Received: 5 May 2023 | Revised: 10 September 2023 | Accepted: 12 October 2023

DOI: 10.1111/apa.17015

ORIGINAL ARTICLE

The head circumference to chest circumference ratio provided

an easy way to detect foetal growth restriction in term infants

Hiroki Saito1,2 | Yayoi Murano1,2 | Suga Ashikawa3 | Daisuke Yoneoka4 |

Hiromichi Shoji1 | Tomoyuki Nakazawa1,2 | Ken Sakamaki3 | Toshiaki Shimizu1

1
Department of Pediatrics, Juntendo
University Faculty of Medicine, Bunkyo- Abstract
ku, Tokyo, Japan
Aim: The head circumference to chest circumference (HC/CC) ratio has been used to
2
Division of Pediatrics, Tokyo
Metropolitan Toshima Hospital, Itabashi-
identify low birth weight infants in developed countries. This study was conducted to
ku, Tokyo, Japan examine whether the ratio could distinguish asymmetrical foetal growth restriction
3
Division of Obstetrics and Gynecology, (FGR).
Tokyo Metropolitan Toshima Hospital,
Itabashi-ku, Tokyo, Japan Methods: This retrospective observational study was conducted with 1955 infants
4
Infectious Disease Surveillance Center, (50.5% male) born at term between 2016 and 2020 at Tokyo Metropolitan Toshima
National Institute of Infectious Diseases,
Hospital, Japan.
Shinjuku-ku, Tokyo, Japan
Results: We found that 120 (6.1%) had FGR. Their mean birth weight was
Correspondence
3052.1 ± 367.3 g, and their mean gestational age was 39.1 ± 1.1 weeks. Logistic regres-
Hiromichi Shoji, Department of Pediatrics,
Juntendo University Faculty of Medicine, sion analysis showed that the association between the HC/CC ratio and FGR had
2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421,
a regression coefficient of −20.6 (p < 0.000). The linear regression analysis showed
Japan.
Email: hshoji@juntendo.ac.jp that the association between the HC/CC ratio and the birth weight z-score had a
regression coefficient of −8.59 (p < 0.000). The coefficient of correlation was −0.33
(p < 0.001). The receiver operating characteristic curve for detecting FGR showed
that the area under the curve was 0.75 and the cut-off value was 0.93, with sensitivity
of 75.8% and specificity of 60.8%.
Conclusion: Our study established the associations between HC/CC ratio and FGR
and birth weight z-scores and confirmed that the ratio provided an easy way to detect
FGR in term-born infants.

KEYWORDS
asymmetrical foetal growth restriction, chest circumference, foetal growth restriction, head
circumference, term infants

1 | BAC KG RO U N D
Measuring the head circumference to chest circumference (HC/CC)
ratio is a way of determining a low birth weight (LBW) of below
2500 g. It is primarily used in developing countries, where equipment
to determine gestational age and birth weight is not always avail-
able.1–3 We previously reported that it is also a useful way to detect
foetal growth restriction (FGR) in preterm infants.4 Infants with FGR
have various complications, 5 and detecting FGR is important in both
developing and developed countries.

Abbreviations: CC, chest circumference; CI, confidence interval; FGR, foetal growth restriction; HC, head circumference; LBW, low birth weight; ROC, receiver operating characteristic;
SD, standard deviation.

© 2023 Foundation Acta Paediatrica. Published by John Wiley & Sons Ltd

Acta Paediatrica. 2024;113:67–71.  wileyonlinelibrary.com/journal/apa | 67

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68
FGR can be divided into two categories: asymmetrical FGR,
which is the most prevalent, and symmetrical FGR, which results
from genetic disorders or infectious diseases. 6 Infants with sym-
metrical FGR can be distinguished from other infants based on
clinical findings. In contrast, infants with asymmetrical FGR have
normal clinical features, excluding small body measurements,
even though it is found in most infants with FGR. The aetiology of
asymmetrical FGR involves normal growth until the third trimes-
ter, but then the growth of the body is suppressed, while the head
remains unaffected. This is due to placental insufficiency. As a 6
result, infants have a larger HC compared to their body, which can
be measured as the CC. Based on this aetiology, we hypothesised
that the HC/CC ratio would be relatively higher in infants with,
than without, FGR.
In clinical practice, FGR is defined based on gestational age,
sex and birth weight. However, the aim of this study was to assess
whether the HC/CC ratio could also be used to detect FGR.
2 | M E TH O D S
This was a retrospective, observational study. The participants com-
prised term infants born between 1 January 2016 and 31 December
2020 at Tokyo Metropolitan Toshima Hospital, Japan. We focused
on healthy singleton babies born at 37–41 weeks of age, without
congenital diseases and genetic disorders and with sufficient data to
investigate the aims of the study.
Data regarding birth weight, length, HC, CC, sex, parity, ges-
tational age and clinical diagnoses of congenital diseases were
extracted from their medical records. Infants born with a birth
weight under the 10th percentile were defined as having FGR. 5
z-Scores of birth weight and length were calculated using the fit-
ting smoothed centile curves to preference data method.7 Some
literature has defined FGR as a birth weight of less than −2 stan-
dard deviations (SD), and we also used this criteria to assess our
cohort. The characteristics of the participants were compared
using the t-test for continuous variables and the chi-squared test
for categorical variables.
Logistic regression analysis was used to assess the associa-
tion between the presence of FGR and the HC/CC ratio. Linear
regression analysis was used to analyse the association between
the birth weight z-scores and the HC/CC ratio. Spearman's cor-
relation was calculated to examine the correlation between the
birth weight z-score and the HC/CC ratio. Finally, the receiver op-
erating characteristic (ROC) curve was estimated to evaluate the
association between the presence of FGR and the HC/CC ratio.
The cut-off value of the HC/CC ratio for detecting FGR was also
calculated.
The statistical analyses were performed using Stata version 15.1
(Stata Corp), and statistical significance was set at p < 0.05.
The study procedures were in accordance with the ethical
standards of the ethical committee of Toshima Hospital on human
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SAITO et al.
Key notes
• This study explored whether the head circumference to
chest circumference (HC/CC) ratio would detect foetal
growth restriction (FGR) in term infants.
• Our cohort comprised 120 term infants, with a mean
birth weight of 3052.1 ± 367.3 g and a mean gestational
age of 39.1 ± 1.1 weeks.
• The associations between the HC/CC ratio and FGR and
birth weight z-scores confirmed that the ratio provided
an easy way to detect FGR in term infants.
experimentation and with the Declaration of Helsinki. Informed con-
sent was not required, as all the data were extracted without individ-
ual information. The study was approved by the ethics committee of
Toshima Hospital (number Rin4-31).
3 | R E S U LT S
There were 2948 infants born at the Tokyo Metropolitan Toshima
Hospital between 2016 and 2020. We excluded 108 infants born
after 42 weeks or before 37 weeks of gestational age, together with
three pairs of twins, two infants with trisomy 21 and one infant with
congenital heart disease. Another 876 participants were excluded
due to a lack of data. The final sample comprised 1955 (50.5% male)
participants and 120 had FGR (6.1%).
The characteristics of the participants are listed in Table 1. The
mean birth weight of the sample was 3052.1 ± 367.3 g, and the mean
gestational age was 39.1 ± 1.1 weeks. More than half (58.1%) were
born to first-time mothers.
The characteristics of the 120 infants with FGR and the 1835
without FGR are compared in Table 2. The mean birth weight was
significantly lower in the FGR group than the group without FGR
(2425.9 ± 212.8 g vs. 3093.1 ± 336.8 g), but no significant differ-
ences were observed regarding gestational age, parity and sex.
The mean birth weights and standard deviations were significantly
different in those with and without FGR (1.8 ± 0.4 vs. 0.3 ± 0.9,
respectively).
The results of the logistic regression analysis to assess any associ-
ation between the presence of FGR and the HC/CC ratio had a coef-
ficient of −20.6, with a 95% confidence interval (CI) of −16.5 to −24.8
(p < 0.001). When FGR was defined as a birth weight under −2SD,
the logistic regression analysis showed that the coefficient was −21.7
(95% CI −28.7 to 14.8, p < 0.001). The linear regression analysis to
assess the association between the birth weight z-score and the HC/
CC ratio had a coefficient of −8.59 (95% CI −7.56 to −9.62, p < 0.001).
The results of the Pearson correlation analysis are shown in Figure 1.
The coefficient of correlation was −0.33 (p < 0.001).
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SAITO et al. 69

The ROC curve that was used to detect the FGR and the HC/CC
ratio is shown in Figure 2. The area under the curve was 0.75 and the
cut-off value was 0.93. The sensitivity and specificity of the cut-off
value for detecting FGR were 75.8% and 60.8%, respectively.
TA B L E 1 Characteristics of the study participants.
Mean ± SD
Birth weight (g) 3052.1 ± 367.3
4 | DISCUSSION
Our results demonstrated a significant association between the HC/
CC ratio and FGR in term infants. The cut-off ratio for detecting FGR
was 0.93. Birth anthropometry is easy to measure and a useful pre-
dictor of neonatal outcome,8 but it is often overlooked. A previous
study investigated whether CC was a predictor of birth anthropo-
metric outcomes in term infants3 and our study similarly assessed

Gestational age (weeks) 39.1 ± 1.1 the role of CC in term infants.

FGR can be classified into asymmetrical and symmetrical types.6
Parity = 0 (%) 1646 (58.1)
As symmetrical FGR often complicates congenital disease,6 infants
Sex (male/female) 987/968
with this condition were excluded from our analysis. Our study re-
FGR
sults can therefore be applied in clinical practice to distinguish FGR
<10th Percentile (%) 120 (6.1%)
with normal clinical features and without congenital diseases.
<−2SD (%) 29 (1.5%)
The HC/CC ratio is a useful tool for detecting LBW in developing
Birth weight z-score 0.1 ± 1.0 countries, where the main perinatal problems are a lack of equip-
Abbreviations: FGR, foetal growth restriction; SD, standard deviation. ment to determine birth weight and precise gestational age.9,10
While these parameters are routinely measured in developing coun-
TA B L E 2 Comparison between the characteristics of infants tries, FGR is an increasing concern in developed countries6 for sev-
without and with FGR. eral reasons. These include increasing maternal age, reproductive
With FGR (n = 120) therapies and maternal smoking. Our study results can contribute
Without FGR (birth weight < 10th to the easy detection of FGR immediately after birth, using the HC/
(n = 1835) percentile) p-Value CC ratio, and identify vulnerable infants in both developed and de-
Birth weight (g) 3093.1 ± 336.8 2425.9 ± 212.8 <0.001 veloping countries.
Gestational age 39.5 ± 1.1 39.6 ± 1.1 0.33 CC is not a common measurement in some countries.1,11 It is
(weeks) routinely measured in Japan, but the data that are produced are
Parity = 0 (%) 1543 (84.1) 103 (85.8) 0.61 not used effectively. Abdominal circumference, which is a similar
Sex (male/female) 922/913 65/55 0.41 measure to CC, is one of the measurements used to detect FGR
Birth weight z-score 0.3 ± 0.9 −1.8 ± 0.4 <0.001 during pregnancy.12 This study now adds the usefulness of CC in
clinical practice to that list. We previously reported that the HC/
Note: Data are shown as mean and standard deviations. Birth weight,
gestational age and birth weight z-score measured with the t-test. CC ratio was a useful predictor of FGR in preterm infants.4 Our
Parity and sex measured with the chi-squared test. current study of full-term infants found that the area under the
Abbreviation: FGR, foetal growth restriction. ROC curve was smaller and the sensitivity was lower than the

F I G U R E 1 Association between
the birth weight z-score and head
circumference to chest circumference
(HC/CC) ratio analysed with Pearson
correlation analysis. The coefficient of
correlation was −0.33 (p < 0.001).
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70
levels that we previously reported for detecting FGR in preterm
infants using the HC/CC ratio. We assume that this lower level
reflected the fact that the infants with the most severe FGR were
not carried to term.
There was a lower proportion of FGR in our study than previ-
5
ously reported. This was because Japan provides more frequent
check-ups during pregnancy compared to other countries and in-
fants with arrested growth are delivered before term.
This study had several limitations. First, we excluded infants
with congenital diseases due to their potential to be affected by
symmetrical FGR, but there was only one infant, who had congeni-
tal heart disease, born during the study period. However, other dis-
eases, such as metabolic diseases, could not be identified from the
medical records. Second, we could not assess a number of maternal
factors, including nutritional status, smoking status, anthropomet-
ric measurements and complications during pregnancy. Third, we
were unable to analyse the pathology of FGR. Further research is
required on the associations between the HC/CC ratio and long-
term outcomes. 5,13
5 | CO N C LU S I O N
This study established the associations between HC/CC ratio and
FGR and birth weight z-scores and confirmed that the ratio provided
an easy way to detect FGR in term-born infants.
AU T H O R C O N T R I B U T I O N S
Hiroki Saito: Formal analysis; investigation; project administration;
resources; writing – original draft. Yayoi Murano: Conceptualization;
formal analysis; methodology; resources; writing – original draft. Suga
Ashikawa: Data curation; resources; validation; writing – ­review and
editing. Daisuke Yoneoka: Formal analysis; investigation; software;
16512227, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/apa.17015 by Ethiopia Hinari access, Wiley Online Library on [08/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SAITO et al.
F I G U R E 2 Receiver operatic
characteristic curve for the detection
of foetal growth restriction. The X-axis
represented 1 − specificity for detecting
intrauterine growth restriction, and the
Y-axis represented the sensitivity. The
area under the curve was 0.75 and the
cut-off value was 0.93, with a sensitivity
and specificity of 75.8% and 60.8%,
respectively.
validation; visualization; writing – review and editing. Hiromichi Shoji:
Conceptualization; supervision; validation; writing – review and edit-
ing. Tomoyuki Nakazawa: Resources; writing – review and editing.
Ken Sakamaki: Resources; supervision; validation; writing – review
and editing. Toshiaki Shimizu: Project administration; supervision;
writing – review and editing.
C O N FL I C T O F I N T E R E S T S TAT E M E N T
The authors have no conflicts of interest to declare.
ORCID
Yayoi Murano https://orcid.org/0000-0003-4097-5104
Hiromichi Shoji https://orcid.org/0000-0003-2532-8910
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