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Pediatrics and Neonatology (2017) xx, 1e5

Available online at www.sciencedirect.com

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journal homepage: http://www.pediatr-neonatol.com

Original Article

Urinary tract infections in neonates with

unexplained pathological indirect
hyperbilirubinemia: Prevalence and
significance
Elif Bahat Ozdogan a,*, Mehmet Mutlu b,
Secil Arslansoyu Camlar a, Gülcin Bayramoglu c,
Sebnem Kader b, Yakup Aslan b

a
Department of Pediatrics, Division of Pediatric Nephrology, Karadeniz Technical University, Faculty
of Medicine, Trabzon, Turkey
b
Department of Pediatrics, Division of Neonatology, Karadeniz Technical University, Faculty of
Medicine, Trabzon, Turkey
c
Department of Microbiology, Karadeniz Technical University, Faculty of Medicine, Trabzon, Turkey

Received Jan 30, 2017; received in revised form Aug 14, 2017; accepted Oct 25, 2017
Available online - - -

Key Words Abstract Background: It is controversial to test for urinary tract infection (UTI) in patients
follow-up; with unexplained indirect hyperbilirubinemia in the first 2 weeks of life. We aimed to study
hyperbilirubinemia; the prevalence and significance of UTIs in such neonates who were requiring phototherapy.
neonate; Methods: Subjects were 2- to 14-day-old neonates with indirect bilirubin levels above photo-
urinary tract therapy limit with no other abnormality in their bilirubinaemia-related etiologic workup. UTI
infection; was diagnosed by 2 consecutive positive cultures obtained by catheterisation, documenting
prevalence growth of >10,000 colonies of the same microorganism with consistent antibiograms. The
UTI (þ) patients were evaluated by renal ultrasonography (US), and some were followed up
for possible recurrent UTI.
Results: 262 neonates were included in the study. UTI prevalence was 12.2%, and bacteraemia
was 6.2% among UTI (þ) patients. The two most common pathogens (81.2%) were Escherichia
coli and Klebsiella. pneumonia. All UTI (þ) patients had undergone US, revealing 12.5% pelvi-
caliectasis, other 12.5% increased renal parenchymal echogenicity, 3.1% concurrent pelvica-
liectasis and increased renal parenchymal echogenicity. 53.1% of UTI (þ) patients had
undergone follow-up, after which 23.5% recurrent UTI were found at the end of a mean of
52 months.

* Corresponding author. Department of Pediatrics, Division of Pediatric Nephrology, Karadeniz Technical University, Faculity of Medicine,
61080, Trabzon, Turkey. Fax: þ90 462 2235199.
E-mail address: elifbahat@yahoo.com (E. Bahat Ozdogan).

https://doi.org/10.1016/j.pedneo.2017.10.010
1875-9572/Copyright ª 2017, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Bahat Ozdogan E, et al., Urinary tract infections in neonates with unexplained pathological indirect
hyperbilirubinemia: Prevalence and significance, Pediatrics and Neonatology (2017), https://doi.org/10.1016/j.pedneo.2017.10.010
 + MODEL
2 E. Bahat Ozdogan et al

Conclusion: We suggest that the neonates with unexplained pathological jaundice should be
tested for possible UTI. Consequently, all newborns with UTI shall be evaluated by the urinary
US and followed up for recurrent UTI.
Copyright ª 2017, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/
by-nc-nd/4.0/).

1. Introduction test, complete blood count, peripheral blood smear,

Neonatal hyperbilirubinemia is seen in the first week of life
in 60% of the term and 80% of the preterm newborns. In
these cases, bilirubin levels may remain in the physiologic
range or may exceed the level requiring phototherapy or
blood exchange. The aetiology of pathologic hyper-
bilirubinemia could not always be determined.
Urinary tract infection (UTI) presents with variable
symptoms in the neonatal period. Nonspecific complaints
(i.e., poor weight gain, vomiting, diarrhoea, fever, irrita-
bility, lethargy, jaundice) may be the only symptoms,1
among which jaundice is documented as one of the most
common.2,3 UTIs are well-known to cause prolonged jaun-
dice and investigated as a standard of care. Along with
prolonged jaundice, UTIs may underlie the unexplained
pathologic jaundice presenting in the first 2 weeks of life. It
is still controversial to test for UTI in patients with unex-
plained jaundice presenting in the first 2 weeks of life.3e9
Hence, some authors suggest investigating these neonates
requiring treatment for pathologic indirect hyper-
bilirubinemia for UTIs,3,4,6,7,9 while some do not.5,8
In this report, we aimed to study the prevalence and
significance of UTIs in neonates presenting with indirect
hyperbilirubinemia in the first 2 weeks of life requiring
phototherapy who were found to have no other abnormality
in their aetiologic workup.
2. Material and methods
This study was performed between November 2004 and
November 2007 in the Karadeniz Technical University Farabi
Hospital neonatal intensive care unit, Turkey. Some pa-
tients were followed up until December 2013 by the Pae-
diatric Nephrology Department. Subjects were 2- to 14-day-
old neonates with indirect bilirubin levels above the pho-
totherapy limit with no other abnormality in their
bilirubinaemia-related aetiologic workup for systemic
infection, isoimmunisation, erythrocyte enzyme defect,
erythrocyte structural defect, hypothyroidism, seques-
trated blood, polycythaemia or metabolic disease. Photo-
therapy limits of bilirubin levels were determined
according to the guidelines of American Pediatrics
Academy.10
Method of delivery, sex, birth weight, weight at pre-
sentation, gestational age, postnatal age at presentation,
weight loss, breast feeding data, onset of jaundice by his-
tory, bilirubin level at presentation, duration of photo-
therapy and requirement of blood exchange were recorded.
Tests for blood group, mother’s blood group, direct Coombs
reticulocyte count, serum total/direct bilirubin, glucose,
blood urea nitrogen, creatinine, sodium and urinalysis were
performed. If the aetiology of jaundice could not be
explained by blood group incompatibility, glucose-6-
phosphate dehydrogenase and pyruvate kinase enzyme
levels, urinary reducing substances, thyroid hormones and
urine cultures were analysed. Polycythaemia was defined as
the haemoglobin concentration greater than two standard
deviations above the normal value for gestational and
postnatal age. Urine samples for urinalysis and urine cul-
ture were obtained using catheterisation. The samples
were analysed with Clinitek 100 (Bayer) or IQ 200 (IRIS)
automatic analysers. Pyuria was defined as the presence of
>5 leukocytes in one high-power field in the sediment of
centrifuged urine.5 Presence of 1 microorganism in one
immersion field by Gram stain was accepted as bacteriuria.
In the urinary culture, 10,000 colonies of a single path-
ogen were regarded as significant.6 In patients with a pos-
itive urine culture, before initiation of related-
antibiotherapy, blood cultures and confirmatory catheter
urine culture were obtained. Immature/total neutrophil
ratio was determined using a peripheral blood smear. C-
reactive protein >5 mg/L and procalcitonin >0.5 mg/L were
regarded as significant. In patients who had elevated acute-
phase reactant levels or positive blood cultures, lumbar
puncture was also performed.
UTI was diagnosed in patients with confirmatory urine
culture 10,000 colonies of the same microorganism with
the first culture and related antibiogram. Patients with
bilirubin levels above the phototherapy cutoff level and
negative cultures were accepted as the UTI () group.
Patients whose second urine culture was negative, positive
for a different organism, or yielded multiple microorgan-
isms or had no parent-given informed were excluded from
the study. UTI (þ) and () patients were compared for the
above parameters (i.e., birth weight, gestational age, sex,
delivery method, weight at presentation, weight loss, onset
of jaundice, time of presentation, total/direct bilirubin at
presentation, blood exchange, duration of phototherapy,
urine density, presence of hypoglycaemia and
hypernatraemia).
As secondary analyses, all UTI (þ) patients were evalu-
ated by renal ultrasonography (US). All were offered to
have voiding cystourethrogram (VCUG) at least 1 month
after the sterilisation of urine cultures and dimercapto-
succinic acid scintigraphy (DMSA). Their follow-up data
were evaluated.
Informed consent was obtained from the parents of all
patients, and the study was approved by the local institu-
tional ethical board (approval number: 200691).

Please cite this article in press as: Bahat Ozdogan E, et al., Urinary tract infections in neonates with unexplained pathological indirect
hyperbilirubinemia: Prevalence and significance, Pediatrics and Neonatology (2017), https://doi.org/10.1016/j.pedneo.2017.10.010
 + MODEL
Urinary tract infections in neonatal hyperbilirubinemia 3

2.1. Statistical analysis comparative demographic data and the jaundice-related

data of the UTI (þ) vs. UTI () patients are outlined in
The variables were investigated to determine whether they Table 2 and Table 3, respectively.
were normally distributed. Numerical variables were given Weight loss was evaluated as percentage of weight loss
as mean  standard deviation for normally distributed after birth (birth weighteweight at presentation [*100/
variables and as median for skew-distributed continuous birth weight]). The weight loss percentage and rebound
variables. Categorical variables were shown as frequencies. bilirubin levels were significantly different between the UTI
Two groups were compared with independent sample t-test (þ) and () patients (p Z 0.02 and p Z 0.01, respectively).
or Mann Whitney U test when necessary. Chi-square test UTI (þ) patients had significantly less weight loss but higher
with Yates correction and Fisher’s exact test were used for rebound bilirubin levels than UTI () patients. Other study
2  2 contingency tables when appropriate for non- parameters were not different between groups.
numerical data. SPSS (statistical package for social sci- All UTI (þ) patients were evaluated by renal ultraso-
ences) for Windows 15.0 was used for statistical analysis. nography (USG) during hospitalisation which revealed
p < 0.05 was accepted as statistically significant. abnormal finding in 9 patients (28.1%) as follows: 4 patients
(12.5%) had only pelvicaliectasis, 4 (12.5%) patients had
3. Results only increased renal parenchymal echogenicity and 1 pa-
tient (3.1%) had both pelvicaliectasis and increased renal
A total of 482 neonates presented to the neonatal intensive parenchymal echogenicity.
care unit with indirect hyperbilirubinemia above the pho- Among the total 32 UTI (þ) patients, 20 (62.5%) con-
totherapy limit. Among them, 262 (54%) fulfilled our in- sented to VCUG (the remaining 37.5% of the UTI (þ) pa-
clusion criteria. Of the 262, 47% (123) were female, and 53% tients either did not consent to VCUG regarding the invasive
(139) were male. All males were uncircumcised. Mean nature of the procedure and radiation exposure or they
gestational age was 37.6  2.1 (31e41) weeks. Mean age at were lost to follow-up). Two VCUG-evaluated patients (10%)
presentation was 5.3  2.2 (2e14) days. Sixty percent (158) had more than grade 1 vesicoureteral reflux (VUR) (one
were born via vaginal delivery, while 40% (104) were born grade 2 and one grade 3 VUR). Both VUR (þ) patients had
via caesarean section. Mean birth weight was 3021  676 abnormal renal US findings; one had pelvicaliectasis, and
(1500e5500) grams, and mean weight at presentation was the other had increased renal echogenicity.
2881  646 (1320e5570) grams. 90.8% (238) were fed only Among the 32 UTI (þ) patients, 6 (18.7%) consented to
with breast milk, 3.8% (10) were fed formula, and 5.3% (14) DMSA. The remaining 81.3% of the UTI (þ) patients either
were fed both formula and breast milk. Mean elapsed time did not consent to DMSA regarding the invasive nature of
to recognition of jaundice was 3.3  1.0 (2e8) days. Mean the procedure and radiation exposure or they were lost
bilirubin level of the patients at presentation was follow-up. One (16.6%) of them was found to have renal
20.9  6.1 (7.6e45.1) mg/dL. 13.4% (35) were treated with scarring. This patient also had grade 2 VUR and increased
blood exchange and phototherapy; the rest were treated renal parenchymal echogenicity.
with only phototherapy. Mean duration of phototherapy Among the 32 UTI (þ) patients, 17 (53.1%) could have
was 64.2  21 (24e120) hours. None of the subjects had been followed up more than 12 months since the others
fever. UTI was diagnosed in 12.2% (32), but not in 87.8%
(230). In UTI (þ) patients, 37.5% (12) had pyuria and
bacteriuria by Gram stain, 9.4% (3) had only pyuria, 18.7% Table 2 Comparative demographic data of UTI (þ) vs UTI
(6) had only bacteriuria and 34.4% (11) had neither pyuria () patients.
nor bacteriuria. The bacteriuria by Gram stain were Gram Parameter UTI (þ) UTI () p
() bacilli in 88.9% (16) and Gram (þ) cocci in 11.1% (2). patients patients
The two most common microorganisms in urine culture (n Z 32) (n Z 230)
were Escherichia coli (50%) and Klebsiella pneumoniae Birth weight (gram) 3099  534 3010  694 0.5
(31.2%) (Table 1). Of UTI (þ) patients, 6.2% (2) had positive Gestational age (week) 37.9  1.6 37.5  2.2 0.5
blood culture for the microorganism positive in the urine Sex 0.6
cultures (i.e., K. pneumoniae and Staphylococcus aureus). Male (n) (%) 19 (59%) 120 (52%)
These cases were confirmed to not have meningitis. C- Female (n) (%) 13 (41%) 110 (48%)
reactive protein, procalcitonin levels and renal function Delivery 0.9
tests were within normal levels in all patients. The Vaginal (n) (%) 20 (63%) 138 (60%)
c/s (n) (%) 12 (37%) 92 (40%)
Table 1 Microorganisms identified in urine cultures Weight (presentation) 3014  510 2863  661 0.2
(n Z 32). (gram)
Microorganism n (%)
a
Weight loss % 6  2.9 8.4  5.5 0.02
(190  89) (290  367)
Escherichia coli 16 (50%)
Klebsiella pneumoniae 10 (31.2%) Data are given as mean  standard deviation.
Enterobacter aerogenes 2 (6.2%) n: number.
Staphylococcus aureus 2 (6.2%) c/s: caesarean section.
a
Weight loss % was calculated as percentage of weight loss
Kluyvera ascorbata 1 (3.1%)
after birth (birth weighteweight at presentation [*100/birth
Enterococcus faecalis 1 (3.1%)
weight]).

Please cite this article in press as: Bahat Ozdogan E, et al., Urinary tract infections in neonates with unexplained pathological indirect
hyperbilirubinemia: Prevalence and significance, Pediatrics and Neonatology (2017), https://doi.org/10.1016/j.pedneo.2017.10.010
 + MODEL
4 E. Bahat Ozdogan et al
Table 3 Comparative jaundice-related data of UTI (þ) vs UTI () patients.
Parameter UTI (þ) patients (n Z 32)
Onset of jaundice (day) 3.4  1.0
Time of presentation (day) 5.3  3.8
Total bilirubin (presentation) (mg/dL) 21.2  5.0
Direct bilirubin (presentation) (mg/dL) 0.6  0.3
Blood exchange (n) (%) 4 (13%)
Duration of phototherapy (hour) 70.9  19.8
Rebound bilirubin (mg/dL) 11.1  1.3
Urine density 1014  7
Hypoglycaemia (n) (%) 3 (9%)
Hypernatraemia (n) (%) 2 (6%)
Data are given as mean  standard deviation.
n: number.
Hypoglycaemia: serum glucose level< 50 mg/dL.
Hypernatraemia: serum Na level >145 mg/dL.
were lost to follow-up. Mean follow-up duration was
52  21 months; median was 53 months. In this follow-up, 4
(23.5%) had recurrent UTI, of whom one had grade 2 VUR
and one had concurrent pelvicaliectasis and increased renal
parenchymal echogenicity.
4. Discussion
Jaundice is one of the most common symptoms of UTIs in
neonates2,3 and may be its sole sign. UTIs are well-known to
cause prolonged jaundice and are investigated routinely.
On the other hand, some authors suggest investigating UTI
also in the neonates requiring treatment for pathologic
indirect hyperbilirubinaemia,3,4,6,7,9 while some do not.5,8
Therefore, it is controversial to look for UTI in these
patients.3e9
In a similar study, Garcia et al.4 included 160 neonates
<8 weeks old with unexplained jaundice and reported UTI
in 7.5%. Chen at al.11 studied 217 neonatal infants <8
weeks old with the initial presentation of hyper-
bilirubinemia and reported UTI in 5.5%. Shahian et al.7
studied 120 neonates <4 weeks old with asymptomatic
jaundice and reported UTI in 12.5%. Our UTI prevalence
(12.2%) was higher than that of Garcia et al.’s (7.5%) and
Chen et al.’s 5.5% studies and comparable to that of Sha-
hian et al.’s (12.5%) study. Garcia et al. noted that most
(75%) of their UTI (þ) patients were younger than 2 weeks
old, suggesting a higher UTI prevalence in the <2-week-old
neonates with unexplained jaundice. This is similar to the
result suggested by our study. On the other hand, Chen
et al. studied patients with the initial presentation of
hyperbilirubinemia. Those patients did not have unex-
plained, isolated jaundice. Therefore, it is not surprising
that they had higher prevalence of other jaundice-related
pathologies and lower percentage of UTI. Additionally,
Chen et al. did not report the prevalence in a <2-week-old
patient subpopulation. Garcia et al. might have had higher
UTI prevalence in the 2-week-old patients than in our
study. Also, a possibility exists that co-existing UTI was
present in our excluded cases, which had predefined
pathologic jaundice aetiology. When there is a predefined
cause of pathologic jaundice, the probability of co-existing
UTI would be expected to be low. Accordingly, if we would
Please cite this article in press as: Bahat Ozdogan E, et al., Urinary tract infections in neonates with unexplained pathological indirect
hyperbilirubinemia: Prevalence and significance, Pediatrics and Neonatology (2017), https://doi.org/10.1016/j.pedneo.2017.10.010
UTI () patients (n Z 230) p
3.3  1.0 0.4
5.2  2.3 0.4
20.8  6.3 0.4
0.6  0.3 0.7
31 (13%) 0.9
63.3  21.0 0.06
10  1.7 0.01
1014  7 1
40 (18%) 0.4
27 (12%) 0.5
look for UTI in all pathologic jaundice cases, including cases
with predefined aetiology, UTI % would be lower and more
similar to the aforementioned reports in the literature.4,11
Two other studies from Turkey examined UTI prevalence in
<2-week-old newborns with asymptomatic, unexplained
indirect hyperbilirubinemia.6,9 Bilgen et al.6 examined 102
patients and reported UTI as 8%. Most recently, Mutlu et al.9
studied 104 patients and reported UTI as 18%. The first
study was reported from a more developed city (Istanbul)6
than the later one (Erzurum).9 The comparable but
different UTI rates from the same country may be due to
the socioeconomic status of the study region affecting
proper baby care. All these studies pointed out the signif-
icance of UTIs in the neonatal infants with unexplained
hyperbilirubinemia, and they suggested urine culture
should be considered in the bilirubin workup of such pa-
tients.4,6,7,9,11 The counter argument is that most of the
neonates become jaundiced in the first 2 weeks of life, and
UTI is not significantly prevalent in these patients and its
work-up is too invasive, expensive and with high false-
positive rates. Therefore, they suggest it is unnecessary
to look for UTI in all jaundiced neonates.2,5 However, we
limited UTI examination to the neonates with unexplained
pathologic indirect hyperbilirubinemia instead of all jaun-
diced neonates, and we had no false-positive UTI, possibly
due to our study design. Therefore, our UTI prevalence of
12.2% suggests it is important to investigate UTI in neonates
with unexplained pathologic indirect hyperbilirubinemia.
The two most common microorganisms in urine culture
were E. coli (50%) and K. pneumoniae (31.2%) in our study;
together, they were the responsible pathogens in 81.2% of
the UTIs, which is a well-expected finding in the neonates.
Of UTI (þ) patients, 6.2% had documented bacteraemia
in this study. This finding is also in accordance with the
results of other studies in the literature, as the prevalence
of bacteraemia and sepsis in children with UTI has been
reported between 3.2% and 31% in various studies.12e15 We
suggest that the relatively earlier detection of UTI in these
patients than in the standard practice might have resulted
in earlier and more timely treatment of the UTI in our
study. This hypothesis is supported by lack of inflammatory
response in the cases with documented bacteraemia.
Hence, our patients with UTI had relatively lower
 + MODEL
Urinary tract infections in neonatal hyperbilirubinemia
prevalence of bacteraemia/sepsis than reported in the
literature. Nevertheless, UTIs may cause urosepsis, renal
scarring, hypertension and chronic renal failure if treated
late or untreated. Hence, our findings show the benefits of
obtaining urine cultures for the diagnosis of possible UTI in
neonates with unexplained pathologic hyperbilirubinemia
requiring phototherapy.
All UTI (þ) patients were further evaluated by renal
USG, documenting abnormal finding in 28.1%. The American
Academy of Pediatrics (AAP) UTI guideline recommends
performing US in all >2-month-old infants with UTI
accompanied by fever but does not make any recommen-
dation for the <2-month-old infants.16 As our study docu-
mented a significant portion of USG abnormality in the non-
pyretic UTI (þ) < 2-week-old neonates, we suggest that the
USG evaluation shall also be performed in the non-pyretic
UTIs of <2-month-old infants.
Almost 2/3 of the patients were evaluated by VCUG,
documenting 10% (2 patients) having VUR more than grade 1
severity. Both of these patients had abnormal renal US
finding. This finding suggests performing VCUG if the pa-
tients have an abnormal finding in USG, which is in line with
AAP recommendations.16
Our study has several strengths and some limitations.
First, the diagnosis of UTI in our study was evidence-based.
Pyuria is not a specific diagnostic criterion for UTI in neo-
nates. Urine dipstick analysis in infants has low sensitivity,
so urine cultures should be used for diagnosis in suspicious
cases.17,18 Bacteria seen in Gram-stained urine sediment is
a finding that supports the diagnosis. However, this is not
sufficient for the diagnosis of UTI, and urine culture is
indicated. In this study, UTI was diagnosed by 2 consecutive
positive cultures obtained by the catheterisation doc-
umenting the growth of >10,000 colonies of the same
microorganism with consistent antibiograms. Obtaining
urine samples from a urine bag is not suitable in neonates.
Rather, urine samples are obtained by USG-guided supra-
pubic aspiration or bladder catheterisation,19,20 and the
latter procedure was applied in this study. Furthermore, we
obtained two consecutive urine cultures for each patient,
representing one of two studies in this aspect.9 This
approach supports the validity of UTI diagnosis, making the
reliability of our study high. Secondly, our study is also the
first with follow-up. Lastly, to our knowledge, this is the
largest case series on this subject. On the other hand, one
should consider that all the cases could not have undergone
VCUG, DMSA analysis and follow-up. So, this study provides
important data but should be examined in larger case
series.
In conclusion, in view of our findings, we suggest that
neonates with unexplained pathologic jaundice should be
examined for possible UTI as a standard of care. Conse-
quently, urinary USdan inexpensive and noninvasive im-
aging techniquedshould be performed in all newborns with
UTI, and these patients should undergo follow-up.
Conflict of interest
No conflict of interest.
Please cite this article in press as: Bahat Ozdogan E, et al., Urinary tract infections in neonates with unexplained pathological indirect
hyperbilirubinemia: Prevalence and significance, Pediatrics and Neonatology (2017), https://doi.org/10.1016/j.pedneo.2017.10.010
5
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