Journal of Perinatology

https://doi.org/10.1038/s41372-018-0207-7

QUALITY IMPROVEMENT ARTICLE

Implementation of the sepsis risk score for chorioamnionitis-

exposed newborns
Ladawna L Gievers 1 Jennifer Sedler2 Carrie A Phillipi1 Dmitry Dukhovny1 Jonah Geddes3 Peter Graven3
● ● ● ● ● ●

Benjamin Chan 4 Sheevaun Khaki1

●

Received: 5 June 2018 / Revised: 4 August 2018 / Accepted: 6 August 2018

© Springer Nature America, Inc. 2018

Abstract
Background: To prevent early onset sepsis (EOS), ~10% of neonates receive antibiotics based on CDC recommendations
regarding chorioamnionitis exposure. A sepsis risk score (SRS) predicts EOS and spares unnecessary evaluation and
treatment.
Local problem: Chorioamnionitis-exposed neonates utilize significant resources.
Methods: An SRS algorithm was implemented to decrease resource utilization in chorioamnionitis-exposed neonates
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≥35 weeks’. Outcome measures included antibiotic exposure, time in NICU, laboratory evaluations, and length of stay
(LOS). Balancing measures were missed cases of EOS and readmissions. Data were assessed using run charts.
Interventions: Plan-Do-Study-Act cycles were utilized to process map, implement and reinforce the algorithm.
Results: A number of 356 patients met inclusion criteria. After algorithm implementation, antibiotic exposure reduced from
95 to 9%, laboratory evaluation from 96 to 22%, NICU observation from 73 to 10%. LOS remained unchanged. No missed
cases of EOS, nor sepsis readmissions.
Conclusions: Algorithm implementation decreased antibiotic and resource utilization without missing cases of EOS.

Introduction accurate diagnosis of chorioamnionitis has significant

Chorioamnionitis is a risk factor for early onset sepsis
(EOS), a potentially life-threatening bacterial infection of
the neonate [1, 2]. The diagnosis of chorioamnionitis is
fraught with variability. Due to the ambiguity of this diag-
nosis, multiple clinical criteria have been developed, such as
the triple I classification system [3]. Maternal fever is the
major clinical feature of chorioamnionitis; however, even
the fever may be caused by a myriad of factors including
epidural analgesia or other infectious sources [4–6]. An
* Ladawna L Gievers
gievers@ohsu.edu
1
Department of Pediatrics, Oregon Health and Science University,
Portland, OR, USA
2
School of Medicine, University of Arizona, Tucson, AZ, USA
3
Center for Health Systems Effectiveness, Oregon Health and
Science University, Portland, OR, USA
4
School of Public Health, Oregon Health and Science University,
Portland, OR, USA
implications for the neonate, such as additional inpatient
evaluation and treatment in the short term and increased risk
for wheezing and poor neurodevelopmental outcomes in the
long term [2, 7, 8]. The incidence of chorioamnionitis as
currently defined is 1–4% [9, 10], underscoring its burden
on maternal and neonatal health.
EOS is defined as a positive blood and/or cerebrospinal
fluid (CSF) culture in the first week of life. The most common
cause of EOS in late preterm and term neonates is group B
Streptococcus (GBS) [11]. Significant strides have been made
in reducing the incidence of EOS, primarily due to the Center
for Disease Control and Prevention (CDC) guidelines in 1996
recommending intrapartum antibiotic prophylaxis for GBS
positive mothers [12]. The national incidence of EOS
decreased dramatically after these guidelines from 3 to 4 cases
per 1000 live births to 0.8–1.0 cases per 1000 live births
[2, 13–15]. Despite this decrease, the number of neonates
being evaluated for EOS remains substantial, with one large
birthing center reporting approximately 10% of neonates
treated with antibiotics [2, 8]. There is significant variability in
management of chorioamnionitis-exposed neonates; a recent
study found that 65% of responding nurseries used

the CDC guidelines and 14% used a neonatal sepsis risk
calculator [16].
Early identification of a neonate with EOS is challen-
ging but necessary to allow for prompt initiation of ther-
apy and in order to improve outcomes. The 2010 CDC
guidelines regarding secondary prevention of GBS state
that all chorioamnionitis-exposed neonates receive
empiric antibiotics [17]. This empiric approach results in
many uninfected neonates receiving antibiotics with
resultant mother-baby separation, exposure to painful
procedures, potential impact on the neonatal microbiome,
and healthcare spending [8, 18–20]. Separation of healthy
neonates from their mothers is associated with decreased
exclusive breastfeeding rates and early breastfeeding
cessation [21, 22]. Significant resource utilization is
required to evaluate and treat chorioamnionitis-exposed
neonates. Mukhopadhyay et al. found that approximately
$400,000 were spent in the evaluation and treatment of
1396 asymptomatic neonates at risk for EOS [8].
There is a clear need to better stratify chorioamnionitis-
exposed neonates. Recent studies describe the Neonatal
Early Onset Sepsis calculator, which uses a quantitative risk
stratification to calculate a sepsis risk score (SRS) to help
guide clinician management. The SRS identifies neonates
who would most benefit from further evaluation based on
objective risk factors, such as gestational age (GA), pro-
longed rupture of membranes, and maternal fever. It per-
forms as well as the CDC recommendations in identifying
EOS but avoids unnecessary evaluation and treatment
[23, 24]. Recent retrospective studies demonstrated that use
of the SRS significantly decreased the proportion of neo-
nates who received antibiotics compared to the CDC
guideline criteria [25–27].
We assembled a quality improvement team to implement
an SRS-based algorithm for chorioamnionitis-exposed neo-
nates with a goal of reducing unnecessary antibiotic exposure,
and thus the downstream benefits of reduced resource utili-
zation and improved outcomes. Our goals were to reduce (1)
antibiotic exposure by 50%, (2) laboratory evaluations by
40%, (3) maternal-neonatal separation by 50% from baseline,
as well as assess the impact on the length of stay.
Methods
Context
This project was a collaboration between the mother baby
unit (MBU) and the neonatal intensive care unit (NICU) at
Oregon Health and Science University (OHSU). OHSU is
an academic, quaternary care center with approximately
2500 deliveries and 600 NICU admissions annually. The
MBU is a 28-bed well-baby unit with a total of
L. L. Gievers et al.
approximately 60 nurses who are assigned at a ratio of 1
nurse to 3 maternal-neonatal dyads on average. OHSU has
7 general pediatric and 31 family medicine providers who
round on neonates in the MBU. The NICU is staffed by 11
neonatology providers. Other important contextual features
include the local chorioamnionitis incidence of 3% and
MBU admission criteria which includes gestational age
≥35 weeks.
Interventions
Key stakeholders were assembled into a multidisciplinary
group to develop an algorithm for implementing the SRS in
the management of chorioamnionitis-exposed neonates.
Pediatric, obstetric and family medicine providers, nurses
from the MBU, NICU, and labor and delivery ward and a
neonatal pharmacist were involved. The current state of
management of chorioamnionitis-exposed neonates was
assessed, standard management included (1) at least 4 h of
NICU observation, (2) laboratory evaluations including a
blood culture, and (3) 48 h of empiric ampicillin and gen-
tamicin, resulting in approximately 75 chorioamnionitis-
exposed neonates receiving this triad annually.
After review of the literature, an algorithm was devel-
oped to promote individualized evaluation and treatment of
chorioamnionitis-exposed neonates (Fig. 1). An early clin-
ical assessment of the neonate was to be performed by a
physician or nurse practitioner within 60 min after birth to
calculate an SRS. This individualized SRS directed neo-
nates into one of three clinical pathways (routine, enhanced
observation, clinical illness). All pathways included serial
reassessments to identify for clinical change.
Revisions were made to the SRS algorithm based on
feedback from a multidisciplinary group of physicians,
midwives, nurses and nurse managers. After approval from
the hospital perinatal best practices committee, the algo-
rithm was incorporated into the electronic medical record
(EMR) and housed within the institutional electronic policy
system. Prior to algorithm implementation, clinical support
tools including bundled order sets and note templates were
developed for provider reference and workflow standardi-
zation. Plan-Do-Study-Act (PDSA) methodologies
were used for implementation and to assess subsequent
change. Providers received electronic and in-person
reminders and didactic educational sessions to reinforce
the algorithm.
Study of the interventions
Our quality improvement team met monthly to measure
outcomes, to formally review algorithm feedback, to
review algorithm compliance, and to monitor for missed
cases of EOS.
Implementation of the sepsis risk score for chorioamnionitis-exposed newborns
Fig. 1 OHSU workflow algorithm for neonates exposed to chorioamnionitis utilizing the sepsis risk score and neonatal clinical exam
Measures
The total number of neonates born to mothers with chor-
ioamnionitis at ≥35 weeks’ GA was examined. The primary
outcome was percentage of chorioamnionitis-exposed neo-
nates who received antibiotics, assessed monthly on a run
chart. Secondary outcomes included percentage of
chorioamnionitis-exposed neonates who underwent labora-
tory evaluation and were observed in the NICU, total
number of hours in the NICU per patient, and length of stay
(LOS).
Antibiotic exposure was defined as receipt of at least one
dose of intravenous (IV) or intramuscular (IM) antibiotics
within the first 48 h of life. Patients were considered to have
underwent laboratory evaluation if either blood culture or
complete blood cell count were obtained during the birth
hospitalization. Time and observation in the NICU were
surrogates for maternal–neonatal separation. Time was
calculated based on transfer times as recorded in the neo-
nate’s EMR. The algorithm was implemented on 1 July
2015 and data were collected 1 October 2012 through 30
September 2016. Balancing measures included EOS and
readmission to our institution for sepsis.
Source of data and variable definitions
The EMR was queried to identify women who developed an
intrapartum fever (≥100.4°F) and trained medical record
analysts manually reviewed each chart to select patients
with a clinical diagnosis of chorioamnionitis documented
within the maternal chart. Subjects were identified using
this process to capture neonates at highest risk for antibiotic
exposure, which, in our MBU, is chorioamnionitis and not
maternal fever alone. Clinical, laboratory, and demographic
data were obtained from neonatal and maternal EMRs.
Neonatal inclusion criteria included: (1) birth at OHSU;
(2) GA at birth ≥35 weeks; (3) maternal diagnosis of
chorioamnionitis. Exclusion criteria were a major birth
defect as defined by the Vermont Oxford Network and
admission to the NICU for >8 h. Explicitly defining a cut
off period for NICU admission allowed this study to focus
on well appearing neonates. Neonates born <35 weeks’
gestation were excluded from our study since they are
admitted to the NICU per OHSU policy.
Cases of culture-confirmed EOS were defined as a
positive blood or CSF culture of a single known pathogenic
species within the first 5 days of culture incubation.
 L. L. Gievers et al.

Cultures growing common skin flora (including S. epi- Analysis

dermidis) or multiple organisms were considered
contaminants. Data were collected over two time periods with regards to
SRS algorithm implementation: 33 months pre-
Table 1 Maternal and neonatal demographics and clinical implementation and 15 months post implementation. The
characteristics pre-implementation period reflects use of the 2010 CDC
Pre-algorithm Post-algorithm p value
guidelines. The post-implementation period reflects use of
n = 213 n = 143 the institutional SRS-driven algorithm.
Outcome measures were analyzed monthly using run
Maternal characteristics charts. Neonatal antibiotic exposure, laboratory evalua-
Age (years), mean ± SD 28.7 ± 5.7 30.3 ± 6.4 <0.05 tion, and NICU admission were dichotomous variables
C-section delivery, 87 (40.8) 57 (39.9) 0.94 that were modeled using logistic regression. All models
n (%)
were estimated unadjusted and adjusted for covariates.
Intrapartum maximum 38.5 ± 0.5 38.5 ± 0.5 0.28
Covariates for all models include: GA, delivery mode,
temperature (°C), mean
± SD APGAR score, birth weight, maternal age, GBS status,
GBS status, positive, 56 (26.3) 34 (23.8) 0.42 maternal maximum temperature, language, and insurance
n (%) type (public, private, military, self-pay). To analyze the
Race, n (%) <0.05 effect of the intervention patient length of stay, we used a
Caucasian 115 (54.0) 94 (65.7) generalized linear regression model, specifying each
Multiracial 66 (31.0) 19 (13.3) variable as following a gamma distribution independent of
Asian 14 (6.5) 12 (8.4) the other.
Black 6 (2.8) 4 (2.8)
Other 3 (1.4) 0
Unknown/Decline 9 (4.2) 14 (9.8)
Results
Language, non-English, 35 (16.4) 14 (9.8) 0.10
n (%) A number of 356 neonates met inclusion criteria; 213 in the
Insurance, Public, n (%) 112 (52) a
62 (43) b
0.10 pre-implementation and 143 in the post implementation
Infant Characteristics cohorts. The frequency of maternal chorioamnionitis for
Male gender, n (%) 108 (50.7) 84 (58.7) 0.16 neonates ≥35 weeks’ gestation was significantly increased
Gestational age at 39.9 ± 1.3 39.8 ± 1.3 0.44
from 3.4% (213/6175) in the pre-implementation to 5.0%
birth (weeks), mean (143/2864) in the post-implementation cohorts (p < 0.05).
± SD The maternal–neonatal dyads’ characteristics and demo-
Birth weight (g), 3538 ± 477 3526 ± 479 0.82 graphics are demonstrated in Table 1. The two cohorts were
mean ± SD similar except for an older mean maternal age in the post-
APGAR, 5 min, 8.6 ± 0.9 8.6 ± 0.9 0.55 implementation cohort (30.3 vs. 28.7 years, p < 0.05) and
mean ± SD
more likely to be Caucasian (Table 1).
GBS group B Streptococcus Antibiotic administration, laboratory evaluation, and
a
Other insurance types included private (n = 96), military (n = 3), and NICU observation decreased significantly after algorithm
self-pay (n = 2) implementation (Table 2). In the pre-implementation
b
Other insurance types included private (n = 79) and military (n = 2) cohort, 95.3% (203/213) of neonates received antibiotics

Table 2 Comparison of
Pre-algorithm n = 213 Post-algorithm n = 143 p valueb
antibiotic exposure, laboratory
evaluation and maternal- Antibiotic exposure, n (%) 203 (95.3) 13 (9.1) <0.01
neonatal separation
Laboratory evaluations
Patients with laboratory tests obtaineda, n (%) 204 (95.8) 31 (21.7) <0.01
Maternal–neonatal separation
Observed in NICU, n (%) 155 (72.8) 14 (9.8) <0.01
NICU neonatal intensive care unit
a
Defined as CBC or blood culture
b
Adjusted for gestational age, delivery mode, APGAR, birth weight, maternal age, GBS status, temperature,
language, and insurance
Implementation of the sepsis risk score for chorioamnionitis-exposed newborns

Fig. 2 Run chart of percentage of chorioamnionitis-exposed neonates receiving antibiotics over time with PDSA interventions

Fig. 3 Run chart of percentage of chorioamnionitis-exposed neonates who underwent laboratory evaluations over time with PDSA interventions

compared to 9.1% (13/143) in the post-implementation
cohort (p < 0.01) with the median decreasing from 100 to
7.7% (Fig. 2). Similarly, in the pre-implementation cohort,
95.8% of neonates had lab tests performed compared to
21.7% in the post-implementation cohort (p < 0.01) with the
median decreasing from 100 to 20% (Fig. 3). Finally, in the
pre-implementation cohort, 72.8% spent time in the NICU
compared to 9.8% in the post-implementation cohort (p <
0.01) with the median decreasing from 75 to 7.4%. Time in
the NICU decreased from a median of 2.6 h per patient to
0.3 h per patient. Length of stay did not change in a sta-
tistically significant manner from 2.40 to 2.47 days
(p = 0.14).
In the post-implementation period, there was one
positive blood culture, S. epidermidis, that was considered
a contaminant. A 3-day-old male was readmitted in the
pre-implementation cohort for neonatal fever with CSF
pleocytosis and pyuria but without identification of a cau-
sative organism. One neonate was readmitted in the
post-implementation phase with hyperbilirubinemia.

Discussion
With the privilege of caring for the youngest patients comes
the responsibility of making careful, evidence-based chan-
ges. The development of an institutional-specific approach
to implementation of the SRS allowed us to individualize
our management in an evidence-based manner. The SRS
highlights an area where value-based care and evidence-
based medicine have come together. While previous pub-
lications have demonstrated the efficacy of the SRS in
reducing antibiotic utilization, we describe a successful
quality improvement process for the implementation of an
algorithm which has led to a sustained decrease in resource
utilization without jeopardizing patient outcomes [25, 26].
Specifically, we prospectively demonstrated that antibiotic
exposure, laboratory evaluation, and maternal-neonatal
separation were decreased.
Implementation of the new algorithm provided
opportunities for discussions amongst an inter-
disciplinary team. Early development of the algorithm
was met with resistance as this was a large shift in
management of neonates at our institution. To demon-
strate early success with the new algorithm, a small test
of change was limited to chorioamnionitis-exposed
neonates as they were at highest risk for unnecessary
antibiotic exposure, with the plan to ultimately incor-
porate the SRS into management of nearly any neonate
>34 weeks’ gestation as the authors intended. Addi-
tionally, there were understandable concerns about
monitoring chorioamnionitis-exposed neonates in the
mother baby unit despite the plan for timely and more
frequent evaluations by the medical team. However,
through presentation of the existing literature and
demonstration of the benefit of having a single team care
for this neonate, we gained individual-level and ulti-
mately institutional buy in. It was accepted that there
may be missed cases of EOS but this would be true of
nearly any management approach. Interestingly, our
incidence of diagnosed chorioamnionitis significantly
increased from 3.4% in the pre-implementation cohort to
5.0% in the post-implementation cohort. Our population
may have changed, or maternal providers may have been
hesitant to diagnose chorioamnionitis and commit neo-
nates to separation and empiric evaluation in the setting
of isolated maternal fever in the pre-implementation
cohort.
There was high educational value hidden in this quality
improvement project. The importance of the family’s
understanding when making medical decisions in the hos-
pital setting is often lost [28, 29]. Housed within this
algorithm were multiple opportunities for observation and
examination of the neonate which led to increased interac-
tions with the family to discuss this nuanced, individualized
L. L. Gievers et al.
care, though this was not formally assessed as these data
could not be obtained for the pre-implementation cohort.
Simultaneously, trainees were educated both formally in
didactic sessions and informally at the bedside. Real time,
the QI process, the value and skill of effective commu-
nication, and the need to critically appraise the science that
drove this project were modeled.
Our study had several limitations. First, patient selec-
tion criteria were imperfect due to the ambiguity of the
diagnosis of chorioamnionitis and its inconsistent location
in EMR documentation, although consistent throughout
the study and likely captured the majority of the patients
at our institution. Second, there may be limited general-
izability given the study’s small sample size at our large
academic quaternary center with specific patient demo-
graphics. However, given the targeted patient population
of well appearing neonates and the number who are
unnecessarily exposed to antibiotics, implementation of
the SRS shows promise to reduce antibiotic exposure in
any setting. Additionally, at our institution, we have in-
house practitioners during all hours which allows for
frequent reassessments, whereas other birth settings may
only have nursing staff. Given that the nurses are the first
to assess and triage the neonate, the use of SRS only
provides a more systematic approach to a decision on
antibiotic use and would engage the neonatal provider.
Finally, there are multiple hospital systems within our
geographic area and therefore we cannot be certain if
neonates were re-admitted elsewhere. Given the low risk
of EOS and that we are a quaternary center, it is unlikely
that those were missed.
In conclusion, we demonstrate successful imple-
mentation of the SRS for chorioamnionitis-exposed neo-
nates with resultant reduced unnecessary antibiotic
exposure, laboratory evaluations, and maternal–neonatal
separation with unchanged hospital length of stay. There
were no adverse outcomes. We plan to apply the SRS to
all neonates at our institution and to investigate the effects
on exclusive breastfeeding rates and maternal postpartum
depression.
Acknowledgements The authors thank the care providers in Labor &
Delivery, MBU and NICU at OHSU. We thank Jose Rodriguez for
data collection. The generous support from the Friends of Doernbecher
cannot be understated. We also thank the neonates and families for
giving us the opportunity to be involved in their care.
Compliance with ethical standards
Conflict of interest Dr. Dukhovny is on faculty and a consultant for
Vermont Oxford Network. All phases of this study were supported by
the Friends of Doernbecher Foundation
Ethical considerations The study was approved by the OHSU insti-
tutional review board.
Implementation of the sepsis risk score for chorioamnionitis-exposed newborns
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