicterus is observed
in one‑third of the neonates with hemolytic anemia and
bilirubin level of 25–30 mg/dL who have not undergone
the treatment. Incidence of kernicterus has been reported
as 2%–16% in the autopsy of premature neonates with
hyperbilirubinemia.[7] Kernicterus has been reported in
term newborns from 1 to 30,000 to 1 in 200,000 live
births in developed countries.[8]
The first presentations of kernicterus are lethargy,
poor feeding, and weakend reflex. Following that,
the neonate is weakened and suffers from respiratory
distress leading to opisthotonus, bulging fontanelle,
abnormal movements in the face and limbs, as well as
specific crying.[9] Discharge avoidance of neonates at
risk of jaundice, appropriate follow‑up after discharge,
informing parents of the importance and follow‑up
of neonatal jaundice, phototherapy, and in resistant
cases, rapid blood exchange in neonates can reduce the
complications of jaundice. The neonates with bilirubin
level  >20  mg/dl should be appropriately monitored and
treated in terms of sensorineural hearing impairment,
developmental status, and eye condition.[10]
Appropriate strategy in the diagnosis, treatment, and
follow‑up of jaundice has always been one of the
major challenges in neonatal medicine. Prevention of
jaundice, early diagnosis, as well as proper treatment
and prevention of related complications, can reduce
the problems of neonatal jaundice. Identifying the
characteristics of neonates with jaundice in different
levels of severity can help physicians in the process
of jaundice, appropriate treatment, and prediction of
complications.
Considering the high prevalence of jaundice in
Asian countries, such as Iran, associated with serious
complications, and since the early referral of neonates
with jaundice to hospitals and proper management
increase the health of neonates and reduce the associated
problems, this study aimed to identify the characteristics
of neonates with jaundice in different levels of severity.
Materials and Methods
In this cross‑sectional study, out of 25,000 neonates
referred to the Neonatal Intensive Care Unit, Clinic, and
Emergency Department in Ghaem Hospital of Mashhad,
Iran, 3005 newborns with jaundice were selected and
enrolled in the study. The neonates with insufficient
evaluation  (n  =  89), no tendency to continue the
cooperation  (n  =  43), no enough data from fetal period
or delivery period  (n  =  63), and those who left the
hospital before the complete evaluation  (n  =  91) were
excluded from the present study.
Journal of Clinical Neonatology ¦ Volume 9 ¦ Issue 1 ¦ January-March 2020
This study was approved by the Ethics Committee of
the Research Deputy of Mashhad University of Medical
Sciences. In addition, consent form was obtained from
the parents of the patients before entering the study.
Patients’ data were recorded in a questionnaire designed
for this purpose. Content validity of the questionnaire was
confirmed by five members of the Faculty of Medicine.
In neonatal evaluation, age at referral, age of jaundice,
cause of jaundice, complications of jaundice, neonate
gender, mode of delivery, and pregnancy problems were
recorded, and the complete examination of newborns
was performed following that. Then, all the requested
tests were conducted to examine the causes of jaundice,
including hematocrit, platelet, direct and indirect
bilirubin, Coombs test, neonatal and maternal blood
groups, glucose‑6‑phosphate dehydrogenase  (G6PD),
urine culture, and other tests, if necessary, depending on
the doctor’s opinion. The neonates were divided into six
groups based on the serum bilirubin level, and then the
characteristics, causes, and prognosis of these neonates
were compared based on the severity of jaundice.
Urine specimens were obtained from the patients with
suprapubic aspiration, and if the parents were not
satisfied, it was provided with a urine bag under clean
conditions, at least two cultures with colony count higher
than 100,000. In addition, the presence of leukocyturia
or bacteriuria was necessary for the diagnosis of urinary
tract infection. The urine specimen was examined in
terms of microscopy, leukocyturia, and bacteriuria.
Leukocyturia refers to the cases in which more than
five leukocytes are observed in the high power field.[11]
Diagnosis of sepsis is based on positive blood culture,
along with clinical symptoms, and the confirmation of
pneumonia is according to radiography with clinical
symptoms. Three groups of sepsis, pneumonia, and
urinary tract infection in a single group have been
introduced as the infectious agents.
The RH incompatibility is diagnosed when the
maternal RH is negative, the neonatal RH is positive,
and direct Coombs test is reported positive. The ABO
incompatibility is diagnosed when the maternal blood
group is O, and the neonatal blood group is A or B, and
there are at least two of the following conditions:
1. First‑day jaundice
2. Positive direct Coombs test
3. Presence of microspherocytosis in the peripheral
blood
4. Positive indirect Coombs test.
When there is no RH or ABO incompatibility but
positive report of direct Coombs test, it is considered
subgroup incompatibility.[6] Three groups of ABO and
47
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Boskabadi, et al.: Neonatal jaundice based on the severity

RH incompatibility, as well as the subgroups, were In this study, the causes of neonatal jaundice
placed in a larger group as blood incompatibility. Activity included unknown causes  (61.25%), increased
of G6PD was evaluated by a semiquantitative and dye bilirubin production  (22%), severe weight loss  (7%),
fluorescence method, and activity level lower than infections  (5.3%), endocrine disorders (2.5%), and other
30 was considered enzyme deficiency. The neonates with causes  (1.7%). The most common causes of jaundice
jaundice were divided based on the causes of jaundice in neonates with bilirubin levels  <15 were unknown
with the increased production of bilirubin, including causes (67.5%), increased bilirubin production (19%), and
the incompatibilities of blood group, RH, subgroups, infection (6.8%). The most common causes of jaundice in
G6PD deficiency, cephalohematoma, polycythemia, skin different levels of bilirubin severity were as follows:
ecchymosis, adrenal bleeding, and brain hemorrhage. 1. Bilirubin levels within 15.1–20  mg/dL:
Unknown causes  (65.4%), increased bilirubin
The neonates with weight loss lower than 10% or daily
production (18.2%), and infection (6.3%)
loss lower than 2% with the unknown causes of jaundice
2. Bilirubin levels within 20.1–25  mg/dL:
were considered jaundice cases with dehydration. The
Unknown causes  (62.2%), increased bilirubin
newborns with diabetic and hypothyroidism mothers
production (22.1%), and dehydration (9.2%)
were categorized as endocrine causes. Other causes
3. Bilirubin levels within 25.1–30  mg/dL:
include Crigler‑Najjar and congenital heart disease.
Unknown causes  (50.8%), increased bilirubin
Follow‑up of newborns with jaundice in terms of
production (24.6%) and dehydration (10.4%)
disease development was performed using Denver
4. Bilirubin levels within 30.1–35  mg/dL: Unknown
II Developmental Screening Test in four domains
causes (43%), increased bilirubin production (40.9%),
of personal‑social, subtle‑adaptive movements,
and dehydration (5.4%)
language (i.e., speech), and rough movements.
5. Bilirubin levels within 35–38  mg/dL: Increased
If there is a problem in each of the four above‑mentioned bilirubin production  (64.4%), unknown
domains, it is considered a developmental delay; if causes (25.4%), and dehydration (6.8%) [Table 2].
there is a problem in just one domain, it is considered
In terms of gender, jaundice was more common in
mild developmental delay; if there is a problem in two
male newborns at all levels of bilirubin  >20, except
domains, it is considered moderate developmental delay;
in the bilirubin levels of 5–15. In bilirubin levels of
and if there is a problem in three or four domains, it
is considered severe developmental delay.[12] The data
were analyzed by SPSS software (version 16, SPSS Inc.,
Chicago, Ill, USA). Moreover, the data were described
using mean, standard deviation, and frequency tables. In
addition, the data were analyzed by the Student’s t‑test
and Chi‑square test. P < 0.05 was considered statistically
significant.

Results
Regarding the frequency of total bilirubin, most neonates
in the present study were reported with the bilirubin
level of 15.1–20 mg/dL [Figure 1].
In most cases, the present age of jaundice was
reported between 2 and 3  days of birth; however, the
age of the neonate referral was between 6 and 8  days Figure 1: Distribution of jaundice frequency regarding the severity of
of birth [Table 1]. jaundice

Table 1: Comparison of neonatal characteristics in different levels of jaundice severity

Variables Groups
5–15 (mg/dL) 15.1–20 (mg/dL) 20.1–25 (mg/dL) 25.1–30 (mg/dL) 301–35 (mg/dL) 35–38 (mg/dL)
Present age of jaundice (day)* 1.14±2.51 1.60±2.95 2.18±3.11 2.04±2.98 1.40±2.29 2.23±2.25
Age of hospitalization (day)* 4.67±6.12 5.21±8.11 4.43±8.38 4.56±8.23 5.38±7.85 4.22±7.10
Hematocrit* 8.21±45.42 7.23±45.52 7.66±45.20 8.17±44.68 5.48±41.35 8.42±45.02
Platelet count* 99.89±250.23 111.03±279.87 98.53±285.26 111.96±297.72 108.92±253.71 108.66±239.36
*Values based on mean±SD. SD: Standard deviation

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Boskabadi, et al.: Neonatal jaundice based on the severity

Table 2: Comparison of neonatal and maternal variables in different levels of jaundice severity
Variables Groups
<15 (mg/dL), 15.1–20 (mg/dL), 20.1–25 (mg/dL), 25.1–30 (mg/dL), 30.1–35 >35 (mg/ P Chi‑square
n (%) n (%) n (%) n (%) (mg/dL), dL), test
n (%) n (%)
Unknown causes 199 (67.5) 679 (65.4) 530 (62.2) 151 (50.8) 40 (43) 15 (25.4) 0.000
Increased bilirubin 56 (19) 189 (18.2) 188 (22.1) 73 (24.6) 38 (40.9) 38 (64.4) 0.000
production
Infection 20 (6.8) 65 (6.3) 28 (3.3) 20 (6.7) 4 (4.3) 2 (3.4) 0.000
Endocrine 8 (2.7) 25 (2.4) 12 (1.4) 19 (6.4) 4 (4.3) 0 (0) 0.000
Dehydration 9 (3.1) 58 (5.6) 78 (9.2) 31 (10.4) 5 (5.4) 4 (6.8) 0.000
Other causes 3 (1) 23 (2.2) 16 (1.9) 3 (1) 2 (2.2) 0 (0) 0.000
Gender
Male 150 (49) 646 (61.1) 503 (57.2) 229 (56.4) 64 (55.2) 50 (61.7) 0.008
Female 156 (51) 412 (38.9) 377 (42.8) 177 (43.6) 52 (44.8) 31 (38.3)
Mode of delivery
Vaginal 157 (53.8) 521 (52.7) 459 (56.3) 139 (52.7) 63 (68.5) 31 (59.6) 0.062
Cesarean section 135 (46.2) 467 (47.3) 356 (43.7) 125 (47.3) 29 (31.5) 21 (40.4)

5–15, 15.1–20, 20.1–25, 25.1–30, and 30.1–35  mg/dL,
27.6%, 24.2%, 23.9%, 27.6%, and 18.6% of mothers
were reported with pregnancy problems, respectively.
In the present study, the complications of neonatal
hyperbilirubinemia included acute kernicterus, abnormal
auditory brainstem response  (ABR), developmental
delay at the age of 3 years old, and abnormal eye status.
Discussion
In the present study, half of the neonates who were
referred due to jaundice had bilirubin levels  >20  mg/dl
that confirms the late referral of the parents. Based on
the results of this study, in most cases, the incidence
age of jaundice was between 2 and 3  days after birth;
however, the age of the neonate referral was between
6 and 8  days after birth. The parents referred to a
physician about 4  days after they noticed jaundice. In
one study, neonates with ABO incompatibility on days
3–8 after birth, newborns with Rh incompatibility on
days 1–7 after birth, neonates with G6PD deficiency
on days 1–10 after birth, and newborns with blood
subgroups incompatibility on days 2–7 after birth
referred to the hospital.[6]
According to the results of a study, jaundice presented in
G6PD‑deficient neonates with 3  days of age who were
referred at 7 days of age. Moreover, although the incidence
age of blood incompatibility in newborns was the first
3  days, they referred about 2  days afterward. Therefore,
the referral of these newborns in the most common time
of occurrence and reception of appropriate and timely
treatment can help reduce serious complications, such as
kernicterus, and increase their health.[13]
Therefore, the late referral of parents despite noticing
jaundice suggests that parents do not know the
importance of jaundice and maybe jaundice is not
taken seriously by medical personnel. As a result,
given the importance of jaundice and its preventable
complications, training mothers since pregnancy period
about the symptoms of jaundice, timely referring of
neonates with jaundice, and informing physicians and
medical team are very helpful in the reduction of the
serious complications of jaundice such as jaundice.
Cause of jaundice was unknown in two‑thirds of the
neonates in the present study, and the most common cause
of jaundice  (22%) was the increased levels of bilirubin
production, including blood group incompatibilities, RH,
G6PD deficiency, cephalohematoma, polycythemia, skin
ecchymosis, adrenal hemorrhage, and brain hemorrhage.
Hemolytic causes play a greater role in increasing the
severity of jaundice so that about 19% of neonates with
bilirubin level  <15 had hemolytic jaundice. However,
64% of neonates with bilirubin level  >35 had hemolytic
jaundices. In addition, the level of hematocrit decreased
with increasing bilirubin levels.[6]
According to the literature, the known causes of
jaundice was identified in 27.9%, known causes of the
jaundice included blood groups incompatibility  (40%),
infection  (19%), deficiency of glucose 6‑phosphate
dehydrogenase  (12%), endocrine disorders  (8%),
hypernatremic dehydration  (7%), polycythemia  (6%),
congenital heart disease  (4%), occult bleeding  (3%) and
Crigler‑Najjar syndrome  (2%).[13] In a study conducted
by Najib et al., the causes of severe hyperbilirubinemia
included ABO and RH incompatibility, G6PD deficiency,
sepsis, and unknown causes.[14]
The second known cause was severe dehydration  (7%),
of which about 80% had jaundice  <25  mg/dl and 40%

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Boskabadi, et al.: Neonatal jaundice based on the severity
<20  mg/dl. Healthy neonates who are hospitalized due
to hyperbilirubinemia may be suffering from dehydration
and prerenal azotemia, which is neglected, leading
to kidney failure or hypernatremia and neurological
outcomes. Therefore, it is recommended to measure
the levels of urea, creatinine, and electrolytes of blood
in hyperbilirubinemia neonates with significant weight
loss.[15] In another study, hypernatremia was associated
with severe hyperbilirubinemia (i.e., bilirubin >25 mg/dl)
in 20% of neonates that increased the probability of
long‑term neurological outcomes; because hypernatremia
and hyperbilirubinemia worsen the cycle of dehydration,
jaundice, and hypernatremia, leading to brain damage.[16]
The third known cause of jaundice is infection that
accounts for about 5% of the causes of jaundice
(i.e., urinary tract infection, sepsis, and pneumonia).
Most infectious cases had bilirubin levels  <20  mg/dl
(i.e., 60% of cases), and the risk of infection as a cause
of jaundice has decreased with the increased severity of
jaundice. Based on the evidence, infections have been
the second most common cause of jaundice with the
highest incidence after the 1st week of life. Urinary tract
infection (13%) and sepsis (5.6%) are the known causes
of jaundice, and the most common cause of jaundice
after 13 days was urinary tract infection (15.5%).[13]
Endocrine disorders  (in neonates of diabetic and
hypothyroid mothers) in 50% of cases have bilirubin
levels  <20  mg/dl. Newborns of diabetic mothers
have several problems, including prematurity and
its complications, hypoglycemia, macrosomia, and
jaundice.[17] There are various causes for the occurrence
of jaundice in the neonates of diabetic mothers, including
prematurity, polycythemia, macrosomia, and poor
control of maternal glucose, increased concentration of
free fatty acids following hypoglycemia, and ineffective
hematopoiesis.[18]
In one study, the neonate of diabetic neonates  (4%) and
hypothyroidism  (4.2%) were the causes of jaundice that
jaundice occurred at 3 days of age in neonates of diabetic
mother and had referred at 8 days of age, while jaundice
occurred at 4  days of age in neonates of hypothyroidism
mothers and had referred at 13 days of age.[13]
In macrosomic neonates of diabetic mothers, bilirubin
levels increase due to hemoglobin F, polycythemia,
or ineffective hematopoiesis.[19] Results of a study
carried out by Keren showed that gestational diabetes
mellitus has various and dangerous side effects on
the neonate, the most common of which is neonatal
jaundice  (17.3%).[20] Karamizadeh demonstrated
that the most common clinical finding in congenital
hypothyroidism is prolonged icter.[21] Cause of jaundice
50 Journal of Clinical Neonatology ¦ Volume 9 ¦ Issue 1 ¦ January-March 2020
in hypothyroidism is not exactly clear; however, it is
probably due to the decreased activity of the enzyme of
uridyl glucuronyl transferase, which may be lower than
normal for weeks or months.[6]
In terms of gender, most of the neonates were male at
all bilirubin levels higher than 20  mg/dl, except for the
bilirubin level of 5–15  mg/dl. In a study carried out by
Saber et al., about 53% of the neonates were male.[22]
In other studies also male gender was a risk factor for
neonatal jaundice.[5,23] No cause for a higher prevalence
of jaundice in boys has been mentioned in the review of
the literature.
Complications of jaundice increased with increasing
the levels of total bilirubin. Mechanism of neurological
damage caused by bilirubin is not completely known,
and several pathways, such as bilirubin‑induced lipid
peroxidation, nerve inflammation, as well as sustained
energy failure, seem to be involved. Unconjugated
bilirubin has direct effects on plasma membranes,
mitochondria, or endoplasmic reticulum, leading to
defects in mitochondrial energy and levels of elevated
intracellular calcium. These mechanisms, either directly
or indirectly, cause apoptosis and cell necrosis. If the
exposure to unconjugated bilirubin lasts for a long time,
it causes irreversible neurological damage.[24] Immaturity
of brain cells, especially in preterm neonates, increases
neuronal damage even at lower levels of bilirubin.[25]
In the bilirubin level  >35  mg/dl, 60% of neonates
had abnormal ABR. According to the evidence, it is
suggested that hearing neural pathways are the most
sensitive system to bilirubin toxicity associated with
hearing loss.[26] Results of one study revealed that
bilirubin level had a predictive power of about 82% for
the prognosis of sensory‑neural hearing disorders.
Hearing disorders in neonates with severe jaundice is
about 10–50 times higher in comparison to the newborns
with other disorders, and this disorder is associated
with the severity, cause, and treatment method of
hyperbilirubinemia. Therefore, the screening of neonates
with jaundice using ABR helps to early diagnose
hearing impairment caused by hyperbilirubinemia,
conduct appropriate treatment, and ultimately promote
children health.[27] Limitation of the present study was
not considering the referral time of neonates. Therefore,
it is recommended to carry out future studies with larger
sample sizes and subjects’ matching in terms of the
referral time to the hospital.
Conclusion
In the present study, the parents of the neonates had
referred about 3–4  days after noticing their neonates’
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Boskabadi, et al.: Neonatal jaundice based on the severity
jaundice that might be the cause of severe jaundice in
their newborns. The most common known causes of
jaundice were increased bilirubin production  (22%),
severe weight loss  (7%), infections  (5.3%), and
endocrine causes  (1.7%). Hemolytic causes played a
greater role in increasing the severity of jaundice so that
64% of neonates with bilirubin levels  >35  mg/dl had
hemolytic causes.
Severity of neonatal jaundice was mild to moderate
with infectious causes, dehydration, endocrine
disorders. However, increased bilirubin production was
determined as the most known cause of jaundice in
cases with bilirubin levels  >25  mg/dl. Rate of jaundice
complications increased with the increase in total
bilirubin levels; therefore, 15% of the neonates had
complication in bilirubin levels <25 mg/dl. Nevertheless,
about 40% of the newborns had complications in
bilirubin levels >35 mg/dl.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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