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. 2022 Jun 30;227(5):735.e1–735.e25. doi: 10.1016/j.ajog.2022.06.052

Outcomes of gynecologic cancer surgery during the COVID-19 pandemic: an international, multicenter, prospective CovidSurg-Gynecologic Oncology Cancer study

Christina Fotopoulou a, Tabassum Khan b, Juraj Bracinik c, James Glasbey d, Nadeem Abu-Rustum e, Luis Chiva f, Anna Fagotti g, Keiichi Fujiwara h, Rahel Ghebre i, Murat Gutelkin j, Thomas O Konney k, Joseph Ng l, Rene Pareja m, Rajkumar Kottayasamy Seenivasagam n, Jalid Sehouli o, Shylasree TS Surappa p, Aneel Bhangu q, Elaine Leung r, Sudha Sundar s,; CovidSurg Gynecological Cancer Collaborators
PMCID: PMC9242690  PMID: 35779589

Abstract

Background

The CovidSurg-Cancer Consortium aimed to explore the impact of COVID-19 in surgical patients and services for solid cancers at the start of the pandemic. The CovidSurg-Gynecologic Oncology Cancer subgroup was particularly concerned about the magnitude of adverse outcomes caused by the disrupted surgical gynecologic cancer care during the COVID-19 pandemic, which are currently unclear.

Objective

This study aimed to evaluate the changes in care and short-term outcomes of surgical patients with gynecologic cancers during the COVID-19 pandemic. We hypothesized that the COVID-19 pandemic had led to a delay in surgical cancer care, especially in patients who required more extensive surgery, and such delay had an impact on cancer outcomes.

Study Design

This was a multicenter, international, prospective cohort study. Consecutive patients with gynecologic cancers who were initially planned for nonpalliative surgery, were recruited from the date of first COVID-19-related admission in each participating center for 3 months. The follow-up period was 3 months from the time of the multidisciplinary tumor board decision to operate. The primary outcome of this analysis is the incidence of pandemic-related changes in care. The secondary outcomes included 30-day perioperative mortality and morbidity and a composite outcome of unresectable disease or disease progression, emergency surgery, and death.

Results

We included 3973 patients (3784 operated and 189 nonoperated) from 227 centers in 52 countries and 7 world regions who were initially planned to have cancer surgery. In 20.7% (823/3973) of the patients, the standard of care was adjusted. A significant delay (>8 weeks) was observed in 11.2% (424/3784) of patients, particularly in those with ovarian cancer (213/1355; 15.7%; P<.0001). This delay was associated with a composite of adverse outcomes, including disease progression and death (95/424; 22.4% vs 601/3360; 17.9%; P=.024) compared with those who had operations within 8 weeks of tumor board decisions. One in 13 (189/2430; 7.9%) did not receive their planned operations, in whom 1 in 20 (5/189; 2.7%) died and 1 in 5 (34/189; 18%) experienced disease progression or death within 3 months of multidisciplinary team board decision for surgery. Only 22 of the 3778 surgical patients (0.6%) acquired perioperative SARS-CoV-2 infections; they had a longer postoperative stay (median 8.5 vs 4 days; P<.0001), higher predefined surgical morbidity (14/22; 63.6% vs 717/3762; 19.1%; P<.0001) and mortality (4/22; 18.2% vs 26/3762; 0.7%; P<.0001) rates than the uninfected cohort.

Conclusion

One in 5 surgical patients with gynecologic cancer worldwide experienced management modifications during the COVID-19 pandemic. Significant adverse outcomes were observed in those with delayed or cancelled operations, and coordinated mitigating strategies are urgently needed.

Key words: complications, COVID-19, delay, gynecologic cancer, pandemic, surgery

Introduction

The COVID-19 pandemic took the entire world off guard and led numerous healthcare systems to redesign their clinical services for the reallocation of available resources and accommodate the changes in treatment priorities.1, 2, 3, 4, 5, 6, 7, 8 This study was conducted when little was known about the true magnitude of the virus and when effective therapeutic strategies were lacking.2, 3, 4, 5, 6

AJOG at a Glance.

Why was this study conducted?

This is a large, prospective, international, gynecologic cancer cohort study summarizing the treatment alternations and their related impact on patients who were planned to have cancer surgery during the initial period of the COVID-19 pandemic (early 2020).

Key findings

In 20.7% (823/3973), care plans were changed compared with prepandemic practice, including operating in alternative hospitals, changes to perioperative systematic treatments, significant delay (>8 week; 11.2%; 424/3784), and cancellation (7.9%; 189/2430), which were associated with more frequent adverse outcomes.

What does this add to what is known?

With significant contribution in gynecologic cancer cases from low- and middle-income countries (26.9%; 1067/3973), this study provided important global data on the magnitude of care changes and the associated adverse outcomes experienced by patients with gynecologic cancer during the early stages of a global pandemic, which could be used to leverage resources for the ongoing mitigating strategies worldwide.

Women with gynecologic cancers were among the most affected populations during the pandemic, and patients appealed for more robust provision of high standard care, even in times of crisis.9 The pandemic has particularly challenged surgical care delivery for those with more advanced or relapsed disease, where surgery can be life-prolonging but not curative. Surgeries were being delayed or replaced by systemic or palliative care options that had previously been associated with poorer and less favorable outcomes.10 Moreover, other COVID-19-related events such as delayed diagnosis through the repeatedly imposed lockdowns, increased perioperative complications and mortality through the active COVID-19, and exhausted healthcare resources such as theater space and intensive care capacity were also observed.1, 2, 3, 4, 5, 6, 7 , 11

This study aimed to assess the early impact of the pandemic-related modifications to clinical management on the outcomes in surgical gynecologic cancer patients. We hypothesized that the COVID-19 pandemic had led to a delay in surgical cancer care, especially in patients who required more extensive surgery, and such delay had an impact on cancer outcomes. This study is an international prospective multicenter analysis of patients with gynecologic cancers treated during the pandemic.

Materials and Methods

Study design

This was a multicenter, international, prospective cohort study analyzing the clinical and surgical outcomes of patients with gynecologic cancer who had or were planned to have treatment as first line during the COVID-19 pandemic era. The study was part of the wider GlobalSurg-CovidSurg Consortium (https://globalsurg.org/CovidSurg/)—an umbrella study encompassing all solid cancer types and aiming to explore the impact of COVID-19 in surgical patients and services across multiple specialties.12 , 13 The study was prospectively registered (NCT04384926) and designed to inform clinical care as the pandemic evolves; the short study period encouraged wider participation at the time that resources were severely restricted owing to the competing needs to the pandemic.

Before the start of the study, each cancer group had the opportunity to add additional questions on the Case Report Form (CRF) to support the need to explore the impact of the COVID-19 pandemic particularly relevant to them. The gynecologic cancer group was particularly concerned about the impact of the pandemic on treatment adjustments and the subsequent clinical outcomes. The related outcomes are stated as secondary outcomes in this report to be consistent with the main CovidSurg-Cancer study.

Equivalent results of other cancer types and generic methods applying to all cancers (eg, inclusion criteria and patient identification) have been published previously.14 This study included hospitals that included all patients discussed for surgery regardless of whether they were operated on or not.

Any hospital that performed elective cancer surgery and was affected by the COVID-19 pandemic, was eligible to participate. The participating hospitals were identified by local principal investigators. Study approvals for participating hospitals were secured by local principal investigators before entry into the study and data collection. The study protocol was either registered as a clinical audit with institutional review or a research study obtaining ethical committee approval, depending on local and national requirements. Investigators were invited to identify a start date, representing the start of the emergence of COVID-19 in their respective hospitals.

All consecutive adult (age≥18 years) surgical patients with multidisciplinary team (MDT) decisions supporting surgery were captured by the participating centers (local principal investigators) from that point for the next 3 months (representing the first peak period of the COVID-19 pandemic). Only centers confirming the complete inclusion and follow-up of all nonoperated patients (labeled as “Group 1 hospitals” by the CovidSurg study team) were included in analyses comparing operated and nonoperated patients. The definition of lockdown stringency and the level of COVID-19 burden areas (classified as a median of at least 25 cases per 100,000 per 14 days, representing the World Health Organization [WHO] recommendations at the time of the study) were previously described.13 , 14

Patients and procedures

Inclusion criteria:

  • 1.

    Patients who underwent surgery for gynecologic cancer with curative or life-prolonging intent during the COVID-19 pandemic

or

  • 2.

    Patients with gynecologic cancer who would have been planned for curative or life-prolonging cancer surgery in the pre-COVID-era but had their surgery delayed or cancelled after multidisciplinary team discussions.

Exclusion criteria:

  • 1.

    Patients who were planned for palliative surgery or nonsurgical treatments

  • 2.

    Patients who were suspected of having or were confirmed to have SARS-CoV-2 infection at the time of the MDT decisions.

Consecutive eligible patients were identified from MDT meetings, operating lists, and outpatient or virtual clinics. The day of surgery was defined as day zero, with patients followed up for 30 days postoperatively using routine follow-up pathways. COVID-19 diagnosis was made through nasopharyngeal swab and polymerase chain reaction, computed tomography thorax, or clinical symptoms consistent with COVID-19.

Patients who had a therapeutic operation for suspected cancer that was subsequently shown to be a preinvasive or benign lesion after histologic examination and full organ resection (eg, high-grade dysplasia or carcinoma in situ) were still included in this study. Elective surgery was defined as any surgery booked in advance of a planned admission to hospital.15 The primary outcomes of the cross-specialty COVIDSurg study were the 30-day postoperative pulmonary complications (COVID-19 infection, pneumonia, acute respiratory distress syndrome, and unexpected ventilation), and they were previously reported.13

Key study outcomes of the gyneco-oncological cohort

The primary outcome of this analysis was as follows:

  • The incidence of pandemic-related changes in care

The secondary outcomes were as follows:

  • 1.

    30-day postoperative morbidity and mortality rates

  • 2.

    Postoperative hospital stay and critical care utilization rates

  • 3.

    Proportion of patients with the time between the decision for surgery to the date of surgery of >8 weeks. In the United Kingdom, the national target for providing cancer treatments from the time of the decision made by the MDT is 31 days (approximately 4 weeks). The 8-week cutoff was chosen to represent a significant delay in the time to surgery, as a recent meta-analysis suggested that a treatment delay for >4 weeks was associated with poorer cancer outcomes in a range of nongynecologic cancers.10

  • 4.

    Proportion of nonoperated patients with progression to incurable disease or death by 3 months after decision for surgery

  • 5.

    A composite outcome of unresectable disease or disease progression (eg, upstaging), emergency surgery, and death to measure the potential impact of any treatment delays or adjustment

Data collection and follow-up

Patients were recruited from the date of first COVID-19-related admission in each participating center for 3 months, as identified by the local investigators. The follow-up period was extended to 3 months from the time of study entry (when care decision was made) for each participant.

Anonymized data were collected online and stored on a secure server running the Research Electronic Data Capture (REDCap) web application16 based in the University of Birmingham, United Kingdom. The CRF of the CovidSurg-GO is presented as Supplemental Figure.

Supplemental Figure.

Supplemental Figure

Case Report Form for COVIDSurg-Cancer (gyneco-oncology)

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

Statistical analysis

The study was conducted according to guidelines set by the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement for observational studies.17 Chi-square tests were used to compare differences in categorical data apart from when cell sizes were small, when the Fisher exact tests were used. Continuous nonparametric data are presented as medians and interquartile ranges, and median differences between groups were compared using the Mann–Whitney U-test. Missing data are included in summary tables when applicable. Analysis was performed used Stata SE version 16.1 (StataCorp, College Station, TX) and open-source data science tools (Pandas Data Frame [Open-Source Software] and Python [Open-Source Software] using Juptyer notebook). The collected data were checked for consistency, cleaned, and exported. Vectorized operations were used when possible to archive fast turnaround time during the debugging phase. For visualization, the Matplotlib and Seaborn packages were used.

Results

Patients and tumor-related characteristics

We recruited a total of 3973 patients from 227 centers across 52 countries with the following geographic distribution: 2402 patients (60%) from Europe and Central Asia, 484 (12%) from Latin America & Caribbean, 376 (10%) from East Asia & Pacific, 277 (7%) from South Asia, 244 (6%) from North America, 160 (4%) from the Middle East and North Africa, and 24 (1%) from Sub-Saharan Africa (Table 1 ). Only 189 patients did not undergo surgery (4.8%); these were excluded from all analyses pertaining to surgical data alone.

Table 1.

Demographics and cancer related characteristics of all included patients—surgical and nonsurgical (n=3973)a

Uterus (n=1811) Ovary (n=1459) Cervix (n=462) Vulva/vagina (n=235) Total (n=3973)
Age (y)
 17–19 1 (0.1) 12 (0.8) 0 (0) 0 (0) 13 (0.3)
 20–29 7 (0.4) 65 (4.5) 24 (5.2) 4 (1.7) 100 (2.5)
 30–39 56 (3.1) 113 (7.8) 122 (26.4) 7 (3.0) 299 (7.5)
 40–49 175 (9.7) 265 (18.2) 144 (31.2) 22 (9.4) 608 (15.3)
 50–59 473 (26.1) 380 (26.1) 99 (21.4) 52 (22.1) 1004 (25.3)
 60–69 554 (30.6) 380 (26.1) 42 (9.1) 49 (20.9) 1027 (25.9)
 70–79 421 (23.3) 198 (13.6) 27 (5.8) 58 (24.7) 705 (17.7)
 80–89 119 (6.6) 46 (3.2) 4 (0.9) 41 (17.5) 210 (5.3)
 >90 5 (0.3) 0 (0) 0 (0) 2 (0.9) 7 (0.2)
Region
 Europe & Central Asia 1122 (62.0) 820 (56.2) 272 (58.9) 188 (80.0) 2408 (60.6)
 Latin America & Caribbean 201 (11.1) 180 (12.3) 85 (18.4) 18 (7.7) 484 (12.2)
 East Asia & Pacific 178 (9.8) 141 (9.7) 53 (11.5) 4 (1.7) 376 (9.5)
 South Asia 74 (4.1) 177 (12.1) 18 (3.9) 8 (3.4) 277 (7.0)
 North America 147 (8.1) 67 (4.6) 20 (4.3) 10 (4.3) 244 (6.1)
 Middle East & North Africa 81 (4.5) 70 (4.8) 4 (0.9) 5 (2.1) 160 (4.0)
 Sub-Saharan Africa 8 (0.4) 4 (0.27) 10 (2.2) 2 (0.9) 24 (0.6)
Income group
 High 1400 (77.3) 982 (67.3) 321 (69.5) 197 (83.8) 2906 (73.1)
 Upper middle 305 (16.8) 222 (15.2) 115 (24.9) 30 (12.8) 705 (17.7)
 Low-middle 106 (5.9) 255 (17.5) 26 (5.6) 8 (3.4) 362 (9.1)
BMI (kg/m2)
 <18.5 25 (1.4) 61 (4.2) 19 (4.1) 8 (3.4) 113 (2.8)
 18.5–24.9 496 (27.4) 683 (46.8) 228 (49.4) 86 (36.6) 1495 (37.6)
 25–29.9 531 (29.3) 423 (29.0) 125 (27.1) 73 (31.1) 1155 (29.1)
 30–34.9 363 (20.0) 184 (12.6) 57 (12.3) 37 (15.7) 642 (16.2)
 35–39.9 195 (10.8) 63 (4.3) 20 (4.3) 18 (7.7) 296 (7.5)
 ≥40 184 (10.2) 37 (2.5) 9 (2.0) 9 (3.8) 239 (6.0)
 Not available 17 (0.9) 8 (0.6) 4 (0.9) 4 (1.7) 33 (0.8)
WHO performance status
 0 1065 (58.8) 863 (59.2) 387 (83.8) 132 (56.2) 2448 (61.6)
 1 520 (28.7) 446 (30.6) 58 (12.6) 71 (30.2) 1095 (27.6)
 2 124 (6.9) 102 (7.0) 5 (1.1) 19 (8.1) 250 (6.3)
 3 20 (1.1) 13 (0.9) 0 (0) 4 (1.7) 37 (0.9)
 4 1 (0.1) 2 (0.1) 0 (0) 3 (1.3) 6 (0.2)
 Not available 81 (4.5) 33 (2.3) 12 (2.6) 6 (2.6) 137 (3.5)
CCI
 0 205 (11.3) 427 (29.3) 274 (59.3) 27 (11.5) 936 (23.6)
 1 387 (21.4) 356 (24.4) 86 (18.6) 42 (17.9) 871 (21.9)
 2 487 (26.9) 341 (23.4) 41 (8.9) 44 (18.7) 914 (23.0)
 3 410 (22.6) 212 (14.5) 37 (8.0) 48 (20.4) 707 (17.8)
 4 207 (11.4) 77 (5.3) 14 (3.0) 39 (16.6) 338 (8.5)
 5 76 (4.2) 31 (2.1) 1 (0.2) 21 (8.9) 130 (3.3)
 6 30 (1.7) 11 (0.8) 6 (1.3) 6 (2.6) 53 (1.3)
 7 5 (0.3) 2 (0.1) 1 (0.2) 6 (2.6) 14 (0.4)
 8 3 (0.2) 1 (0.1) 1 (0.2) 2 (0.9) 7 (0.2)
 9 1 (0.1) 1 (0.1) 1 (0.2) 0 (0) 3 (0.1)
ASA grade
 1 381 (21.0) 417 (28.6) 216 (46.8) 34 (14.5) 1048 (26.4)
 2 1013 (55.9) 786 (53.9) 205 (44.4) 137 (58.3) 2145 (54.0)
 3 402 (22.2) 240 (16.5) 39 (8.4) 61 (26.0) 743 (18.7)
 4 9 (0.5) 15 (1.0) 1 (0.2) 2 (0.9) 27 (0.7)
 5 1 (0.1) 0 (0) 1 (0.2) 0 (0) 2 (0.1)
 Not available 5 (0.3) 0 (0) 0 (0) 0 (0) 8 (0.2)
FIGO stage
 Not cancer 58 (3.2) 81 (5.6) 57 (12.3) 24 (10.2) 221 (5.6)
 1 1276 (70.5) 452 (31.0) 300 (64.9) 142 (60.4) 2173 (54.7)
 2 175 (9.7) 124 (8.5) 51 (11.0) 22 (9.4) 373 (9.4)
 3 202 (11.2) 555 (38.0) 45 (9.7) 37 (15.7) 839 (21.1)
 4 62 (3.4) 227 (15.6) 9 (2.0) 4 (1.7) 302 (7.6)
 Not available 38 (2.1) 20 (1.4) 0 (0) 6 (2.6) 65 (1.6)
Histology
 SCC 22 (1.2) 31 (2.1) 323 (69.9) 198 (84.3) 578 (14.6)
 Adenocarcinoma 1611 (89.0) 1116 (76.5) 118 (25.5) 9 (3.8) 2854 (71.8)
 GCST 13 (0.7) 110 (7.5) 0 (0) 3 (1.3) 127 (3.2)
 Other 139 (7.7) 34 (2.3) 7 (1.5) 18 (7.7) 198 (5.0)
 Benign/preinvasive/borderline 21 (1.2) 133 (9.1) 14 (3.0) 5 (2.1) 173 (4.4)
 Not available 5 (0.3) 35 (2.4) 0 (0) 2 (0.9) 43 (1.1)

Data are presented as total number (percentage). Details of operated vs non-operated group separately, are presented in Supplemental Table 2 and 4.

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; GCST, germ cell, sex cord stromal or trophoblastic tumors; NACT, neoadjuvant chemotherapy; SCC, squamous cell carcinoma; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Six patients (0.1%) did not have a recorded cancer site.

Almost half (n=1949; 49%) of the patients were ≥60 years old. Most of the patients had either uterine or ovarian cancer (n= 3270; 82%), were from high-income countries (n=2906; 73%), were either overweight or obese (n=2332; 59%), had a performance status of 0 (n=2448; 62%), had an American Society of Anaesthesiologists (ASA) grade of 1 or 2 (n=3193; 80%), and an International Federation of Gynaecology and Obstetrics (FIGO) stage 1 cancer (n=2173; 55%). The patient- and tumor-related characteristics are summarized in Table 1 and Supplemental Tables 1 and 2.

Approximately 1 in 13 (189/2430; 7.9%) operations were cancelled (Table 2 ). Those in low- and middle-income countries (LMICs; 36/156; 23%) who had stage 3 or 4 cancers (81/705; 11.5%), those in areas where there was a full lockdown (153/1339; 11%), and those in areas with low COVID-19 burden (53/321; 16%) were associated with a higher proportion of nonoperated patients. Table 2 includes only Group 1 hospitals, as they were the only ones that also included a nonoperated cohort to make a valid comparison of operated and nonoperated patients.

Table 2.

Comparison of operated and non-operated cohorts at hospitals that have included all patients discussed at tumor boards (group 1 hospitals; n=2430)

Non-operated (n=189) Operated (n=2241) Proportion not operated P value
Age (y)
 17–19 0 (0) 6 (0.3) 0/6 (0) .793
 20–29 6 (3.2) 53 (2.4) 6/59 (10.2)
 30–39 11 (5.8) 163 (7.3) 11/174 (6.3)
 40–49 24 (12.7) 297 (13.3) 24/321 (7.5)
 50–59 38 (20.1) 555 (24.8) 38/593 (6.4)
 60–69 49 (25.9) 584 (26.1) 49/633 (7.7)
 70–79 34 (18.0) 449 (20.0) 34/483 (7.0)
 80–89 26 (13.8) 130 (5.8) 26/156 (16.7)
 >90 1 (0.5) 4 (0.2) 1/5 (20)
Income group
 High 132 (69.8) 1885 (84.1) 132/2017 (6.5) .003
 Upper middle 21 (11.1) 236 (10.5) 21/257 (8.2)
 Low-middle 36 (19.1) 120 (5.4) 36/156 (23.1)
BMI (kg/m2)
 <18.5 4 (2.1) 53 (2.4) 4/57 (7.0) .933
 18.5–24.9 72 (38.1) 796 (35.5) 72/868 (8.3)
 25–29.9 43 (22.8) 636 (28.4) 43/679 (6.3)
 30–34.9 34 (18.0) 371 (16.6) 34/405 (8.4)
 35–39.9 12 (6.4) 198 (8.8) 12/210 (5.7)
 ≥40 19 (10.1) 160 (7.1) 19/179 (10.6)
 Not available 5 (2.7) 27 (1.2) 5/32 (15.6)
WHO performance status
 0 77 (40.7) 1408 (62.8) 77/1485 (5.2) .054
 1 79 (41.8) 601 (26.8) 79/680 (11.6)
 2 25 (13.2) 153 (6.8) 25/178 (14.0)
 3 4 (2.1) 24 (1.1) 4/28 (14.3)
 4 2 (1.1) 2 (0.1) 2/4 (50)
 Not available 2 (1.1) 53 (2.4) 2/4 (50)
CCI
 0 40 (21.2) 477 (21.3) 40/517 (7.7) .568
 1 28 (14.8) 475 (21.2) 28/503 (5.6)
 2 43 (22.8) 532 (23.7) 43/575 (7.5)
 3 28 (14.8) 424 (18.9) 28/452 (6.2)
 4 27 (14.3) 198 (8.8) 27/225 (12.0)
 5 10 (5.3) 86 (3.8) 10/96 (10.4)
 6 12 (6.3) 32 (1.4) 12/44 (27.3)
 7 1 (0.5) 9 (0.4) 1/10 (10)
 8 0 (0) 5 (0.2) 0/5 (0)
 9 0 (0) 3 (0.1) 0/3 (0)
ASA grade
 1 36 (19.1) 536 (23.9) 36/572 (6.3) .259
 2 91 (48.2) 1235 (55.1) 91/1326 (6.9)
 3 55 (29.1) 450 (20.1) 55/505 (10.9)
 4 3 (1.6) 16 (0.7) 3/19 (15.8)
 5 0 (0) 1 (<0.1) 0/1 (0)
 Not available 4 (2.1) 3 (0.1) 4/7 (57)
Cancer site
 Uterus 60 (31.8) 1036 (46.2) 60/1096 (5.5) .101
 Ovary 104 (55.0) 798 (35.6) 104/902 (11.5)
 Cervix 13 (6.9) 254 (11.3) 13/267 (4.9)
 Vagina/vulva 12 (6.4) 152 (6.8) 12/164 (7.3)
 Not available 0 (0) 1 (<0.1) 0/1 (0)
FIGO stagea
 Not cancer 9 (4.8) 121 (5.4) 9/130 (6.9) .044
 1 or 2 93 (49.2) 1440 (64.3) 93/1533 (6.1)
 3 or 4 81 (42.9) 624 (27.8) 81/705 (11.5)
 Not available 6 (3.2) 56 (2.5) 6/62 (9.7)
Lockdown stringency
 Full 153 (81.0) 1186 (52.9) 153/1339 (11.4) .001
 Moderate 29 (15.3) 457 (20.4) 29/486 (6.0)
 Light 7 (3.7) 598 (26.7) 7/605 (1.2)
COVID-19 burden
 High burden 136 (72.0) 1973 (88.0) 136/2109 (6.5) .008
 Low burden 53 (28.0) 321 (13.2) 53/321 (16.5)

Data presented as total number (percentage) or proportion (percentage).

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Comparison of those with cancer and FIGO-stage only.

The treatment intent, surgical details, and postoperative outcomes are summarized in Table 3 . The median time from MDT decision to surgery was 3 weeks (interquartile range, 1–5 weeks); 11.2% (424/3784) patients underwent surgery more than 8 weeks after the initial MDT decision.

Table 3.

Treatment intent, surgical details and postoperative outcomes of patients who underwent gynecologic cancer surgery (n=3784)

Uterus (n=1751) Ovary (n=1355) Cervix (n=449) Vulva/vagina (n=223) Total (n=3784) P value
Treatment intenta
 Curative 1669 (95.3) 1095 (80.8) 426 (94.8) 204 (91.5) 3400 (89.9) .977
 Life-prolonging 79 (4.5) 258 (19.0) 23 (5.1) 19 (8.5) 379 (10.0)
 Palliative 2 (0.1) 2 (0.2) 0 (0) 0 (0) 4 (0.1)
 Not available 1 (0.1) 0 (0) 0 (0) 0 (0) 1 (<0.1)
Neoadjuvant therapy
 Chemotherapy 29 (1.7) 279 (20.6) 15 (3.3) 5 (2.2) 328 (8.7) <.0001
 Radiotherapy 19 (1.1) 1 (0.1) 2 (0.5) 3 (1.4) 25 (0.7) .008
 Hormonal therapy 14 (0.8) 2 (0.1) 0 (0) 0 (0) 16 (0.4) .024
 Targeted therapy 0 (0) 4 (0.3) 0 (0) 0 (0) 4 (0.1) .127
 Other 0 (0) 1 (0.1) 0 (0) 0 (0) 1 (<0.1) .774
Time to operation 3 (1–5) 3 (1–5) 3 (1–5) 3 (2–5) 3 (1–5) <.0001
 ≤8 wk 1605 (91.7) 1142 (84.3) 405 (90.2) 202 (90.6) 3360 (88.8)
 >8 wk 146 (8.3) 213 (15.7) 44 (9.8) 21 (9.4) 424 (11.2)
Areas of surgical resectionb
 Pelvis/Perineal 1443 (82.4) 616 (45.5) 374 (83.3) 189 (84.8) 2624 (69.3) <.0001
 Midabdominal 122 (7.0) 430 (31.7) 6 (1.3) 4 (1.8) 562 (14.9)
 Upper-abdominal 120 (6.9) 171 (12.6) 27 (6.0) 1 (0.5) 319 (8.4)
 Others 66 (3.8) 138 (10.2) 42 (9.4) 29 (13.0) 279 (7.4)
Bowel surgery
 No 1734 (99.0) 1252 (92.4) 439 (97.8) 220 (98.7) 3651 (96.5) <.0001
 Yes 17 (1.0) 103 (7.6) 10 (2.2) 3 (1.4) 133 (3.5)
Approach
 Open 751 (42.9) 1101 (81.3) 292 (65.0) 204 (91.5) 2353 (62.2) <.0001
 Minimally-invasive 963 (55.0) 211 (15.6) 150 (33.4) 17 (7.6) 1342 (35.5)
 Converted 37 (2.1) 42 (3.1) 5 (1.1) 0 (0) 84 (2.2)
 Not available 0 (0) 1 (0.1) 2 (0.5) 2 (0.9) 5 (0.1)
Postoperative stay (d) 3 (1–5) 5 (3–8) 3 (1–5) 3 (2–6) 4 (2–6) .0001
30-d surgical morbidity
 Any complications 274 (15.7) 303 (22.4) 88 (19.6) 65 (29.2) 731 (19.3) <.0001
 Respiratory complications 18 (1.0) 32 (2.4) 4 (0.9) 4 (1.8) 58 (1.5) .030
 COVID-19 infection 7 (0.4) 14 (1.0) 1 (0.2) 0 (0) 22 (0.6) .087
 Wound infection 67 (3.8) 54 (4.0) 20 (4.4) 28 (12.6) 169 (4.5)
 Hemorrhage 44 (2.5) 78 (5.8) 7 (1.6) 2 (0.9) 131 (3.5) <.0001
 Ileus 25 (1.4) 52 (3.8) 12 (2.7) 0 (0) 89 (2.4) <.0001
 Urinary tract infection 25 (1.4) 29 (2.1) 18 (4.0) 5 (2.2) 77 (2.0) <.0001
 Wound dehiscence 30 (1.7) 11 (0.8) 5 (1.1) 25 (11.2) 71 (1.9) .016
 Sepsis 14 (0.8) 16 (1.2) 4 (0.9) 3 (1.3) 37 (1.0) <.0001
 Thromboembolism 12 (0.7) 17 (1.3) 0 (0) 1 (0.4) 30 (0.8) .817
 Kidney Injury 7 (0.4) 17 (1.3) 3 (0.7) 1 (0.4) 28 (0.7) .095
 Other organ injury 8 (0.5) 10 (0.7) 6 (1.3) 1 (0.4) 25 (0.7) .092
 Anastomosis leak 2 (0.1) 4 (0.3) 1 (0.2) 1 (0.4) 8 (0.2) .337
 Cardiac arrest 0 (0) 8 (0.6) 0 (0) 0 (0) 8 (0.2) .764
 Myocardial infarction 2 (0.1) 1 (0.1) 1 (0.2) 0 (0) 4 (0.1) .006
 Stroke 1 (0.1) 2 (0.1) 0 (0) 0 (0) 3 (0.1) .915
 Other complications 84 (4.8) 97 (7.2) 35 (7.8) 20 (9.0) 237 (6.3) .836.007
30-d surgical mortality 8 (0.5) 20 (1.5) 0 (0) 2 (0.9) 30 (0.8) .003

Six patients (0.1%) did not have a recorded cancer site. Data presented as total number (percentage) or median (interquartile range).

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Curative+life-prolonging vs palliative operation

b

Midabdominal=any operation involving mid-abdominal procedures, but not upper-abdominal surgery; Upper-abdominal=any operations involving upper-abdominal procedures.

Overall, 20.2% (279/1355) of ovarian cancer patients received neoadjuvant chemotherapy. Of those, 712/1355 (52.3%) had FIGO Stage III/IV disease. In this group, 253/712 (35.5%) had neoadjuvant chemotherapy, and 165/712 (23.2%) experienced a significant delay (>8 weeks) for their operations. In those who had FIGO Stage III/IV disease and experienced significant delays, 138/165 (83.6%) had neoadjuvant chemotherapy, compared with 115/547 (21.0%) for those who did not experience a delay (P<.0001). In those who had FIGO stage I/II disease and experienced significant delays (7.3%; 40/548), 10/40 (25.0%) had neoadjuvant chemotherapy compared with 15/508 (3.0%) for those who did not experience a delay (P<.0001).

Most areas of surgical resection were confined to the pelvis and/or perineum (2624/3784; 69%); 15% (562/3784) involved the midabdomen and 8.4% (319/3784) involved the upper abdomen. The overall bowel resection rate was 3.5% (133/3784). A minimally-invasive approach was applied in 35.5% of all patients (1342/3784) and in 55% (963/1751) and 33% (150/449) of uterine and cervical cancers, respectively.

The surgical 30-day morbidity and mortality profile of the surgical cohort is presented in Table 3. The overall complication rate was 19.3% (731/3784). The postoperatively confirmed COVID-19 infection rate was 0.6% (22/3784) in the entire surgical cohort. Patients with ovarian and uterine cancer represented 95% (21/22) of the entire COVID-19 infected group. Thirty (0.8%) patients died within 30 days of their operations.

Examining separately the surgical morbidity profile of the patients who acquired postoperative COVID-19 infections (Supplemental Table 4), significant differences were noted compared with the uninfected cohort, with a notable increase in respiratory complications (27.3% vs 1.4%; P<.0001), wound infection (18.2% vs 4.4%; P=.002), postoperative ileus (13.6% vs 2.3%; P<.0001), urinary tract infection (13.6% vs 2.0%; P<.0001), and anastomotic leak (for those who had bowel surgery, 1/4; 25% vs 7/129; 5.4%; P<.0001). The length of stay was significantly longer in the COVID-19-infected group (median of 8.5 days vs 4 days; P=.0001). The 30-day mortality rate was 18.2% (2/22) vs 0.7% (26/3762) in the COVID-19-infected and uninfected groups, respectively (P<.0001). Only 1 preoperative factor and 1 intraoperative factor were significantly associated with COVID-19 infection; they were WHO performance status (P=.003) and the rate of bowel resection (18.2% vs 3.4%; P<.0001). Multivariate modeling was not performed owing to the very low number of postoperative COVID-19 infections (n=22).

We also compared the patient characteristics and outcomes for those who had a prolonged hospital stay of ≥14 days. The cutoff is used for the continual National Health Service England audit that required mandatory data submission for every hospital in the United Kingdom. Those patients with poorer performance status and higher ASA score, higher disease stage, higher comorbidities index, having had an open surgery, respiratory complications, bowel surgery, and low COVID-19 burden had a higher risk of staying in the hospital longer than 14 days postoperatively (Supplemental Table 5).

When evaluating the impact of the COVID-19 pandemic on the type of treatment the patients received, we demonstrated that 20.7% (823/3973) of all patients (both operated and nonoperated) had their standard of care adjusted (Table 4 and Supplementary Table 3).

Table 4.

Summary of pandemic-related changes in care in operated patients by cancer type (n=3778)a

Uterus (n=1751) Ovary (n=1355) Cervix (n=449) Vulva/vagina (n=223) Total (n=3778) P value
Any change in care 332 (19.0) 201 (14.8) 58 (12.9) 43 (19.3) 634 (17.0) .001
Alternative hospitals 215 (12.3) 117 (8.6) 42 (9.4) 28 (12.6) 402 (10.6) .006
Delay to definitive surgery 198 (11.3) 115 (8.5) 34 (7.6) 34 (15.3) 381 (10.1) .001
Change of choice of operations 77 (4.4) 15 (1.1) 7 (1.6) 6 (2.7) 105 (2.8) <.0001
Expedited surgery 39 (2.2) 31 (2.3) 6 (1.3) 4 (1.8) 80 (2.1) .631
Non-routine use of neoadjuvant treatments 18 (1.0) 24 (1.8) 0 (0) 0 (0) 42 (1.1) .005
Neoadjuvant treatments not given 5 (0.3) 4 (0.3) 2 (0.5) 0 (0) 11 (0.3) .796
Longer neoadjuvant treatments 1 (0.1) 36 (2.7) 0 (0) 0 (0) 37 (1.0) <.0001
Shorter neoadjuvant treatments 2 (0.1) 15 (1.1) 0 (0) 0 (0) 17 (0.5) <.0001
Non-routine use of adjuvant treatments 4 (0.2) 3 (0.2) 1 (0.2) 0 (0) 8 (0.2) .918
Adjuvant treatments not given 14 (0.8) 4 (0.3) 4 (0.9) 0 (0) 22 (0.6) .145
Not recruited to a clinical trial 3 (0.2) 1 (0.1) 1 (0.2) 0 (0) 5 (0.1) .771
Recruited to a clinical trial (not routine) 2 (0.1) 0 (0) 0 (0) 0 (0) 2 (0.1) .509

Data presented as total number (percentage). Multiple changes were reported for each patient when appropriate.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Six patients (0.1%) did not have a recorded cancer site and were excluded from this table.

Patients in LMICs (76/326; 23.3%; P<.0001) and areas under full lockdown (P<.0001) had poorer performance status (P<.0001), more comorbidities (P=.024), higher ASA grade (P=.010), ovarian cancer (213/1355, 15.7%; P<.0001) and FIGO stage 3 or 4 diseases (198/1060, 18.7%; P<.0001) were more likely to have their operations more than 8 weeks after the initial decision (Table 5 ).

Table 5.

Comparisons of patients and outcomes who have received any operations by time to surgery (≤8 weeks vs >8 weeks; n=3784)

≤8 wk (n=3360) >8 wk (n=424) Proportion >8 wk P value
Age (y)
 17–19 12 (0.4) 1 (0.2) 1/13 (7.7) .165
 20–29 84 (2.5) 10 (2.4) 10/94 (10.6)
 30–39 259 (7.7) 29 (6.8) 29/288 (10.1)
 40–49 507 (15.1) 77 (18.2) 77/584 (13.2)
 50–59 853 (25.4) 113 (26.7) 113/966 (11.7)
 60–69 882 (26.3) 96 (22.6) 96/978 (9.8)
 70–79 603 (18.0) 68 (16.0) 68/671 (10.1)
 80–89 156 (4.6) 28 (6.6) 28/184 (15.2)
 >90 4 (0.1) 2 (0.5) 2/6 (33.3)
Income group
 High 2501 (74.4) 273 (64.4) 273/2774 (9.8) <.0001
 Upper middle 609 (18.1) 75 (17.7) 75/684 (11.0)
 Low-middle 250 (7.4) 76 (17.9) 76/326 (23.3)
BMI (kg/m2)
 <18.5 91 (2.7) 18 (4.3) 18/109 (16.5) .364
 18.5–24.9 1260 (37.5) 163 (38.4) 163/1423 (11.5)
 25–29.9 995 (29.6) 117 (27.6) 117/1112 (10.5)
 30–34.9 549 (16.3) 59 (13.9) 59/608 (9.7)
 35–39.9 250 (7.4) 34 (8.0) 34/284 (12.0)
 ≥40 190 (5.7) 30 (7.1) 30/220 (13.6)
 Not available 25 (0.7) 3 (0.7) 3/28 (10.7)
WHO performance status
 0 2152 (64.0) 219 (51.7) 219/2371 (9.2) <.0001
 1 858 (25.5) 158 (37.3) 158/1016 (15.6)
 2 189 (5.6) 36 (8.5) 36/225 (16.0)
 3 29 (0.9) 4 (0.9) 4/33 (12.1)
 4 4 (0.1) 0 (0) 0/4 (0)
 Not available 128 (3.8) 7 (1.7) 7/135 (5.2)
CCI
 0 791 (23.5) 105 (24.8) 105/896 (11.7) .024
 1 740 (22.0) 103 (24.3) 103/843 (12.2)
 2 789 (23.5) 82 (19.3) 82/871 (9.4)
 3 617 (18.4) 62 (14.6) 62/679 (9.1)
 4 266 (7.9) 45 (10.6) 45/311 (14.5)
 5 100 (3.0) 20 (4.7) 20/120 (16.7)
 6 37 (1.1) 4 (0.9) 4/41 (9.8)
 7 13 (0.4) 0 (0) 0/13 (0)
 8 5 (0.2) 2 (0.5) 2/7 (28.6)
 9 2 (0.1) 1 (0.2) 1/3 (33.3)
ASA grade
 1 917 (27.3) 95 (22.4) 95/1012 (9.4) .010
 2 1834 (54.6) 220 (51.9) 220/2054 (10.7)
 3 582 (17.3) 106 (25.0) 106/688 (15.4)
 4 21 (0.6) 3 (0.7) 3/23 (12.5)
 5 4 (0.1) 0 (0) 0/4 (0)
 Not available 2 (0.1) 0 (0) 0/2 (0)
Cancer site
 Uterus 1605 (47.8) 146 (34.4) 146/1751 (8.3) <.0001
 Ovary 1142 (34.0) 213 (50.2) 213/1355 (15.7)
 Cervix 405 (12.1) 44 (10.4) 44/449 (9.8)
 Vagina/vulva 202 (6.0) 21 (5.0) 21/223 (9.4)
 Not available 6 (0.2) 0 (0) 0/6 (0)
FIGO stage
 Not cancer 179 (5.3) 33 (7.8) 33/212 (15.6) <.0001
 1 or 2 2262 (67.3) 191 (45.1) 191/2453 (7.8)
 3 or 4 862 (25.7) 198 (46.7) 198/1060 (18.7)
 Not available 57 (1.7) 2 (0.5) 2/59 (3.4)
Lockdown stringency
 Full 1577 (46.9) 340 (80.2) 340/1917 (17.7) <.0001
 Moderate 853 (25.4) 51 (12.0) 51/904 (5.6)
 Light 839 (25.0) 22 (5.2) 22/861 (2.6)
COVID-19 burden
 High burden 2376 (70.7) 283 (66.8) 283/2659 (10.6) .240
 Low burden 917 (27.3) 131 (30.9) 131/1048 (12.5)
 Not available 67 (2.0) 10 (2.4) 10/77 (13.0)
Surgery performed
 Pelvis/perineal 2366 (70.4) 258 (60.9) 258/2624 (9.8) <.0001
 Midabdominal 451 (13.4) 111 (26.2) 111/562 (19.8)
 Upper-abdominal 291 (8.7) 28 (6.6) 28/319 (8.8)
 Others 252 (7.5) 27 (6.4) 27/279 (9.7)
Bowel surgery
 No 3251 (96.8) 400 (94.3) 400/3651 (11.0) .011
 Yes 109 (3.2) 24 (5.7) 24/133 (18.1)
Approach
 Open 2042 (60.8) 311 (73.4) 311/2353 (13.2) <.0001
 Minimally-invasive 1235 (36.8) 107 (25.2) 107/1342 (8.0)
 Converted 78 (2.3) 6 (1.4) 6/84 (7.1)
 Not available 5 (0.2) 0 (0) 0/5 (0)
Postoperative complication
 Any complications 640 (19.1) 91 (21.5) 91/731 (12.5) .235
 Respiratory complications 51 (1.5) 7 (1.7) 7/58 (12.1) .834
Mortality 26 (0.8) 4 (0.9) 4/30 (13.3) .711
Compositea 601 (17.9) 95 (22.4) 95/696 (13.7) .024

Data presented as total number (percentage) or proportion (percentage). For postoperative outcomes, data were collected at 30 days after the surgeries.

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

A composite outcome of unresectable disease or disease progression, emergency surgery and death.

In those who had an operation more than 8 weeks after the initial decision, the operations were more likely to be open surgery (P<.0001), involve midabdominal surgery (P<.0001), and require bowel resections (P=.011).

There was no significant difference in 30-day mortality (26/3360; 0.8% vs 4/424; 0.9%, P=0.771) in those who had delayed operations. However, a significance difference was observed for the composite of adverse outcomes owing to delay in operations, which included unresectable disease or disease progression, emergency surgery, and death (95/424; 22.4% vs 601/3360; 17.9%, P=.024), compared with those who had operations within 8 weeks of their MDT decisions.

In nonoperated patients (Supplementary Table 3) (189/2430; 7.9%), 1 in 20 (5/189; 2.7%) died within 3 months of MDT decision for surgery, and 1 in 5 (34/189; 18%) experienced disease progression and death.

Comment

Principal findings

This was a large prospective international study (with 1 in 4 participants from LMICs) to evaluate the impact of the COVID-19 crisis on the treatment delivery and outcomes of gynecologic cancer patients initially had plans for nonpalliative cancer surgery during the initial months of the pandemic. We demonstrated that 1 in 5 surgical gynecologic cancer patients had their standard of care adjusted as a result of the COVID-19 pandemic.

Although treatment alterations were not associated with a significant difference in 30-day postoperative mortality, significant delay (>8 weeks) in the time to surgery was associated with a composite of adverse outcomes (Table 5), including disease progression and death compared with those who did not experience a delay. In those in whom operation was cancelled, 1 in 5 had disease progression, and 1 in 20 died within 3 months of their MDT decisions.

Results in the context of what is known

Our results suggest that the surgical morbidity profile appeared to be equivalent to the historic surgical morbidity data outside of the COVID-19 pandemic18, 19, 20 in contrast to previous single-center data, suggesting higher morbidity rates.11 It is plausible that the modifications of surgical approaches have influenced the overall morbidity profile during the pandemic. For example, in patients undergoing colorectal cancer surgery,14 there was a significant increase in the overall rate of stoma formation (34.2% vs 27.2% in the prepandemic era), especially end stoma formation (70% vs 43.6% prepandemic).

Despite this study being conducted during the first wave of the COVID-19 pandemic, a low perioperative COVID-19 infection rate (0.6%) was observed. Our data appeared more favorable than the previously reported experience,13 , 14 , 21 with a lower incidence of postoperative COVID-19 infection (0.6% vs 3.8%) and lower 30-day mortality in the non-COVID19-infected patients’ cohort (0.7% vs 1.8%). Consistent with previous reports,13 , 14 , 21 patients infected with COVID-19 had a significantly longer postoperative stay and higher surgical morbidity and mortality (63.6% and 18.2%, respectively) than uninfected patients. The cause of the more favorable outcomes in patients with gynecologic cancer than previously reported experiences is likely to be multifactorial and could be related to the overall less radical surgical procedures. Only 3.5% of our operated patients underwent bowel resections, which is a surrogate marker of surgical radicality. Nevertheless, similar to previous reports,14 our data also confirmed that bowel resection was associated with higher risks of perioperative COVID-19 infection, other surgical morbidity, and longer hospitalization. These data consistently demonstrated the significant difference in surgical mortality between COVID-19-infected and uninfected patients, regardless of the type and site of surgery.

In addition to the well-established risk factor of prolonged hospital stay, we showed that low COVID-19 burden areas were associated with significantly higher rates of increased hospitalization (>14 days). It is possible that the healthcare systems that were least affected by the pandemic continued to operate for complex patients with a high disease burden, who in turn required a longer hospital stay.

Although published recommendations highlighted expected delays in gynecologic cancer delivery, the published evidence demonstrated some variations of the impact of COVID-19. For example, Bruce et al22 suggested that the number of referrals to gynecologic oncology decreased during the early stages of the pandemic, but the time to evaluation and treatment initiation were unaffected. In contrast, a number of surveys and retrospective cohort studies have described delays in consultations and treatments.23, 24, 25, 26 This study specifically evaluated the impact of the significant delay in the time to surgery on oncologic outcomes in patients with gynecologic cancers. One in 10 patients experienced significant delay (>8 weeks) to surgery (Table 5), particularly patients with ovarian cancer (213/1355; 15.7%), multiple comorbidities, stage III/IV disease (198/1060; 18.7%), and those in LMICs (76/326; 23.3%). A significant delay in time to surgery was associated with neoadjuvant chemotherapy use in patients with ovarian cancer (83.6% vs 21% for FIGO Stage III/IV disease; 25% vs 3.0% for FIGO stage I/II disease). The results highlighted this delay disproportionately affect those who required more complex surgery, at higher anesthetic risks and in areas where resources were scarce (LMICs and areas in full lockdown with subsequently low COVID-19 burden). Consistent with a previous systematic review,10 treatment delay was associated with poorer outcomes.

Strengths and limitations

This work evaluated the outcomes of the largest cohort of surgical gynecologic cancer patients during the COVID-19 pandemic. Our data covered all regions of the world to minimize geographic bias and generate conclusions that could be applied to different healthcare systems. It delivered a global view on cancer surgery delivery and outcomes—an area where comprehensive prospective data are scarce. Similar to other large-scale international datasets, this study includes heterogeneity between the cohorts; bias toward high-income countries; and significant variations in the surgical practice, pathways, and infrastructures; which made direct translation to practice for individual patients challenging.

There are very limited existing multicentered international studies with similar coverage of LMICs reporting detailed outcomes and complication rates of gynecologic cancer surgery.18, 19, 20 However, they had different classifications and recording methods compared with this current study. Therefore, direct comparison was inappropriate, which limited our ability to identify any change in the morbidity and mortality rates because of the COVID-19 pandemic.

The study and follow-up periods for CovidSurg-Cancer were deliberately short to encourage wider participations and a rapid turnover of data to inform practice. Although the comparison of a retrospective cohort could aid direct comparison of management adjustments and outcomes and it would have been performed in a single-center setting,11 the resources required to do so globally at the first peak of the pandemic could not be justified. We also acknowledge that post-MDT patient selections have contributed to the associations between surgical delay or cancellation and poorer outcomes, but the results highlight the need to target resources for those with complex care needs to ensure that they receive their planned urgent life-prolonging operations.

Clinical implications

Gynecologic cancer surgery during the early stages of the COVID-19 pandemic and before the availability of vaccination and effective treatments appeared to be safe, with a low risk of COVID-19 infection.14 With significant contribution from LMICs (26.9%; 1067/3973), these data also provide a global snapshot of the morbidity and mortality rates experienced by patients undergoing gynecologic cancer surgery. This study identified that a significant proportion of patients had their surgical plans delayed or cancelled, which was associated with poorer outcomes. The results represent an early and clear signal that robust mechanisms and pathways are urgently needed to ensure adequate cancer care even in times of crisis without detrimental oncologic compromise. With this large data set estimating the number of treatment plan alternations globally, the results could be used to coordinate plans and allocate resources as required to rescue and salvage the detrimental effects. Yet, few health systems have established consensus agreements to date.1 , 8 These results will also add to the evidence for future pandemics and the planning of relevant studies during a worldwide crisis in the future.

Research implications

The data were collected during the initial phase of the pandemic when the impingement of the virus was completely new, when none of the patients were vaccinated, and when protective measures were immature. Continued evaluation of the impact of the COVID-19 pandemic on cancer care delivery in the medium- and long-term is required. Population-based studies will be required to evaluate which patient subgroups (eg, cancer types or stage) were the most adversely affected. Comparative studies are also required to identify effective ways to mitigate the detrimental impact of the pandemic on cancer care.

Conclusions

The new rising incidence of COVID-19 worldwide owing to emerging variants combined with incomplete vaccination coverage has continued to disrupt healthcare delivery, and our results remain highly relevant. Despite the very low risk of perioperative COVID-19 infection, those infected had substantially poorer outcomes. The high rates of pandemic-related treatment plan modifications were associated with early negative impact on oncological outcomes. Robust strategies for the safe provision of surgical cancer care when the pandemic is transitioning into an endemic state are urgently needed.

Acknowledgments

We thank all contributing centers for their work on this study and for delivery care during the pandemic.

Footnotes

Additional members of the COVIDSurg Gynecological Cancer Collaborators have been listed in the Appendix.

E.L. and S.S. share senior authorship.

The authors report no conflict of interest.

The British Gynaecological Cancer Society supported this study with a small grant. N.A.R. is funded through the National Institutes of Health/National Cancer Institute Cancer Centre Support Grant P30 CA008748. The funders played no role in the design or interpretation of this study.

Cite this article as: Fotopoulou C, Khan T, Bracinik J, et al. Outcomes of gynecologic cancer surgery during the COVID-19 pandemic: an international, multicenter, prospective CovidSurg-Gynecologic Oncology Cancer study. Am J Obstet Gynecol 2022;227:735.e1-25.

Contributor Information

CovidSurg Gynecological Cancer Collaborators:

Dmitri Nepogodiev, Kwabena Siaw-Acheampong, Ruth A. Benson, Edward Bywater, Daoud Chaudhry, Brett E. Dawson, Jonathan P. Evans, James C. Glasbey, Rohan R. Gujjuri, Emily Heritage, Conor S. Jones, Sivesh K. Kamarajah, Chetan Khatri, Rachel A. Khaw, James M. Keatley, Andrew Knight, Samuel Lawday, Elizabeth Li, Harvinder S. Mann, Ella J. Marson, Kenneth A. McLean, Siobhan C. Mckay, Emily C. Mills, Gianluca Pellino, Maria Picciochi, Elliott H. Taylor, Abhinav Tiwari, Joana FF. Simoes, Isobel M. Trout, Mary L. Venn, Richard JW. Wilkin, Aneel Bhangu, Joana FF. Simoes, Tom EF. Abbott, Sadi Abukhalaf, Michel Adamina, Adesoji O. Ademuyiwa, Arnav Agarwal, Murat Akkulak, Ehab Alameer, Derek Alderson, Felix Alakaloko, Markus Albertsmeier, Osaid Alser, Muhammad Alshaar, Sattar Alshryda, Alexis P. Arnaud, Knut Magne Augestad, Faris Ayasra, José Azevedo, Brittany K. Bankhead-Kendall, Emma Barlow, David Beard, Ruth A. Benson, Ruth Blanco-Colino, Amanpreet Brar, Ana Minaya-Bravo, Kerry A. Breen, Chris Bretherton, Igor Lima Buarque, Joshua Burke, Edward J. Caruana, Mohammad Chaar, Sohini Chakrabortee, Peter Christensen, Daniel Cox, Moises Cukier, Miguel F. Cunha, Giana H. Davidson, Anant Desai, Salomone Di Saverio, Thomas M. Drake, John G. Edwards, Muhammed Elhadi, Sameh Emile, Shebani Farik, Marco Fiore, J Edward Fitzgerald, Samuel Ford, Tatiana Garmanova, Gaetano Gallo, Dhruva Ghosh, Gustavo Mendonça Ataíde Gomes, Gustavo Grecinos, Ewen A. Griffiths, Magdalena Gruendl, Constantine Halkias, Ewen M. Harrison, Intisar Hisham, Peter J. Hutchinson, Shelley Hwang, Arda Isik, Michael D. Jenkinson, Pascal Jonker, Haytham MA Kaafarani, Debby Keller, Angelos Kolias, Schelto Kruijff, Ismail Lawani, Hans Lederhuber, Sezai Leventoglu, Andrey Litvin, Andrew Loehrer, Markus W. Löffler, Maria Aguilera Lorena, Maria Marta Modolo, Piotr Major, Janet Martin, Hassan N. Mashbari, Dennis Mazingi, Symeon Metallidis, Ana Minaya-Bravo, Helen M. 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Al-Sarireh, Clancy R, Cripps P, Dobbs T, Egan R, Fabre I, Harries R, Henry A, Kittur M, Li Z, Parkins K, Soliman F, Spencer N, Thompson D, Burgess C, Gemmell C, Grieco C, Hollyman M, Hunt L, Morrison J, Ojha S, Abbadessa F, Barnard S, Chan C, Dawe N, Hammond J, Koshy RM, Mahmoud Ali F, McPherson I, Mellor C, Moir J, Pandanaboyana S, Powell J, Rai B, Rogers A, Roy C, Sachdeva A, Saleh C, Tingle S, Williams T, Manickavasagam J, McDonald C, McGrath N, McSorley N, Ragupathy K, Ramsay L, Solth A, Aristotelous C, Kakisi O, Seebah K, Shaikh I, Sreedharan L, Touil L, Youssef M, Shah J, Ameerally P, Baguley M, Gnanachandran C, Heer B, Rogers M, Woods R, Aujayeb A, Mills S, Abu J, E. Addae-Boateng, Bratt D, Brock L, Burnside N, S. Cadwell-Sneath, Gajjar K, Gan C, Grundy C, Hallam K, Hassell K, Hawari M, Joshi A, Khout H, Konstantinidi K, R.X.N. Lee, Nunns D, Schiemer R, Walton T, Weaver H, Whisker L, Williamson K, McVeigh J, Myatt R, M.A. Williams, Ahmed ME, Bukhari SI, Illingworth B, Kanthasamy S, Knights E, Ong SL, Pujari R, Tan KHM, Vanker R, Michel M, Patil S, Ravindran S, Sarveswaran J, Scott L, Biliatis I, Edmond M, King E, Babawale O, Hodgson D, Ismail M, Khan J, Lokman U, Phan YC, Almond M, Bhangu A, Breik O, Cato LD, Chowdhury YA, Desai A, Ford S, Griffiths E, Idle M, Kamal M, Karia K, Kisiel A, Kulkarni R, Mak JKC, Martin T, Nankivell P, Parente A, Parmar S, A.M. Pathanki, Phelan L, Praveen P, Saeed S, Sharma N, Singh J, Solomou G, Soon WC, Stevens A, Tirotta F, Topham C, Ughratdar I, Vijayan D, Ballantyne K, Barker L, Chapman K, Charalambous M, Chianakwalam C, English C, Evans J, Fell A, Frimpong D, Halkias C, Iyer R, Merh R, Neagu G, Nikolaou S, Poddar A, Pronisceva V, Reddy V, Williams N, Alakandy L, Bhattathiri P, Brown J, Canty M, Day E, Geddes A, Grivas A, Hassan S, Lammy S, Littlechild P, Maseland C, Mathieson C, McCaul J, McMahon J, O’Kane R, St. George E, Suttner N, Taylor W, Tilling E, English W, Kaul S, Khan AH, Khan F, Mansuri A, Mukherjee S, Patel M, Sarigul M, Singh S, Smith C, Tan KL, Vulliamy P, Woodham A, Yang YH, Adiamah A, Brewer H, Chowdhury A, Evans J, Humes D, Jackman J, Koh A, C. Lewis-Lloyd, Navarro A, Oyende O, Reilly J, Vohra R, Worku D, Cool P, Cribb G, Shepherd K, Bisset C, Moug S, Chadha R, Elson N, Galleano R, Faulkner G, Langone A, Panayi Z, Saleh P, Tuminello F, Underwood C, Brixton G, Findlay L, Klatte T, Majkowska A, Manson J, Potter R, W. Al-Khyatt, Awad S, Bhalla A, Chia Z, Daliya P, Goyal A, Grimley E, Hamad A, Kumar A, Malcolm FL, Ng JCK, Phillips A, Theophilidou E, Williams S, Bowden J, Campain N, Daniels I, Evans C, Fowler G, John J, Massey L, McDermott F, McGrath J, McLennan A, Ng M, Pascoe J, Rajaretnam N, Angamuthu N, Bulathsinhala S, Chowdhury S, Davidson B, Fusai G, Gilliland J, Hart C, Hidalgo Salinas C, Knowles J, Machairas N, Mirnezami R, Pissanou T, Pollok JM, Raptis DA, Soggiu F, Tzerbinis H, Varcada M, Xyda S, Beamish A, Davies E, Foulkes R, Magowan D, Nassa H, Ooi R, Price C, Smith L, Solari F, Tang A, Williams G, Abd Kahar NN, Y. Al-Tamimi, Bacon A, Beasley N, Catto J, Chan LH, Chew D, Crank M, Ilenkovan N, Macdonald M, Narice B, Rominiyi O, Saad S, Sinha S, Thompson A, Varley I, Brennan P, Drake T, Harrison EM, Linder G, Mayes J, McGregor R, Pasricha R, Skipworth RJE, Zamvar V, Davies E, Hawkin P, Raymond T, Ryska O, Baron R, Dunne D, Gahunia S, Halloran C, Howes N, McKinney R, McNicol F, Rajput K, Russ J, Sutton R, Szatmary P, Tan JR, Thomas A, Whelan P, Anzak A, Banerjee A, Fuwa O, Hughes F, J.D. Jayasinghe, Knowles C, Kocher HM, Leal Silva I, Ledesma FS, Minicozzi A, Navaratne L, Patki P, Rahman R, Ramamoorthy R, Sohrabi C, Tanabalan C, Thaha M, Thakur B, Venn M, Yip V, Baumber R, Parry J, Evans S, Jeys L, Morris G, Parry M, Stevenson J, Ahmadi N, Aresu G, Z.M. Barrett-Brown, Coonar A, Durio Yates H, Gearon D, Hogan J, King M, Peryt A, Pradeep IS, Smith C, Adishesh M, Atherton R, Baxter K, Brocklehurst M, Chaudhury M, Krishnamohan N, McAleer J, Owens G, Parkin E, Patkar P, Phang I, Aladeojebi A, Ali M, Ali S, Barmayehvar B, Gaunt A, Gowda M, Halliday E, Kitchen M, Mansour F, Nanjaiah P, Thomas M, Zakai D, N. Abbassi-Ghadi, Assalaarachchi H, Currie A, Flavin M, Frampton A, Hague M, Hammer C, Hopper J, Horsnell J, Humphries S, Kamocka A, Madhuri TK, Preston S, Singh P, Stebbing J, Tailor A, Walker D, Coomber E, Jaunoo S, Kennedy L, Williams O, Airey A, Bunni J, Crowley R, Fairhurst K, Frost J, George R, Lee S, Mitchell S, Phull J, Richards S, Aljanadi F, Campbell A, Glass A, Hraishawi I, Jones M, McIlmunn C, McIntosh S, Mhandu P, O’Donnell C, Turkington R, Z. Al-Ishaq, Bhasin S, Bodla AS, Burahee A, Crichton A, A. El-Ghobashy, Fossett R, Pigadas N, Rahman E, Snee D, Vidya R, Yassin N, Colombo F, Fountain D, M.T. Hasan, Karabatsou K, Laurente R, Pathmanaban O, Barlow C, Ding D, Foster J, Longstaff L, C. Brett-Miller, Buruiana FE, Kaur R, Leung E, Sundar S, Al-mukhtar A, Brown S, Edwards J, Giblin A, Kelty C, Lee M, Lye G, Newman T, Sharkey A, Steele C, Sureshkumar Shah N, Whitehall E, Blair J, Lakhiani A, W. Parry-Smith, Sahu B, Athwal R, Baker A, Jones L, Konstantinou C, Ramcharan S, Singh S, Vatish J, Wilkin R, Alzetani A, Amer K, Badran A, Colvin HV, Ethunandan M, Sekhon GK, Shakoor Z, Shields H, Singh R, Talbot T, Wensley F, Lawday S, Lyons A, Newman S, Chung E, Hagger R, Hainsworth A, Hunt I, Karim A, Owen H, Ramwell A, Santhirakumaran G, Smelt J, Tan C, Vaughan P, Williams K, Baker C, Davies A, Gossage J, Kelly M, Knight W, Bromage S, Hall J, Kaushik V, Rudic M, Vallabh N, Zhang Y, Harris G, James G, Kang C, Lin DJ, Rajgor AD, Royle T, Scurrah R, Steel B, Watson LJ, Kocher HM, Choi D, Hutchison R, Jain A, Luoma V, Marcus HJ, May R, Menon A, Pramodana B, Webber L, Hayes A, Jones R, Sivarajah G, Smith M, Smrke A, Strauss D, Abouelela FAM, Aneke IA, Asaad P, Brown B, Collis J, Duff S, Khan A, Moura F, Taylor M, Wadham B, Warburton H, Elmoslemany T, M.D. Jenkinson, Millward CP, Zakaria R, Mccluney S, Parmar C, Shah S, Allison J, M.S. Babar, Bowen J, Collard B, Goodrum S, Lau K, Patel A, Sargent M, Scott R, Thomas E, Whitmore H, Balasubramaniam D, Jayasankar B, Kapoor S, Ramachandran A, Semple C, Elhamshary A, Imam SMB, Kapriniotis K, Kasivisvanathan V, Lindsay J, S. Rakhshani-Moghadam, Beech N, Chand M, Green L, Kalavrezos N, Kiconco H, McEwen R, Schilling C, Sinha D, Pereca J, Singh J, Chopra S, Egbeare D, Thomas R, Arumugam S, Ibrahim B, Khan K, Combellack T, Hill G, Jones S, Kornaszewska M, Mohammed M, Tahhan G, Valtzoglou V, Williams J, Blencowe N, Eskander P, Gash K, Gourbault L, Hanna M, Maccabe TA, Main B, Olivier J, Newton C, Roswadowski S, Ryan N, Teh E, West D, Al-omishy H, Baig M, Bates H, Di Taranto G, Dickson K, Dunne N, Gill C, Howe D, Jeevan D, Khajuria A, A. Martin-Ucar, McEvoy K, Naredla P, Ng V, Robertson S, Sait M, Sarma DR, Shanbhag S, Shortland T, Simmonds S, Skillman J, Tewari N, Walton G, M.A. Akhtar, Brunt A, McIntyre J, Milne K, Rashid MM, Sgrò A, Stewart KE, Turnbull A, A.K. Abou-Foul, Gossedge G, O’Donnell S, Oldfield F, Thomson S, Aguilar Gonzalez M, Talukder S, Boyle C, Fernando D, Gallagher K, Laird A, Tham D, Bath M, Patki P, Sohrabi C, Tanabalan C, Basnyat P, Davis H, Montauban P, Shrestha A, Agarwal K, Arif T, Magee C, Nambirajan T, Powell S, Vinayagam R, Flindall I, Hanson A, Mahendran V, Green S, Lim M, MacDonald L, Miu V, Onos L, Sheridan K, Young R, Alam F, Griffiths O, Houlden C, Jones R, Kolli VS, Lala AK, Leeson S, Peevor R, Seymour Z, Consorti E, Gonzalez R, Grolman R, R. Kwan-Feinberg, Liu T, Merzlikin O, San Francisco, Brown A, Cooper Z, Hirji S, Jolissaint J, Mahvi D, Okafor B, Raut CP, Roxo V, Salim A, Bessen S, Chen L, Dagrosa L, Fay K, Fleischer C, Hasson R, Henderson E, Leech M, Loehrer A, Markey C, Paydarfar J, Rosenkranz K, Telma K, Tocci N, I. Wilkinson-Ryan, Wilson M, Bokenkamp M, Brown K, Fleming D, Haynes A, Heron C, Hill C, Kay H, Leede E, McElhinney K, Olson KA, Osterberg EC, Riley C, Srikanth P, Barbour J, Blazer D, DiLalla GA, Fayanju O, Hwang ES, Kahmke R, Kazaure H, Lazarides A, Lee W, Lidsky M, Menendez C, Moris D, Plichta J, Pradhan MC, Puscas L, Rice HE, Rocke D, Rosenberger L, Scheri R, B.D. Smith, M.T. Stang, Tolnitch L, Turnage K, Visgauss J, Walton FS, Watts T, Zani S, Farma J, Cardona K, Russell MC, Clark J, Kwon D, Goel N, Kronenfeld J, Bigelow B, Etchill E, A. Gabre-Kidan, Jenny H, Kent A, Ladd MR, Long C, Malapati H, Margalit A, Rapaport S, Rose J, Stevens K, Tsai L, Vervoort D, Yesantharao P, Dehal A, Klaristenfeld D, Huynh K, Kaafarani H, Naar L, Qadan M, Brown L, Ganly I, Mullinax JE, Alpert N, Gillezeau C, F.A.C.S.B.A. Miles DDS MD, Taioli E, Cha DE, Gleeson E, Horn C, Sarpel U, Gusani N, Hazelton J, Maines J, Oh JS, Ssentongo A, Ssentongo P, Bhama A, Colling K, Najarian M, Azam M, Choudhry A, Marx W, Abedin Y, Arzumanov G, Chokshi R, Gabrilovich S, Glass N, Kalyoussef E, F.P. Parvin-Nejad, Roden D, Stein J, A. Suarez-Ligon, Tsui G, Zhao K, Fleming J, Fuson A, Gigliotti J, Ovaitt A, Ying Y, Abel MK, Andaya V, Bigay K, M.A. Boeck, Chen L, Chern H, Corvera C, I. El-Sayed, Glencer A, Ha P, B.C.S. Hamilton, Heaton C, Hirose K, D.M. Jablons, Kirkwood KS, Kornblith LZ, Kratz JR, Lee RH, Miller PN, Nakakura EK, B. Nunez-Garcia, O’Donnell RJ, Ozgediz D, Park P, Robinson B, Sarin A, Sheu B, Varma MG, Wai KC, Wustrack R, Xu MJ, Zimel M, San Francisco, CA) Beswick D, Goddard J, Manor J, Song J, Denver/Colorado Springs/Loveland, Cioci A, Pavlis W, Rakoczy K, Ruiz G, Saberi R, Fullmer T, Gaskill C, Gross N, Kiong K, Roland CL, Zafar SN, Abdallah M, Abouassi A, Aigbivbalu E, Almasri M, Eid J, George B, Kulkarni G, Marwan H, Mehdi M, San Andrés M, Sundaresan J, Aoun SG, Ban VS, Batjer HH, Bosler K, Caruso J, Sumer B, Abbott D, Acher A, Aiken T, Barrett J, Foley E, Schwartz PB, Zafar SN, Hawkins AT, Maiga A, Ruzgar NM, Sion M, Ullrich S, Laufer J, Scasso S, H. Al-Naggar, M. Al-Shehari, Almassaudi A, Alsayadi M, Alsayadi R, Nahshal M, Shream S, AL-Ameri S, and Aldawbali M

Appendix

Supplemental Table 1.

Demographics of patients who underwent any operations (n=3778)a

Uterus (n=1751) Ovary (n=1355) Cervix (n=449) Vulva/vagina (n=223) Total (n=3778)
Age (y)
 17–19 1 (0.1) 12 (0.9) 0 (0) 0 (0) 13 (0.3)
 20–29 7 (0.4) 60 (4.4) 23 (5.1) 4 (1.8) 94 (2.5)
 30–39 53 (3.0) 106 (7.8) 121 (27.0) 7 (3.1) 287 (7.6)
 40–49 172 (9.8) 246 (18.2) 142 (31.6) 22 (9.9) 582 (15.4)
 50–59 460 (26.3) 362 (26.7) 96 (21.4) 48 (21.5) 966 (25.6)
 60–69 539 (30.8) 353 (26.1) 37 (8.2) 47 (21.1) 976 (25.8)
 70–79 409 (30.8) 179 (13.2) 26 (5.8) 56 (25.1) 670 (17.7)
 80–89 106 (6.1) 37 (2.7) 4 (0.9) 37 (16.6) 184 (4.9)
 >90 4 (0.2) 0 (0) 0 (0) 2 (0.9) 6 (0.2)
Region
 Europe & Central Asia 1078 (61.6) 756 (55.8) 268 (59.7) 177 (79.37) 2279 (60.3)
 Latin America & Caribbean 196 (11.1) 174 (12.8) 81 (18.0) 17 (7.6) 467 (12.4)
 East Asia & Pacific 178 (10.2) 141 (10.4) 50 (11.1) 4 (1.8) 373 (9.9)
 South Asia 73 (4.2) 150 (11.1) 18 (4.0) 8 (3.6) 249 (6.6)
 North America 142 (8.1) 65 (4.8) 20 (4.5) 10 (4.5) 237 (6.3)
 Middle East & North Africa 79 (4.5) 65 (4.8) 4 (0.9) 5 (2.2) 153 (4.1)
 Sub-Saharan Africa 6 (0.3) 4 (0.3) 8 (1.8) 2 (0.9) 20 (0.5)
Income group
 High 1351 (77.2) 914 (67.5) 317 (70.6) 186 (83.4) 2768 (73.3)
 Upper middle 298 (17.0) 249 (18.4) 108 (24.1) 29 (13.0) 684 (18.1)
 Low-middle 102 (5.8) 192 (14.2) 24 (5.4) 8 (3.6) 326 (8.6)
BMI (kg/m2)
 <18.5 24 (1.4) 58 (4.3) 19 (4.2) 8 (3.6) 109 (2.9)
 18.5–24.9 482 (27.5) 637 (47.0) 222 (49.4) 80 (35.9) 1421 (37.6)
 25–29.9 520 (29.7) 393 (29.0) 125 (27.8) 71 (31.8) 1109 (29.4)
 30–34.9 350 (20.0) 170 (12.6) 52 (11.6) 35 (15.7) 607 (16.1)
 35–39.9 188 (10.7) 59 (4.4) 20 (4.5) 17 (7.6) 284 (7.5)
 ≥40 174 (9.9) 31 (2.3) 7 (1.6) 9 (4.0) 220 (5.8)
 Not available 14 (0.8) 7 (0.5) 4 (0.9) 3 (1.4) 28 (0.7)
WHO performance status
 0 1045 (59.7) 815 (60.2) 380 (84.6) 130 (58.3) 2370 (62.7)
 1 491 (28.0) 409 (30.2) 53 (11.8) 63 (28.3) 1016 (26.9)
 2 115 (6.6) 87 (6.4) 4 (0.9) 19 (8.5) 225 (6.0)
 3 18 (1.0) 11 (0.8) 0 (0) 4 (1.8) 33 (0.9)
 4 1 (0.1) 1 (0.1) 0 (0) 2 (0.9) 4 (0.1)
 Not available 81 (4.6) 32 (2.4) 12 (2.7) 5 (2.2) 130 (3.4)
CCI
 0 200 (11.4) 396 (29.2) 270 (60.1) 27 (12.1) 893 (23.6)
 1 378 (21.6) 340 (25.1) 85 (18.9) 40 (17.9) 843 (22.3)
 2 477 (27.2) 317 (23.4) 35 (7.8) 41 (18.4) 870 (23.0)
 3 398 (22.7) 199 (14.7) 36 (8.0) 46 (20.6) 679 (18.0)
 4 196 (11.2) 64 (4.7) 13 (2.9) 37 (16.6) 310 (8.2)
 5 71 (4.1) 28 (2.1) 1 (0.2) 19 (8.5) 119 (3.2)
 6 23 (1.3) 7 (0.5) 6 (1.3) 5 (2.2) 41 (1.1)
 7 4 (0.2) 2 (0.2) 1 (0.2) 6 (2.7) 13 (0.3)
 8 3 (0.2) 1 (0.1) 1 (0.2) 2 (0.9) 7 (0.2)
 9 1 (0.1) 1 (0.1) 1 (0.2) 0 (0) 3 (0.1)
ASA grade
 1 375 (21.4) 392 (28.9) 212 (47.2) 33 (14.8) 1012 (26.8)
 2 991 (56.6) 729 (53.8) 199 (44.3) 131 (58.7) 2050 (54.3)
 3 374 (21.4) 221 (16.3) 36 (8.0) 56 (25.1) 687 (18.2)
 4 8 (0.5) 13 (1.0) 1 (0.2) 2 (0.9) 24 (0.6)
 5 1 (0.1) 0 (0) 1 (0.2) 0 (0) 2 (0.1)
 Not available 2 (0.1) 0 (0) 0 (0) 1 (0.5) 3 (0.1)
FIGO Stage
 Not cancer 57 (3.3) 76 (5.6) 57 (12.7) 21 (9.4) 211 (5.6)
 1/2 1406 (80.3) 548 (40.4) 339 (75.5) 156 (70.0) 2449 (64.8)
 3/4 255 (14.6) 712 (52.6) 53 (11.8) 40 (17.9) 1060 (28.1)
 Not available 33 (1.9) 19 (1.4) 0 (0) 6 (2.7) 58 (1.5)
Histology
 SCC 22 (1.3) 31 (2.3) 310 (69.0) 188 (84.3) 551 (14.6)
 Adenocarcinoma 1554 (88.8) 1030 (76.0) 118 (26.3) 9 (4.0) 2711 (71.8)
 GCST 13 (0.7) 106 (7.8) 0 (0) 3 (1.4) 122 (3.2)
 Other 137 (7.8) 34 (2.5) 7 (1.6) 17 (7.6) 195 (5.2)
 Benign/preinvasive/borderline 21 (1.2) 129 (9.6) 14 (3.1) 4 (1.8) 168 (4.5)
 Not available 4 (0.2) 25 (1.9) 0 (0) 2 (0.9) 31 (0.8)

Data are presented as total number (percentage). Details of operated vs non-operated group separately, are presented in Supplemental Tables 2 and 4.

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; GCST, germ cell, sex cord stromal or trophoblastic tumors; NACT, neoadjuvant chemotherapy; SCC, squamous cell carcinoma; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Six patients (0.1%) did not have a recorded cancer site and were excluded from this table.

Supplemental Table 2.

Demographics of patients did not undergo any operations (n=189)

Uterus (n=60) Ovary (n=104) Cervix (n=13) Vulva/vagina (n=12) Total (n=189)
Age (y)
 17–19 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
 20–29 0 (0) 5 (4.8) 1 (7.7) 0 (0) 6 (3.2)
 30–39 3 (5.0) 7 (6.7) 1 (7.7) 0 (0) 11 (5.8)
 40–49 3 (5.0) 19 (18.3) 2 (15.4) 0 (0) 24 (12.7)
 50–59 13 (21.7) 18 (17.3) 3 (23.1) 4 (33.3) 38 (20.1)
 60–69 15 (25.0) 27 (26.0) 5 (38.5) 2 (16.7) 49 (25.9)
 70–79 12 (20.0) 19 (18.3) 1 (7.7) 2 (16.7) 34 (18.0)
 80–89 13 (21.7) 9 (8.7) 0 (0) 4 (33.3) 26 (13.8)
 >90 1 (1.7) 0 (0) 0 (0) 0 (0) 1 (0.5)
Region
 Europe & Central Asia 44 (73.3) 64 (61.5) 4 (30.8) 11 (91.7) 123 (65.1)
 Latin America & Caribbean 6 (10.0) 6 (5.8) 4 (30.8) 1 (8.3) 17 (9.0)
 East Asia & Pacific 0 (0) 0 (0) 3 (23.1) 0 (0) 3 (1.6)
 South Asia 1 (1.7) 27 (26.0) 0 (0) 0 (0) 28 (14.8)
 North America 5 (8.3) 2 (1.9) 0 (0) 0 (0) 7 (3.7)
 Middle East & North Africa 2 (3.3) 5 (4.8) 0 (0) 0 (0) 7 (3.7)
 Sub-Saharan Africa 2 (3.3) 0 (0) 2 (15.4) 0 (0) 4 (2.1)
Income group
 High 49 (81.7) 68 (65.4) 4 (30.8) 11 (91.7) 132 (69.4)
 Upper middle 7 (11.7) 6 (5.8) 7 (53.9) 1 (8.3) 21 (11.1)
 Low-middle 4 (6.7) 30 (28.9) 2 (15.4) 0 (0) 36 (19.1)
BMI (kg/m2)
 <18.5 1 (1.7) 3 (2.9) 0 (0) 0 (0) 4 (2.1)
 18.5–24.9 14 (23.3) 46 (44.2) 6 (46.2) 6 (50) 72 (38.1)
 25–29.9 11 (18.3) 30 (28.9) 0 (0) 2 (16.7) 43 (22.8)
 30–34.9 13 (21.7) 14 (13.5) 5 (38.5) 2 (16.7) 34 (18.0)
 35–39.9 7 (11.7) 4 (3.9) 0 (0) 1 (8.3) 12 (6.4)
 ≥40 11 (18.3) 6 (5.8) 2 (15.4) 0 (0) 19 (10.1)
 Not available 3 (5.0) 1 (1.0) 0 (0) 1 (8.3) 5 (2.7)
WHO Performance Status
 0 20 (33.3) 48 (46.2) 7 (53.9) 2 (16.7) 77 (40.7)
 1 29 (48.3) 37 (35.6) 5 (38.5) 8 (66.7) 79 (41.8)
 2 9 (15.0) 15 (14.4) 1 (7.7) 0 (0) 25 (13.2)
 3 2 (3.3) 2 (1.9) 0 (0) 0 (0) 4 (2.1)
 4 0 (0) 1 (1.0) 0 (0) 1 (8.3) 2 (1.1)
 Not available 0 (0) 1 (1.0) 0 (0) 1 (8.3) 2 (1.1)
CCI
 0 5 (8.3) 31 (29.8) 4 (30.8) 0 (0) 40 (21.2)
 1 9 (15.0) 16 (15.4) 1 (7.7) 2 (16.7) 28 (14.8)
 2 10 (16.7) 24 (23.1) 6 (46.2) 3 (25.0) 43 (22.8)
 3 12 (20.0) 13 (12.5) 1 (7.7) 2 (16.7) 28 (14.8)
 4 11 (18.3) 13 (12.5) 1 (7.7) 2 (16.7) 27 (14.3)
 5 5 (8.3) 3 (2.9) 0 (0) 2 (16.7) 10 (5.3)
 6 7 (11.7) 4 (3.9) 0 (0) 1 (8.3) 12 (6.4)
 7 1 (1.7) 0 (0) 0 (0) 0 (0) 1 (0.5)
ASA grade
 1 6 (10.0) 25 (24.0) 4 (30.8) 1 (8.3) 36 (19.1)
 2 22 (36.7) 57 (54.8) 6 (46.2) 6 (50.0) 91 (48.2)
 3 28 (46.7) 19 (18.3) 3 (23.1) 5 (41.7) 55 (29.1)
 4 1 (1.7) 2 (1.9) 0 (0) 0 (0) 3 (1.6)
 5 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
 Not available 3 (5.0) 1 (1.0) 0 (0) 0 (0) 4 (2.1)
FIGO stage
 Not cancer 1 (1.7) 5 (4.8) 0 (0) 3 (25.0) 9 (4.8)
 1/2 45 (75.0) 28 (26.9) 12 (92.3) 8 (66.7) 93 (49.2)
 3/4 9 (15.0) 70 (67.3) 1 (7.7) 1 (8.3) 81 (42.9)
 Not available 5 (8.3) 1 (1.0) 0 (0) 0 (0) 6 (3.2)
Histology
 SCC 0 (0) 0 (0) 13 (100.0) 10 (83.3) 23 (12.2)
 Adenocarcinoma 57 (95.0) 86 (82.7) 0 (0) 0 (0) 143 (75.7)
 GCST 0 (0) 4 (3.9) 0 (0) 0 (0) 4 (2.1)
 Other 2 (3.3) 0 (0) 0 (0) 1 (8.3) 3 (1.6)
 Benign/preinvasive/borderline 0 (0) 4 (3.9) 0 (0) 1 (8.3) 5 (2.7)
 Not available 1 (1.7) 10 (9.6) 0 (0) 0 (0) 11 (5.8)

Data presented as total number (percentage) unless stated otherwise.

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; GCST, germ cell, sex cord stromal or trophoblastic tumors; NACT, neoadjuvant chemotherapy; SCC, squamous cell carcinoma; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

Supplementary Table 3.

Summary of pandemic-related changes in care and outcomes at the last follow-up in non-operated patients by cancer type (n=189)

Uterus (n=60) Ovary (n=104) Cervix (n=13) Vulva/vagina (n=12) Total (n=189) P value
Did not have surgery owing to the pandemic 50 (83.3) 87 (83.7) 10 (76.9) 11 (91.7) 158 (83.6) .802
Operation cancelled owing to the pandemic 9 (15.0) 11 (10.6) 2 (15.4) 1 (8.3) 23 (12.2) .804
Postponed owing to the pandemic 28 (46.7) 62 (59.6) 8 (61.5) 6 (50.0) 104 (55.0) .403
Changed to nonsurgical treatment 9 (15.0) 9 (8.7) 3 (23.1) 2 (16.7) 23 (12.2) .344
Managed by interventional radiologists 1 (1.7) 1 (1.0) 0 (0) 0 (0) 2 (1.1) .921
Received neoadjuvant treatment 5 (8.3) 18 (17.3) 2 (15.4) 1 (8.3) 26 (13.8) .404
Neoadjuvant treatments not given 3 (5.0) 3 (2.9) 0 (0) 0 (0) 6 (3.2) .683
Longer neoadjuvant treatments 1 (1.7) 15 (14.4) 0 (0) 0 (0) 16 (8.5) .014
Shorter neoadjuvant treatments 1 (1.7) 2 (1.9) 0 (0) 0 (0) 3 (1.6) .923
Limited access to staging procedure 0 (0) 5 (4.8) 0 (0) 0 (0) 5 (2.7) .241
Limited access to staging investigations 0 (0) 2 (1.9) 0 (0) 0 (0) 2 (1.1) .648
Mortality 2 (3.3) 3 (2.9) 0 (0) 0 (0) 5 (2.7) .846
Compositea 6 (10.0) 21 (20.2) 5 (38.5) 2 (16.7) 34 (18.0) .084

Data presented as total number (percentage). Multiple changes were reported for each patient when appropriate.

Fotopoulou. Gynecological cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

A composite outcome of unresectable disease or disease progression, emergency surgery and death.

Supplemental Table 4.

Complication rates by COVID-19 status of patients who have received any operations (n=3784)

Uninfected (n=3762) COVID-19 (n=22) P value
Cancer site
 Uterus 1774 (46.4) 7 (31.8) .087
 Ovary 1341 (35.7) 14 (63.6)
 Cervix 448 (11.9) 1 (4.6)
 Vulva/vagina 223 (5.9) 0 (0)
Age (y)
 17–19 13 (0.4) 0 (0) .266
 20–29 92 (2.5) 2 (9.1)
 30–39 288 (7.7) 0 (0)
 40–49 581 (15.4) 3 (13.6)
 50–59 962 (25.6) 4 (18.2)
 60–69 974 (25.9) 4 (18.2)
 70–79 664 (17.7) 7 (31.8)
 80–89 182 (4.8) 2 (9.1)
 >90 6 (0.2) 0 (0)
BMI (kg/m2)
 <18.5 107 (2.8) 2 (9.1) .257
 18.5–24.9 1413 (37.6) 10 (45.5)
 25–29.9 1105 (29.4) 7 (31.8)
 30–34.9 608 (16.2) 0 (0)
 35–39.9 283 (7.5) 1 (4.6)
 ≥40 218 (5.8) 2 (9.1)
 Not available 28 (0.7) 0 (0)
WHO Performance Status
 0 2364 (62.8) 7 (31.8) .003
 1 1006 (26.7) 10 (45.5)
 2 220 (5.9) 5 (22.7)
 3 33 (0.9) 0 (0)
 4 4 (0.1) 0 (0)
 Not available 135 (3.6) 0 (0)
CCI
 0 891 (23.7) 5 (22.7) .097
 1 841 (22.4) 2 (9.1)
 2 869 (23.1) 2 (9.1)
 3 672 (17.9) 7 (31.8)
 4 308 (8.2) 3 (13.6)
 5 117 (3.1) 3 (13.6)
 6 41 (1.1) 0 (0)
 7 13 (0.4) 0 (0)
 8 7 (0.2) 0 (0)
 9 3 (0.1) 0 (0)
ASA grade
 1 1006 (26.7) 6 (27.3) .177
 2 2046 (54.4) 8 (36.4)
 3 681 (18.1) 7 (31.8)
 4 23 (0.6) 1 (4.6)
 5 2 (0.1) 0 (0)
 Not available 4 (0.2) 0 (0)
FIGO stage
 Not cancer 2442 (64.9) 11 (50.0) .315
 1/2 1050 (27.9) 10 (45.5)
 3/4 59 (1.6) 0 (0)
 Not available 211 (5.6) 1 (4.6)
Surgery performed
 Pelvis/perineal 2609 (69.4) 15 (68.2) .884
 Midabdominal 558 (14.8) 4 (18.2)
 Upper-abdominal 318 (8.5) 1 (4.6)
 Others 277 (7.4) 2 (9.1)
Bowel surgery
 No 3633 (96.6) 18 (81.8) <.0001
 Yes 129 (3.4) 4 (18.2)
Approach
 Open 2335 (62.1) 18 (81.8) .178
 Minimally-invasive 1339 (35.6) 3 (13.6)
 Converted 83 (2.2) 1 (4.6)
 Not available 5 (0.1) 0 (0)
Postoperative stay (d) 4 (2–6) 8.5 (5–17) .0001
Postoperative complication
 Any complications 717 (19.1) 14 (63.6) <.0001
 Respiratory complications 52 (1.4) 6 (27.3) <.0001
 Wound infection 164 (4.4) 4 (18.2) .002
 Hemorrhagea 129 (3.4) 2 (9.1) .147
 Ileus 86 (2.3) 3 (13.6) <.0001
 Urinary tract infection 74 (2.0) 3 (13.6) <.0001
 Wound dehiscence 69 (1.8) 2 (9.1) .012
 Sepsis 34 (0.9) 3 (13.6) <.0001
 Thromboembolism 30 (0.8) 0 (0) .674
 Kidney injury 27 (0.72) 1 (4.6) .037
 Other organ injury 24 (0.6) 1 (4.6) .024
 Anastomosis leak 7 (0.2) 1 (4.6) <.0001
 Cardiac arrest 8 (0.2) 0 (0) .829
 Myocardial infarction 4 (0.1) 0 (0) .878
 Stroke 3 (0.1) 0 (0) .895
 Other complications 233 (6.2) 4 (18.2) .021
Mortality 26 (0.7) 4 (18.2) <.0001

Data are presented as total number (percentage) or mean (interquartile range). For postoperative outcomes, data were collected at 30 days after the surgeries.

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Haemorrhage requiring blood transfusion.

Supplemental Table 5.

Comparisons of patients and outcomes who have received any operations by length of stay (<14 days vs ≥14 days; n=3772)a

<14 d (n=3595) ≥14 d (n=177) Proportion ≥14 d P value
Age (y)
 17–19 13 (0.4) 0 (0) 0/13 (0) .034
 20–29 92 (2.6) 2 (1.1) 2/94 (2.1)
 30–39 281 (7.8) 7 (4.0) 7/288 (2.4)
 40–49 563 (15.7) 21 (11.9) 21/584 (3.6)
 50–59 929 (25.8) 37 (20.9) 37/966 (3.8)
 60–69 919 (25.7) 56 (31.6) 56/975 (5.7)
 70–79 622 (17.3) 43 (24.3) 43/665 (6.5)
 80–89 170 (4.7) 11 (6.2) 11/181 (6.1)
 >90 6 (0.2) 0 (0) 0/6 (0)
Income group
 High 2634 (73.3) 129 (72.9) 129/2763 (4.7) .888
 Upper middle 652 (18.1) 31 (17.5) 31/683 (4.5)
 Low-middle 309 (8.6) 17 (9.6) 17/326 (5.2)
BMI (kg/m2)
 <18.5 100 (2.8) 9 (5.1) 9/109 (8.3) .164
 18.5–24.9 1349 (37.5) 73 (41.2) 73/1422 (5.1)
 25–29.9 1058 (29.4) 52 (29.4) 52/1110 (4.7)
 30–34.9 579 (16.1) 27 (15.3) 27/606 (4.5)
 35–39.9 276 (7.7) 6 (3.4) 6/282 (2.1)
 ≥40 211 (5.9) 8 (4.5) 8/219 (3.7)
 Not available 22 (0.6) 2 (1.1) 2/24 (8.3)
WHO performance status
 0 2293 (63.8) 75 (42.4) 75/2368 (3.2) <.0001
 1 947 (26.3) 61 (34.5) 61/1008 (6.1)
 2 193 (5.4) 31 (17.5) 31/224 (13.8)
 3 28 (0.8) 5 (2.8) 5/33 (15.2)
 4 3 (0.1) 1 (0.6) 1/4 (25)
 Not available 131 (3.6) 4 (2.3) 4/135 (3.0)
CCI
 0 869 (24.2) 27 (15.3) 27/896 (3.0) .001
 1 815 (22.7) 28 (15.8) 28/843 (3.3)
 2 819 (22.8) 49 (27.7) 49/868 (5.7)
 3 638 (17.8) 37 (20.9) 37/675 (5.5)
 4 288 (8.0) 21 (11.9) 21/309 (6.8)
 5 109 (3.0) 9 (5.1) 9/118 (7.6)
 6 36 (1.0) 4 (2.3) 4/40 (10)
 7 13 (0.4) 0 (0) 0/13 (0)
 8 6 (0.2) 1 (0.6) 1/6 (14.3)
 9 2 (0.1) 1 (0.6) 1/2 (33.3)
ASA grade
 1 980 (27.3) 31 (17.5) 31/1011 (3.1) <.0001
 2 1957 (54.4) 89 (50.3) 89/2046 (4.4)
 3 632 (17.6) 53 (29.9) 53/685 (7.7)
 4 21 (0.6) 3 (1.7) 3/24 (12.5)
 5 2 (0.1) 0 (0) 0/2 (0)
 Not available 3 (0.1) 1 (0.6) 1/4 (25)
Cancer site
 Uterus 1709 (47.5) 34 (19.2) 34/1743 (2.0) <.0001
 Ovary 1249 (34.7) 104 (58.8) 104/1353 (7.7)
 Cervix 428 (11.9) 21 (11.9) 21/449 (4.7)
 Vagina/vulva 203 (5.7) 18 (10.2) 18/221 (8.1)
 Not available 6 (0.2) 0 (0) 0/6 (0)
FIGO stage
 Not cancer 205 (5.7) 6 (3.4) 6/211 (2.8) <.0001
 1 or 2 2384 (66.3) 59 (33.3) 59/2443 (2.4)
 3 or 4 947 (26.3) 112 (63.3) 112/1059 (10.6)
 Not available 59 (1.6) 0 (0) 0/59 (0)
Lockdown stringency
 Full 1819 (50.6) 91 (51.4) 91/1910 (4.8) .006
 Moderate 846 (23.5) 57 (32.2) 57/903 (6.3)
 Light 829 (23.1) 28 (15.8) 28/857 (3.3)
COVID-19 burden
 High burden 2557 (71.1) 90 (50.9) 90/2647 (3.4) <.0001
 Low burden 961 (26.7) 87 (49.2) 87/1048 (8.3)
 Not available 77 (2.1) 0 (0) 0/77 (0)
Surgery performed
 Pelvis/perineal 2521 (70.1) 93 (52.5) 93/2614 (3.6) <.0001
 Midabdominal 523 (14.6) 39 (22.0) 39/562 (6.9)
 Upper-abdominal 304 (8.5) 15 (8.5) 15/319 (4.7)
 Others 247 (6.9) 30 (17.0) 30/277 (10.8)
Bowel surgery
 No 3494 (97.2) 145 (81.9) 145/3639 (4.0) <.0001
 Yes 101 (2.8) 32 (18.1) 32/133 (24.1)
Approach
 Open 2190 (60.9) 159 (89.8) 159/2349 (6.8) <.0001
 Minimally-invasive 1324 (36.8) 11 (6.2) 11/1335 (0.8)
 Converted 76 (2.1) 7 (4.0) 7/83 (8.4)
 Not available 5 (0.1) 0 (0) 0/5 (0)
Postoperative complication
 Any complications 608 (16.9) 120 (67.8) 120/728 (16.5) <.0001
 Respiratory complications 35 (1.0) 23 (13.0) 23/58 (39.7) <.0001
Mortality 20 (0.6) 10 (5.7) 10/30 (33.3) <.0001

Data presented as total number (percentage) or proportion (percentage).

ASA grade, American Society of Anaesthesiologists Physical Status Classification system; BMI, body mass index; CCI, Charlson Comorbidity Index; FIGO, International Federation of Gynaecology and Obstetrics; WHO, World Health Organization.

Fotopoulou. Gynecologic cancer surgery during the COVID-19 pandemic. Am J Obstet Gynecol 2022.

a

Twelve patients (0.32%) did not have recorded length of stay. For postoperative outcomes, data were collected at 30 days after the operations.

Supplementary Data

Appendix
mmc1.docx (68.6KB, docx)

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Associated Data

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Supplementary Materials

Appendix
mmc1.docx (68.6KB, docx)

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