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OPINION
published: 07 July 2020
doi: 10.3389/frph.2020.00005
Frontiers in Reproductive Health | www.frontiersin.org 1July 2020 | Volume 2 | Article 5
Edited by:
Spyridon N. Karras,
Aristotle University of Thessaloniki,
Greece
Reviewed by:
Christos Venetis,
University of New South
Wales, Australia
*Correspondence:
Mathew Leonardi
mathew.leonardi@sydney.edu.au
†ORCID:
Mathew Leonardi
orcid.org/0000-0001-5538-6906
Andrew W. Horne
orcid.org/0000-0002-9656-493X
Mike Armour
orcid.org/0000-0001-7539-9851
Stacey A. Missmer
orcid.org/0000-0003-3147-6768
Horace Roman
orcid.org/0000-0002-9237-0628
Luk Rombauts
orcid.org/0000-0003-2656-2792
Lone Hummelshoj
orcid.org/0000-0003-1490-7802
Arnaud Wattiez
orcid.org/0000-0002-9396-7581
George Condous
orcid.org/0000-0003-3858-3080
Specialty section:
This article was submitted to
Reproductive Epidemiology,
a section of the journal
Frontiers in Reproductive Health
Received: 07 May 2020
Accepted: 22 June 2020
Published: 07 July 2020
Citation:
Leonardi M, Horne AW, Armour M,
Missmer SA, Roman H, Rombauts L,
Hummelshoj L, Wattiez A, Condous G
and Johnson NP (2020)
Endometriosis and the Coronavirus
(COVID-19) Pandemic: Clinical Advice
and Future Considerations.
Front. Reprod. Health 2:5.
doi: 10.3389/frph.2020.00005
Endometriosis and the Coronavirus
(COVID-19) Pandemic: Clinical
Advice and Future Considerations
Mathew Leonardi 1,2,3
*†, Andrew W. Horne4† , Mike Armour 5,6† , Stacey A. Missmer 7,8,9,10† ,
Horace Roman 10,11,12† , Luk Rombauts 10,13† , Lone Hummelshoj 10,14†, Arnaud Wattiez 15, 16†,
George Condous 1,2† and Neil P. Johnson 10,17,18, 19
1Acute Gynaecology, Early Pregnancy, and Advanced Endoscopy Surgery Unit, Nepean Hospital, Kingswood, NSW,
Australia, 2Sydney Medical School Nepean, University of Sydney, Sydney, NSW, Australia, 3Department of Obstetrics and
Gynecology, McMaster University, Hamilton, ON, Canada, 4MRC Centre for Reproductive Health, University of Edinburgh,
Edinburgh, United Kingdom, 5NICM Health Research Institute, Western Sydney University, Penrith, NSW, Australia,
6Translational Health Research Institute (THRI), Western Sydney University, Penrith, NSW, Australia, 7Department of
Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States, 8Boston Center for Endometriosis,
Boston Children’s Hospital and Brigham & Women’s Hospital, Boston, MA, United States, 9Department of Obstetrics,
Gynecology, and Reproductive Biology College of Human Medicine, Secchia Center, Michigan State University,
Grand Rapids, MI, United States, 10 World Endometriosis Society, Vancouver, BC, Canada, 11 Endometriosis Centre, Clinic
Tivoli-Ducos, Bordeaux, France, 12 Department of Obstetrics and Gynaecology, Aarhus University Hospital, Aarhus, Denmark,
13 Department of Obstetrics and Gynaecology, School of Medicine, Monash University, Melbourne, VIC, Australia,
14 Endometriosis.org, London, United Kingdom, 15 Latifa Hospital, Dubai, United Arab Emirates, 16 Department of Obstetrics
and Gynecology, University of Strasbourg, Strasbourg, France, 17 Robinson Research Institute, University of Adelaide,
Adelaide, SA, Australia, 18 Department of Obstetrics and Gynaecology, University of Auckland, Auckland, New Zealand,
19 Auckland Gynaecology Group and Repromed Auckland, Auckland, New Zealand
Keywords: endometriosis, pelvic pain, infertility, COVID-19, coronavirus, recommendations, laparoscopic surgery,
assisted reproductive technology
INTRODUCTION
The COVID-19 pandemic has led to a dramatic shift in the clinical practice of women’s health
and routine care for endometriosis has been severely disrupted. Endometriosis is defined as an
inflammatory disease characterized by lesions of endometrial-like tissue outside the uterus that
is associated with pelvic pain and/or infertility (1). It affects ∼10% of reproductive age women
worldwide, is diagnosed by surgical visualization or by radiological imaging, and is managed with
hormone treatments or by laparoscopic removal of lesions (2–4).
At the time of writing, under the guidance of international gynecological organizations (5–7),
many centers temporarily ceased offering outpatient appointments, diagnostic imaging for non-
acute pelvic pain, surgery for endometriosis, and fertility treatments. In the absence of routine
care pathways and uncertainty about when health services will be available again, endometriosis
sufferers are likely to feel vulnerable and that resultant stress and anxiety may contribute to a
worsening of symptoms. The pandemic poses several important questions for healthcare providers
on how best to deliver care within these restrictions. Herein, we present clinical advice on
the management of endometriosis during the COVID-19 pandemic and future considerations
(Table 1).
Leonardi et al. Endometriosis and the COVID-19 Pandemic
ARE ENDOMETRIOSIS PATIENTS A
HIGH-RISK POPULATION OF BECOMING
INFECTED WITH SARS-CoV-2 OR
DEVELOPING MORE SEVERE COVID-19
DISEASE SYMPTOMS?
To date, there is no evidence that those with endometriosis
are at increased risk of becoming infected with SARS-CoV-2
or developing COVID-19 disease1. A rare subgroup of those
with endometriosis have thoracic endometriosis (lesions within
the pleural cavity or on the diaphragm). The exact prevalence
is unknown but some case series suggest that up to 12% of
those with endometriosis have extra-pelvic endometriosis, with
the thorax being the most common site (8). In general, there is
a paucity of literature labeling this form of endometriosis as a
risk factor for respiratory or systemic illness beyond catamenial
pneumothorax (9). As such, it is challenging to know whether
this group is at increased risk of becoming infected with SARS-
CoV-2 or developing COVID-19. Similarly, there is no evidence
that COVID-19 will hasten the progression/development of
endometriosis. Nonetheless, the pandemic will likely contribute
to a reduction in quality of life secondary to a delay in
diagnosis and/or the management of endometriosis owing
to the temporary closure of outpatient services, (including
complementary therapies), postponement of planned surgical
or fertility treatments, and an eventual increase in the waitlist
for services once they resume. The extent of the impact will
depend on the duration of service postponement and regional
resource variations (e.g., access to operating theater time when
surgeries resume).
MANAGEMENT OPTIONS AVAILABLE
DURING THE COVID-19 PANDEMIC
We encourage individuals in need of help to seek a clinical
assessment with their general practitioners (GP), gynecologists,
physiotherapists, and/or complementary medical providers
through telehealth avenues or in-person when services resume
exercising caution to follow local risk-reduction practices.
Referral to a gynecologist with expertise in endometriosis may
also be appropriate to offset the new diagnostic and therapeutic
challenges faced during this time. Those with an established
diagnosis who are seeking help, regardless of their intentions to
pursue surgical management, should discuss with their clinician
the potential to modify their current medication regimen. Some
with suspected endometriosis may accept a clinical diagnosis in
the absence of imaging or laparoscopy and empirical medical
therapy can be initiated (2). In those given a clinical diagnosis,
and who don’t respond to medical therapy, non-invasive imaging
could be the first investigation arranged when it is safe to do so to
evaluate for features that can reliably be identified such as deep
endometriosis, ovarian endometriomas, and pouch of Douglas
1People Who Are at Higher Risk for Severe Illness | Coronavirus | COVID-19
| CDC. Available online at: https://www.cdc.gov/coronavirus/2019-ncov/need-
extra-precautions/groups- at-higher-risk.html (accessed April 18, 2020).
TABLE 1 | Advice summary for endometriosis care during the COVID-19
pandemic and future considerations.
Be aware of the risks of the COVID-19 pandemic on endometriosis
patients
• Reduction in quality of life secondary to
◦Delayed diagnosis and treatment due to
the closure of outpatient clinical services (consultations, diagnostic
imaging, allied health appointments) and
the eventual increase in the waitlist for services once they resume.
◦The high degree of uncertainty of surgical or fertility interventions
Treatment options for patients with endometriosis
• Postponement of elective surgery and fertility therapy should be guided by
medical colleges and societies and made by governing bodies
• Continue current management if symptoms are stable or contact a healthcare
provider for changes to medication if symptoms are not well-managed
• Patients should seek telehealth appointments over in-person visits
• Patients with pain due to endometriosis may still consider the use of NSAIDs or
other over-the-counter analgesic medications
• Empirical medical therapy with hormonal medications is appropriate in the
absence of an imaging or surgical diagnosis
• Patients should consider the numerous complementary and alternative pain
management strategies available via telehealth services
Use of the emergency department
• Patients should use telehealth services as much as possible before resorting to
visiting the emergency department
Future considerations for endometriosis management
• Resumption of surgery and fertility therapy should be guided by medical
colleges and societies and made by governing bodies
• When surgery resumes, serious consideration should be given to:
◦Screening for COVID-19 pre-operatively
◦Adopting appropriate PPE behaviors
◦Mitigating release of aerosolized gas by modifying surgical techniques
• Telehealth services should be considered as a viable method of assessment
once routine outpatient services resume
• Self-management strategies should continue to be highly encouraged as
adjuncts to traditional management
• Preoperative triaging tools including advanced clinical algorithms and imaging
strategies should be implemented to avoid diagnostic laparoscopy and
multiple/repeated surgical procedures.
obliteration; whilst recognizing that at present superficial
peritoneal endometriosis is not reliably detected using imaging
(10,11). Non-endometriosis pathologies may also be diagnosed.
Knowledge of these entities has the potential to change clinical
management, so awareness of them is important. However, if
a patient is responding well to empiric treatment and does not
intend to alter management, it may be reasonable to proceed
without imaging. Laparoscopy as a diagnostic tool should be
avoided unless the intention is to simultaneously surgically treat
any endometriosis that is found (12). This could be considered
in those who are experiencing failed medical management, have
endometriosis-related infertility seeking to avoid or unable to
access assisted reproductive technologies, or simply prefer to
undergo surgery instead of using medical management.
Initially, caution in the use of non-steroidal anti-inflammatory
drugs (NSAIDs), commonly used for endometriosis-related
pain, was being advised (13). At present, the World Health
Organization states that there is no evidence of severe adverse
events, acute health care utilization, decreased long-term
survival, or diminished quality of life in patients with
COVID-19, as a result of the use of NSAIDs (14). As such,
Frontiers in Reproductive Health | www.frontiersin.org 2July 2020 | Volume 2 | Article 5
Leonardi et al. Endometriosis and the COVID-19 Pandemic
those with endometriosis-related pain who use NSAIDs can
continue to do so as needed, ensuring appropriate dosing
according to medication labels and/or healthcare providers,
bearing in mind that long-term use of NSAIDs come with
its own set of side-effects including peptic ulceration and
adverse impact on ovulation (2). Beyond traditional medical
therapies, problem-focused interventions such as education,
modifying work/school/social life, taking advantage of virtual
and telephone support provided by national endometriosis
organizations, improving sleep hygiene, low-intensity
physical activity (including pelvic exercises, yoga), dietary
changes, application of heat, and medical cannabis should
be considered, either with the assistance of a healthcare
provider via telehealth or independently by patients themselves
(15). Similarly, emotion-focused strategies, which include
relaxation/mindfulness, acceptance of chronic illness (e.g.,
via Acceptance and Commitment Therapy with the help
of a clinical psychologist through telehealth), reducing
catastrophizing, and improving a balance toward positive
attitude can be considered (15). These strategies are not
unique to the COVID-19 pandemic and are recognized as
an integral part of the usual multidisciplinary management
of endometriosis.
Patients should be aware that, if they experience acute
exacerbations of their chronic pain, they may warrant urgent
medical assessment, as such cases, especially those with suspected
endometrioma or severe acute recalcitrant exacerbation of pain,
may require urgent surgery. However, most pain exacerbations
are not life- or organ-threatening and with appropriate
counseling and support, a face-to-face consultation in the
emergency department may be avoided. Some GPs may find it
challenging to confidently reassure patients that they are safe
to avoid an emergency department visit, so urgent telehealth
consultation with a gynecologist or pain specialist may be
helpful. That said, we do not advocate for the avoidance of the
emergency department out of fear, so patients and providers
should continue to judiciously and safely use this service
when warranted.
ADVICE ON RESUMING PRE-PANDEMIC
“REGULAR” CARE FOR ENDOMETRIOSIS
As restrictions begin to lift, healthcare services, including
surgery for endometriosis, will resume. The decision about
when clinical care should resume will be determined by medical
colleges and societies, in compliance with governing bodies
informed by emerging viral disease pandemic experts. The
provision of appropriate medical and surgical care should
resume with an emphasis on safety for patients, healthcare
staff, and society. The American College of Surgeons (16), the
Royal College of Obstetricians and Gynaecologists (17), and
a collaborative effort by nine women’s health care societies
(18) outline important guidance for resuming surgical practice
and reintroducing these procedures. Though endometriosis is
a non-malignant disease, we believe it must be treated with
high priority due to the major impact it has on quality of
life (19). That said, facilities should employ a prioritization
policy committee, including a gynecologist with expertise in
managing the various facets of endometriosis (surgery, pain
management, fertility treatment), to ensure an appropriate
strategy is developed across all specialties. Amongst several
strategies (16), previously canceled and postponed endometriosis
surgeries should be prioritized. An objective priority scoring
tool could also be implemented [e.g., MeNTS instrument (20)].
Based on the procedure, disease type, and patient factors
that go into this scoring tool, endometriosis surgery would
be relatively low risk. Objectively judging the impact of a 2-
or 6-week delay on disease outcome is challenging as timing
surgical management (e.g., immediate vs. delayed) has never
been evaluated (21). It is unlikely for there to be a change
in the surgical difficulty/risk with a 2- or 6-week delay (22).
For urgent/emergency surgeries that have continued through
the COVID-19 pandemic, there has been discussion about the
safety of surgery based on theoretical evidence that aerosolization
of the virus can occur with ultrasonic/electrosurgery (23).
During this time, a minimally invasive surgical approach is
being recommended (24) and felt to be lower risk (20).
This COVID-19 specific recommendation aligns with the
typical approach to endometriosis preceding the pandemic.
Benefits include improved visibility of subtle endometriosis
lesions (and therefore targeted treatment), decreased blood
loss, reduced post-operative pain levels, and shorter in-hospital
stay post-operatively. We support the joint statement by
several gynecologic surgical societies, where expert opinion
recommendations on intraoperative precautions have been put
forward (25).
Adequate preoperative screening and diagnosis of SARS-CoV-
2 will be an important consideration for the resumption of
endometriosis surgery (26). Though most patients undergoing
surgery for endometriosis are relatively young and healthy,
we must be cognizant of the increased risk in those with
perioperative SARS-CoV-2 infection. It has recently been noted
that post-operative pulmonary complications occur in half of
the patients with perioperative SARS-CoV-2 infection and are
associated with high mortality (27).
At this time, we do not believe that the COVID-19 pandemic
warrants a sustained change in the overall medical approach
to the management of endometriosis (e.g., avoid surgery
and favor medical management). Regardless of a pandemic,
we encourage healthcare providers to comprehensively
counsel patients on the therapeutic options available for
each individual with endometriosis. The possible risks
and realistic scheduling obstacles secondary to COVID-19
must be part of this conversation, but patients should still
retain their autonomy to choose the option that is best
for them.
FUTURE CONSIDERATIONS
We believe that the COVID-19 pandemic can lead to sustained
improvements in the care for those with endometriosis. Firstly,
there may be an ongoing openness to telehealth (28). This
Frontiers in Reproductive Health | www.frontiersin.org 3July 2020 | Volume 2 | Article 5
Leonardi et al. Endometriosis and the COVID-19 Pandemic
could dramatically minimize the geographic barriers to care
that many women experience, and facilitate the development
of endometriosis networks of expertise, which is recommended
by the World Endometriosis Society (2). Telehealth may also
be an appropriate alternative for patients with pain that limits
their ability to travel to their healthcare provider in some
settings. Secondly, there may be increased awareness to self-
management strategies that have always existed, yet were
under-utilized (e.g., mindfulness, physical exercise, and diet)
until COVID-19 resulted in them becoming valuable tools for
patients (15). Finally, the current situation mandates a more
discerning approach to surgery now and in the future, so that
we “operate sparingly and operate well.” This approach can be
guided by preoperative triaging tools including advanced clinical
algorithms and imaging strategies (29) to avoid multiple repeated
surgical procedures.
AUTHOR’S NOTE
This manuscript has been released as a pre-print in
Authorea (30).
AUTHOR CONTRIBUTIONS
All authors meet justification criteria of authorship as per
ICMJE: substantial contributions to conception and design
or acquisition of data or analysis and interpretation of data,
drafting the article or revising it critically for important
intellectual content, final approval of the version to be published,
and agreement to be accountable for all aspects of the
work in ensuring that questions related to the accuracy or
integrity of any part of the work are appropriately investigated
and resolved.
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Disclaimer: This viewpoint article is endorsed by the World Endometriosis Society
(WES) and the International Federation of Fertility Societies (IFFS).
Conflict of Interest: ML reports grants from Australian Women and Children’s
Research Foundation, outside the submitted work. AH reports grants from Chief
Scientist Office, NIHR EME, MRC, Wellbeing of Women, Ferring, and Roche
Diagnostics during the conduct of the study; and honoraria for consultancy for
Ferring, Roche, and AbbVie, outside the submitted work. MA reports grants
from Metagenics and Spectrum outside the submitted work. SM reports a grant
and consulting fees from Abbvie, and consulting fees from Roche outside the
submitted work. LR reports personal fees from Monash IVF Group, grants from
Ferring Australia, personal fees from Ferring Australia, non-financial support
from Merck Serono, non-financial support from MSD, non-financial support
from Guerbet, outside the submitted work; and Minority shareholder and Group
Medical Director for Monash IVF Group and the President-Elect of the World
Endometriosis Society. HR reports personal fees from Olympus, personal fees
from Ethicon, personal fees from Nordic Pharma, personal fees from Plasma
Surgical Ltd., outside the submitted work. LH reports personal fees from AbbVie,
is the chief executive of the World Endometriosis Society, and the owner of
Endometriosis.org., outside the submitted work. GC reports personal fees from
Roche, personal fees from GE Healthcare, grants from Australian Women and
Children’s Research Foundation, outside the submitted work. NJ reports personal
fees from Guerbet, personal fees from Vifor Pharma, grants and personal fees
from Myovant Sciences, grants from AbbVie, personal fees from Roche, outside
the submitted work.
The remaining author declares that the research was conducted in the absence of
any commercial or financial relationships that could be construed as a potential
conflict of interest.
Copyright © 2020 Leonardi, Horne, Armour, Missmer, Roman, Rombauts,
Hummelshoj, Wattiez, Condous and Johnson. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other forums is permitted, provided the
original author(s) and the copyright owner(s) are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
terms.
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