J Neurosurg Pediatrics 14:184–189, 2014

©AANS, 2014

Poor correlation between head circumference and cranial

ultrasound findings in premature infants with
intraventricular hemorrhage
Clinical article

Martha-Conley E. Ingram, B.S.,1 Anna L. Huguenard, B.S., B.A.,1

Brandon A. Miller, M.D., Ph.D.,1 and Joshua J. Chern, M.D., Ph.D. 2
Department of Neurosurgery, Emory University; and 2Pediatric Neurosurgery Associates at Children’s
1

Healthcare of Atlanta, Georgia

Object. Intraventricular hemorrhage (IVH) is the most common cause of hydrocephalus in the pediatric popula-
tion and is particularly common in preterm infants. The decision to place a ventriculoperitoneal shunt or ventricular
access device is based on physical examination findings and radiographic imaging. The authors undertook this study
to determine if head circumference (HC) measurements correlated with the Evans ratio (ER) and if changes in ven-
tricular size could be detected by HC measurements.
Methods. All cranial ultrasound (CUS) reports at the authors’ institution between 2008 and 2011 were queried
for terms related to hydrocephalus and IVH, from which a patient cohort was determined. A review of radiology
reports, HC measurements, operative interventions, and significant clinical events was performed for each patient in
the study. Additional radiographic measurements, such as an ER, were calculated by the authors. Significance was set
at a statistical threshold of p < 0.05 for this study.
Results. One hundred forty-four patients were studied, of which 45 (31%) underwent CSF diversion. The mean
gestational age and birth weight did not differ between patients who did and those who did not undergo CSF diver-
sion. The CSF diversion procedures were reserved almost entirely for patients with IVH categorized as Grade III or
IV. Both initial ER and HC were significantly larger for patients who underwent CSF diversion. The average ER and
HC at presentation were 0.59 and 28.2 cm, respectively, for patients undergoing CSF diversion, and 0.34 and 25.2
cm for those who did not undergo CSF diversion. There was poor correlation between ER and HC measurements
regardless of gestational age (r = 0.13). Additionally, increasing HC was not found to correlate with increasing ERs
on consecutive CUSs (φ = -0.01, p = 0.90). Patients who underwent CSF diversion after being followed with multiple
CUSs (10 of 45 patients) presented with smaller ERs and HC than those who underwent CSF diversion after a single
CUS. Just prior to CSF diversion surgery, the patients who received multiple CUSs had ERs, but not HC measure-
ments, that were similar to those in patients who underwent CSF diversion after a single CUS.
Conclusions. The HC measurement does not correlate with the ER or with changes in ER and therefore does not
appear to be an adequate surrogate for serial CUSs. In patients who are followed for longer periods of time before
CSF shunting procedures, the ER may play a larger role in the decision to proceed with surgery. Clinicians should
be aware that the ER and HC are not surrogates for one another and may reflect different pathological processes.
Future studies that take into account other physical examination findings and long-term clinical outcomes will aid in
developing standardized protocols for evaluating preterm infants for ventriculoperitoneal shunt or ventricular access
device placement.
(http://thejns.org/doi/abs/10.3171/2014.5.PEDS13602)

Key Words      •      intraventricular hemorrhage      •      hydrocephalus      •

cranial ultrasound      •      head circumference      •      prematurity

I
ntraventricular hemorrhage (IVH) is the most com-
mon cause of hydrocephalus in the pediatric popula-
tion. It is estimated that approximately 30%–59% of
all live-born, preterm infants will develop IVH and that
36% of all extremely premature infants (gestational age
Abbreviations used in this paper: CUS = cranial ultrasound; ER
= Evans ratio; HC = head circumference; ICP = intracranial pres-
sure; IVH = intraventricular hemorrhage; VAD = ventricular access
device; VPS = ventriculoperitoneal shunt.
< 25 weeks) will develop severe hemorrhage classified as
Grade III or IV.6,13 The long-term sequelae of IVH include
parenchymal injury, hydrocephalus, cerebral palsy, and
cognitive delay.1,16,17 Currently, there is no consensus re-
garding the indications for, or the timing of, the treatment
of hydrocephalus following IVH in premature infants.
Clinical suspicion for IVH can be raised through as-
sessment of several factors including apneic or bradycard-
ic episodes, a bulging anterior fontanelle, and increased
head circumference (HC), and is confirmed by findings

184 J Neurosurg: Pediatrics / Volume 14 / August 2014

Head circumference and ultrasound findings
on cranial ultrasound (CUS). The presence of an apneic or
bradycardic episode suggests that hemorrhage is already
severe and strongly predicts placement of a temporizing
device or shunt.13 Studies have demonstrated a positive
correlation between findings on palpation of the anterior
fontanelle and intracranial pressure (ICP).9,15 The reliabil-
ity of this physical examination finding has been verified,
with an acceptable interrater reliability in evaluating the
anterior fontanelle.18 Nevertheless, guidelines for how
these assessments can be used in clinical practice have not
yet been established.
Measuring HC at regular intervals in this population
has long been thought to be an objective way to assess
progression of hydrocephalus. However, the criterion of a
2 cm/week increase in HC as an indicator of posthemor-
rhagic hydrocephalus has been shown to be unreliable.13
Using serial CUSs has become standard practice for many
pediatric neurosurgeons to evaluate the need for shunt
placement, although there is no evidence-based rationale
for this practice.4,14
Current practice is for physicians to use physical ex-
amination and radiographic findings without evidence
of which factors are most predictive of a need for shunt
placement. There is also no clear understanding of how
well clinical and radiographic findings correlate in pre-
term infants. This study was undertaken to establish the
correlation, or lack thereof, between HC and CUS find-
ings, and to determine which of these clinical factors are
most predictive for CSF diversion.
Methods
Patient Selection
Institutional review board permission was obtained
for this study. We queried our electronic medical record
for CUS reports entered between 2008 and 2011 and
containing the phrases “intracranial hemorrhage,” “intra-
ventricular hemorrhage,” “germinal matrix,” “bleed,” or
“IVH.” Patients with concurrent diagnosis of congenital
malformations or hydrocephalus due to causes other than
IVH were excluded. Patients born of term pregnancy (> 38
weeks) were excluded.
A retrospective chart review was then conducted to
collect data on the 144 patients identified. The following
information was collected for each patient: gestational age
at birth; birth weight; HC measurements; characteristics
of each ultrasound performed, including the time interval
between the scans; grade of IVH; presence and progres-
sion of associated hydrocephalus; and Evans ratio (ER).
Other forms of imaging, including CT scans and MRI,
were not included for analysis because the number of pa-
tients receiving imaging by these modalities was small.
Additional clinical information was analyzed, including
the date of placement of a VAD or shunt, the age at which
diversion occurred, any revisions of shunts or shunt infec-
tions, and the date and cause of death of the patient where
available.
Ultrasound Imaging
The authors evaluated all CUS images and reports.
Grading of IVH followed the scale defined by Papile et
al.12 Children who presented to our facility with a history
J Neurosurg: Pediatrics / Volume 14 / August 2014
of hemorrhage and documented posthemorrhagic hy-
drocephalus, but in whom no IVH was present on CUS
imaging obtained at our institution, were labeled as hav-
ing “resolved hemorrhage” but were still included in the
study. If periventricular leukomalacia and cystic brain
parenchymal changes followed a diagnosis of Grade IV
hemorrhage, the patient was considered to continue car-
rying a Grade IV classification for analysis. The label of
hydrocephalus was applied if the radiographic dictation
included the terms “hydrocephalus,” “ventriculomegaly,”
“ventricular dilatation,” or “enlarged ventricles.” We mea-
sured the ER, the ratio of the bifrontal horn diameter to
the biparietal bone diameter, for each CUS scan.7,10
Statistical Analysis
Potential predictors of CSF diversion were analyzed,
including initial birth weight, gestational age, presence
of hydrocephalus on the initial CUS, interval worsening
of hydrocephalus between CUSs, and ER on each CUS.
Data were analyzed using the Student t-test of means. For
the analysis of differences in ER and HC by IVH grade,
ANOVA, Student t-test, and correlation studies were used
as indicated in the text. Interscan changes in ER and HC
were calculated and compared using the Pearson chi-
square test for association. Significance was set at p < 0.05
for all parts of this study.
Results
Initial ER and HC as Predictors of CSF Diversion
Presenting patients’ demographic data, initial HC
mea­surements, and radiographic findings are shown in
Ta­ble 1, allowing comparison between patients who pro-
gressed to surgical CSF diversion (n = 45) and those who
did not (n = 99). The vast majority of patients in the study
who underwent CSF diversion did so after receiving only
1 CUS at our institution (35 of 45 patients, 78%). Birth
weight and gestational age at birth did not differ between
patients who underwent CSF diversion and those who did
not.
As shown in Table 1, there was a significant differ-
ence in initial ER for children who did and did not un-
dergo CSF diversion. Overall, the average ER in the group
undergoing diversion was 0.59, compared with 0.34 in
the group not progressing to diversion (p < 0.001). When
patients were stratified by hemorrhage severity, a larger
initial ER was observed in patients needing CSF diversion
for resolved, mild-moderate, and severe hemorrhage. As
with the ER, the initial HC was significantly different be-
tween children who did and did not progress to CSF diver-
sion (p < 0.001), but this difference became less reliable
as patients were stratified by hemorrhage severity. For pa-
tients with Grade I or II hemorrhage, initial HC was not a
significant predictor of diversion (p = 0.087); patients with
CSF diversion who had resolved or severe (Grade III or
IV) hemorrhage had initial HC measurements that were
significantly larger, but by a relatively narrow margin (p =
0.029 and 0.041, respectively).
Correlation Between ER and HC
We used a correlation analysis to determine if HC
185
 M. C. E. Ingram et al.
TABLE 1: Comparison between demographic data in patients receiving CSF diversion and those who underwent no
surgical diversion*

Surgical CSF Diversion

Quality on Presentation No Yes p Value†
no. of patients 99 45
GA in wks at birth 27.4 (4.5) 27.2 (3.0) 0.79
birth weight in g 1153.9 (784.3) 1058.2 (446.8) 0.45
GA in wks at initial assessment 32.15 (24.5) 29.51 (4.4) 0.48
hemorrhage category
 resolved 6 (6.1%) 5 (11.1%) 0.32
  mild-moderate (Grade I or II) 54 (54.5%) 4 (8.9%) <0.001
  severe (Grade III or IV) 39 (39.4%) 36 (80.0%) <0.001
initial ER
 overall 0.34 (0.08) 0.59 (0.12) <0.001
  resolved hemorrhage 0.27 (0.07) 0.62 (0.11) <0.001
  mild-moderate hemorrhage 0.31 (0.04) 0.59 (0.16) <0.001
  severe hemorrhage 0.39 (0.09) 0.59 (0.12) <0.001
initial HC in cm
 overall 25.2 (4.4) 28.2 (3.5) <0.001
  resolved hemorrhage 34.5 (3.0) 30.3 (2.2) 0.029
  mild-moderate hemorrhage 25.5 (4.3) 29.3 (1.8) 0.087
  severe hemorrhage 23.4 (2.7) 24.7 (2.7) 0.041

*  Key demographic data obtained for all patients, stratifying many categories by grade of hemorrhage (resolved; mild-moderate
[Grade I or II]; severe [Grade III or IV]) to demonstrate factors significantly different between patients who later received surgical
CSF diversion and those who did not. Unless otherwise indicated, the numbers in parentheses represent the SD. GA = gestational
age.
†  The p values were calculated with either a chi-square or Student t-test. Significant differences (p < 0.05) are in boldface.

and ER correlated on initial scans for patients overall or
if stratified by gestational age (≥ 30 or < 30 weeks) at the
time of imaging (Fig. 1). Initial HC measurements were
not available for 14 patients. Contrary to our hypothesis,
there was a significant correlation between initial ER and
HC only in patients who underwent the first CUS at less
than 30 weeks gestational age, and no significant correla-
tion between initial CUS and ER overall (Table 2).
Correlation Between Changes in ER and HC
A contingency analysis was used to test if increases in
ER were accompanied by changes in HC. We examined
all patients who received > 1 scan without undergoing
CSF diversion, analyzing all intervals between scans. A
significant change in ER was set at 0.2, because this was
similar to the difference between initial ERs in patients
who did and did not undergo CSF diversion (Table 1). We
chose 1.5 cm as a meaningful change in HC, taken from
the study by Müller and Urlesberger, which showed 1.5
cm to be a sensitive indicator of increasing hydrocepha-
lus.11 The contingency association was analyzed with the
Pearson chi-square test, revealing no significant associa-
tion between changes in ER and changes in HC (Table 3).
Characteristics of Patients Undergoing Delayed Versus
Immediate CSF Diversion
To better understand the decision to proceed with
CSF diversion in patients who are followed for longer pe-
riods before surgery, we compared patients who received
multiple CUS images before CSF diversion to those who
received only 1 CUS prior to CSF diversion (Table 4). In
10 (22%) of 45 patients, > 1 scan was obtained before un-
dergoing CSF diversion. Patients in this late CSF diver-
sion group received an average of 4 CUSs before under-
going CSF diversion. Gestational age at birth and birth
weight were not significantly different between patients
who underwent early versus late CSF diversion, nor was
the presence of high-grade IVH. Additionally, gestation-
al age at the time of CSF diversion was not significantly
different between the 2 groups. Initial HC and ER were
significantly smaller in patients who underwent delayed
CSF diversion (p < 0.01 for each); however, ER did not
differ significantly between groups just prior to diversion
(p = 0.22). Head circumference remained slightly smaller
in patients who underwent CSF diversion at a later time
(p = 0.034).
Discussion
Predictors of CSF Diversion: ER Versus HC
Management of infants with hydrocephalus from IVH
has been the subject of controversy, because many infants
with IVH may have spontaneous resolution of symptoms
without shunt insertion.5 However, early interventions
such as lumbar puncture have been associated with lower

186 J Neurosurg: Pediatrics / Volume 14 / August 2014

Head circumference and ultrasound findings
Fig. 1.  Scatterplot showing ER and HC for all patients on initial scan,
stratified by < 30 weeks and ≥ 30 weeks gestational age (GA). The cor-
responding correlation study results are shown in Table 2. There were
130 patients in this group; 14 patients did not have initial HC measure-
ments and were not included.
rates of ventricular shunting and improved outcomes after
IVH;17 therefore, it is intuitive that any treatment for pre-
term hydrocephalus should be carried out as expeditiously
as possible. There is little consensus on the management
of patients with neonatal IVH and hydrocephalus, with
high variability in treatment between centers.8 Our data
demonstrate, as expected, that infants who receive CSF di-
version tend to present with higher grades of hemorrhage
initially and that both initial HC and initial ER are larger
in patients who undergo CSF diversion.
Correlation of ER With HC
Contrary to our hypothesis, we found a correlation
between HC and ER only in patients less than 30 weeks
gestational age at first scan, but not in our population
overall. We also found no correlation between ER and
HC changes that were deemed clinically significant and
likely to be reliably detected. These findings cast doubt on
the utility of HC as a surrogate for expanding ventricular
TABLE 2: Correlation between ER and HC at initial scan in all patients, with corresponding regression analysis*
No. of Pearson Coefficient of
Group Patients Correlation r (df = n − 2)
overall 130† r (128) = 0.13
<30 wks GA at initial scan 69 r (67) = 0.26
≥30 wks GA at initial scan 61 r (59) = −0.04
*  Correlation between initial HC and ER in all patients prior to diversion, stratified by age as shown in Fig. 1. Correlation was
significant (p < 0.05; boldface) only for the subgroup of patients < 30 weeks old at initial scan, but not for patients ≥ 30 weeks old
or overall.
†  Fourteen patients did not have an HC measured at initial scan.
J Neurosurg: Pediatrics / Volume 14 / August 2014
TABLE 3: Contingency association between interval changes in
HC and ER on all scans taken prior to diversion in all patients*
Contingency |ΔER| ≥ 0.2 |ΔER| < 0.2 Totals
|ΔHC| ≥ 1.5 3 87 90
|ΔHC| < 1.5 4 138 142
totals 7 225 232
*  Contingency association in changes of HC and ER over the entire
observation period prior to diversion; includes all patients in whom >
1 scan was performed. Significant absolute changes in HC or ER be-
tween any 2 sequential scans was defined as ≥ 1.5 cm in HC or ≥ 0.2 in
ER (see text). Scans obtained after diversion were not included in this
analysis. φ = −0.01; p = 0.90 according to the Fisher test. This contin-
gency association is not significant.
size as measured by ER or may reflect the inherent vari-
ability of the measurement itself. In either instance, this
reveals reservations for the utility of following serial HC
measurements to assess progressive hydrocephalus. To
our knowledge, there is no study of interrater reliability of
HC measurement, nor are there any data indicating how
variable either HC or ER may be within the same patient
when evaluated within short time periods, such as < 24
hours. Most importantly, there is no evidence regarding
how either HC or ER correlates with ICP, which is thought
to be the underlying cause of brain injury in preterm in-
fants with IVH. Comparing these 2 measurements with
actual ICP readings could help determine a gold standard
for choosing patients who would be most likely to benefit
from early CSF diversion, and could help surgeons avoid
performing unnecessary procedures.
Changes in ER and HC as Patients Progress Toward CSF
Diversion
The vast majority of patients in our study who under-
went CSF diversion had a VPS or VAD placed after the
first CUS performed at our institution. This indicates that
the clinical decision to place a diverting device is typi-
cally made rapidly. When CSF diversion occurred after
serial imaging studies, the ER, but not HC, was found to
have “caught up” with the measurements present in those
who had undergone diversion after 1 imaging study. This
finding indicates that neurosurgeons may rely on imag-
ing characteristics more than HC changes when following
the progression of hydrocephalus and deciding to place a
R 2 Regression
Coefficient M (slope) Intercept p Value
0.018 3.65 24.9 0.13
0.068 6.87 22.3 0.03
0.001 −1.08 28.56 0.74
187
 M. C. E. Ingram et al.

TABLE 4: Comparison between patients with early surgical intervention after 1 CUS image and those who underwent
intervention after ≥ 2 CUS images*

CSF Diversion
Characteristic Early Late† p Value
no. of patients 35 10
GA in wks at birth 27.5 (3.1) 26.1 (2.6) 0.18
GA in wks at time of diversion 31.1 (3.3) 31.4 (3.2) 0.80
birth weight in g 1114.6 (469.0) 860.8 (298.8) 0.11
initial hemorrhage category
 resolved 5 (14.3%) 0 (0%) 0.57
  Grade I or II 3 (8.6%) 1 (10%) 1.00
  Grade III or IV 27 (77.1%) 9 (90%) 0.66
ER
 initial 0.61 (0.11) 0.50 (0.13) <0.01
  before CSF diversion 0.61 (0.11) 0.57 (0.11) 0.22
HC in cm
 initial 29.0 (3.0) 25.8 (4.0) <0.01
  before CSF diversion 29.0 (3.0) 26.7 (1.8) 0.034
no. of scans before CSF diversion 1 (0) 4.0 (2.4) <0.001

*  Demographic and measured data for patients who received early surgical intervention, defined as CSF diversion after 1 CUS,
compared to patients with later surgical intervention. Both HC and ER were significantly smaller in patients who underwent delayed
CSF diversion (p < 0.001 for both measures). Although initial ER measurements differed significantly between the 2 groups, the
ER on the last scan before diversion did not differ significantly between the early diversion and delayed surgery groups. The HC
measurements remained significantly different prior to diversion, regardless of whether patients underwent diversion early or late
(p = 0.034). Unless otherwise indicated, the numbers in parentheses represent the SD. Significant differences (p < 0.05) are in
boldface.
†  At least 2 CUSs were done before VAD placement.

VPS or VAD at a later time. Future work on identifying
baseline characteristics of patients with IVH who develop
progressive hydrocephalus would allow this subgroup to
be identified and treated earlier.
Weaknesses of This Study and Future Directions
A weakness of our study is that other clinical indica-
tors, such as fontanelle tension or apneic/bradycardic epi-
sodes, were not evaluated. Neurosurgeons do take these
into account when determining the need for CSF diversion
in infants, although these episodes are not always pres-
ent, even with severe hydrocephalus. Although fontanelle
tension has been shown to have good interrater reliabil-
ity, there is no common method of measuring this tension
quantitatively.8,9 Correlation of our findings to measured
fontanelle tension or actual ICP measurement would help
determine whether ER or HC relates most closely to the
elevated ICP.
Patients who underwent late CSF diversion presented
with significantly smaller ER and HC than those who un-
derwent early CSF diversion. When these patients with so-
called late CSF diversion were examined just prior to sur-
gery, their ER, but not their HC, no longer differed from
those in patients with so-called early CSF diversion. This
suggests that clinicians may place more weight on ER than
HC measurements when following patients over time. Al-
ternatively, these patients’ hydrocephalus could have been
slower progressing, and CSF diversion may have prevent-
ed them from developing HCs as large as the early CSF
diversion group. It is important to note that an enlarging
ER in the absence of increased HC or other signs of hydro-
cephalus could be due to parenchymal loss rather than hy-
drocephalus. This highlights the fact that a single clinical
measurement should not be used in isolation to determine
if patients require CSF diversion and that relying on ven-
tricular size alone could lead to overtreatment.
Additional work is needed to develop standardized
clinical practices for CSF diversion in infants. Although
our study did not show a correlation between HC mea-
surements and ER, it is possible that our retrospective de-
sign was not optimally suited for this, because CUSs were
performed at nonstandardized intervals. Prospective trials
with clinical assessments of the anterior fontanelle timed
closely with CUS studies could better determine if clini-
cal assessments of the fontanelle can be sensitive enough
to predict development of hydrocephalus. Additionally,
emerging research has emphasized the potential for using
MRI flow monitoring to predict relative responses to CSF
diversion.2 Continued investigation into these diagnostic
assessments may lead to improved evaluation of IVH and
allow for decreased incidence and morbidity of associated
hydrocephalus.
Conclusions
Despite the realization that hydrocephalus leads to

188 J Neurosurg: Pediatrics / Volume 14 / August 2014

Head circumference and ultrasound findings
poor clinical outcomes and impaired cognitive function,
there is no standardized way to evaluate the efficacy of
shunt placement by an institution.3 Ultimately, the stan-
dardization of criteria for which patients undergo CSF
diversion or other treatments for hydrocephalus, and the
confirmation that these standards are efficacious, could
lead to an efficient protocol for placing VPSs in neonates.
Such improvements in treatment algorithms could reduce
unnecessary testing and subjective test interpretations,
and could potentially improve overall outcomes for in-
fants with IVH.
Disclosure
The authors report no conflict of interest concerning the mate-
rials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript preparation
include the following. Conception and design: Miller. Acquisition of
data: Ingram, Huguenard. Analysis and interpretation of data: Miller,
Ingram, Huguenard. Drafting the article: Ingram. Critically revising
the article: all authors. Reviewed submitted version of manuscript:
all authors. Approved the final version of the manuscript on behalf of
all authors: Miller. Statistical analysis: Ingram, Huguenard. Ad­min­i­
strative/technical/material support: Chern. Study supervision: Miller,
Chern.
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Manuscript submitted November 26, 2013.
Accepted May 8, 2014.
Please include this information when citing this paper: pub-
lished online June 20, 2014; DOI: 10.3171/2014.5.PEDS13602.
Address correspondence to: Brandon A. Miller, M.D., Ph.D.,
Department of Neurosurgery, Emory University, 1365 Clifton Rd.
NE, Bldg. B, Ste. 2200, Atlanta, GA 30322. email: brandon.miller@
emory.edu.
189