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\begin{document}

\title{Comparison of fetal growth assessment by conventional method and by
using Intergrowth 21 st chart for detection of small for gestational age
foetuses: A prospective observational study among Indian population}



\author[1]{Millo Suka}%
\author[1]{Manju Puri}%
\author[1]{Anuradha Singh}%
\affil[1]{Lady Hardinge Medical College}%


\vspace{-1em}



  
  \date{May 26, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
\textbf{Objectives}: Primary objective was to compare screening accuracy
of fetal growth assessment by conventional fundal height assessment by
palpation with plotting of symphysio-fundal height (SFH) measurement on
21 \textsuperscript{st} Intergrowth charts for detecting small for
gestational age (SGA) foetuses. Secondary objective was to find an
agreement between these two methods. \textbf{Design}: Prospective
observational analytic study \textbf{Setting}: Lady Hardinge Medical
College and associated hospitals, Delhi, India \textbf{Population}: Five
hundred low risk pregnant women with singleton pregnancy, with reliable
dates at \textbf{[?]}28 weeks from Antenatal Clinic of Lady Hardinge
Medical College and associated hospitals from November 2019 to October
2021. \textbf{Outcome measures}: Assessment of fundal height in weeks by
palpation and a lag of \textbf{[?]}3 weeks, suggested SGA fetus. SFH
measured in centimetres and plotted on Intergrowth 21
\textsuperscript{st} foetal growth charts. SFH of less than 10
\textsuperscript{th} centile suggested SGA. Birthweight of new-born was
plotted on Intergrowth 21 \textsuperscript{st} Estimated Foetal Weight
Chart. Birthweight of less than 10 \textsuperscript{th} centile was
classified as SGA. \textbf{Results}: Thirteen percent women delivered
new-borns with birthweight below 10 \textsuperscript{th} centile. Fundal
height palpation had 98.6 \% specificity and 69.9\% sensitivity compared
to 99.5\% specificity and 83.3\% sensitivity by SFH measurement for
detecting SGA neonates. \textbf{Conclusions}: SFH measurement plotted on
Intergrowth 21 \textsuperscript{st} chart is more sensitive and specific
for detecting SGA neonates compared to conventional fundal height
palpation. Agreement between the methods measured by Cohen's Kappa
Statistic was 0.804, indicating substantial agreement between the
methods. SFH measurement is a more accurate and practical tool, for use
in low resource settings.%
\end{abstract}%



\sloppy


\textbf{INTRODUCTION}

Low birthweight is one of the three important causes accounting for 78\%
of all neonatal deaths in India, neonatal infections and birth asphyxia
being the other two\textsuperscript{1}. Low birthweight can be
consequent to pre-term birth, fetal growth restriction or a
constitutionally small baby. Assessment of fetal growth for early
diagnosis and timely intervention can reduce the adverse perinatal
outcomes associated with growth restricted fetuses.

There are various methods for detection of small for gestational age
(SGA) fetuses. Conventionally, it is done by clinical palpation of
fundal height. The assessment is based on the relative position of the
level of fundal height from an imaginary line passing through the upper
border of the umbilicus dividing the abdomen into two parts. Serial
ultrasound scans in the third trimester is another tool for early
diagnosis of foetal growth disorders\textsuperscript{2}. However, it is
not a cost-effective screening tool in low resource settings.

Serial measurement of symphysio-fundal height plotted on customized
charts is considered a reliable objective tool for monitoring growth of
a fetus\textsuperscript{3}. The International Symphysis Fundal Height
Standards Chart by Intergrowth 21\textsuperscript{st} Project study
created international standards to measure symphysis fundal height as
first level screening tool for foetal growth
disturbance\textsuperscript{4}. It also provides a graphical record of
the changes in fundal height with the advancement of gestational age and
is likely to minimize the subjective variation with the conventional
method.

Small for gestational age being an important predictor of poor perinatal
outcome, warrants studies to find a simple tool for low resource
settings which is cost effective and accurate in early detection of
growth restriction.

Hence, the current study was designed to compare the screening accuracy
of clinical assessment of fundal height by palpation with symphysio
fundal height measurement charted on Intergrowth 21 Project standard
charts for early detection of small for gestational age fetuses.

\textbf{MATERIALS AND METHODS} :

\textbf{Study design and selection criteria:} This prospective
observational analytic study was conducted in the antenatal clinic and
antenatal wards of Department of Obstetrics and Gynaecology, Shrimati
Sucheta Kriplani Hospital and Lady Hardinge Medical College, Delhi,
India from November 2019 to October 2021.

The study population comprised of 500 pregnant women with singleton
pregnancy, with good dating based on regular menstrual cycles and
confirmed date of last menstrual period based on foetal crown rump
length on ultrasound between 9 to 13 weeks gestation. They were
recruited at or beyond 28 weeks of gestation.

Pregnant women with any factor affecting fundal height assessment such
as multiple pregnancies, hydramnios, fibroid uterus, uterine
malformation, abdominal mass, women with diabetes mellitus or
malpresentation were excluded.

\textbf{Materials:} The test tools included:

\textbf{1. International Symphysis Fundal Height Standards C/hart:} The
international standard for symphysio fundal height measurement based on
serial measurement by prospective longitudinal study from Foetal Growth
Longitudinal Study of Intergrowth project\textsuperscript{4}.

\textbf{2. International Foetal Growth Standards Estimated Foetal Weight
Chart:} The international foetal growth standards estimated foetal
weight chart based on serial ultrasound assessment of foetal
anthropometric measurements in pregnant women involved in Foetal Growth
Longitudinal Study of 21\textsuperscript{st} Intergrowth
project\textsuperscript{4}.

\textbf{Methodology} : Ethical clearance was taken from the
Institutional Ethical Committee. All women fulfilling selection criteria
were recruited from antenatal clinic and antenatal wards of Lady
Hardinge Medical College and Smt. Sucheta Kriplani Hospital in third
trimester and serially followed up. Informed consent was obtained from
all subjects.

Fundal height (FH) was assessed by the conventional method of palpation
by the primary investigator and recorded. For symphysio-fundal height
(SFH) measurement, a metric tape of non-elastic material was used. With
patient lying supine after voiding the bladder, the upper border of the
symphysis pubis was marked, and the 0 cm marking of the metric tape was
secured at this point. The tape was then passed in a straight line from
the symphysis pubis over to the fundus of the uterus till a resistance
was felt on the abdominal wall. The tape was sustained at this point on
the fundus of uterus and the measurement was recorded in centimetres as
described in Intergrowth 21\textsuperscript{st} study.

Serial SFH measurements were taken during each follow up antenatal
visit, and findings were plotted against gestational age in
International Symphysis Fundal Height Graph. Any woman with suspected
small for gestational age foetus was admitted and managed as per
hospital protocol.

Small for gestational age was suspected if,

There was a difference of more than 3 weeks in gestational age
assessment by clinical palpation as compared to the calculated period of
gestation.

The measured symphysio-fundal height was less than 10th percentile of
the standard symphysio-fundal height for that gestational age.

All women were serially followed up with conventional assessment and SFH
measurement on each visit till delivery. The birthweight of new-borns
was documented and charted on International Foetal Growth Standards
Chart from Intergrowth 21\textsuperscript{st} Project. New-born weight
less than 10\textsuperscript{th} centile was considered as small for
gestational age (SGA).

\textbf{Sample size estimation:} Taking expected proportion of small for
gestational age detected by conventional method to be 10\%, and
proportion of small for gestational age detected by SFH measurement to
be 15\% and a confidence interval of 95\%, sample size was calculated
using formula applied for comparison of two proportions

n = (Z\selectlanguage{greek}α/\selectlanguage{english}2 + Z\selectlanguage{greek}β\selectlanguage{english})\textsuperscript{2} *
(p\textsubscript{1}(1-p\textsubscript{1}) + p\textsubscript{2}
(1-p\textsubscript{2}))/
(p\textsubscript{1}-p\textsubscript{2})\textsuperscript{2}

Sample size calculated was 683. For convenience, sample size of 500 was
taken.

\textbf{Statistical analysis} : Data entry was done using Microsoft
Excel sheet and analysed. Diagnostic accuracy of conventional FH method
and SFH measurement was compared by computing sensitivity, specificity,
positive predictive value, negative predictive value of the two tests.
The 95\% confidence interval was calculated wherever applicable.
Agreement between the two tests was calculated using kappa statistic
(\selectlanguage{greek}κ\selectlanguage{english}).

\textbf{RESULTS:}

\textbf{Maternal Characteristics} : The age of the women enrolled in the
study ranged from 18 years to 42 years, with mean age of 25.5 years \selectlanguage{ngerman}±3.7
years. Majority (81.4\%) of women were below 30 years of age, and 0.6\%
were \textgreater{}35years. The average height of the subjects was
154.2±3.7 cm, with a minimum of 142 cm and a maximum of 166cm. Only
0.6\% subjects were shorter than 145 cm.

Among the study subjects, 65.2\% were multigravidae and, 34.8\% were
primigravida. There was an equal distribution of nulliparous (49.6\%)
and multiparous women (50.4\%). Majority (71.4\%) of the women had no
prior history of abortions, 28.6\% had at least one abortion of these
1.8\% had history of 3 or more abortions.

According to Asian BMI cut off, 64.8\% of women had a normal BMI, 28.6\%
were overweight, 6\% were pre-obese and 0.6\% were underweight. The
average BMI was 22.4± 1.53 kg/m\textsuperscript{2} (ranging from 17.7
kg/m\textsuperscript{2} to 29.2 kg/m\textsuperscript{2}). As per Indian
Council of Medical Research (ICMR) classification of anaemia in
pregnancy, 52.2\% of women were anaemic, of which 41.8\% had mild
anaemia and 10.4\% had moderate anaemia. Majority 89.60\% (448 out of
500) had a normal vaginal delivery. 10.4\% (52 out of 500) women had
caesarean birth.

\textbf{Fetal Outcome} : Of the 500 new-borns, 66 (13.2\%) were small
for gestational age as defined by birthweight less than
10\textsuperscript{th} centile on the International Foetal Growth
Standards Estimated Foetal Weight Chart and 434 (86.8\%) were
appropriate for gestational age (AGA).

The mean birthweight of the new-borns was 2.78±0.30 kg, ranging from
1.72 kg to 4.0 kg. Of the women clinically suspected to have small for
gestational age foetus, 78.8\% (52 out of 66) had a birthweight less
than 2.5 kg, while 2.8\% (12 out of 434) women assessed to have normal
foetal growth antenatally gave birth to a small for gestational age
neonate (less than 2.5 kg). Of the SGA neonates 9.1\% (6 out of 66) were
born preterm, compared to 5.3\% (23 out of 434) of AGA neonates.

In the study population, 57.6\% of small for gestational age new-borns
were females, compared to 42.4\% males. Perinatal complications were
seen in 15.2\% of small for gestational age neonates compared to 3.7\%
of AGA neonates (Fig. 1). A higher proportion of SGA new-borns (12.1\%)
required NICU admission as compared to 1.2\% AGA neonates. The
difference was statistically significant (p=0.001).

Of the total study population, 66/500 (13.3\%) delivered new-borns with
birthweight below 10\textsuperscript{th} centile for the gestational age
using International Foetal Growth Standards Estimated Foetal

Weight Charts.

On clinical examination, 52 (10.4\%) women were suspected to have a
small for gestational age fetus by fundal height palpation compared to
57 (11.4\%) women by SFH measurement as charted on International
Symphysis Fundal Height Standards.

Of the 57 women suspected with small for gestational age fetuses based
on SFH measurement charted on standard charts, SGA was correctly
detected in 96.5\% (55/57) as compared to 88.5\% (46/52) among the 52
women suspected to have SGA by conventional FH palpation. SGA was
over-diagnosed in 3.5\% (2/57) by SFH measurement in comparison to
11.5\% (6/52) by the conventional method of fundal height palpation. In
women in whom normal growth was assessed by SFH measurement on standard
charts, 97.5\% (432/443) delivered AGA new-borns compared to 95.5\%
(428/448) with fundal height palpation method. SGA was missed in only
2.4\% (11/443) of women by SFH measurement as compared to 4.5\% (20/448)
by fundal height palpation.

Significance measured by Chi-Square test gives a p-value of
\textless{}0.001, indicating test results to be significant.

\textbf{DISCUSSION:}

The number of infants born small for gestation is higher in low and
middle-income countries, with prevalence being highest in South
Asia\textsuperscript{5}. Such fetus are at higher risk of neonatal
morbidity, stillbirth, and neonatal mortality compared to appropriate
for gestational age fetus\textsuperscript{6}. Antenatal identification
of SGA fetus with structured surveillance of those identified, lowers
the risk of adverse fetal outcomes\textsuperscript{7}.

The outcome of the pregnancies, as measured by birthweight of new-born
charted on International Foetal Growth Standards Chart from Intergrowth
21\textsuperscript{st} Project showed that out of 500 pregnancies,
13.2\% (66/500) resulted in new-borns with birthweight below
10\textsuperscript{th} centile for the period of gestation.

The conventional method of FH palpation detected SGA foetus in 52/500
women (10.4\%), of which, 46/52 pregnancies (69.6\%) resulted in
new-borns with birthweight below 10\textsuperscript{th} centile (True
Positive), and 6/52 (11.5\%) were over diagnosed. SGA new-born was
correctly ruled out in 95.5\% (428/448) pregnancies, while 4.5\%
(20/448) were missed (Fig.2).

SFH measurement charted on Intergrowth 21\textsuperscript{st} Project
charts detected SGA foetus in 57/500 women (11.4\%). Among these, 55/57
pregnancies (83.3\%) had new-borns with birthweight below
10\textsuperscript{th} centile (True Positive) and 2/57 pregnancies
(3.5\%) were over-diagnosed (False Positive). The method correctly ruled
out small for gestational age neonate in 97.5\% (432/443) pregnancies
(True Negative) and missed 2.4\% (11/443) cases (False Negative)
(Fig.2).

A total of 21 cases of SGA new-borns were missed during the study, of
which 10 cases were missed solely on conventional FH palpation, 10 cases
were missed by both the methods and one by only SFH measurement.
Overall, FH palpation missed 20 cases of small for gestational age
new-born while SFH measurement missed 11 cases.

Of the 10 cases missed by both methods, all had healthy babies. Seven
cases (7/10) had a neonatal birthweight of 2.5 kg or above, which is
above the accepted cut off 2.5 kg for Indian standards. Remaining 3/10
cases with a birthweight below 2.5 kg (LBW) were babies born to mothers
with a short height (two were 150 cm, and one 149 cm compared to mean
height of 154.2 cm in the study population). All these three new-borns
were healthy, possibly constitutionally small and were shifted to
mothers' side.

Of the 10 cases missed only on fundal height palpation, 5/10 cases had
birthweight \selectlanguage{english}[?]2.5kg, which, though below 10\textsuperscript{th} centile
for the gestational age on Intergrowth 21\textsuperscript{st} growth
chart, is more than the accepted cut off for Indian population. All
these babies were born healthy. Remaining 5 cases had birthweight below
2.5 kg, 4 out of 5 were in mothers who had short maternal height (146
cm, 146 cm, 148 cm and 150 cm compared to a mean height of 154.2 cm in
study population). All these babies were born with normal APGAR score
and shifted to mothers' side after birth and were possibly
constitutionally small. One of the missed cases was a pre-term birth and
required neonatal ICU admission.

One case of SGA new-born missed solely on SFH measurement, had a
birthweight of 2.5 kg, acceptable as normal in Indian context.

Clinically, FH palpation over-diagnosed SGA foetus in 6 cases, all of
which had a birthweight above 2.5 kg. Four cases were over-diagnosed
possibly due to engagement of foetal head in the last trimester with
resultant decrease in estimated fundal height. One case was
over-diagnosed in a woman with a tall height (165 cm) as compared to the
average height of study population (154.2 cm). This could be due to
increased length of maternal torso, leading to under-estimation of
fundal height. One case had a birthweight falling just above
10\textsuperscript{th} centile for the gestational age (2.5 Kg at 37+5
weeks gestation) and could be due to subjective variation in assessment.

SFH measurement missed detection in 11 cases, of which 10 cases were
also missed by the method of palpation.

Two cases were over-diagnosed on SFH measurement, one had a birthweight
of 2.6 kg, and other case had a birthweight falling exactly on
10\textsuperscript{th} centile, and therefore was not included in small
for gestational age as per the cut off value of below
10\textsuperscript{th} centile as per definition.

Symphysis fundal height measurement used as a measure for detection of
SGA new-born had a positive predictive value of 96.49\% and a negative
predictive value of 97.52\%, a positive likelihood ratio of 180.3, a
negative likelihood ratio of 0.17 and an accuracy of 97.4\% (Table 1)

Fundal height palpation for detection of SGA new-born had a positive
predictive value of 88.46\% and a negative predictive value of 95.54\%,
a positive likelihood ratio of 50.4 and a negative likelihood ratio of
0.31. The method had an accuracy of 94.8\%. The agreement between the
two methods for detecting SGA new-born as measured by Cohen's Kappa
Statistic showed a Kappa value = 0.804, indicating a substantial
agreement between the two methods for detection of SGA new-born.

In low-income countries, growth restriction has been found to be
significantly associated with admission in special baby care
unit\textsuperscript{8}. Similar observations were made in the study
with a higher proportion (12.1\%) of total SGA neonates requiring
Neonatal ICU admission compared to 1.2\% of AGA neonates
(p\textless{}0.001). Pre-term delivery was higher among SGA newborn
(9.1\%) than in AGA newborns (5.3\%), and more perinatal complications
were seen in SGA newborns (15.2\%) compared to AGA newborns (3.7\%).

The percentage of fetus born small for gestation (13.2\%) was comparable
to the prevalence of SGA studied in Indian tertiary care hospital
(13.6\%)\textsuperscript{9}.

\textbf{Strengths and Limitations:} The strength of the study lies in
the application of customised growth charts developed from international
standards involving geographically diverse regions including Indian
population. The dating of pregnancy was good in the study population.

The main limitation of this study was a lack of ultrasound biometry and
doppler correlation to compare the fulfilment of Delphi criteria for
foetal growth restriction among those detected to be \textless{}
10\textsuperscript{th} centile but
\textgreater{}3\textsuperscript{rd}centile on estimated foetal growth
charts by 21\textsuperscript{st}Intergrowth.

Also, the International foetal growth standards estimated foetal weight
charts by Intergrowth 21\textsuperscript{st} Project used as an outcome
measure, have higher birthweight cut offs for the
10\textsuperscript{th}centile compared to that for Indian population,
which could potentially lead to over-diagnosis of foetal growth
restriction.

The measurements and palpation involved in the study are subject to
variation according to the built of the mother, and other possible
anatomical variations. Also, the frequency of measurement, interval
between measurements, and experience of the performer can further affect
the study outcome.

\textbf{CONCLUSION:}

Symphysis fundal height measurement plotted on
21\textsuperscript{st}Intergrowth chart was found to be more sensitive
and specific in detecting SGA new-borns compared to conventional fundal
height palpation. The use of SFH measurement charts led to correct
detection of additional cases, which were otherwise missed by palpation
and timely initiation of management of the same. Hence, this method
seems to be more reliable compared to conventional FH palpation for
assessment of foetal growth on antenatal visits for screening SGA
foetuses and possibly a more cost and time effective tool compared to
serial growth monitoring by ultrasonography in low resource settings.

However, this study observed a higher birth weight cut offs
corresponding to the 10\textsuperscript{th} centile on the
21\textsuperscript{st} Intergrowth chart with resultant overdiagnosis of
SGA foetuses when applied to Indian population.

ACKNOWLEDGEMENT:

\textbf{Disclosures:} There is no conflict of interest among authors to
declare.

\textbf{Contribution to Authorship:}

Millo Suka- Conducting the work, analysis of data, writing the
manuscript.

Manju Puri- Concept, design and co-writing the manuscript.

Anuradha Singh- Co-designing, analysis of data, revising the manuscript.

\textbf{Ethics Approval:}

The study was conducted after clearance from the institutional ethics
committee.

Clearance was obtained from- Institutional Ethics Committee, Lady
Hardinge Medical College and Associated Hospitals, New Delhi

Dated- 28-10-2019

Reference number: LHMC/IEC/Thesis/2019/30

\textbf{Funding:} No funding received

\textbf{Figure legend:}

\textbf{Figure 1:} Percentage distribution of perinatal complications
among AGA and SGA neonates

\textbf{Figure 2:} Comparison of Fundal Height palpation with SFH
measurement on standard charts for detection of SGA neonates

\textbf{Table 1:} Comparison of diagnostic tests for fundal height
palpation and SFH measurement in the detection of SGA neonates

\textbf{References:}

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SP. Serial third-trimester ultrasonography compared with routine care in
uncomplicated pregnancies: a randomized controlled trial. Obstetrics \&
Gynecology. 2018 Dec 1;132(6):1358-67.

3. Roex, A., Nikpoor, P., van Eerd, E., Hodyl, N. and Dekker, G., Serial
plotting on customised fundal height charts results in doubling of the
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4. Papageorghiou AT, Ohuma EO, Altman DG, Todros T, Ismail LC, Lambert A
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5. Lee AC, Kozuki N, Cousens S, Stevens GA, Blencowe H, Silveira MF;
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INTERGROWTH-21\textsuperscript{st}~standard: analysis of CHERG~datasets.
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6. Mendez-Figueroa H, Truong VT, Pedroza C, Khan AM, Chauhan SP.
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7. Lindqvist PG, Molin J. Does antenatal identification of
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PMID: 15717289.

8. Olusanya BO. Intrauterine growth restriction in a low-income country:
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WHO Multicenter Growth Reference. Early Hum Dev. 2010 Jul;86(7):439-44.

9. Subramanian, Subhadra \& S, Remadevi \& Subramaniam, Karthik. (2020).
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