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\begin{document}

\title{Impact of the COVID-19 pandemic on surgery for severe endometriosis in
the UK: a national database study}



\author[1]{Jonathan Lewin}%
\author[2]{Ertan Saridogan}%
\author[3]{Dominic Byrne}%
\author[4]{T Justin Clark}%
\author[5]{Arvind Vashisht}%
\affil[1]{University College London}%
\affil[2]{University College London Hospitals NHS Foundation Trust}%
\affil[3]{Royal Cornwall Hospitals NHS Trust}%
\affil[4]{Birmingham Women's NHS Foundation Trust}%
\affil[5]{University College London Hospitals NHS Foundation Trust Women's Health Service}%


\vspace{-1em}



  
  \date{May 26, 2024}


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\selectlanguage{english}
\begin{abstract}
Objective: To determine the impact of the COVID-19 pandemic on surgery
for severe endometriosis in the UK at a national, regional and
centre-level. Design: Population-based national cohort study.
Population: All women undergoing endometriosis surgery requiring
dissection of the pararectal space in the UK from 2017 to 2020
inclusive. Methods: The British Society for Gynaecological Endoscopy
(BSGE) collects data nationally on all operations for severe
endometriosis which involve dissection of the pararectal space. Annual
audits of this database were obtained from the BSGE. Publicly available
data on COVID-19 deaths and population were obtained from the UK Office
for National Statistics. Main outcome measures: Numbers of annual
BSGE-registered endometriosis operations. Results: A total of 5916
operations were performed. The number of operations decreased by 49.4\%
overall between 2019 and 2020. The number of endometriosis centres
remained the same, however the median number of operations per centre
decreased from 21 to 12.5, with a median percentage decrease at each
centre of 51.0\% (IQR 29.4\% -- 75.0\%). There was no significant change
in the type of surgery performed. All 11 administrative regions of Great
Britain had reduced numbers of BSGE-registered operations in 2020
compared with the average for 2017-2019, with a median 56.6\% decrease
(range 6.13\% - 68.62\%). Regional reduction in operations was
significantly correlated with COVID-19 death rates (r=0.557, 95\% CI of
r 0.048 -- 1.00, p=0.037). Conclusions: There has been a dramatic fall
in the number of operations for severe endometriosis in Britain during
the COVID-19 pandemic.%
\end{abstract}%



\sloppy


Authors: Dr Jonathan Lewin, University College London Hospital,
Department of Gynaecology. 235 Euston Road London NW1 2BU Professor
Ertan Saridogan, University College London Hospital, Department of
Gynaecology. 235 Euston Road London NW1 2BU Mr Dominic Byrne, Royal
Cornwall Hospital, Department of Gynaecology. Treliske, Truro TR1 3LJ
Professor Thomas Justin Clark, Birmingham Women's and Children's
Hospital, Department of Gynaecology. Mindelsohn Way, Birmingham B15 2TG
Mr Arvind Vashisht, University College London Hospital, Department of
Gynaecology. 235 Euston Road London NW1 2BU

Corresponding Author: Dr Jonathan Lewin. Contact Address: Flat F, 14
John Spencer Square, London N1 2LZ. Tel: +447968842291. Email:
Jonathan.lewin1@nhs.net

Running Title: Impact of COVID-19 on endometriosis surgery in the UK

Full Abstract: Objective: To determine the impact of the COVID-19
pandemic on surgery for severe endometriosis in the UK at a national,
regional and centre-level.

Design: Population-based national cohort study. Population: All women
undergoing endometriosis surgery requiring dissection of the pararectal
space in the UK from 2017 to 2020 inclusive. Methods: The British
Society for Gynaecological Endoscopy (BSGE) collects data nationally on
all operations for severe endometriosis which involve dissection of the
pararectal space. Annual audits of this database were obtained from the
BSGE. Publicly available data on COVID-19 deaths and population were
obtained from the UK Office for National Statistics. Main outcome
measures: Numbers of annual BSGE-registered endometriosis operations.
Results: A total of 5916 operations were performed. The number of
operations decreased by 49.4\% overall between 2019 and 2020. The number
of endometriosis centres remained the same, however the median number of
operations per centre decreased from 21 to 12.5, with a median
percentage decrease at each centre of 51.0\% (IQR 29.4\% -- 75.0\%).
There was no significant change in the type of surgery performed. All 11
administrative regions of Great Britain had reduced numbers of
BSGE-registered operations in 2020 compared with the average for
2017-2019, with a median 56.6\% decrease (range 6.13\% - 68.62\%).
Regional reduction in operations was significantly correlated with
COVID-19 death rates (r=0.557, 95\% CI of r 0.048 -- 1.00, p=0.037).
Conclusions: There has been a dramatic fall in the number of operations
for severe endometriosis in Britain during the COVID-19 pandemic.
Funding: None Keywords: Endometriosis, COVID-19, Pandemic, BSGE

Tweetable Abstract: The number of operations for severe endometriosis in
Britain fell by 49\% in 2020 vs pre-pandemic levels.

\section*{Introduction}

{\label{introduction}}

The COVID-19 pandemic has had a significant impact on surgical services
in the UK, with more than 1.5 million operations cancelled or postponed
in 2020. In order to increase ITU capacity to care for ventilated
patients, operating theatres throughout the country were transformed
into high-dependency units. Anaesthetists required for elective surgery
were unavailable as their unique skills in caring for the critically ill
were needed for COVID patients. Many other non-emergency teams and
healthcare professionals were redeployed to help as frontline workers to
combat the pandemic and treat afflicted patients. Many other staff have
been unable to work in operating theatres due to illness or shielding
for pre-existing health conditions. Patients have faced reduced access
to general practitioner (GP) services and specialist surgical clinics,
all of which have prevented or delayed the scheduling of operations.

Prior to the pandemic patients already faced long waits for elective
surgery, and this is particularly true of endometriosis surgery.
Endometriosis patients in the UK wait on average 8 years for diagnosis
alone, and 30\% wait more than 10 months for surgery. The delay in
surgery incurs secondary economic costs such as time out of education
and employment, and places additional strain on emergency services from
attendances for uncontrolled pain. It is vital that the backlog of
endometriosis surgery is quantified, and a plan is made to reduce the
waiting times for endometriosis surgery to a sustainable level. The
pandemic will undoubtedly have adversely impacted this position,
although the distribution and scale of the interruption to endometriosis
surgery is not yet known.

The British Society for Gynaecological Endoscopy (BSGE) is an
organisation set up by clinicians to improve standards, training and
exchange of information in gynaecological minimal access surgery, and is
the primary national aggregator of data on endometriosis surgery in the
UK. To gain accreditation as a BSGE-approved endometriosis centre, a
unit must provide data on complex operations to a centralised database
which is audited annually to maintain accreditation. This database
provides a register of the state of surgical services for severe
endometriosis in the UK, and therefore has the potential to help assess
the impact of the COVID-19 pandemic on these services. The purpose of
this study is to assess the impact of COVID-19 on surgery for severe
endometriosis at a national, regional and centre-level using the BSGE
database, and to assess the correlation between pandemic severity and
disruption to these services.

\section*{Methods}

{\label{methods}}

To be granted BSGE annual accreditation as an endometriosis centre,
criteria must be met including a minimum number of complex surgical
cases, multidisciplinary team involvement and submission of an exemplar
surgical video. Auditing is performed annually and case numbers per
surgeon must be adequate for each centre to maintain its accreditation
each year. At least 12 cases of laparoscopic surgical excision of
rectovaginal endometriosis requiring dissection of the pararectal space
per surgeon are required, and any such case must be registered on the
national BSGE database.

Annual audits of the BSGE database were obtained from the BSGE
endometriosis centres committee including data from all accredited
centres from 2017 -- 2020 inclusive to analyse the impact of the
COVID-19 pandemic. Data included the number of operations performed
annually at each centre and the type of bowel surgery performed.
Region-level data on operations were aggregated according to the region
of the centre at which the operations were performed. Centres from
outside the UK were excluded, as well as Northern Ireland due to lack of
data.

Data on regional COVID deaths were obtained from publicly available data
compiled by the UK Office of National Statistics (ONS) and the National
Registry of Scotland. Regional population estimates were obtained from
the ONS and used to calculate registered COVID deaths per 1000
population. Statistical analysis was performed using Pearson r
correlation coefficient and Chi\textsuperscript{2} goodness-of-fit test
in R with the Base package. Graphs were plotted in R using RStudio with
the GGPLOT2 package, and regional mapping templates were obtained from
the ONS.

\section*{Results}

{\label{results}}

\subsection*{Centres}

{\label{centres}}

A total of 73 centres were registered with the BSGE between 2017 to
2020. Over this time period, the number of centres submitting data for
registered operations each year increased from 56 to 66 (Figure 1). Four
centres submitted registered operations for the first time in 2020,
while seven previously registered centres did not register any
operations in 2020. Out of 73 centres, 48 submitted registered
operations every year, 13 only for 3 years, 8 only for 2 years and 4
only for 1 year.

\subsection*{Operations}

{\label{operations}}

Over the time period from 2017 -- 2020, a total of 5916 operations were
performed for deep endometriosis requiring pararectal dissection at
BSGE-accredited centres (Figure 2). The total number of registered
operations increased by an average of 13.5\% per year between 2017-2019,
then decreased by 49.4\% between 2019-2020.

At a centre-level, 60 endometriosis centres had reduced operation
numbers in 2020 compared with the average for 2017-2019, while 9 centres
had increased numbers of operations. Overall, the annual median number
of operations per centre decreased from 21 operations to 12.5
operations, with a median decrease in operations per centre of 51.0\%
(IQR 29.4\% -- 75.0\%).

Between 2017 and 2019, on average 33.0\% of patients had no surgery on
the bowel, 60.2\% underwent shaving of endometriosis from the bowel
surface, 1.8\% underwent a disc resection and 5.0\% underwent resection
of a segment of bowel. In 2020, 34.5\%, 59.3\%, 2.6\% and 3.6\% of
patients underwent no bowel surgery, bowel shave, disc resection and
segmental bowel resection respectively, which was not significantly
different to previous years (p=0.08).

\subsection*{Regions}

{\label{regions}}

At a regional level, all 11 administrative regions of Great Britain had
reduced numbers of BSGE-registered operations for endometriosis in 2020
compared with averages for 2017-2019, with a median 56.6\% decrease
(range 6.13\% - 68.62\%) (Figures, 3 Figure 4). Regions had a median of
1.49 deaths from COVID-19 per 1000 population (range 0.80 -- 1.91). At a
regional level, reduction in these operations was significantly
correlated with COVID-19 death rates (r=0.56, 95\% CI of r 0.048 --
1.00, p=0.037).

\section*{Discussion}

{\label{discussion}}

\subsection*{Main Findings}

{\label{main-findings}}

Our study demonstrates the dramatic reduction in endometriosis surgery
by nearly 50\% overall, . This is significantly higher than the 38.6\%
reduction in elective procedures nationwide, indicating that
endometriosis surgery has been particularly badly affected. the number
of endometriosis operations per centre decreased by a median 51\%, while
the number of centres remained approximately the same. Only 9 centres
had increased operation numbers, which may have been newer centres in
the process of growing their workload as usually occurs when centres
acquire additional staff. Despite these changes, the proportions of
patients undergoing the different types of surgery on the bowel
(shaving, disc resection and segmental resection) remains unaffected.
Reduction in endometriosis operations at a regional level were
correlated with regional COVID-19 death rates.

\subsection*{Strengths and Limitations}

{\label{strengths-and-limitations}}

This study is the first to provide a comprehensive assessment of the
effect of the COVID-19 pandemic on surgery for severe endometriosis in
the UK. A nation-wide, standardised approach was taken in data
collection, however only BSGE-registered operations were taken into
account, and there may have been other operations performed which were
not registered with the BSGE. There was also a lack of data from
Northern Ireland, restricting analysis to Great Britain.

\subsection*{}

{\label{section}}

\subsection*{Interpretation}

{\label{interpretation}}

The magnitude of the reduction in operations for this common, chronic,
unremitting gynaecological condition is of major concern, and highlights
the challenges for the restoration of endometriosis services. There is a
pressing need in the pandemic recovery period for substantial investment
to provide the necessary resources for adequate surgical service
provision. Despite national prioritisation guidance stating that surgery
for severe endometriosis with uncontrolled pain should be performed
within 3 months, it is likely that patients will experience
significantly longer wating times than this, as they did prior to the
pandemic. Indeed, NHS England statistics from March 2021 show only
65.3\% of patients receive treatment within 18 weeks of referral for
gynaecological disease, and this figure may be considerably worse for
endometriosis treatment.

Most endometriosis surgery is performed laparoscopically, and part of
the decline in operations may have been due to concerns early in the
pandemic about laparoscopy as an aerosol-generating procedure. The
increased use of pre-operative testing of patients and measures to
improve the COVID-safety of laparoscopy have allowed the careful
re-starting of endometriosis surgery at some centres through 2020 and
2021, mitigating some of the disruption. However, a survey by the Royal
College of Obstetricians and Gynaecologists in December 2020 found that
only 20\% of respondents felt that elective gynaecology activity at
their units had returned to pre-2020 levels, indicating that the effect
of the pandemic is likely to have extended well into 2021.

The reduction in operations for severe endometriosis is unsurprising
given the lack of operating theatre capacity and redeployment of staff.
However, reduced patient access to GP services may be equally important,
as well as other obstacles to obtaining a referral for endometriosis
treatment, such as the need to self-isolate and reductions in
endometriosis clinic capacity. In support of this, a report into
elective care in England found that while there was a large decrease in
the number of referred patients receiving definitive care in 2020
compared to 2019, there was an even larger decrease in the number of new
referrals made, so that the total number of patients waiting for surgery
actually decreased. As more patients are able to access GPs and obtain
referrals to specialist endometriosis services, it is likely that most
hospitals will experience a surge in referrals. Increased demand from
primary care will add to those patients already awaiting surgery whose
operations have been delayed, and existing services are unlikely to have
capacity to meet the increasing demand. Furthermore, the ensuing delays
in surgical treatment will cause additional costs to the NHS through
emergency and pain management services, as well as other costs from lost
time at work and education.

Considering the almost universal decline in centre activity, the BSGE
has made a decision not to use operation numbers from 2020 as part of
the accreditation process. This will allow many centres to remain on the
BSGE centres list, and thereby ensure that the infrastructure is in
place for an increase in operation numbers in the pandemic recovery
period. Nevertheless, the effect on waiting times for endometriosis
surgery will be dramatic, and the full extent of the impact on the wait
for surgery is not yet known.

The sharp reduction in surgical case-load for highly complex surgery
will undoubtedly have caused ripple-effects on proficiency, training and
hands-on experience for both experienced and trainee-level endometriosis
surgeons. ``Buddy'' operating, where experienced surgeons operate
together, has been suggested by some to help reattain pre-pandemic
levels of proficiency and confidence. This is a difficult debate as it
represents a further cost pressure to organisations to fund what is
regarded by some as a necessity. Meanwhile, new endometriosis surgeons
will have felt the impact on their training acutely, with significant
delays to the acquisition of new skills. Additional resources may
therefore be required for advanced laparoscopic surgery training in
order to maintain any benefit in additional surgical capacity for the
longer term.

This study finds that reduction in endometriosis operations at a
regional level are correlated with regional COVID-19 death rates. There
are several reasons why this may be the case. Firstly, the repurposing
of operating theatres for the care of COVID patients left few operating
theatres available, particularly for elective surgery, and this effect
may have been greater in regions with higher numbers of critically
unwell COVID patients. Staffing required for endometriosis surgery is
likely to have been worse affected by redeployment in regions worse
affected by the pandemic, particularly affecting the availability of
anaesthetists. Staff absence due to illness with COVID or a household
member with COVID may have played a significant role. In fact, a survey
by the Royal College of Physicians in April 2020 showed 21\% of staff
away from work primarily due to these two reasons. Also, regions with
worse COVID outbreaks may have seen fewer patients accessing GP services
and endometriosis clinics due to a combination of reduced primary care
services and patient avoidance of healthcare
facilities\textsuperscript{15}. Evidence that regions worse affected by
the pandemic suffered greater reductions in endometriosis operations may
be helpful in planning the allocation of resources so that operating
capacity is increased where it is most needed. Indeed, greater sharing
of patient pathways and working beyond single hospital boundaries may be
required to smooth out some of the inequities in waiting times and
access to care. However, this is only one of several factors to
consider, and pre-pandemic waiting times will need to be taken into
account alongside other concerns.

\section*{Conclusion}

{\label{conclusion}}

The effect of the COVID-19 pandemic on endometriosis surgery has been
dramatic and should be addressed with urgency. A co-ordinated effort is
required to establish increased capacity, wider access to care and
greater support for patients and their clinical teams. This study puts
the scale of the problem into focus, and it is hoped that this will
encourage efforts to meet the challenge of promoting awareness and
excellence in care for patients with endometriosis.

\section*{Contributions to Authorship}

{\label{contributions-to-authorship}}

JL: primary author of paper including data aggregation and analysis,
creation of figures, drafting and revision of text, corresponding
author. ES: Editing of text, advising on methods and focus, revision of
manuscript. DB: Editing of text, advising on methods and focus, revision
of manuscript. JC: Editing of text, advising on methods and focus,
revision of manuscript. AV: Conceptualisation of study, coordination of
authors, editing of text, advising on methods and focus, revision of
manuscript.

\section*{Statement on Ethics}

{\label{statement-on-ethics}}

This study did not involve any departure from routine clinical practice
or divisions/randomisation of patients into groups. It was retrospective
in nature, using pre-existing audits of national database data from the
British Society for Gynaecological Endoscopy (BSGE). Full anonymity of
patients was ensured through lack of any patient-specific data used,
only the number of operations were known for each endometriosis centre
per year. For these reasons prior approval from a research ethics
committee was not required. The audits were registered annually and
performed by the BSGE, and are publicly available on their website.
Approval was gained from the BSGE for the study.

\section*{Funding}

{\label{funding}}

No funding was provided or required for the study.

\section*{Discolsure of Interests}

{\label{discolsure-of-interests}}

Professor Thomas Justin Clark is the current president of the British
Society for Gynaecological Endoscopy. There are no other relevant
financial, personal, political, intellectual or other interests to
declare.

\section*{Figure List}

{\label{figure-list}}

Figure 1: Number of BSGE registered operations and centres in each year.

\emph{Figure 2: Boxplot of number of BSGE registered operations in each
year at each endometriosis centre. Each datapoint represents data from
one centre in each year.}

Figure 3: Graph showing correlation between the percentage reduction in
operations for endometriosis (compared to 2017-2019 mean) with COVID
deaths per 1000 of population. Linear regression line and 95\%
confidence interval band shown.

Figure 4: Geographic plot of reduction in operations compared to
previous 3-year average (left) and COVID deaths per 1000 population.

\emph{References}

\section*{Acknowledgements}

{\label{acknowledgements}}

The authors would like to thank Conor Byrne and team at the ICEway IT
services for management of the database and data download used in this
study.

\textbf{Hosted file}

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