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 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
Measuring the head circumference to chest circumference (HC/CC) foetal growth restriction (FGR) in preterm infants.4 Infants with FGR
ratio is a way of determining a low birth weight (LBW) of below have various complications, 5 and detecting FGR is important in both
2500 g. It is primarily used in developing countries, where equipment 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 SAITO et al.

FGR can be divided into two categories: asymmetrical FGR,

which is the most prevalent, and symmetrical FGR, which results
Key notes
from genetic disorders or infectious diseases. 6 Infants with sym-
metrical FGR can be distinguished from other infants based on • This study explored whether the head circumference to
clinical findings. In contrast, infants with asymmetrical FGR have chest circumference (HC/CC) ratio would detect foetal
normal clinical features, excluding small body measurements, growth restriction (FGR) in term infants.
even though it is found in most infants with FGR. The aetiology of • Our cohort comprised 120 term infants, with a mean
asymmetrical FGR involves normal growth until the third trimes- birth weight of 3052.1 ± 367.3 g and a mean gestational
ter, but then the growth of the body is suppressed, while the head age of 39.1 ± 1.1 weeks.
remains unaffected. This is due to placental insufficiency. As a 6 • The associations between the HC/CC ratio and FGR and
result, infants have a larger HC compared to their body, which can birth weight z-scores confirmed that the ratio provided
be measured as the CC. Based on this aetiology, we hypothesised an easy way to detect FGR in term infants.
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 experimentation and with the Declaration of Helsinki. Informed con-
whether the HC/CC ratio could also be used to detect FGR. 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).
2 | M E TH O D S

This was a retrospective, observational study. The participants com- 3 | R E S U LT S

prised term infants born between 1 January 2016 and 31 December
2020 at Tokyo Metropolitan Toshima Hospital, Japan. We focused There were 2948 infants born at the Tokyo Metropolitan Toshima
on healthy singleton babies born at 37–41 weeks of age, without Hospital between 2016 and 2020. We excluded 108 infants born
congenital diseases and genetic disorders and with sufficient data to after 42 weeks or before 37 weeks of gestational age, together with
investigate the aims of the study. three pairs of twins, two infants with trisomy 21 and one infant with
Data regarding birth weight, length, HC, CC, sex, parity, ges- congenital heart disease. Another 876 participants were excluded
tational age and clinical diagnoses of congenital diseases were due to a lack of data. The final sample comprised 1955 (50.5% male)
extracted from their medical records. Infants born with a birth participants and 120 had FGR (6.1%).
weight under the 10th percentile were defined as having FGR. 5 The characteristics of the participants are listed in Table 1. The
z-Scores of birth weight and length were calculated using the fit- mean birth weight of the sample was 3052.1 ± 367.3 g, and the mean
ting smoothed centile curves to preference data method.7 Some gestational age was 39.1 ± 1.1 weeks. More than half (58.1%) were
literature has defined FGR as a birth weight of less than −2 stan- born to first-time mothers.
dard deviations (SD), and we also used this criteria to assess our The characteristics of the 120 infants with FGR and the 1835
cohort. The characteristics of the participants were compared without FGR are compared in Table 2. The mean birth weight was
using the t-test for continuous variables and the chi-squared test significantly lower in the FGR group than the group without FGR
for categorical variables. (2425.9 ± 212.8 g vs. 3093.1 ± 336.8 g), but no significant differ-
Logistic regression analysis was used to assess the associa- ences were observed regarding gestational age, parity and sex.
tion between the presence of FGR and the HC/CC ratio. Linear The mean birth weights and standard deviations were significantly
regression analysis was used to analyse the association between different in those with and without FGR (1.8 ± 0.4 vs. 0.3 ± 0.9,
the birth weight z-scores and the HC/CC ratio. Spearman's cor- respectively).
relation was calculated to examine the correlation between the The results of the logistic regression analysis to assess any associ-
birth weight z-score and the HC/CC ratio. Finally, the receiver op- ation between the presence of FGR and the HC/CC ratio had a coef-
erating characteristic (ROC) curve was estimated to evaluate the ficient of −20.6, with a 95% confidence interval (CI) of −16.5 to −24.8
association between the presence of FGR and the HC/CC ratio. (p < 0.001). When FGR was defined as a birth weight under −2SD,
The cut-off value of the HC/CC ratio for detecting FGR was also the logistic regression analysis showed that the coefficient was −21.7
calculated. (95% CI −28.7 to 14.8, p < 0.001). The linear regression analysis to
The statistical analyses were performed using Stata version 15.1 assess the association between the birth weight z-score and the HC/
(Stata Corp), and statistical significance was set at p < 0.05. CC ratio had a coefficient of −8.59 (95% CI −7.56 to −9.62, p < 0.001).
The study procedures were in accordance with the ethical The results of the Pearson correlation analysis are shown in Figure 1.
standards of the ethical committee of Toshima Hospital on human 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 4 | DISCUSSION
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 Our results demonstrated a significant association between the HC/
value for detecting FGR were 75.8% and 60.8%, respectively. 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-
TA B L E 1 Characteristics of the study participants.
dictor of neonatal outcome,8 but it is often overlooked. A previous
Mean ± SD study investigated whether CC was a predictor of birth anthropo-
Birth weight (g) 3052.1 ± 367.3 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 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.

levels that we previously reported for detecting FGR in preterm validation; visualization; writing – review and editing. Hiromichi Shoji:
infants using the HC/CC ratio. We assume that this lower level Conceptualization; supervision; validation; writing – review and edit-
reflected the fact that the infants with the most severe FGR were ing. Tomoyuki Nakazawa: Resources; writing – review and editing.
not carried to term. Ken Sakamaki: Resources; supervision; validation; writing – review
There was a lower proportion of FGR in our study than previ- and editing. Toshiaki Shimizu: Project administration; supervision;
5
ously reported. This was because Japan provides more frequent writing – review and editing.
check-ups during pregnancy compared to other countries and in-
fants with arrested growth are delivered before term. C O N FL I C T O F I N T E R E S T S TAT E M E N T
This study had several limitations. First, we excluded infants The authors have no conflicts of interest to declare.
with congenital diseases due to their potential to be affected by
symmetrical FGR, but there was only one infant, who had congeni- ORCID
tal heart disease, born during the study period. However, other dis- Yayoi Murano https://orcid.org/0000-0003-4097-5104
eases, such as metabolic diseases, could not be identified from the Hiromichi Shoji https://orcid.org/0000-0003-2532-8910
medical records. Second, we could not assess a number of maternal
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