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\begin{document}

\title{Fetal surveillance from 39 weeks' gestation: an alternative to earlier
induction of labour to reduce stillbirth in South Asian born women? A
Retrospective Cohort Study}



\author[1]{Miranda Davies-Tuck}%
\author[2]{Mary-Ann Davey}%
\author[3]{Ryan Hodges}%
\author[2]{Euan Wallace}%
\affil[1]{Hudson Institute of Medical Research}%
\affil[2]{Monash University}%
\affil[3]{Monash Health}%


\vspace{-1em}



  
  \date{May 29, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Objectives: In July 2017, Victoria's largest maternity service
implemented a new clinical guideline aimed to reduce the rates of
stillbirth at term for South Asian-born women. Here we present the
evaluation of the change in care on rates of stillbirth, neonatal and
obstetric interventions. Design: Cohort Study Setting: Victoria's
largest metropolitan university-affiliated teaching hospital.
Population: All women receiving antenatal care who gave birth in the
term period between January 2016 and December 2020. Methods: Differences
in rates of stillbirths, neonatal deaths, perinatal morbidities, and
interventions after July 2017 were determined. Multigroup interrupted
time-series analysis was used to assess changes in rates of induction of
labour. Main Outcome Measures: Rates of stillbirths, neonatal deaths,
perinatal morbidities, and obstetric interventions. Results: 3506 south
Asian-born women gave birth prior to, and 8532 after the change. There
was a 64\% reduction in term stillbirth (95\%CI 87\% to 2\%; p=0.047)
for south Asian-born women after the change in practice from 2.3 per
1000 births to 0.8 per 1000 births. The rates of early neonatal death
(3.1 per 1000 vs 1.3 per 1000; p=0.03) and SCN admission (16.5\% vs
11.1\%; p\textless{}0.001) also decreased. There were no significant
differences in admission to NICU, Apgar\textless{}7 at 5 minutes,
birthweight or differences in the trends of induction of labour per
month. Conclusions: Fetal monitoring from 39 weeks' may offer an
alternative to routine earlier induction of labour to reduce the rates
of stillbirth without causing an increase in neonatal morbidity or
obstetric interventions.%
\end{abstract}%



\sloppy


\textbf{Introduction}

It is widely acknowledged that the rates of stillbirth are higher among
women of South Asian background (e.g. India, Sri Lanka, Pakistan and
Bangladesh) compared to other women in high income countries around the
world\textsuperscript{1-10}. The drivers of this are likely
multifactorial, but one potential contributing mechanism is earlier
feto-placental maturation. Evidence in support of this hypothesis
includes south Asian women having a shorter duration of
pregnancy\textsuperscript{8, 9}, higher rates of fetal compromise in
late pregnancy\textsuperscript{11} and during
labour\textsuperscript{12}, more functionally mature babies at preterm
gestations\textsuperscript{13} and an earlier and more rapid increase in
the risk of stillbirth at the end of pregnancy than in other
women\textsuperscript{8}. We have previously shown that south Asian
women at 39 weeks' gestation have similar rate of stillbirth to
Australian born women at 41 weeks\textsuperscript{8}.

Leading maternity guidelines (NICE guidelines, Royal Australia and New
Zealand College of Obstetricians and, Gynaecologists Guidelines
(RANZCOG)) recommend routine ultrasound assessment and/or induction of
labour at 41 weeks to reduce the rates of stillbirth. However, by the
time south Asian born women are offered these tests to assess fetal
wellbeing they are already at between 2 and up to five times the risk of
stillbirth compared to the Australian-born population\textsuperscript{1,
14, 15}. The most recent NICE guidelines have recommended earlier
induction of labour from 39 weeks for all women of South Asian
background. However, widespread criticism and concern around this
recommendation\textsuperscript{16} have been highlighted and there is
currently no evidence to suggest that earlier induction for south Asian
women would reduce their rates of stillbirth.

In July 2017, informed by our observations of biological variation in
gestation length and gestation specific stillbirth rates in South Asian
women, Monash Health, Victoria's largest maternity service implemented a
new clinical guideline. The new guideline recommended twice weekly
``post-term'' monitoring to assess fetal wellbeing (cardiotocography
(CTG) and measurement of amniotic fluid) from 39 weeks for south Asian
women rather than the 41 weeks it had previously been and remains for
all other women. Here we present the evaluation of the impact of the
change in clinical care for south Asian women on rates of stillbirth,
neonatal and obstetric interventions.



\textbf{Methods}

\emph{Study Design}

A cohort study of all women receiving antenatal care and planning to
give birth at Monash Health, Victoria's largest metropolitan
university-affiliated teaching hospital caring for about 10,000 women
per year~across~three separate hospital sites~of different acuity levels
(Clayton, Dandenong and Casey) between January 1st, 2016 and Dec 31st,
2020 was undertaken. Women who gave birth at term or beyond ([?] 37
completed weeks gestation) to a singleton baby and who were booked and
received antenatal care at the health service were included.

Maternal self-reported country of birth was classified into regional
groups, as defined by the United Nations\textsuperscript{17}. As the
change in clinical practice was specific only to women from south Asia,
we then classified women as either as being born in South Asia (SA) if
they were born in Afghanistan, Bangladesh, Bhutan, India, Iran, the
Maldives, Nepal, Pakistan, or Sri Lanka or not (``Other women'').

Data was extracted from the Monash Health Birthing Outcomes System
(BOS). BOS is an electronic database recording all births [?]20 weeks'
gestation. For each birth the attending midwife, supported by routine
data validation, enters 46 data items into BOS. This data is included in
formal state and national perinatal statistics.

\emph{Exposure Definition}

All births that occurred between January 2016 and June
30\textsuperscript{th} 2017 were classified as ``unexposed'' and those
occurring between July 1\textsuperscript{st} 2017 and December 2020 were
classified as ``exposed'' to the clinical practice change.

\emph{Description of the Clinical Practice Change}

In collaboration with Monash Health, we amended the Monash Health
Prolonged pregnancy guideline to include a specific pathway for women
who were of South Asian background (based on women self-identifying
their background regardless of where they were born). The original
clinical guideline recommended twice weekly fetal surveillance with
cardiotocography (CTG) and measurement of amniotic fluid at 41 weeks
gestation. Our change to the guideline recommended that takes place from
39 weeks' gestation for women born in South Asia. The fetal surveillance
monitoring remained unchanged for all other women. For all women,
including south Asian women, an induction of labour is recommended from
41 weeks and close to 42 weeks unless sooner as clinically indicated.
The clinical guideline is provided as Appendix 1.

\emph{Primary Outcome Measure}

The primary outcome was stillbirth occurring either before the onset of
labour (antepartum death) or during labour (intrapartum death).

\emph{Secondary Outcome Measures}

Secondary outcomes included neonatal death \textless{}7 days, admission
to special care nursery, admission to neonatal intensive care, Apgar
score\textless{} 7 at 5 minutes, baby birth weight (grams), gestation of
birth, induction of labour, and mode of birth.

\emph{Maternal Demographics}

The following maternal demographics were also extracted: Maternal age
(years), maternal body mass index, parity, maternal medical conditions
(pre-existing hypertension, pre-existing type 2 diabetes, pre-existing
thyroid disease, gestational hypertension, pre-eclampsia and gestational
diabetes).

\emph{Statistical Analysis}

All continuous data were assessed for normality and summary statistics
were reported as mean (standard deviation), median (interquartile range)
or number(percent) as appropriate. Demographics of the women before and
after the guideline was implemented were tabulated compared using either
a t-test, a Kruskal Wallis or chi\textsuperscript{2} test as
appropriate. The rate of stillbirth per 1000 births before and after the
guideline for south Asian born women and all other women were
determined. The association between the change in clinical practice and
rates of stillbirth was then determined using log linked generalised
linear regression. Adjustment with maternal age, BMI, parity, and
presence of pre-existing medical conditions (pre-existing hypertension,
type 2 diabetes or thyroid disease) or obstetric conditions (gestational
hypertension, pre-eclampsia and gestational diabetes) was also
performed. The rate of stillbirth per ongoing week for south Asian born
and all other women before and after the change in practice was
determined and plotted. Differences in secondary outcomes stratified by
maternal exposure group before and after the change in practice were
also tabulated and compared using standard approaches. When evaluating
the impact of interventions to reduce stillbirth, understanding
potential harms or changes to intervention rates need to be balanced.
The rates of induction of labour are widely acknowledged to be
increasing therefore pooling and comparing rates before and after the
change is not appropriate. Therefore we performed a two-group,
interrupted time-series analysis using Newey-West standard errors and a
lag of 1 to determine the change in rates of induction of labour over
time following the implementation of the guideline, taking into account
the trends in induction over time prior to the guideline between south
Asian and all other women\textsuperscript{18}. We did not correct for
seasonality. All statistics were performed using StataCorp 12.

\emph{Patient and Public Involvement.}

Patients and the public were not involved in this research however the
experiences of clinical staff have been formally
captured\textsuperscript{19} and the experiences of South Asian born
women themselves will be reported elsewhere.

\emph{Funding}

This study was funded by the Red Nose Foundation through an externally
peer reviewed grant process. MDT was also funded by the National Health
and Medical Research Council (NHMRC) Centre for Research Excellence(CRE)
in Stillbirth. EW was supported by a NHMRC programme grant (APP1113902).
MAD and RH have no funds to disclose. The funders had no role in the
study design; collection, analysis, interpretation of data; in the
writing of the report; and in the decision to submit the article for
publication. All researchers were independent from funders and all
authors had full access to all the data (including statistical reports
and tables) in the study and can take responsibility for the integrity
of the data and the accuracy of the data analysis.



\textbf{Results}

Between January 2016 and December 2020, a total of 12 095 women with a
singleton pregnancy gave birth at term prior to the change in clinical
practice and 28 162 gave birth after it was implemented. One third of
women giving birth at Monash Health in both time periods were themselves
born in South Asia. The characteristics of the women who gave birth in
the two time periods are presented in Table 1. There was a total of 3506
south Asian born women in the period prior to and 8532 in the period
after the change in practice.

The rates of stillbirth at term before and after the change in practice
are presented in Table 2. Prior to the change in practice the rate of
stillbirth at term for south Asian born women was 2.3 per 1000 births.
This was 2.6-fold higher than the overall rate for all other women (0.9
per 1000 births) at the health service (p=0.06). After the change in
practice there was a 64\% reduction in rate of stillbirth (95\%CI 87\%
to 2\%; p=0.047) for south Asian born women after adjustment for
potential confounders. The rate of stillbirth for south Asian born women
after the change in practice reduced to a rate that was equivalent all
other women giving birth at Monash Health.

The rates of stillbirth per on going week before and after the change in
practice are presented in Figure 1. For south Asian born women prior to
the change in practice the rates of stillbirth increased earlier and at
a steeper rate for each advancing week of gestation when compared to all
other women. After the change in practice, we observed a 45\% reduction
in the rate of stillbirth at 38 weeks, a 60\% reduction at 39 weeks and
there were no stillbirths that occurred at 40 weeks or beyond. The rates
of stillbirth per on going week for all other women are also presented.
Overall, the rates of stillbirth from 37-39 weeks remained the same
across the whole study period and there was an observed 25\% reduction
in the rate of stillbirths at 40 and 41 weeks in the post period.

The rates of secondary outcomes before and after the change in practice
and the impact of the practice change on the rates of induction of
labour are presented in Table 3 and Figure 2. For south Asian born
women, the rates of early neonatal death (3.1 per 1000 vs 1.3 per 1000;
p=0.03) and SCN admission (16.5\% vs 11.1\%; p\textless{}0.001)
decreased after the change in practice and there were no significant
differences in admission to NICU, Apgar\textless{}7 at 5 minutes or baby
birthweight. Similar to what was observed with stillbirth rates, the
rate of NND for south born women following the change in practice became
equivalent to all other women. Review of the timing of NNDs revealed
that prior to the guideline NNDs were experienced following birth
between 38- and 41-weeks' gestation and following the change in practice
the NNDs that occurred were all born below 40 weeks' gestation. Prior to
the change in practice the median gestation of birth for south Asian
born women was 39\textsuperscript{+3}(IQR 38\textsuperscript{+4} to
40\textsuperscript{+1}) weeks and this reduced by 1 day in the period
after the change in practice
39\textsuperscript{+2}(38\textsuperscript{+3} to 40) weeks
(p\textless{}0.001). There were no differences in the mode of birth
following the change in practice. For comparison the rates for all other
women who were not undergoing earlier monitoring are also presented.

The overall rates of induction of labour were significantly higher
following the change in practice for both south Asian and all other
women. The impact of the change in practice on trends in rates of
induction of labour for South Asian born women compared to all other
women are presented in Figure 2. South Asian born women initially
(January 2016) had an absolute 3\% higher rate of induction of labour
(95\% CI 0.3\% to 4.8\%; p=0.03) compared to all other women at the
maternity service. For both south Asian and all other women, the rates
of induction of labour increased in the period prior to the change in
practice, however there was no difference in the slope of this increase
between south Asian and all other women (-0.05\%, 95\% CI -0.3\% to
0.2\%; p=0.67). Immediately following the change in practice, the rates
of induction in south Asian born women were 4.9\% higher (95\% CI 1.3\%
to 8.5\%; p=0.008) than in all other women however there was no
significant difference in the rate of change of induction rates per
month after the change in practice in south Asian born women when
compared to all other women (-0.1\%, 95\%CI-0.3\% to 0.1\%; p=0.41).
Finally, in the period after the change in practice the rates of
induction did not significantly change per month in south Asian born
women (0.02\%, 95\% CI -0.08\% to 0.1\%) however all other women
experienced a 0.17\% increased rate of induction per month (95\% CI
0.10\% to 0.20\%; p\textless{}0.001).

\textbf{Discussion}

\emph{Main Findings}

We found that a change in clinical care to offer fetal wellbeing
surveillance from 39 rather than 41 weeks in gestation for south Asian
born was associated with a significant reduction in the rates of both
stillbirth and neonatal death at term without increasing rates of
perinatal morbidity, early term birth or interventions such as induction
of labour or caesarean birth. Following the change in clinical care the
rates of stillbirth for south Asian born women were equivalent to all
other women at the maternity service and we did not observe any
stillbirths or neonatal deaths after 39 weeks' gestation. To our
knowledge this is the first stillbirth prevention intervention for
migrant women globally.

\emph{Strengths and Limitations}

Strengths of our study include the uniformity of the implementation of
the change in practice across the 3 three separate hospital sites, the
large number of south Asian born women (Monash Health cares for one
third of all south Asian born women giving birth in Victoria), a longer
follow up post implementation of 3.5 years thus determining whether any
benefits or harms were sustained over time, and we studied all women who
received antenatal care and gave birth at Monash health using routinely
reported mandatory validated health data to minimise bias. Limitations
of our study were that it was an observational study at one Health
Service. However, Monash Health is the largest maternity service in
Victoria, caring for women of all acuity level. While it is also
possible that other stillbirth prevention approaches may have influenced
the rates of stillbirth in south Asian women this is unlikely as rates
did not change for all other women. This analysis included 2020. The
COVID 19 pandemic and extended lockdowns in Victoria may have influenced
our results, however cases of COVID 19 were low in Victoria and there
were no impacts on the rates of stillbirth either at Monash
Health\textsuperscript{20} or more broadly in
Victoria\textsuperscript{21}. Finally, we have analysed the data by
maternal region of birth not identified maternal background. The
clinical guideline offered earlier monitoring to any woman of south
Asian background, regardless of where she gave birth. Any associations
we report are therefore likely underestimated.

\emph{Interpretation}

While there is good evidence that induction of labour from 41 weeks'
gestation reduces the rates of perinatal mortality\textsuperscript{22},
what to do prior to 41 weeks is less clear. The increasing rates of
induction of labour and early term birth are a growing global concern
due to their association with adverse neonatal\textsuperscript{23},
childhood\textsuperscript{24}, neurodevelopmental and educational
outcomes\textsuperscript{25, 26}. Induction of labour from 39 weeks'
gestation has been suggested as a solution to balancing these risks,
however this has yet to be demonstrated as
effective\textsuperscript{27}. Evidence suggests that many women would
also prefer to wait for labour to start naturally\textsuperscript{28} or
regret their decision to accept an induction of
labour\textsuperscript{29}. Observational data from the Netherlands has
suggested that over 3500 inductions at 39 weeks would be needed to
prevent adverse neonatal outcomes in African women, another group at
higher risk of stillbirth\textsuperscript{30}. To our knowledge there
have been no studies examining the impact of earlier induction labour
for south Asian women. It is therefore not surprising that the new NICE
guidelines, recommending that Asian and Black women should undergo
induction of labour from 39 weeks have received widespread criticism due
to their lack of evidence, for being racist, discriminatory and for not
placing the desires and expectations of the woman at the
centre\textsuperscript{16, 31-33}.

Our approach to offer earlier fetal monitoring for south Asian women
provides an alternative solution, using established clinical tools that
are already embedded in clinical care. The implications to maternity
care providers are that this change in practice can be readily
implemented. While a randomised controlled trial of earlier monitoring
would offer the best evidence, this may no longer be possible as
equipoise is lost. Future studies should therefore focus on improving
the sensitivity and predictive ability of fetal monitoring through the
addition of other ultrasound or serum biomarkers, determining the
economic cost to services associated with offering earlier monitoring
compared to earlier induction of labour and capturing the views and
experiences of south Asian born women on stillbirth prevention
strategies.

\emph{Conclusion}

In conclusion, earlier fetal monitoring from 39 weeks gestations offers
an alternative to routine earlier induction of labour to not only reduce
the rates of stillbirth, but also neonatal death at term in south Asian
born women without causing an increase in neonatal morbidity or
obstetric interventions.

\textbf{Acknowledgements}

We would like to acknowledge the staff at Monash Health for their hard
work caring for women following the implementation of the new guideline.

\textbf{Disclosure of Interests}

All authors have completed the\emph{~Unified Competing Interest form~}
(available on request from the corresponding author) and declare
financial support from the Red Nose Foundation, the National Health and
Medical Research Council (NHMRC) Centre for Research Excellence(CRE) and
a NHMRC programme grant (APP1113902); no financial relationships with
any organisations that might have an interest in the submitted work in
the previous three years, no other relationships or activities that
could appear to have influenced the submitted work.

\textbf{Contribution to Authorship}

MDT and EW conceived the study. All authors designed the study. MDT
aquired the data and performed the data analysis. All authors were
involved in the review of the data analysis and interpretation. MDT
drafted the manuscript and all authors contributed to revisions and
approved the final version for publication.

\textbf{Details of Ethics Approval}

This low risk research was approved by The Human Research Ethics
Committee of Monash Health (HREC/18/MonH/171)

\textbf{Transparency Statement}

MDT affirms that the manuscript is an honest, accurate, and transparent
account of the study being reported; that no important aspects of the
study have been omitted; and that any discrepancies from the study as
originally planned (and, if relevant, registered) have been explained.

\textbf{Data Sharing}

The datasets analysed for the current study are not publicly available
as they are a clinical dataset of patient outcomes

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33. Birth Rights UK. Induction proposals ignore black and brown women's
experience of maternity services. 2021 {[}cited; Available from:

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\verb`BJOG Tables_Earlier Fetal Survillence.docx`  available at \url{https://authorea.com/users/440386/articles/541146-fetal-surveillance-from-39-weeks-gestation-an-alternative-to-earlier-induction-of-labour-to-reduce-stillbirth-in-south-asian-born-women-a-retrospective-cohort-study}

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\verb`BJOG_Earlier Fetal_Figure 1.docx`  available at \url{https://authorea.com/users/440386/articles/541146-fetal-surveillance-from-39-weeks-gestation-an-alternative-to-earlier-induction-of-labour-to-reduce-stillbirth-in-south-asian-born-women-a-retrospective-cohort-study}

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\verb`BJOG_Figure 2_Earlier Fetal.docx`  available at \url{https://authorea.com/users/440386/articles/541146-fetal-surveillance-from-39-weeks-gestation-an-alternative-to-earlier-induction-of-labour-to-reduce-stillbirth-in-south-asian-born-women-a-retrospective-cohort-study}

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