Blood Culture and Bacteremia Predictors in Infants Less Than

ORIGINAL STUDIES
Blood Culture and Bacteremia Predictors in Infants Less Than
Three Months of Age With Fever Without Source
Borja Gómez, MD, Santiago Mintegi, MD, Javier Benito, MD, Andere Egireun, MD,
Diego Garcia, MD, and Eider Astobiza, MD
Objectives: (1) To assess the rate of bacteremia in febrile infants less than
3 months of age admitted to a pediatric emergency department at a tertiary
hospital; (2) to describe the bacteria isolated; and (3) to analyze factors
related to increased probability of having a positive blood culture.
Methods: A retrospective, cross-sectional, 5-year descriptive study that
includes all infants less than 3 months of age who presented with fever
without source (FWS) and had a blood culture performed.
Results: A blood culture was performed in 1018 (91.5%) of 1125 infants
admitted, and a bacterial pathogen was grown in 23 (2.2%) of these; 8 were
associated with a positive urine culture. The most frequently isolated
pathogen was Escherichia coli (9), followed by Streptococcus pneumoniae
(4). The risk factors detected by multivariate analysis were: (a) being
classified as “not well-appearing” (12.5% vs. 1.8%; odds ratio: 8.37) and
(b) leukocyturia and/or nitrituria in a urine dipstick test (5.6% vs. 1.6%;
odds ratio: 3.73). C-reactive protein value was higher than white blood cell
count and absolute neutrophil count in detecting bacteremia; a 70 g/L
cut-off had a specificity of 93.8%, but sensitivity of only 69.6%.
Conclusions: A positive blood culture rate of 2.2% was found in infants
less than 3 months of age with FWS. C-reactive protein, white blood cell
count, and absolute neutrophil count were not good bacteremia predictors.
We recommend obtaining a blood culture in infants less than 3 months of
age with FWS, particularly those patients considered “not well-appearing”
and those with leukocyturia and/or nitrituria.
Key Words: fever, young infant, blood culture, diagnostic tests,
bacteremia
(Pediatr Infect Dis J 2010;29: 000 – 000)
F
ever is the most common reason for healthy young children to
be brought to a pediatric emergency department.1,2 Most of
these infants have fever without source (FWS). Despite the fact
that most cases of FWS are caused by viral infections, for which
no treatment is required, they can also be caused by a severe
underlying bacterial infection, mainly in young infants.3 Serious
bacterial infection (SBI) is found in 10% to 15% of febrile infants
younger than 3 months.4 – 6 Infants eventually diagnosed with SBI
can appear well and have nonspecific signs. Several management
protocols have been designed to evaluate these children to identify
those at high risk of developing SBI. The traditional approach to
febrile young infants involves performing a white blood cell count
(WBC) and blood and urine cultures, administering antibiotics, and
Accepted for publication October 20, 2009.
From the Paediatric Emergency Department, Cruces Hospital, Barakaldo, Spain.
Address for correspondence: Borja Gómez, MD, Paediatric Emergency Department, Cruces Hospital, Plaza de Cruces s/n, Barakaldo, Spain. E-mail:
borja.gomezcortes@osakidetza.net.
Supplemental digital content is available for this article. Direct URL citations
appear in the printed text and are provided in the HTML and PDF versions
of this article on the journal’s Web site (www.pidj.com).
Copyright © 2009 by Lippincott Williams & Wilkins
ISSN: 0891-3668/10/2901-0001
DOI: 10.1097/INF.0b013e3181c6dd14
admitting them to hospital. Recent articles analyzing the usefulness of
classic indices such as WBC, absolute neutrophil count (ANC), and
C-reactive protein (CRP) for predicting the risk of an SBI at this age
have had conflicting results.7–9 Infants have commonly been split into
following 3 different age groups: neonates (0 –28 days old), young
infants (1–3 months old), and older infants (3–36 months old).10,11
Some authors have recently suggested reducing the cut-off age in
febrile young infants to include only children between 1 and 2 months
old as young infants.12 In addition, a less aggressive management has
been suggested in recently published guidelines for well-appearing
infants more than 28 days old.3,13,14
The rate of SBI in young infants has apparently changed in
recent years, as have the pathogens producing them. Group B
Streptococcus, for example, a classic bacterial pathogen in these
children, has been associated with high rates of meningitis (39%),
nonmeningeal infection foci (10%), and sepsis (7%).15 The use of
intrapartum antibiotic prophylaxis has reduced the incidence of
early-onset infections caused by group B Streptococcus, but a
parallel reduction in the incidence of late-onset diseases has not
been reported.16 –18 The early detection of urinary malformations
using prenatal ultrasound19,20 and the introduction of the heptavalent pneumococcal conjugate vaccine21 have also decreased SBI
rates in these patients.
The objectives of our study were as follows: (1) to assess
the rate of bacteremia in febrile infants less than 3 months of age
admitted to the Pediatric Emergency Department of a tertiary
hospital; (2) to describe the bacteria isolated in these children; and
(3) to analyze any factors related to a higher probability of having
a positive blood culture.
MATERIALS AND METHODS
Setting and Participants
We conducted a retrospective, cross-sectional, descriptive
study that included all infants younger than 90 days of age with
FWS admitted to our Pediatric Emergency Department during 5
consecutive years (September 2003 through August 2008). Our
tertiary teaching hospital has a Pediatric Emergency Department
that provides care for approximately 63,000 children less than 14
years of age every year.
Design
Data were extracted from our registry of infants with FWS
younger than 3 months old. Infants younger than 90 days with a
measured temperature ⱖ38.0°C at home or on arrival in the
Pediatric Emergency Department are eligible for inclusion in the
registry. All subjects received clinical care as determined by
the emergency physician. Our Pediatric Emergency Department
algorithm for the management of infants less than 3 months of age
with FWS recommends urine dipstick testing, CBC, CRP, blood
culture, and urine culture for all children. Gram stain of urine is not
routinely performed. We consider performing a lumbar puncture,
including Gram stain, bacterial culture, viral culture, and enterovirus polymerase chain reaction, on an individual basis. If an infant
is well-appearing, over 15 days old, and all ancillary tests appear
The Pediatric Infectious Disease Journal • Volume 29, Number 1, January 2010
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Gómez et al
The Pediatric Infectious Disease Journal • Volume 29, Number 1, January 2010
to be normal, we recommend that the patient be discharged without
antibiotic treatment after several hours of observation in the
Pediatric Emergency Department, generally up to 24 hours after
fever developed (this means that if an infant is brought to the
Pediatric Emergency Department 6 hours after fever was first
registered, this infant remains in our Observation Unit for about 18
hours for clinical evaluation). We recommend hospital admission
for infants less than 15 days of age, those with abnormal laboratory
tests and when the clinical situation worsens during the patient’s
stay in the Observation Unit. Although most guidelines recommend that all febrile infants under 28 to 30 days of age be
hospitalized, 16- to 30-day-old infants at our Pediatric Emergency
Department are observed in the Observation Unit, as explained
above, and then either hospitalized or discharged depending on
their clinical evolution.
An electronic log of Pediatric Emergency Department visits
was reviewed monthly by a pediatric emergency physician to
ensure proper identification of all potentially eligible febrile infants and to assess the capture rate for the study.
Data Collection
Electronic Pediatric Emergency Department medical records
were reviewed, and the following data recorded for each patient:
demographics (age, gender, month when care was provided), medical
history, time elapsed between moment when fever was first detected
and when the infant was brought to the hospital, temperature registered at home and at the Pediatric Emergency Department, whether
the child appeared ill upon arrival or not, symptoms and findings on
physical examination, results of any tests performed, treatment received, diagnosis, site of care, and evolution.
Final discharge patient charts were reviewed if the infants
were admitted. If infants were not admitted to hospital, a follow-up
phone call was made by resident doctors, after training, to assess
their evolution. The hospital database was checked to determine
whether there had been any new, unscheduled emergency visits
after the initial discharge.
Definitions
• FWS: axillary or rectal temperature at home, or rectal temperature in the Pediatric Emergency Department, of ⱖ38°C, without catarrhal or respiratory symptoms/signs (such as tachypnea)
or a diarrheal process, in patients with normal physical examination, according to the diagnostic codes issued by the Spanish
Society of Pediatric Emergencies (SEUP).22 Infants were included even if fever was assessed by parents at home without
using a thermometer. The degree of sensitivity in terms of
subjective fever assessments carried out by parents ranges between 74% and 84%, with a specificity of 76% to 96%.23,24
• Well-appearing: defined by a normal pediatric assessment after
being evaluated by a pediatric emergency physician during the
first hour after attending the Pediatric Emergency Department.
Appearance, respiratory and circulatory items had to be classified as normal for infants to be classified as well-appearing, and
data had to be reflected on the patient’s charts.
• Positive blood culture: blood culture from which a true bacterial
pathogen was grown (Streptococcus pneumoniae, Neisseria
meningitidis, Enterococcus, Escherichia coli, Klebsiella pneumoniae, Staphylococcus aureus, group A and B Streptococcus,
Listeria monocytogenes, or Salmonella species). Staphylococcus
epidermidis, Propionibacterium acnes, and diphtheroids grown
from previously healthy immunocompetent infants (with no history
of heart disease, ventriculoperitoneal shunt, indwelling catheter, or
other prosthetic devices) were categorized as contaminants.
• SBI: isolation of a bacterial pathogen from the cerebrospinal
fluid (CSF), blood, or urine.
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• Occult bacteremia: positive blood culture in a well-appearing
infant diagnosed with FWS.
• Bacterial meningitis: (a) positive CSF culture or CSF gram, (b)
positive blood culture with pleocytosis.
• Urinary tract infection (UTI): growth of more than 50,000
colony forming units/mm3 of a unique bacterial pathogen in a
urine sample collected by bladder catheterization. Growth of
10,000 to 50,000 colony forming units/mm3 was also considered
an UTI when associated with leukocyturia and or nitrituria.
• Previously healthy infant. To be classified as previously healthy,
the patient must meet all the following criteria: born at term
(after ⱖ37 weeks’ gestation), not treated for unexplained hyperbilirubinemia, not hospitalized longer than the mother, not receiving current or prior antimicrobial therapy, no previous hospitalization, and no chronic or underlying illness.
• Low-risk SBI patient. To be classified as a low-risk SBI patient,
the infant must meet all the following criteria: previously healthy
infant, well-appearing, urine dipstick testing without leukocyturia or nitrituria, WBC between 5000 and 15,000/mm3, ANC
⬍10,000/mm3, no pleocytosis if lumbar puncture was performed, and staying several hours in the Observation Unit with
normal clinical evaluations.
Exclusion Criteria
Patients in whom the history and/or the physical examination performed upon arrival in the Pediatric Emergency Department allowed the origin of the fever to be identified. Patients with
fever referred to us by parents reporting a mild nasal congestion
were included in the study. Patients with a diarrheal process or
certain respiratory symptoms/signs (such as tachypnea, breathing
difficulties, wheezing, grunting, nasal flaring, retractions, rhonchi,
rales, focal areas of decreased breath sounds) were not included.
Risk Factors
We analyzed blood culture-positive rates in relation to
factors that can easily be assessed before performing a blood
culture: general appearance, medical history, gender, sex, highest
temperature detected, and urine dipstick result.
Statistical Analyses
Statistical analyses were conducted using the Statistical
Program for the Social Sciences version 15 (SPSS 15, Chicago,
IL). Data are expressed as the mean and standard deviation for
quantitative variables or numbers and percentages for categorical
variables. Continuous data were compared using the Student t test.
Categorical data were examined using the ␹2 test or the Fisher
exact test probability test. Statistical significance was defined as
P ⬍ 0.05. Prevalence rates were expressed as a percentage with
their respective confidence intervals (CI). The performance levels
of WBC, ANC, and CRP for identifying bacteremia were assessed
by receiver operating characteristics (ROC) curves analysis. ROC
curves were constructed by comparing patients with positive and
negative blood culture.
This study was approved by the Research Committee of the
Pediatric Emergency Department. Since the data were extracted
from a registry, the information contained in it is anonymous, and
that no intervention was performed on patients, informed consent
was not requested.
RESULTS
During the study period, 1125 infants younger than 3
months with FWS were admitted. Blood culture was performed in
1018 cases (91.5%). General information concerning the global
sample is provided in Table, Supplemental Digital Content 1,
http://links.lww.com/INF/A324. The final diagnoses for all pa© 2009 Lippincott Williams & Wilkins
The Pediatric Infectious Disease Journal • Volume 29, Number 1, January 2010
TABLE 1. Final Diagnoses for the 1018 Patients
Included in This Study
No SBI
SBI
UTI
Occult bacteremia
UTI and bacteremia
Bacterial meningitis
Sepsis
Cellulitis
Acute otitis media
820 (80.6%)
198 (19.4%)
172
9
8
4
2
2
1
Results are expressed as number (%).
tients are listed in Table 1. A true bacterial pathogen grew in 23
(2.2%; CI: 1.3%–3.1%) of the 1018 blood culture cases (Table,
Supplemental Digital Content 2, http://links.lww.com/INF/A325).
Of them, 8 were associated with a positive urine culture. The most
common final diagnoses for these 23 infants with a positive blood
culture were occult bacteremia in 9 cases (39.1%, 0.88% of the
global sample) and UTI in 8 (34.7%). Blood culture- and occult
bacteremia-positive rates by age group are listed in Table 2.
Infants in whom blood culture was not performed were
older than the study performed (80.4% of patients were older than
2 months vs. 35.2% of those with blood culture; P ⬍ 0.0001); 5
were diagnosed with a UTI and 24 with influenza (positive rapid
influenza test). None of them was diagnosed with bacteremia in a
posterior unscheduled visit and all of them recovered well.
The most frequently isolated bacterial pathogen was Escherichia coli (9 infants, 8 of whom had positive urine cultures)
(Table 3). Only 2 samples were positive for Group B Streptococcus (both in infants more than 28 days old who were not wellappearing upon arrival at the Pediatric Emergency Department).
Univariate analysis of the risk factors studied is shown in
Table 4. All showed an increase in the rate of positive blood
culture, although statistical significance could only be shown for
general appearance, highest temperature detected, and urine dipstick outcome. The results of a multivariate analysis by polychotomous logistic regression (Table, Supplemental Digital Content 3,
http://links.lww.com/INF/A326) showed that only the combination
of general appearance (odds ratio: 8.37, CI: 2.84 –21.97, for those
who were not well appearing) and urine dipstick outcome (odds
ratio: 3.73, CI: 1.54 – 8.80, for those with leukocyturia and/or
TABLE 2. Positive Blood Cultures and Occult
Bacteremia Cases by Age
Age
Positive Blood Culture
Occult Bacteremia
ⱕ1 mo
1–2 mo
2–3 mo
8/243; 3.29% (1.04%–5.53%)
9/417; 2.15% (0.76%–3.55%)
6/358; 1.67% (0.34%–3.00%)
2/243; 0.82% (0%–1.95%)
3/417; 0.71% (0%–1.53%)
4/358; 1.11% (0.02%–2.20%)
TABLE 3. Bacteria Isolated From Blood Cultures
Bacterium
No. Cases
Escherichia coli
Streptococcus pneumoniae
Group B Neisseria meningitidis
Enterococcus faecalis
Streptococcus agalactiae
Klebsiella pneumoniae
Staphylococcus aureus
9
4
3
3
2
1
1
© 2009 Lippincott Williams & Wilkins
Bacteremia in Infants
TABLE 4. Risk of Bacteremia Related to Factors That
Can be Assessed Before Performing a Blood Culture
(Unadjusted)
Risk Factor
Positive Blood
Culture
Medical history
Not previously healthy vs
5/119 (4.2%)
Previously healthy
18/899 (2.0%)
General appearance
Not well-appearing vs
6/48 (12.5%)
Well-appearing
17/970 (1.8%)
Age
ⱕ30 d vs
8/243 (3.3%)
⬎30 d
15/775 (1.9%)
Gender
Male vs
17/585 (2.9%)
Female
6/433 (1.4%)
Highest temperature detected
38°C–39.5°C vs
17/895 (1.9%)
ⱖ39.5°C
6/98 (6.1%)
Urine dipstick*
Leukocyturia and/or nitrituria vs 10/178 (5.6%)
Normal
13/822 (1.6%)
OR (95% CI)
2.15 (0.68 – 6.29)
8.01 (2.76 –23.05)
1.72 (0.66 – 4.39)
2.13 (0.78 – 6.09)
3.37 (1.16 –9.36)
3.70 (1.48 –9.19)
Results are expressed as number (%).
*This information was not recorded for 9 patients.
nitrituria) was predictive for a positive blood culture. We therefore
designed a flow-chart based on these results to determine the yield
of blood culture according to these 2 characteristics (Fig. 1).
Exclusion of these factors results in a decrease in the blood
culture-positive rate, which means that the rate in well-appearing
infants with normal urine dipsticks is 1%.
Among the 1018 infants, 217 (21.3%) had a rectal temperature lower than 38°C on arrival in the Pediatric Emergency
Department (22 lower than 37°C). In all cases, the parents had
recorded a temperature greater than 38°C at home, although in
most cases, it is not known whether this temperature was measured
rectally or axillary. There were 2 blood culture-positive cases in
infants who were afebrile upon arrival in the Pediatric Emergency
Department (cases 11 and 15 in Table, Supplemental Digital
Content 2, http://links.lww.com/INF/A325) but whose parents had
noted fever at home (38.3°C and 40°C, respectively).
We also analyzed the value of WBC, ANC, and CRP for
predicting bacteremia. The ROC curves for this analysis are shown in
Figure, Supplemental Digital Content 5, http://links.lww.com/INF/A328.
CRP, at 0.847 (0.754 – 0.940), had the largest area, but the difference between this area and those for ANC and WBC was not
statistically significant. A CRP value of 70 g/L had a 93.8%
specificity (CI: 92.1%–95.1%) for the detection of positive blood
culture and a 99.3% (CI: 98.5%–99.6%) negative predictive value
(NPV) in our population, but a sensitivity of only 69.6% (CI:
49.1%– 89.4%). Selecting lower cut-offs does not improve these
results: decreasing this cut-off to 20 g/L increased the sensitivity to
only 73.9% (CI: 53.5%– 87.5%), and the specificity was reduced to
74.8% (CI: 72.0%–77.5%). The common cut-off points for ANC
(ⱖ10,000/mm3) and WBC (ⱖ15,000/mm3) present lower degrees
of sensitivity and NPV in our population (data not shown). The
selection of well-appearing infants with normal urine dipstick
results brought the areas under the ROC curves for CRP, WBC,
and ANC closer as the sensitivity and NPV decrease for CRP and
increase for WBC and ANC (data not shown).
Three infants with a positive blood culture were classified as
low-risk SBI patients. As shown in the flow chart, the blood
culture-positive rate in low-risk SBI patients was 0.6% (3/480).
The use of our low-risk SBI criteria gave a sensitivity of 87%
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Gómez et al
FIGURE 1. Flow chart.
(67.9%–95.5%) for detecting bacteremia, with a 99.4% NPV
(98.2%–99.8%). The mean length of stay of the 464 low-risk SBI
infants older than 15 days in the Observation Unit was 11.1 hours.
All of the 23 children recovered well, although HIV infection was eventually diagnosed in 1 patient.
DISCUSSION
Our data (a 2.2% blood culture-positive rate in the global
sample; 1% in well-appearing and previously healthy infants with a
normal urine dipstick) suggest that a blood culture should be performed in all infants less than 3 months of age with FWS and it is
essential in infants with a suspected UTI (leukocyturia and/or nitrituria in the dipstick), in whom the blood culture-positive rate is 4.4%.
Some authors have recommended this approach only for
infants under 2 months of age.7,8 We found a higher prevalence of
positive blood culture among febrile infants younger than 1 month,
although the difference was not statistically significant. It may be
unnecessary to obtain a blood culture systematically in all febrile
infants between 1 and 3 months of age, but a larger sample from
a multicenter study is required to negate these recommendations.
We are currently considering reducing the cut-off from 3 to 2
months of age and to manage these infants in a similar way to
those older than 3 months. The former infants who were previously
healthy and well-appearing, with low fever (⬍39.5°C) and with a
normal urine dipstick result, would be managed as outpatients
without performing CBC, CRP, and blood culture. In our series, 1
infant who met all these requirements had a positive blood culture
(E. faecalis; blood culture-positive rate in this group: 0.5%).
The most frequently isolated bacterium was E. coli, followed by S. pneumoniae and Group B N. meningitidis. Only 2
cases of S. agalactiae were reported. The systematic screening of
women in their third term of pregnancy (rectal and vaginal culture
in weeks 35–37) for this bacterium, and the use of intrapartum
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antibiotic prophylaxis, have reduced the incidence of infected
newborns.13,14 We use a risk-based approach at our hospital to
identify candidates suitable for intrapartum prophylaxis—the pregnant women who receive intrapartum antibiotic prophylaxis (intravenous penicillin) include those with the risk factors listed in Table,
Supplemental Digital Content 4, http://links.lww.com/INF/A327.
According to our results, the blood culture-positive rate is
related to following 2 factors that can be easily evaluated when
evaluating a febrile infant: general appearance and urine dipstick
result. These factors can help identify infants at increased risk of
having bacteremia. UTI, with a prevalence of about 7.5%,25,26 is
the most commonly found SBI in young infants. The blood
culture-positive rate in patients younger than 3 months with a
positive urine culture in our sample was 4.4%, thus highlighting the
importance of obtaining a blood culture in young febrile infants with
a suspected UTI. The bacteremia rate detected in young infants with
a UTI in previous studies was even higher; Bachur and Caputo27
reported an incidence of 21% for infants less than 1 month, 13% for
infants 1 to 2 months, and 4% for infants 2 to 3 months.
In our study, CRP, WBC, and ANC were not good predictors of bacteremia in young febrile infants as test sensitivity in
terms of positive blood culture was quite low and even the use of
our low-risk SBI criteria gave a sensitivity of only 87%. Consequently, we do not systematically admit low-risk infants, although
we recommend they be monitored in the Observation Unit of our
Pediatric Emergency Department for up to 24 hours to detect a
possible worsening of their condition irrespective of their CBC,
WBC, and ANC values. Hsiao and Baker28 reviewed some of the
recent literature on these classic markers. In their 2005 manuscript,
they concluded that WBC was neither sensitive nor specific as an
indicator of bacteremia and other SBI in infants and that although
CRP seems to be a reliable indicator of bacterial infection in
children, no study have targeted young infants.
© 2009 Lippincott Williams & Wilkins
The Pediatric Infectious Disease Journal • Volume 29, Number 1, January 2010
In November 2007, we included the procalcitonin (PCT) in
the evaluation of the infant less than 3 months of age with FWS.
We have not analyzed the value of this new marker for the
detection of bacteremia in this group of infants because, since its
introduction, we still have few patients in whom PCT was performed. According to previous studies, PCT offers higher specificity than CRP for differentiating between the viral and bacterial
etiology of the fever.29,30 However, to the best of our knowledge,
the use of PCT to detect occult bacteremia in young infants has not
been studied and most children with SBI included in previous
studies evaluating the value of PCT for the detection of SBI were
not well-appearing,31,32 which means that its practical utility is not
fully established. Maniaci et al33 reported recently that PCT has
favorable test characteristics for detecting SBIs in young febrile
infants. The figure given for the prevalence of positive blood
culture (2.5%) is similar to that in our study. However, only 6
infants with bacteremia were included in this study and, as stated
by the authors, 2 of the 6 bacteremia cases were caused by E. coli
and their relatively low PCT values should be noted.
This study had several limitations. A prospective study
would have allowed for better patient follow-up than the retrospective study performed, although the telephone follow-up carried out by a properly trained pediatric resident may serve to
minimize this limitation. Second, it was not a multicenter study, so
the results might not apply to other populations. Third, the availability of a larger sample would have allowed us to analyze test
performance levels in different age groups. The fact that all infants
enrolled in this study were evaluated by an experienced pediatric
emergency physician in the first hour after arriving in the emergency department can be considered a constraint as regards making these outcomes more widespread.
We conclude that the blood culture-positive rate in young
febrile infants admitted to a pediatric emergency department is
approximately 2% and that higher rates can be related to the
infants’ appearance and their dipstick results. Blood culture is
important for infants upon admission to the emergency department, although larger samples are required to establish whether a
blood culture should or should not be recommended in the case of
selected infants over 1 month old.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
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