The impact of surgical delay on resectability of colorectal cancer: An international prospective cohort study

Abstract

Aim:
The SARS-CoV-2 pandemic has provided a unique opportunity to explore the impact of surgical delays on cancer resectability. This study aimed to compare resectability for colorectal cancer patients undergoing delayed versus non-delayed surgery.

Methods:
International prospective cohort study of consecutive colorectal cancer patients with a decision for curative surgery (January-April 2020). Surgical delay was defined as an operation taking place more than 4 weeks after treatment decision, in a patient who did not receive neoadjuvant therapy. A subgroup analysis explored effects of delay in elective patients only. The impact of longer delays was explored in a sensitivity analysis. The primary outcome was complete resection, defined as curative resection with a R0 margin.

Results:
Overall, 5453 patients from 304 hospitals in 47 countries were included, of which 6.6% (358/5453) did not receive their planned operation. Of the 4304 operated patients without neoadjuvant therapy, 40.5% (1744/4304) were delayed beyond four weeks. Delayed patients were more likely to be older, male, more comorbid, have higher BMI, have rectal cancer and early-stage disease. Delayed patients had higher unadjusted rates of complete resection (93.7% vs 91.9%, p=0.032) and lower rates of emergency surgery (4.5% vs 22.5%, p<0.001). After adjustment, delay was not associated with a lower rate of complete resection (OR 1.18, 95%CI 0.90-1.55, p=0.224), which was consistent in elective patients only (OR 0.94, 95%CI 0.69-1.27, p=0.672). Longer delays were not associated with poorer outcomes.

Conclusion:
One in fifteen colorectal cancer patients did not receive their planned operation during the first wave of COVID-19. Surgical delay did not appear to compromise resectability, raising the hypothesis that any reduction in long-term survival attributable to delays is likely to be due to micro-metastatic disease.

Full text

Colorectal Disease. 2022;00:1–19.
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1wileyonlinelibrary.com/journal/codi
Received: 23 November 2021
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Revised: 9 February 2022
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Accepted: 6 March 2022
DOI: 10.1111/cod i.16117
ORIGINAL ARTICLE
The impact of surgical delay on resectability of colorectal
cancer: An international prospective cohort study
COVIDSurg Collaborative*
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2022 The Authors. Colorectal Disease published by John Wiley & Sons Ltd on behalf of Association of Coloproctology of Great Britain and Ireland.
*Collaborating auth ors are listed i n Appendix A.
Regist ration number: C l i n i c a l T r i a l s . g o v ident ifier: NCT0 4384926.
Correspondence
Joana F. F. Simoes, NIHR Global Health
Research Unit on Global Surgery,
University of Birmingham, Birmingham,
UK.
Email: jfs945@bham.ac.uk
Abstract
Aim: The SARS- CoV- 2 pandemic has provided a unique opportunity to explore the impact
of surgical delays on cancer resectability. This study aimed to compare resectability for
colorectal cancer patients undergoing delayed versus non- delayed surgery.
Methods: This was an international prospective cohort study of consecutive colorectal
cancer patients with a decision for curative surgery (January– April 2020). Surgical delay
was defined as an operation taking place more than 4 weeks after treatment decision,
in a patient who did not receive neoadjuvant therapy. A subgroup analysis explored the
effects of delay in elective patients only. The impact of longer delays was explored in a
sensitivity analysis. The primary outcome was complete resection, defined as curative
resection with an R0 margin.
Results: Overall, 5453 patients from 304 hospitals in 47 countries were included, of
whom 6.6% (358/5453) did not receive their planned operation. Of the 4304 operated
patients without neoadjuvant therapy, 40.5% (1744/4304) were delayed beyond 4 weeks.
Delayed patients were more likely to be older, men, more comorbid, have higher body
mass index and have rectal cancer and early stage disease. Delayed patients had higher
unadjusted rates of complete resection (93.7% vs. 91.9%, P = 0.032) and lower rates of
emergency surgery (4.5% vs. 22.5%, P < 0.001). After adjustment, delay was not associ-
ated with a lower rate of complete resection (OR 1.18, 95% CI 0.90– 1.55, P = 0.224),
which was consistent in elective patients only (OR 0.94, 95% CI 0.69– 1.27, P = 0.672).
Longer delays were not associated with poorer outcomes.
Conclusion: One in 15 colorectal cancer patients did not receive their planned operation
during the first wave of COVID- 19. Surgical delay did not appear to compromise resect-
ability, raising the hypothesis that any reduction in long- term survival attributable to de-
lays is likely to be due to micro- metastatic disease.
KEYWORDS
colorectal cancer, coronavirus, COVID- 19, SARS- CoV- 2, surgery, surgical delay

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SIMOES an d COVIDSURG COLLABORATIVE
INTRODUCTION
Globally, colorectal cancer is the third most commonly diagnosed
cancer type and the second largest cause of cancer death [1]. The
severe acute respiratory syndrome coronavirus 2 (SARS- CoV- 2) pan-
demic has affected all aspects of healthcare and has led to variable
delays to the delivery of colorectal cancer surgery across the globe
[2,3]. It is estimated that over 28 million operations were cancelled
in the initial 3 months of disruption alone [4,5]. This creates a unique
‘natural experiment’ to explore the effects of treatment delay on
outcomes of colorectal cancer surgery.
Although there is no international guidance on the optimal tim-
ing for colorectal cancer resection, it is generally perceived as a time
critical intervention. In the UK, the National Health Service sets a
target of 4 weeks from a treatment decision to definitive treatment
in cancer care, but global practice and policy varies significantly. A
number of modelling studies and systematic reviews have explored
the impact of delays on long- term survival in colorectal cancer, but
it is unclear whether this is related to poorer initial cancer control
(i.e., lower rates of complete resection) or micro- metastatic disease
spread [6].
Understanding the effects of surgical delay during the SARS-
CoV- 2 pandemic will help inform future prioritization of surgical
waiting lists during post- pandemic recovery and postoperative sur-
veillance by the multidisciplinary team.
This study aimed to explore the association between delayed
surgery for colorectal cancer in patients not undergoing neoadjuvant
therapy and surgical resectabilit y during the SARS- CoV- 2 pandemic.
METHODS
Study design and setting
This was an international prospective cohort study which included
consecutive patients with a decision for elective curative surgery
from the multidisciplinary team meeting, tumour board or equiva-
lent. Any hospital worldwide undertaking elective colorectal cancer
surgery was eligible for inclusion in this analysis. Each participating
site recruited consecutive eligible patients for a period of 3 months
following the emergence of COVID- 19 in their local area (first noti-
fication of SARS- CoV- 2 ranging between January and April 2020).
Each site obtained ethical approval according to local regulations,
and the COVIDSurg- Cancer study (overall inclusion by cancer type
available in Table S12) was pre- registered with Clini calTr ials.gov
(identifier NCT04384926).
Patient inclusion, pathways and follow- up
All patients with a decision for curative cancer surgery or who would
normally have been offered curative surgery in the pre- pandemic
setting but an alternative treatment was offered due to COVID- 19
were included. Patients were excluded from this study if they had
(1) planned palliative surgery, (2) a suspected cancer that was later
found to be benign on histopathology, (3) a suspected benign tumour
that was later found to be cancerous or (4) received endoscopic
treatment only (e.g., transanal endorectal microsurgery).
From all the included patients, some of them did receive their
planned curative surgery but some ended up not receiving it during
the study period. For patients who were operated, follow- up
data were collected at 30 days after surgery. For patients who re-
mained non- operated, their last known status was recorded. All
follow- up was completed by 31 August 2020 with a minimum fol-
low- up of 3 months for all included patients. The characteristics of
non- operated patients were described and reasons for the non-
performance of the planned surgery were reported. This allows a
comprehensive understanding of the whole sample and an informed
discussion on how treatment pathways that were in place during the
study influenced the patient groups that we are comparing.
Of all the operated patients, some required surgical resection
alone and some required neoadjuvant therapy (chemotherapy and/
or radiotherapy prior to surgery). Due to differences in disease biol-
ogy, and potential effects of treatment intervals in patients under-
going neoadjuvant therapy, the patients who received neoadjuvant
therapy were excluded from the main analysis as their disease be-
haviour is expected to be fundamentally different. However, tumour
location and the type of neoadjuvant treatment are reported in the
supplement for completeness.
Delay to surgery
The main analysis on surgical delays focused on patients who re-
ceived their planned surgery with curative intent, without having re-
ceived neoadjuvant therapy. Delay to surgery was defined according
to the number of weeks from the date of the decision for curative
surgery to the date when the patient received surgery. For the pri-
mary analysis, patients who were operated more than 4 weeks after
their decision for surgery were classified as delayed and those who
were operated within 4 weeks were defined as non- delayed. This
4- week cut- off was informed by UK National Institute for Clinical
Excellence guidance and standards for timely delivery of cancer care
[7].
What does this paper add to the literature?
This was a prospective cohort study of 5453 patients with
a decision for curative colorectal cancer surgery. Surgical
delays of up to 12 weeks were not associated with worse
rates of complete resection. Any reduction in long- term
survival attributable to delays is likely to be due to micro-
metastatic disease and should be the focus of postopera-
tive surveillance programmes.

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SIMOES and COVIDSURG COLLABORATIVE
Outcomes
The primary outcome measure for the study was complete resec-
tion, defined as disease amenable to surgical removal at the time
of surgery with a negative circumferential resection margin (R0, no
microscopic or macroscopic disease within 1 mm of the circumferen-
tial resection margin). Patients whose disease became unresectable
during the study period or whose surgical resection was achieved
with positive resection margins (R1 or R2) were classified as having
an incomplete resection.
Secondary outcomes were also compared between patients
undergoing delayed and non- delayed surgery. These included the
30- day postoperative mortality rate, 30- day major postoperative
complication rate (defined as Clavien– Dindo Grade III– V complica-
tions) [8], stage change from baseline (clinical) to pathology (accord-
ing to the American Joint Committee on Cancer [AJCC] 8th edition
of the TNM staging system [9], defined as upstaged for any increase
in stage, downstaged for any decrease in stage and no change for
patients remaining at the same stage group), detection of new meta-
static disease (clinically, intra- operatively or on radiological imaging
that was not present at the time of decision for surgery) and the rate
of emergency surgery (i.e., as all patients had an initial plan for elec-
tive surgery at study entry, emergency surgery can be interpreted
as a cancer- related complication requiring emergency intervention).
The indications for emergency surgery are presented.
Data variables
Baseline information was collected for each patient at the point
of entry to the study. This included age, sex, American Society
of Anesthesiologists (ASA) physical status classification, Eastern
Cooperative Oncology Group (ECOG) performance score, Revised
Cardiac Risk Index (RCRI), body mass index (BMI) (defined as under-
weight if <18.5 kg/m2, normal if 18.5– 24.9 kg/m2, overweight if 25–
29.9 kg /m2 or obese if ≥30 kg/m2), clinical (based on imaging and
clinical observation at the time of decision for surgery) and patho-
logical TNM stage groups collected according to the AJCC 8th edi-
tion, country income (grouped as high, upper middle and low/low
middle income, as per the World Bank index classification based on
gross national income per capita), surgical approach (open, laparo-
scopic or converted), anastomotic performance (with or without de-
functioning stoma) and anastomotic method (handsewn or stapled).
Data handling and statistics
All the data collected were non- identifiable and uploaded to a se-
cure online server hosted by the University of Birmingham, using
the Research Electronic Data Capture (REDCap) system. Data man-
agement and analysis used RStudio version 4.0.3 with the ‘readr’,
‘tidyverse’, ‘dplyr’, ‘gmodels’, ‘Hmisc’ and ‘finalfit’ packages (R
Foundation for Statistical Computing). Unadjusted categorical data
were compared using the chi- squared test with Fisher's exact modi-
fication where required. A P value <0.05 was considered statisti-
cally significant. Logistic regression models were used to explore the
association between delay to surger y and complete resection, ad-
justing for clinically plausible patient and disease factors selected a
priori. All missing data were recorded and are reported in the tables
and figures.
Reflecting differences in treatment timelines and capacity across
different resource settings, we performed a sensitivity analysis ex-
ploring longer delays of 6, 8 and 12 weeks from treatment decision
to surgery, and the primary outcome measure.
Given that patients undergoing emergency surgery could have
shown distinct clinical features at the time of decision for surgery
that made them more likely to receive an urgent intervention, a
pre- planned subgroup analysis was performed for patients under-
going planned (elective) surgery only. Further subgroup analyses
were performed looking exclusively at colon cancers, rectal cancers,
early disease and advanced disease. For this purpose, early disease
stage was defined as organ confined, non- nodal, non- metastatic
(T1– 3 N0 M0) and advanced disease was defined as reaching the se-
rosa, nodal or metastatic disease (T4, N+ or M1). A sensitivit y analy-
sis of the adjusted and unadjusted results was conducted to explore
the impact of longer delays in resectability: 0– 4, 5– 8, 9– 12 and more
than 12 weeks from decision to surgery.
RESULTS
In total, 5453 patients eligible for elective curative colorectal cancer
surgery were included from 304 hospitals in 47 countries. This cor-
responds to 24.4% of all the patients included in the COVIDSurg-
Cancer study (the remaining being patients with other cancer types)
[10]. Of these 66.3% (3616/5453) had colon cancer and 33.7%
(1837/5453) had rectal cancer. The clinical colorectal cancer stage
was advanced in 63.6% (3466/5453) of the patients and early in
36.4% (1987/5453). Around two- thirds of the patients were ASA
grade 1– 2 (66.7%, 3619/5453) and one- third were ASA grade 3– 5
(33.2%, 1809/5453). The majority of the patients were from high
income countries (84.3%, 4599/5453), with 9.2% (500/5453) being
from upper middle income countries and 6.4% (351/5453) from
lower middle or low income countries.
Non- operated patients
From all the included patients, 6.6% (358/5453) did not receive their
pl anne d oper ation du ring the stu dy perio d (Figure 1), of whom 74.3%
(266/358) were still planned to have curative surgery at the time of
follow- up. Patients who were not operated were more likely to have
rectal cancer (52.5% vs. 32.4%, P < 0.001), worse performance status
(5.9% vs. 2.9% were ECOG 3– 4, P < 0.001), lower BMI (9.3% vs. 3.5%
were underweight, P < 0.001), higher stage disease (14.6% vs. 10.3%
had clinical Stage IV, P = 0.004) and be from a low/lower middle

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SIMOES an d COVIDSURG COLLABORATIVE
income country (18.2% vs. 5.6%, P < 0.001) (Table S1). The reasons
why patients did not receive their planned operation are detailed in
Table S2, with the most common reasons being a multidisciplinary
team decision to avoid surgery due to patient risk (72.6%, 260/358),
disease progression (29.1%, 104/358) and patient being unable to
travel to hospital during the pandemic (26.3%, 94/358).
Operated patients
Of the 5095 operated patients, 15.5% (791/5095) received neoad-
juvant therapy and 85.4% (4304/5095) underwent surgery without
neoadjuvant treatment. The majority of the patients receiving neo-
adjuvant therapy had rectal cancer (81.8%, 647/791). Neoadjuvant
therapy regimens by cancer location are shown in Figure S1.
From the 4304 patients who received an operation with-
out neoadjuvant therapy, 59.5% (2559/4303) had surgery within
4 weeks of treatment decision and 40.5% (1744/4304) were de-
layed beyond 4 weeks. Delayed patients were more likely to be older
(53.0% vs. 46.3% aged over 70 years, P < 0.001), men (58.7% vs.
54.6%, P = 0.008), more comorbid (37.7% vs. 30.9% were ASA 3– 5,
P < 0.001), have a lower performance status (46.4% vs. 53.4% were
ECOG 0), be from a higher income country (90.1% vs. 83.7% were
from high income countries), have a higher BMI (22.5% vs. 17.4%
were obese) and have a rectal cancer (26.9% vs. 20.8%, P < 0.001)
and early stage disease (41.9% vs. 32.8% were clinical Stage I). Full
demographics are shown in Table 1.
Outcomes of delayed surgery
Delayed patients did not have lower rates of complete resection,
compared to non- delayed patients. In the unadjusted analysis, de-
layed patients were more likely to have resectable disease (93.7%
vs. 91.9%, P = 0.032) and less likely to develop new metastases
(6.2% vs. 10.1%, P < 0.001) than non- delayed patients. Changes
in disease stage from baseline to pathological staging were more
common in delayed patients, including both upstaging and down-
staging (Table 2). Delayed patients were also less likely to have
had emergency surgery (4.5% vs. 22.9%, P < 0.001) whilst waiting
for their planned surgery, mainly due to obstructive symptoms.
Other indications for emergency surgery in this cohort are shown
in Table S3. There were no significant differences in 30- day major
postoperative complications (9.3% vs. 9.8%, P = 0.648) or post-
operative mortality rates (1.5% vs. 2.2%, P = 0.126). After adjust-
ment for case mix, delay was not associated with significantly
lower rates of complete resection (OR = 1.18, 95% CI 0.90– 1.55,
P = 0.224) (Figure 2). The full adjusted model can be found in
Table S4.
Subgroup analysis
In the subgroup analysis of patients undergoing elective surger y
only, delay was not associated with lower rates of complete resec-
tion (OR = 0.94, 95% CI 0.69– 1.27, P = 0.672) (logistic regression
FIGURE 1 Flowchart of patient inclusion, with outcomes stratified by delay versus non- delay. Delay was defined as a time from decision
to treat to surgery of >4 weeks
All colorectal patients
(n=5453)
Operated
93.4% (n=5095)
Neoadjuvant therapy
15.5% (n=791)
Non-delayed
59.5% (n=2559)
Resectable disease 91.9% (n=2261) Resectable disease 93.7% (n=1583)Resectable disease 91.9% (n=2261)
New metastatic disease 10.1% (n=229)
30-day mortality 2.2% (n=56)
Emergency surgery 22.9% (n=585)
New metastatic disease 6.2% (n=98)
30-day mortality 1.5% (n=26)
Emergency surgery 4.5% (n=78)
Delayed
40.5% (n=1744)
No neoadjuvant therapy
85.4% (n=4304)
No neoadjuvant therapy
66.5% (n=238)
Neoadjuvant therapy
33.5% (n=120)
Not Operated
6.6% (n=358)

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SIMOES and COVIDSURG COLLABORATIVE
model available in Figure S2). Demographic trends of delayed pa-
tients were also similar to the main analysis (Table S5). When look-
ing at colon and rectal cancers in isolation, a delay of 4 weeks was
not associated with a reduced rate of complete resection in colon
(OR = 1.33, 95% CI 0.95– 1.87, P = 0.101) or rec tal cancer (OR = 0.91,
95% CI 0.58– 1.44, P = 0.692). Delay was not associated with poorer
TAB LE 1 Demographic features of patients having delayed and non- delayed surgery
Non- delayed
(n =2559) Delayed (n =174 4 ) P value
Site Colon 2028 (79.2) 1274 (73.1) <0.001
Rectum 531 (20.8) 470 (26.9)
Age <70 years 1374 (53.7) 819 (47.0) <0.001
≥70 years 1185 (46.3) 925 (53.0)
Sex Female 1162 (45.4) 720 (41.3) 0.008
Male 1397 (54.6) 1024 (58.7)
ASA grade 1– 2 1764 (69.1) 1084 (62.3) <0.001
3 – 5 789 (30.9) 657 (37.7)
Missing 63
ECOG score 01343 (53.1) 795 (46.4) <0.001
1– 2 1101 (43.5) 867 (50.6)
3 – 4 85 (3.4) 50 (2.9)
Missing 30 32
Revised Cardiac Risk Index 1– 2 2382 (93.1) 1598 (91.6) 0.086
≥3 177 (6.9) 146 (8.4)
Body mass index Underweight 92 (3.7) 45 (2.6) <0.001
Normal 1,121 (44.7) 634 (37.1)
Overweight 858 (34.2) 646 (37.8)
Obese 437 (17.4) 385 (22.5)
Missing 51 34
Stage group Stage I 806 (32.8) 709 (41.9) <0.001
Stage II 560 (22.8) 365 (21.6)
Stage III 863 (35.1) 503 (29.7)
Stage IV 230 (9.4) 116 (6.9)
Missing 100 51
Country income High income 2143 (83.7) 1571 (90.1) <0.001
Upper middle income 259 (10.1) 116 (6.7)
Low/lower middle income 157 (6.1) 57 (3.3)
Approach Open 1203 (47.1) 800 (45.9) 0.733
Minimally invasive 1216 (47.6) 850 (48.8)
Converted to open 137 (5.4) 92 (5.3)
Missing 3 2
Anastomosis Yes (with defunctioning stoma) 330 (13.1) 199 (11.6) 0.316
Yes (without defunctioning stoma) 1716 (68.3) 1187 (69.1)
No 467 (18.6) 331 (19.3)
Missing 46 27
Anastomotic method Stapled 1646 (80.5) 1125 (81.2) 0.641
Handsewn 398 (19.5) 260 (18.8)
Missing 515 359
Notes: Delay was defined as a time from decision to treat to surgery of >4 weeks. Data reported as n (%). Percentages expressed of column total.
P values calculated using chi- squared test.
Abbreviations: ASA, American Society of Anesthesiologists classification; ECOG, Eastern Cooperative Oncology Group.

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resectability in patients with early disease only (OR = 1.20, 95% CI
0 . 6 7 – 2 . 1 8 , P = 0.537) or advanced disease only (OR = 1.11, 95% CI
0 . 8 1 – 1 . 5 2 , P = 0.517). Full logistic regression models for the sub-
group analysis are shown in Tables S 6 – S 9 .
Sensitivity analysis of longer surgical delays
In a sensitivity analysis exploring the association of longer delays and
complete resection, 59.5% (2559/4304) of patients were operated
in 0– 4 weeks, 25.3% (1089/4304) in 5– 8 weeks, 8.9% (384/4304) in
9– 12 weeks and 6.3% (271/4304) in >12 weeks from decision to sur-
gery (all demographics available in Table S10). Longer delays were
not associated with worse resectability outcomes in unadjusted
(Table S11) or adjusted analyses (Table 3). Compared to patients
undergoing surgery within 4 weeks of treatment decision, the odds
of complete resection were not significantly different at 5– 8 weeks
from treatment decision (OR = 1.16, 95% CI 0.86– 1.59, P = 0.344),
at 9– 12 weeks (OR = 1.40, 95% CI 0.85– 2.41, P = 0.206) or beyond
12 weeks (OR = 1.03, 95% CI 0.62– 1.80, P = 0.920).
DISCUSSION AND CONCLUSIONS
During the first wave of the SARS- CoV- 2 pandemic, one in 15 pa-
tients did not receive their planned operation for colorectal cancer.
In those who did undergo surgery, delays of more than 4 weeks did
not appear to be associated with reduced rates of complete resec-
tion. This was robust to several sensitivity and subgroup analyses.
Although there are inherent biases in this study design, including
selection bias in those that were exposed to treatment delay, this
study represents a unique natural experiment to better understand
the pathobiology of survival after colorectal cancer surgery.
Whilst long- term oncological outcome data are not yet available
for this cohort, these data provide important insight into the poten-
tial mechanism for the relationship between long- term survival and
treatment delay. Although the previous studies show controversial
findings on the impact of delay to oncological outcomes [1 1– 1 4 ],
a systematic review looking at long- term survival for patients un-
dergoing colorectal cancer surgery 1 month and 3 months after the
diagnosis showed a reduction in overall and disease- free survival
with surgical delays [15]. Another multi- specialty review of delays
TAB LE 2 Unadjusted outcomes compared between delayed and non- delayed patients
Non- delayed
(n =2559) Delayed (n =174 4 ) P value
Resectability Complete resection 2261 (91.9) 1583 (93.7) 0.032
Incomplete resection 199 (8.1) 106 (6.3)
Missing 99 55
Resection margins Positive 107 (4.4) 74 (4.4) 1
Negative 2310 (95.6) 1599 (95.6)
Missing 142 71
Progression to unresectable disease Yes 127 (5.0) 40 (2.3) <0.001
No 2432 (95.0) 1703 (97.7)
Missing 0 1
New metastatic disease Yes 229 (10.1) 98 (6.2) <0.001
No 2036 (89.9) 1472 (93.8)
Missing 294 174
Stage change
(from baseline to pathology)
Downstaged 393 (18.1) 335 (22.0) 0.001
No change 1236 (56.9) 775 (50.8)
Upstaged 543 (25.0) 416 (27.3)
Missing 387 218
30- day mortality Died 56 (2.2) 26 (1.5) 0.126
Alive 2502 (97.8) 1718 (98.5)
Missing 1 0
30- day major postoperative complications Yes 251 (9.8) 163 (9.3) 0.648
No 2307 (90.2) 1581 (90.7)
Missing 1 0
Urgency Emergency 585 (22.9) 78 (4.5) <0.001
Elective 1973 (77.1) 1663 (95.5)
Missing 1 3
Notes: Delay was defined as a time from decision to treat to surgery of >4 weeks. Data reported as n (%). Percentages expressed of column total.
P values calculated using chi- squared test.

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in multimodal cancer treatment showed a negative impact on long-
term oncological outcomes [6]. This study suggests that a delay to
surgery does not affect short- term patho- oncological outcomes. It
raises the hypothesis that any decrease in long- term survival ob-
served is unlikely to be due to initial cancer control and may be re-
lated to micro- metastatic disease spread. Patients whose surgery is
delayed might therefore benefit from closer follow- up strategies for
early detection of relapse and metastatic disease. Further research
is required to understand the effectiveness of enhanced follow- up
pathways on long- term survival, alongside their performance in dif-
ferent tumour biology patterns (not captured in this study).
The clinical features of non- operated patients suggest clinical
selection based on a perceived high risk of surgical complications,
given that these patients had worse performance status, were more
likely to be underweight and had more advanced disease. Although
these decisions probably aimed to protect frail patient s from the ad-
ditional risk conveyed by perioperative SARS- CoV- 2 infection, they
might have exposed some patients with advanced disease to a risk of
progression to palliative disease. Changes in the management of col-
orectal cancer during the COVID- 19 pandemic have been described
by several research groups, including reduction of the number of
patients receiving surgery and shorter treatment regimens [1 6 – 1 8 ].
This study provides further insight on the drivers of these clinical
decisions and on which patients might have been more impacted by
them.
Advanced (non- organ confined) and rectal cancers were also
more likely to be operated promptly, as opposed to early and colon
cancers which were more likely to be delayed. This suggests that
additional features of the disease were perceived by surgical teams
as justifying early surgery, which might explain why non- delayed pa-
tients had higher non- adjusted rates of progression to unresectable
disease and new metastasis. Changes in disease stage observed in
this study include higher rates of both upstage and downstage with
increased delay. As delayed patients were more likely to have ad-
vanced disease, this might reflect lower reliability of clinical staging
and imaging studies in advanced cancers, particularly when nodal
disease is present [19].
The performance of elective colorectal cancer surgery within
4 weeks of treatment decision might not be feasible in many settings
worldwide, even in a pre- pandemic setting [20,21]. Additionally,
there might be variation in the usual timeframes from decision to
surgery across settings, depending on local practices and pathways
(e.g., preoperative assessment efficiency, existence of routine pre-
habilitation programmes). This study looked at longer delays of 8
and 12 weeks which showed no association with resectability im-
pairment either, ensuring the generalizability of the findings.
Symptoms of obstruction, perforation or bleeding in patients
awaiting elective surger y might have prompted earlier surgery, ex-
plaining why emergency surgery was more common in non- delayed
patients (undergoing surgery within 4 weeks of treatment decision).
FIGURE 2 Multivariate logistic regression model exploring the association between delay to surgery and resectability, adjusting for
patient and disease factors. Number in dataframe 3966, number in model 3966, missing 0, Akaike information criterion 1786.9, C statistic
0.776. Full model presented in Table S4. Delay was defined as a time from decision to treat to surgery of >4 weeks. Data reported as
odds ratio (95% confidence interval, P value). OR >1 means higher odds of resectability for delayed patients, OR <1 means lower odds of
resectability for delayed patients. ASA, American Society of Anesthesiologists classification; ECOG, Eastern Cooperative Oncology Group;
RCRI. Revised Cardiac Risk Index
Resectability: OR (95% CI, p-value)
Delay
Delayed
Colon
Rectum
<70
>=70
Female
Male
Grades 1-2
Grades 3-5
0
1-2
1-2
3-4
>=3
Stage I
Stage II
Stage III
Stage IV
Non-delayed -
-
-
-
-
-
-
-
1.18 (0.90-1.55, p=0.224)
0.51 (0.38-0.67, p<0.001)
1.03 (0.78-1.36, p=0.833)
0.92 (0.71-1.19, p=0.510)
0.99 (0.73-1.36, p=0.972)
0.74 (0.55-0.99, p=0.041)
0.29 (0.17-0.53, p<0.001)
1.17 (0.70-2.07, p=0.558)
0.65 (0.40-1.03, p=0.066)
0.33 (0.23-0.49, p<0.001)
0.05 (0.03-0.07, p<0.001)
Odds ratio (95% CI, log scale)
0.5 1.0 1.5 2.0 2.5
Site
Age
Sex
ASA grade
ECOG score
RCRI score
Stage group

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SIMOES an d COVIDSURG COLLABORATIVE
Although we presented the reasons for emergency surgery in this
cohort of patients awaiting planned resection, some could have had
symptoms of obstruction or other acute complication at the time of
treatment decision, to whom a delay beyond 4 weeks would not be
clinically acceptable. To address the selection bias that these clini-
cal findings might have had in the length of delay from decision to
surgery, we performed a subgroup analysis of patients undergoing
elective surgery only, that again showed no difference in resectabil-
ity with surgical delays.
This study has several important limitations. Longer- term fol-
low- up of this cohort will be required to explore the true clinical
impact of treatment delay for these patients. The second is the risk
of selection bias in the comparison of delayed and non- delayed pa-
tients. We attempted to overcome this through multivariable mod-
elling and several subgroup and sensitivity analyses, but the analysis
may still be subject to residual bias from unmeasured confounders.
Third, patients who remained non- operated may have had a poorer
prognosis at baseline and/or may have been subject to disease pro-
gression and other cancer- related sequelae which could lead to
underestimation of the impact of delay (7% of the cohort overall).
Fourth, we were unable to explore the impact of treatment delay
in patients with prior neoadjuvant therapy, who pose a biologically
distinct treatment group. Finally, histological data were not col-
lected and therefore we were unable to explore whether molecu-
lar subtypes or mutational status differed between the groups, and
whether this impacted resection.
SARS- CoV- 2 waves are not the only pressure that health systems
face, and many factors can cause delays in the delivery of surgical
care. These findings can inform clinical decision making, manage-
ment of surgical waiting lists and patient informed consent before
surgery. Guidance on management of colorectal cancer should also
take these findings into account when designing follow- up strate-
gies for patients who are operated for colorectal cancer. The pos-
sibility of performing cancer resection with a few weeks of delay
without a negative impact on local control could be important for
patients who may benefit from longer periods of pre- habilitation and
pre- conditioning before surgery, in order to achieve a better fitness
status and optimize perioperative outcomes.
TABLE3 Multivariate logistic regression model exploring the association between stratified delay to surgery and resectability, adjusting
for patient and disease factors
Non- resectable
(n =297)
Resectable
(n =3669) OR(univariable) OR(multivariable)
Delay 0– 4 weeks 193 (8.2) 2154 (91.8) – –
5– 8 weeks 66 (6.5) 955 (93.5) 1.30 (0.98– 1.74, P = 0.079) 1.16 (0.86– 1.59, P = 0.344)
9– 12 weeks 19 (5.3) 338 (94.7) 1.59 (1.01– 2.67, P = 0.060) 1.40 (0.85– 2.41, P = 0.206)
>12 weeks 19 (7.9) 222 (92.1) 1.05 (0.66– 1.76, P = 0.855) 1.03 (0.62– 1.80, P = 0.920)
Site Colon 200 (6.6) 2846 (93.4) – –
Rectum 97 (10.5) 823 (89.5) 0.60 (0.46– 0.77, P < 0.001) 0.51 (0.38– 0.68, P < 0.001)
Age <70 158 (7.9) 1850 (92.1) – –
≥70 139 (7.1) 1819 (92.9) 1.12 (0.88– 1.42, P = 0.358) 1.03 (0.78– 1.36, P = 0.828)
Sex Female 127 (7.3) 1604 (92.7) – –
Male 170 (7.6) 2065 (92.4) 0.96 (0.76– 1.22, P = 0 .749) 0.91 (0.70– 1.18, P = 0.491)
ASA grade 1– 2 187 (7.1) 2437 (92.9) – –
3 – 5 110 (8.2) 1232 (91.8) 0.86 (0.67– 1.10, P = 0.226) 0.99 (0.73– 1.36, P = 0.96 4)
ECOG grade 0129 (6.4) 1874 (93.6) – –
1– 2 144 (7.9) 1690 (92.1) 0.81 (0.63– 1.03, P = 0.090) 0.74 (0.55– 0.98, P = 0.039)
3 – 4 24 (18.6) 105 (81.4) 0.30 (0.19– 0.50, P < 0.001) 0.29 (0.17– 0.53, P < 0.001)
RCRI grade 1– 2 278 (7.6) 3387 (92.4) – –
≥3 19 (6.3) 282 (93.7) 1.22 (0.77– 2.03, P = 0.421) 1.18 (0.71– 2.08, P = 0.544)
Stage group Stage I 39 (2.7) 1418 (97.3) – –
Stage II 35 (4.0) 838 (96.0) 0.66 (0.41– 1.05, P = 0.078) 0.65 (0.40– 1.03, P = 0.066)
Stage III 102 (7.8) 1205 (92.2) 0.32 (0.22– 0.47, P < 0.001) 0.34 (0.23– 0.49, P < 0.001)
Stage IV 121 (36.8) 208 (63.2) 0.05 (0.03– 0.07, P < 0.001) 0.05 (0.03– 0.07, P < 0.001)
Notes: Number in dataframe 3966, number in model 3966, missing 0, Akaike information criterion 1790.1, C statistic 0.776. Delay was measured from
decision to treat to surgery. Data reported as odds ratio (95% confidence interval, P value). OR >1 means higher odds of resectabilit y for delayed
patients, OR <1 means lower odds of resectability for delayed patients.
Abbreviations: ASA, American Society of Anesthesiologists classification; ECOG, Eastern Cooperative Oncology Group; RCRI, Revised Cardiac Risk
Index.

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FUNDING INFORMATION
This study was funded and supported by the National Institute for
Health Research Global Health Research Unit on Global Surgery,
Association of Coloproctology of Great Britain and Ireland, Bowel
and Cancer Research, Bowel Disease Research Foundation,
Association of Upper Gastrointestinal Surgeons, British Association
of Surgical Oncology, British Gynaecological Cancer Society,
European Society of Coloproctology, Medtronic, Sarcoma UK, the
Urology Foundation, Vascular Society for Great Britain and Ireland,
and Yorkshire Cancer Research. The funders did not interfere with
the data collection or presentation of results.
AUTHOR CONTRIBUTION
Individual contributions to this paper are listed in the appendix. The
writing group and statistical analysis group have analysed, interpreted
and drawn conclusions from the data. The COVIDSurg operations
team, international cancer leads and dissemination committees led
the conduct of the study and contributed to data curation. The listed
collaborators have contributed with patient level data from their sites.
CONFLICT OF INTEREST
There are no conflicts of interest to declare.
ETHICAL STATEMENT
This study was approved in every participating country and hospital
as per local requirements. National and hospital leads were respon-
sible and guaranteed the necessary approvals ahead of data upload.
DATA AVAIL AB I LI T Y STATE MEN T
Data- sharing requests will be considered by the management group
upon written request to the corresponding author. If agreed, de-
identified participant data will be available, subject to a data- sharing
agreement.
TWITTER
@CovidSurg
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SUPPORTING INFORMATION
Additional supporting information may be found in the online
version of the article at the publisher’s website.

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How to cite this article: COVIDSurg Collaborative@Covid
Surg. The impact of surgical delay on resectability of
colorectal cancer: An international prospective cohort study.
Colorectal Dis. 2022;00:1–19. https://doi.org /10.1111/
codi.16117
APPENDIX A
LIST OF PUBMED CITABLE COVIDSURG
COLLABORATORS
Writing group: Michel Adamina (Switzerland), Adesoji Ademuyiwa
(Nigeria), Adewale Adisa (Nigeria), Aneel A Bhangu (UK), Ana Minaya
Bravo (Spain), Miguel F Cunha (Portugal), Sameh Emile (Egypt),
Dhruva Ghosh (India), James C Glasbey (UK), Benjamin Harris
(UK)*, Debby Keller (USA), Samuel Lawday (UK), Hans Lederhuber
(Germany), Sezai Leventoglu (Turkey), Elizabeth Li (UK), Maria
Marta Modolo (Argentina), Rohin Mittal (India), Helen M Mohan
(Ireland), Dmitri Nepogodiev (UK), Marie Dione Parreño- Sacdalan
(Philippines), Francesco Pata (Italy), Peter Pockney (Australia),
Martin Rutegård (Sweden), Joana FF Simões (Portugal)*, Neil Smart
(UK), Chris Varghese (New Zealand).
*Joint first authors.
Statistical analysis and data handling
James C Glasbey, Joana FF Simoes, Benjamin Harris, Aneel A
Bhangu.
COVIDSurg Operations Committee
Dmitri Nepogodiev (Chai r), 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.
International Cancer Leads (*denotes specialty Principal Investigators)
James C Glasbey (Chair)
Colorectal: Neil J Smart*, Ana Minaya- Bravo*, Jonathan P Evans,
Gaetano Gallo, Susan Moug, Francesco Pata, Peter Pockney,
Salomone Di Saverio, Abigail Vallance, Dale Vimalchandran.
Oesophagogastric: Ewen A Griffiths*, Sivesh K Kamarajah,
Richard PT Evans, Philip Townend.
Hepatopancreatobiliary: Keith Roberts*, Siobhan McKay*, John
Isaac, Sohei Satoi.
Thoracic: John Edwards*, Aman S Coonar, Adrian Marchbank,
Edward J Caruana, Georgia R Layton, Akshay Patel, Alessandro
Brunelli.
Sarcoma: Samuel Ford*, Anant Desai*, Alessandro Gronchi*,
Marco Fiore*, Max Almond, Fabio Tirotta, Sinziana Dumitra.
Neurosurgery: Angelos Kolias*, Stephen J Price, Daniel M
Fountain, Michael D Jenkinson, Peter Hutchinson, Hani J Marcus,
Rory J Piper, Laura Lippa, Franco Servadei, Ignatius Esene, Christian
Freyschlag, Iuri Neville, Gail Rosseau, Karl Schaller, Andreas K
Demetriades, Faith Robertson, Alex Alamri.
Head and neck: Richard Shaw*, Andrew G Schache, Stuart C
Winter, Michael Ho, Paul Nankivell, Juan Rey Biel, Martin Batstone,
Ian Ganly.
Breast: Raghavan Vidya*, Alex Wilkins, Jagdeep K Singh, Dinesh
Thekinkattil.
Gynaecology: Sudha Sundar*, Christina Fotopoulou*, Elaine YL
Leung, Tabassum Khan, Luis Chiva, Jalid Sehouli, Anna Fagotti, Paul
Cohen, Murat Gutelkin, Rahel Ghebre, Thomas Konney, Rene Pareja,
Rob Bristow, Sean Dowdy, Shylasree TS, Rajkumar Kottayasamy
Seenivasagam, Joe Ng, Keiichi Fujiwara.
Urology: Grant D Stewart*, Benjamin Lamb, Krishna Narahari,
Alan McNeill, Alexandra Colquhoun, John S McGrath, Steve
Bromage, Ravi Barod, Veeru Kasivisvanathan*, Tobias Klatte.
Dissemination Committee
Joana FF Simoes (Chair); 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,
A l ex is P A rn a ud , Kn u t Ma gn e Au g es ta d, Fa ri s Ay as ra , Jo s é Aze v ed o,
Brittany K Bankhead- Kendall, Emma Barlow, David Beard, Ruth A
Benson, Ruth Blanco- Colino, Amanpreet Brar, Ana Minaya- Bravo,
Kerry A Bree n, Chri s Bret herto n, Igo r Lima Bua rqu e, Joshu a 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 Mohan, Rachel Moore,
David Moszkowicz, Susan Moug, Joshua S Ng- Kamstra, Mayaba
Maimbo, Ionut Negoi, Milagros Niquen, Faustin Ntirenganya,
Maricarmen Olivos, Kacimi Oussama, Oumaima Outani, Marie
Dione Parreño- Sacdalan, Francesco Pata, Carlos Jose Perez Rivera,
Thomas D Pinkney, Willemijn van der Plas, Peter Pockney, Ahmad
Qureshi, Dejan Radenkovic, Antonio Ramos- De la Medina, Toby
Richards, Keith Roberts, April C Roslani, Martin Rutegård, Juan
José Segura- Sampedro, Irène Santos, Sohei Satoi, Raza Sayyed,
Andrew Schache, Andreas A Schnitzbauer, Justina O. Seyi- Olajide,
Neil Sharma, Catherine A Shaw, Richard Shaw, Sebastian Shu,
Kjetil Soreide, Antonino Spinelli, Grant D Stewart, Malin Sund,
Sudha Sundar, Stephen Tabiri, Philip Townend, Georgios Tsoulfas,
Gabrielle H van Ramshorst, Raghavan Vidya, Dale Vimalachandran,

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SIMOES and COVIDSURG COLLABORATIVE
Oliver J Warren, Duane Wedderburn, Naomi Wright, EuroSurg,
European Society of Coloproctology (ESCP), Global Initiative for
Children’s Surgery (GICS), GlobalSurg, GlobalPaedSurg, ItSURG,
PTSurg, SpainSurg, Italian Society of Colorectal Surgery (SICCR),
Association of Surgeons in Training (ASiT), Irish Surgical Research
Collaborative (ISRC), Transatlantic Australasian Retroperitoneal
Sarcoma Working Group (TARPSWG), Italian Society of Surgical
Oncology (SICO).
Collaborators (*denotes hospital leads)
Argentina: Valenzuela JI* (Hospital Velez Sarsfield, City of Buenos
Aires); Alurralde C, Caram EL, Eskinazi DG* (Sanatorio 9 De Julio
Sa, Tucuman); Badra R, García JS, Lucchini SM* (Sanatorio Allende,
Cordoba).
Australia: Vasey C*, Watson E (Ballarat Base Hospital, Ballarat
Central); Cecire J, Salindera S*, Sutherland A (Coffs Harbour Health
Campus, Coffs Harbour NSW); Ahn JH, Chen S, Gauri N, Jang S,
Jia F, Mulligan CS, Yang W, Ye G, Zhang H (Concord Repatriation
General Hospital, Concord West, Sydney); Moss J*, Richards T, Thian
A, Vo UG* (Fiona Stanley Hospital, Perth); Bagrai<