Early Human Development 99 (2016) 5356

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Early Human Development

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

Inuence of hyperbilirubinemia on neonatal sucking

Ruben Bromiker a,b, Barbara Medoff-Cooper c, Hadar Flor-Hirsch b, Michael Kaplan a,b,
a
b
c

Department of Neonatology, Shaare Zedek Medical Center, Jerusalem, Israel

The Faculty of Medicine of the Hebrew University, Jerusalem, Israel
University of Pennsylvania School of Nursing and The Children's Hospital of Philadelphia, Philadelphia, PA

a r t i c l e

i n f o

Article history:
Received 5 March 2016
Received in revised form 12 April 2016
Accepted 19 April 2016
Available online xxxx
Keywords:
Neonatal hyperbilirubinemia
Newborn feeding
Newborn sucking

a b s t r a c t
Background: Mothers of hyperbilirubinemic newborns frequently report to us that their infant is feeding poorly.
As poor feeding in an extremely hyperbilirubinemic newborn may be an early sign of bilirubin encephalopathy,
we hypothesized that neonatal hyperbilirubinemia would suppress the volume of feed ingested and diminish
sucking parameters in comparison with minimally jaundiced neonates.
Objective: To determine whether hyperbilirubinemia does diminish feeding and sucking in neonates.
Study design: Neonates in a well-baby nursery with serum total bilirubin (STB) 15.0 mg/dL were compared with
those with transcutaneous bilirubin 10 mg/dL. Neonur, a modication of Krohn's Nutritive Sucking Apparatus,
was used to quantify sucking parameters. Measurements during a 5 min feeding period included volume
ingested (measured manually), number of sucks, average maximum sucking pressure, number of bursts, average
burst duration, pause between bursts duration, number of sucks per burst, and average intersuck interval.
Outcome measures were volume ingested and, presuming decreased volume, sucking parameter analysis
would determine the component affected by hyperbilirubinemia.
Results: 17 hyperbilirubinemic newborns (STB 17.8 1.6 mg/dL) were compared with 24 controls, all with
transcutaneous bilirubin b10.0 mg/dL. The volume of feed ingested was similar between the hyperbilirubinemic
newborns and controls (30.00 [20.0042.50] ml vs. 25.00 [15.0030.00] ml, p = 0.2) (median [95% condence
interval]). No signicant differences were noted in any of the other sucking parameters measured.
Conclusions: At concentrations of STB in the range of 1520 mg/dL, hyperbilirubinemia did not diminish feed
volume or sucking parameters in term newborns. Poor feeding in moderately hyperbilirubinemic newborns
cannot be attributed to the level of bilirubin per se.
2016 Elsevier Ireland Ltd. All rights reserved.

Neonatal jaundice is common, usually harmless, and transient.

Breast milk jaundice may lead to lethargy and poor feeding [1] while
in the rare, extremely hyperbilirubinemic newborn who had previously
been nursing and feeding well, poor feeding may be an early sign of
bilirubin neurotoxicity [2,3,4]. In our neonatal service, mothers of
hyperbilirubinemic neonates frequently report their infant is nursing
and feeding less well than before the jaundice became apparent. It
is not known whether this maternal observation, if substantiated,
may be a precursor of the poor feeding associated with bilirubin
encephalopathy.
The objective of this study was to determine the effect, if any, of
neonatal hyperbilirubinemia on newborns' feeding, by quantitatively
comparing sucking parameters between those hyperbilirubinemic
and those with minimal, or clinically insignicant, jaundice. Based on

Abbreviations: STB, serum total bilirubin; TcB, transcutaneous bilirubin.

Corresponding author at: 20 Sheshet Hayamim St, PO Box 317, Mevasseret Zion
9073019, Israel.
E-mail address: mkaplan@mail.huji.ac.il (M. Kaplan).

http://dx.doi.org/10.1016/j.earlhumdev.2016.04.008
0378-3782/ 2016 Elsevier Ireland Ltd. All rights reserved.

maternal accounts, we hypothesized that hyperbilirubinemic neonates

would feed a lesser amount during the study period. Should this be
substantiated, the device used would enable us to determine which of
the sucking components was responsible for the decreased volume
ingested. (See description of device below) To our knowledge, few
studies of this nature have been previously been reported.
1. Methods
The study was approved by the Institutional Review Board of the
Shaare Zedek Medical Center. Signed informed consent was obtained
prior to enrollment.
This was a convenience study of otherwise healthy, term and late
preterm (N36 weeks gestation) neonates, some of whom developed
hyperbilirubinemia. As there are no previously published data on the
subject, we could not estimate the size of the study and control groups
necessary. Newborns with any medical condition requiring admission
to the NICU, major congenital abnormality, sepsis, or respiratory distress, were ineligible for enrollment. During birth hospitalization, daily

54

R. Bromiker et al. / Early Human Development 99 (2016) 5356

transcutaneous bilirubin (TcB) was measured routinely in all and the

results plotted on the Bhutani et al. nomogram [5]. Serum total bilirubin
(STB) was determined in those with TcB readings N75th percentile,
or N 50th percentile in the presence of risk factors including gestational
age b 37 weeks, glucose-6-phosphate dehydrogenase deciency, ABO
blood group incompatibility with positive direct agglutination titer,
cephalhematoma or clinically signicant echymoses, as previously
described [6]. Breast feeding was encouraged in all.
Transcutaneous bilirubin testing was performed using a JM-103
bilirubinometer (Drager, Lbeck, Germany). STB was determined routinely on heparinized, centrifuged capillary tube samples by absorbance
of bilirubin at 455 nm (Bilimeter 3; Pfaff Medical, Germany). Phototherapy was instituted in accordance of the hyperbilirubinemia guidelines
of the Israel Neonatal Society [7] which in turn are based on and similar
to those of the American Academy of Pediatrics (2004) [8].
1.1. Study procedure
For the purpose of the study, parents of appropriate babies were
approached to request enrollment in the study. The hyperbilirubinemic
group was studied either during birth hospitalization or when
readmitted for hyperbilirubinemia, in both situations prior to the
onset of phototherapy. The control group was selected from babies during birth hospitalization, also on a convenience basis, from the identical
pool of neonates but who did not meet the criteria for clinically signicant jaundice. Apart from the study procedure, there was no interference in the regular daily nursery routine. Study measurements were
performed using either expressed breast milk from that specic infant's
mother, when available, or formula. Infants were held, swaddled, and
brought to a quiet alert state, in almost all cases by the mother, before
sucking measurements were performed. Parameters were tested over
a 5 minute recording period at the beginning of a feed. After the measurement was completed, the infants continued routine breast or bottle
feeding till completion of the feed.
1.1.1. Investigational apparatus and parameters tested
The Neonur is an advanced-model mobile nutritive sucking device
(Fig. 1). The system employs a bottle unit with signal processing and
storage functionality, and a computer with software for data analysis,
display, and report generation. The signal processor (electronics component in the gure) gathers and digitizes the data from the pressure
sensor every 5 msec and stores it on-board in a ash memory. At test
completion, the data are downloaded to a PC through a standard
cable and further data processing is carried out on the PC with specially
designed MATLAB software (MathWorks, Natick, Massachusetts,
U.S.A). The software analyzes the varying pressures generated during
a sucking bout using temporal and pressure threshold criteria, capable
of distinguishing true sucks from non-sucking movements or other artifacts. The initial output is a graph of the sucking record followed by an
Excel spreadsheet of the sucking parameters including: a. total number
of sucks per 5-minute session, b. sucking duration (interval from rst to
last suck in session), c. number of bursts (a 2-s pause denes the separation of 2 bursts), d. mean burst duration, e. total burst time as percent
of bout, f. within-burst suck frequency, and g. mean peak sucking pressure for each participant. The ingested volume was manually recorded.
1.1.2. Denitions
For the purpose of the study, clinically signicant hyperbilirubinemia
was dened as those with STB 15 mg/dL, equivalent to 95th percentile
at 60 postnatal hours. Neonates with TcB readings 10 mg/dL, or who
had a STB determination which fell in the 10 mg/dL range were
regarded as not hyperbilirubinemic and served as controls.

Fig. 1. Photograph of the Neonur nutritive sucking device.

appropriate for value sets with a normal or non-parametric distribution,

respectively, was calculated for each of the sucking measurements
over the 5 min test period. Continuous values were compared using
Student's t-test or the Mann-Whitney test, as appropriate for normal or
non-parametric distribution, and categorical values using chi-square
analysis. A p value b0.05 was regarded as statistically signicant.
2. Results
A total of 41 newborns was studied, of whom 17 were designated
hyperbilirubinemic (mean [SD]) bilirubin immediately prior to the
study test 17.8 1.6, range 15.020.2 mg/dL) and 24 non-jaundiced,
all with TcB measurements b 10.0 mg/dL immediately prior to the
study. Age at testing was 2.9 2.6 days in the jaundiced group and
2.8 1.6 days in the control group (P = 0.8).
Demographic data are summarized in Table 1 and feeding and
sucking parameters are compared between the groups in Table 2. No
signicant differences were noted between any of the demographic
data or in sucking measurements between the hyperbilirubinemic and
non-hyperbilirubinemic groups.
3. Discussion

1.1.3. Statistical analysis

Data were incorporated into an Excel le (Microsoft Corp). The
mean and standard deviation, or median and interquartile range, as

Neonatal jaundice is a common occurrence in the rst postnatal week [9,10]. Usually the jaundice is transient, but occasionally

R. Bromiker et al. / Early Human Development 99 (2016) 5356

Table 1
Demographic data of the infants studied.
Category

Jaundiced
(n = 17)

Control
(n = 24)

Signicance

Birth weight (kg)

Gestational age (wk)
Male:female
Any breast feeding (n)
Exclusive breast feeding (n)
Weight at time of test (kg)
Percentage of birth weight at
time of test (%)

3.40 0.46
39.0 1.2
11:6
17 (100%)
11 (65%)
3.20 0.44
94.1 3.1

3.37 0.46
39.7 1.7
16:7
22 (95.7%)
9 (38%)
3.23 0.40
94.3 3.7

P = 0.9
P = 0.9
P = 0.9
P = 0.9
P = 0.2
P = 0.7
P = 0.4

TcB: transcutaneous bilirubin. STB: serum total bilirubin. TcB measurements in the control
group did not meet indications for STB testing.

hyperbilirubinemia may develop with high STB concentrations. In extreme cases, acute bilirubin encephalopathy with the potential sequel
of permanent bilirubin neurotoxicity may result. An early sign of acute
bilirubin encephalopathy is poor feeding in a baby who had previously
been nursing or feeding well [2,3,4]. It therefore concerned us that the
mothers of many newborns under our care reported that their infants
fed less enthusiastically when even moderately hyperbilirubinemic,
compared to the period prior to appearance of the icterus. As this
information is subjective we studied this phenomenon using objective
measurements to quantify sucking parameters in newborn infants
with STB values 15.0 mg/dL. We compared the results with newborn
controls with only minimal jaundice (TcB values b 10.0 mg/dL). No
signicant differences in the volume ingested or in the sucking parameters studied were noted between the hyperbilirubinemic and nonhyperbilirubinemic control groups.
Oral feeding in infants is a complex process requiring coordination
of sucking, swallowing, and breathing to allow for feeding, on the one
hand, while avoiding aspiration into the airways, on the other, and
requires intact neuro-motor function [11]. Successful sucking activity
requires integration of multiple central nervous system sensory and
motor functions [12]. To obtain milk, the newborn must produce negative intraoral pressure simultaneous with compression of the nipple between the tongue and hard palate in a rhythmic fashion [13]. Neonatal
nutritive sucking is organized in a series of sucking bursts interspersed
with pauses [14]. The frequency, maximal negative pressure of sucks,
and the duration of the sucking bursts increase in tandem with advancing postmenstrual age as a result of maturation of the developing neurologic mechanisms involved in feeding [15,16]. While much has been
written regarding the effect of breast feeding or breast milk on the
development of neonatal jaundice, to our knowledge, the effect of neonatal hyperbilirubinemia on newborn feeding patterns has not been
previously reported.
Because both bilirubin encephalopathy and extreme hyperbilirubinemia are rare we studied newborns with moderate

Table 2
Comparison of sucking parameters between jaundiced newborns and controls.
Test parameter

Jaundiced
(n = 17)

Non-Jaundiced
(n = 24)

Signicance

Feeding volume (ml/5 min)

30.00
(20.0042.50)
97.9 29.7
168.0
(140.3322.3)
5.3 2.3
13.8 (10.024.6)
4.2 2.5
21.0 (13.130.1)
0.9 (0.81.2)

25.00
(15.0030.00)
81.0 28.8
157.4
(121.6216.2)
5.77 2.4
11.1 (8.924.2)
5.5 0.6
12.8 (9.830/0)
1.1 (1.01.3)

P = 0.2

Number of sucks (/5 min)

Maximum negative pressure
(mmHg)
Number of bursts (/5 min)
Burst duration (sec)
Pause duration (sec)
Sucks per burst (n)
Intersuck interval (sec)

P = 0.08
P = 0.32
P = 0.5
P = 0.41
P = 0.15
P = 0.23
P = 0.06

Data with normal distribution are presented as mean SD. Data with non-normal
distribution are distributed as median (95% condence interval).

55

hyoerbilirubinemia as a surrogate for the former entities. In light of

the mothers' observations, we expected that the feeding parameters
studied would be affected even in the presence of moderate hyperbilirubinemia approaching phototherapy indications. Our failure to
demonstrate sucking impairment may be due to the moderate elevation
of STB and do not exclude the possibility of poor feeding in those with
severe hyperbilirubinemia. Our ndings are, however, reassuring,
as we can now reassure mothers of moderately hyperbilirubinemic
newborns that poor feeding is not related, in and of itself, to the
jaundice. In fact, there was a tendency in the measurements towards
somewhat more vigorous feeding among the hyperbilirubinemic newborns. This was likely not due to unsuccessful nursing predisposing to
jaundice, with resultant hunger among those affected neonates, as the
percentage weight loss at the time of the testing was similar between
the 2 groups.
Few studies have quantied the effect of hyperbilirubinemia on
feeding in human newborns. Alexander and Roberts reported a maturational effect characterized by serial increases in milk consumption,
duration and pressure of sucking during the rst 6 postnatal days in bottle fed newborns [17]. Moderate hyperbilirubinemia (mean maximum
STB 13.5 mg/dL on the 3rd day and considerably lower than the STB
values in our study) was clinically correlated with disinterest in feeds,
lack of alertness and hunger, but these observations were not supported
by decrease in milk volume ingested.
Using a sheep model, Bourgoin-Heck et al. studied the effect of moderate hyperbilirubinemia (8.814.6 mg/dL [150250 mol/L]), induced
by intravenous infusion of a bilirubin-albumin solution, into preterm
lambs [18]. Using an invasive measuring system they found that
hyperbilirubinemia was associated with less frequent swallowing and
smaller volumes than controls. Swallowing-breathing coordination
was impaired and hyperbilirubinemic lambs tended to experience
more severe desaturations during bottle-feeding than controls. The respiratory rate was signicantly lower, along with increased apnea duration in the hyperbilirubinemic lambs. We did not monitor the infants
studied for respiratory function or saturation: as the lambs studied
were preterm, the analogy to the term human newborn may not be
completely appropriate.
Limitations of our study include the convenience nature of the population sampled. While the controls were not matched individually for
each study infant, the birth weights and gestational ages of both groups
were, in fact, similar. We recognize that the apparatus used in the study
requires the infant to suck through a teat, differing perhaps from the
natural in those newborns who were breastfeeding. However, the fact
that the identical apparatus and teats were used between the study
and control groups should exclude bias in this respect. We are aware
that the programming of the device allowed for only the rst 5 min of
a feed to be studied whereas in most instances an entire feed will continue for a longer period.
Our observations of course are limited to the moderate
hyperbilirubinemia in the range of STB studied. These results do not exclude any potential effect of STB values considerably higher than
20.0 mg/dL in modifying neonatal feeding activity, or of moderate or severe hyperbilirubinemia in preterm infants. Protocols for management
of neonatal hyperbilirubinemia avoid reaching STB values much higher
than those encountered in this study, and our negative results can, in
fact, be regarded as reassuring that bilirubin at the concentrations encountered was not clinically neurotoxic to brainstem swallowing centers. Parental concern for poor feeding should be taken seriously,
however, and should more severe hyperbilirubinemia be excluded,
other causes for poor feeding should be explored.
In summary, moderately elevated STB, in the range of 1520 mg/dL,
does not appear to suppress feeding or diminish sucking parameters in
otherwise healthy, term, primarily breastfeeding newborns. It would be
of interest to apply a similar study to infants with acute bilirubin encephalopathy, or to preterm newborns, to determine the bilirubin effect
on feeding in these neonates.

56

R. Bromiker et al. / Early Human Development 99 (2016) 5356

Financial disclosure
The authors have no nancial relationships relevant to this article to
disclose.
Funding source
This project was performed without specic funding.
Conict of interest
The authors have no conicts of interest to declare with regard to the
material included in this manuscript.
Contributors' statements
Dr Bromiker participated in the conceptualization and planning of
the study, performed studies on the hyperbilirubinemic infants, collated
and analyzed the data, and approved the nal manuscript as submitted.
Dr Medoff-Cooper supplied the study apparatus, participated in the
planning of the study and the analysis of the data, and approved the
nal manuscript as submitted.
Dr Flor-Hirsch participated in the planning of the study, performed
study measurements on many of the newborns, participated in the analysis of the data, and approved the nal manuscript as submitted.
Dr Kaplan conceptualized the study, planned the study, participated
in performing the studies, analyzed the data, drafted the initial manuscript, and approved the nal manuscript as submitted.
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